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WHO
South-East Asia Journal of Public Health

(World Health Organization, Regional Office for South-East Asia)
ISSN 2224-3151
E-ISSN 2304-5272
EDITORIAL BOARD
Advisory Board
Samlee Plianbangchang (Chair)

Richard Horton
David Sanders
Lalit M Nath
Hooman Momen
Fran Baum
Chitr Sitthi-amorn
Editorial Board
Poonam K Singh (Chair)

Sattar Yoosuf
Nyoman Kumara Rai
Aditya P Dash
Athula Kahandaliyanage
Nata Menabde
Mahmudur Rahman
Chencho Dorji
Hasbullah Thabrany
Nay Soe Maung
Suniti Acharya
Phitaya Charupoonphol
Kenneth Earhart
Sangay Thinley
Quazi Munirul Islam
Maureen E Birmingham
Rohini de A Seneviratne
Mariam Cleason
Jacques Jeugmans
Editorial Team
Sarah Ramsay (Chief Editor)

Jennie Greaney (Coordinator)
Rajesh Bhatia (Associate Editor)
Nyoman Kumara Rai
Sudhansh Malhotra
Nihal Abeysinghe
Renu Garg
Prakin Suchaxaya
Roderico Ofrin
Leonard Ortega
Aditya P Dash
Sunil Senanayake
Richard Brown
WHO South-East Asia Journal of Public Health | January-March 2014 | 3 (1)
WHO

GENERAL INFORMATION
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WHO

January-March| Volume 3 | Issue 1
Contents
Foreword ........................................................................................................................................ 1
Editorial
Vector-borne diseases in South-East Asia: burdens and key challenges to be addressed

Rajesh Bhatia, Leonard Ortega, A P Dash, Ahmed Jamsheed Mohamed............................................................... 2
Perspective
Expediency of dengue illness classification: the Sri Lankan perspective

Hasitha Tissera, Jayantha Weeraman, Ananda Amarasinghe, AnandaWijewickrama, Paba Palihawadana,
LakKumarFernando............................................................................................................................. 5
Reviews
Highly infectious tick-borne viral diseases: Kyasanur forest

disease and Crimean-Congo hemorrhagic fever in India
Devendra T. Mourya, Pragya D Yadav, Deepak Y Patil..................................................................................... 8
Current status of dengue and chikungunya in India

Dayaraj Cecilia..................................................................................................................................22
Original research
Vector-borne diseases in central India, with reference

to malaria,filaria, dengue and chikungunya
Neeru Singh, Manmohan Shukla, Gyan Chand, Pradip V Barde, Mrigendra P Singh..................................................28
Co-circulation of dengue virus serotypes with chikungunya

virus in Madhya Pradesh, central India
Pradip V Barde, Mohan K Shukla, Praveen K Bharti, Bhupesh K Kori, Jayant K Jatav, Neeru Singh..............................36
Barriers to malaria control in rural south-west Timor-Leste: a qualitative analysis

Penny E Neave, Maria L Soares...............................................................................................................41
Dengue fever in a rural area of West Bengal, India, 2012: an outbreak investigation
Dilip K Biswas, Rama Bhunia, Mausumi Basu...............................................................................................46
Dengue vectors in urban and suburban Assam, India: entomological observations

V Dev, K Khound, GG Tewari..................................................................................................................51
An evaluation of the surveillance system for dengue virus infections in Maldives

Aishath Aroona Abdulla, Fathimath Rasheeda, Ibrahim Nishan Ahmed, Maimoona Aboobakur...................................60
iii
Research briefs
Atypical presentation of visceral leishmaniasis (kala-azar) from non-endemic area

Yatendra Singh, Paramjeet Singh, Subhash Chandra Joshi, Mohammad Khalil.......................................................69
Profile of dengue infection in

Jamnagar city and district, west India
Krunal D Mehta, Prakash S Gelotar, Swati C Vachhani, Naresh Makwana, Mala Sinha..............................................72
Policy and practice
Mass primaquine preventive treatment for control of Plasmodium vivax malaria

in the Democratic Peoples Republic of Korea: a country success story
Shushil Dev Pant, Kim Yun Chol, Yonas Tegegn, Partha Pratim Mandal, Ri Kwang Chol............................................75
Monitoring the durability of long-lasting insecticidal nets in field conditions in Nepal

J Hii, GD Thakur, BR Marasini, YR Pokhrel, MP Upadhyay, KRRijal, NR Adhikar, SK Pant, L Ortega, N Singh, P Ghimire.....81
Malaria elimination in Sri Lanka: what it would take to reach the goal
Risintha Premaratne, Leonard Ortega, Navaratnasingam Janakan, Kamini N Mendis..............................................85
Containing artemisinin resistance of Plasmodium falciparum in

Myanmar: achievements, challenges and the way forward
Thar Tun Kyaw, Thaung Hlaing, Krongthong Thimasarn, Khin Mon Mon, Gawrie N. L. Galappaththy, Valaikanya Plasai,
Leonard Ortega.................................................................................................................................90
Economic burden of malaria in India: the need for effective spendings

Indrani Gupta, Samik Chowdhury............................................................................................................95
Towards universal health coverage: an example of malaria intervention in Nepal

Shiva Raj Adhikari............................................................................................................................ 103
Report from the field
The National Academy of Vectors and Vector Borne Diseases in India: two decades
of progress
Neena Valecha and M.R. Ranjit............................................................................................................ 113
Public health classic
On some peculiar pigmented cells found in two mosquitos fed on malarial blood
Ronald Ross.................................................................................................................................... 117
Recent WHO Publications
Aide-mmoires Dengue, Kala-azar, Lymphatic filariasis, Malaria............................................ 121

Bibliography on Vector-borne Diseases from the South-East Asia Region,
20092013....................................................................................................................................................................... 121
Dengue Bulletin, Volume 37, 2013.................................................................................................................. 122
iv
Access this article online
Foreword
Website: www.searo.who.int/
DOI: 10.4103/2224-3151.115828
Quick Response Code:
Foreword
The South-East Asia Region of the

World Health Organization (WHO),
home to a quarter of the global
population, faces several publichealth challenges and high disease
burdens with relatively weak health
systems. The social, cultural and
economic situations in the Region are
quite distinct and demand innovative
solutions suited to local communities.
Lessons learned need to be rapidly
disseminated within the Region to stimulate adaptation and
application. In 2009, the WHO South-East Asia Advisory
Committee on Health Research endorsed the recommendation
of the regional meeting on research priorities in communicable
diseases that the WHO South-East Asia Regional Office
should facilitate sharing and dissemination of research by
various means, including a public-health journal. These factors
prompted the Regional Office to begin quarterly publication of
the WHO South-East Asia Journal of Public Health in 2012.
The World Health Assembly in its first meeting in 1948
decided to celebrate 7 April of each year, with effect from
1950, as World Health Day. The day marks the founding of the
World Health Organization; each year a theme is selected that
highlights a priority area of public health. The theme for 2014
is vector-borne diseases illnesses to which more than half of
the worlds population are at risk.
in disease management but the effectiveness of the available

vector-control methods is limited by logistic problems, high
cost, insecticide resistance and concerns about environmental
pollution. Vector-borne diseases have not only adversely
affected human health but also impeded overall socioeconomic
development. While we have gained considerable insights into
the transmission biology and management of certain vectorborne diseases over the past few decades, limited capacity
exists to apply that knowledge.
To mark World Health Day 2014, this special issue of the
WHO South-East Asia Journal of Public Health is devoted to
vector-borne diseases. The 18 articles cover a range of current
research and policy aspects of vector-borne diseases, including
malaria, dengue, Kyasanur forest disease and Crimean-Congo
haemorrhagic fever. The articles are from different countries
in the Region including the Democratic Republic of Korea,
Maldives and Timor-Leste. We conclude this special issue by
reproducing the classic article by Sir Ronald Ross published in
the British Medical Journal in 1897. Ross, whose research was
done in the South-East Asia Region, would go on to receive the
Nobel Prize in Physiology or Medicine in 1902 for his work
on malaria, by which he has shown how it enters the organism
and thereby has laid the foundation for successful research on
this disease and methods of combating it.
I sincerely hope that readers will find this special issue very
informative and useful.
In recent years, vector-borne diseases have emerged as serious

public-health problems worldwide, particularly in the SouthEast Asia Region. These diseases still represent a significant
threat to human health despite considerable national and
international efforts. Population growth, urbanization,
migration and poor environmental sanitation are some of the
major causes of the emergence and re-emergence of vectorborne diseases. Control of vectors remains a major component
Dr Poonam Khetrapal Singh

World Health Organization
Regional Director for South-East Asia
Editorial
DOI: 10.4103/2224-3151.115828
Vector-borne diseases in South-East Asia:

burdens and key challenges to be addressed
WORLD HEALTH DAY AND

ITS SIGNIFICANCE
fitting that the theme of World Health Day 2014 focuses on

vector-borne diseases.1
World Health Day is celebrated on 7 April every year to mark the

anniversary of the founding of the World Health Organization
(WHO) in 1948. Each year a theme is selected that highlights
a priority area of public health. It provides an opportunity for
individuals in every community to get involved in activities
that can lead to better health. World Health Day 2014 focuses
on vector-borne disease with the following aims: (a) families
living in areas where diseases are transmitted by vectors know
how to protect themselves; (b) travellers know how to protect
themselves from vectors and vector-borne diseases; (c)in
countries where vector-borne diseases are a public-health
problem, ministries of health put in place measures to improve
the protection of their populations; and (d) in countries where
vector-borne diseases are an emerging threat, health authorities
work with environmental and other authorities locally and in
neighbouring countries to improve integrated surveillance of
vectors and to take measures to prevent their proliferation.1
Many vector-borne diseases are prevalent in the SouthEast Asia Region. These include, among others, mosquitoborne diseases (e.g. malaria, dengue, chikungunya, Japanese
encephalitis, lymphatic filariasis), sandfly-borne disease (kalaazar) and snail-transmitted disease (e.g. schistosomiasis). The
higly infectious and fatal tick borne viral diseases, Kyasanur
forest disease and Crimean Congo hemorrhagic fever are
present in India6 but not much is known about these in the
Region probably due to poor surveillance and very limited
diagnostic facilities to detect it.
This special issue of the WHO South-East Asia Journal of

Public Health focusing on vector-borne diseases is one of the
highlights of World Health Day 2014 activities in the WHO
Regional Office for South-East Asia.
VECTOR-BORNE DISEASES
Vectors are living organisms that can transmit infectious
diseases between humans or from animals to humans.
Mosquitoes are the best known disease vector. Others include
ticks, flies, sandflies, fleas, triatomine bugs and some freshwater
aquatic snails.2
Vector-borne diseases account for more than 17% of all
infectious diseases, causing more than 1 million deaths
annually.2 Yet, five vector-borne diseases Chagas disease,
dengue/severe dengue, human African trypanosomiasis,
leishmaniasis, lymphatic filariasis and schistosomiasis are
among the 17 neglected tropical diseases.3 The incidence of
dengue has increased 30-fold over the last 50 years. Up to
50100 million infections are now estimated to occur annually
in over 100 endemic countries, putting almost half of the
worlds population at risk.4 In 2012, there were an estimated
207 million cases and an estimated 627 000 deaths due to
malaria, mostly (90%) in sub-Saharan Africa.5 It is therefore
Malaria is endemic in all countries in the Region except

Maldives, which has been malaria-free since 1984. WHO
estimated that there were 27 million cases and 42000 deaths
due to malaria in 2012 in the Region, where around 1.4 billion
people are at risk.5 In India, the total economic burden from
malaria could be around $1940 million, mainly from lost
earnings (75%) while 24 percent comes from treatment costs.7
Of the 1.3 billion people globally at risk of lymphatic filariasis,
871 million reside in the South-East Asia Region, of whom
297 million (34%) are children. Of the 120 million infected
people globally, 60 million are in the Region. The Region thus
accounts for about 65% of the global population at risk and
50% of the infected people.8 About 147 million people in three
countries (Bangladesh, India and Nepal) are at risk of kalaazar, mainly the poor and marginalized populations. Recently,
a small focus of kala-azar has been identified in Bhutan.
Estimates indicate about 100 000 cases of kala-azar per year in
this Region.9 Schistosomiasis in the Region is limited to small
areas in two districts in Indonesia where the number of schoolage children requiring preventive chemotherapy in 2012 was
only 2998 compared with 114 348 387 globally, mainly in
Africa.10
The South-East Asia Region has become hyperendemic with
regular reporting of dengue cases since 2000. The maximum
number of cases (355 525) and deaths (1982) were recorded
during 2010.11 In 2012, a total of 257 204 cases and 1229
deaths were reported from the Region.12 Chikungunya occurs
in Africa, Asia and the Indian subcontinent. Human infections
in Africa have been at relatively low levels for a number of
years. A major outbreak occurred in the islands of the Indian
Ocean in 2005 and since then, India, Indonesia, Maldives,
Bhatia et al.: Vector-borne diseases in South-East Asia
Myanmar and Thailand have reported over 1.9 million cases.13

Japanese encephalitis is endemic in 24 countries in the WHO
South-East Asia and Western Pacific regions. It is the main
cause of viral encephalitis in many countries of Asia with
nearly 68 000 clinical cases every year. The case-fatality
rate among those with encephalitis can be as high as 30%.
Permanent neurological or psychiatric sequelae can occur in
3050% of those with encephalitis. Safe and effective vaccines
are available to prevent the disease. Treatment is focused on
relieving severe clinical signs and supporting the patient to
overcome the infection.14
with delayed parasite clearance in patients treated with

artemisinin has been identified, which could help improve
global surveillance of artemisinin resistance.26 There is an
urgent need for all stakeholders to work together to address
insecticide resistance and drug resistance in accordance with
WHO-recommended strategies.22, 27 In the Greater Mekong
Subregion, WHO is coordinating the emergency response to
artemisinin resistance28 that is being implemented by ministries
of health and nongovernmental organizations, with support
from development partners. A recent report from Myanmar29,
indicates several challenges should be addressed to improve
further the achievements in containing artemisinin resistance.
ADDRESSING KEY CHALLENGES

Most vector-borne diseases have unique epidemiological
features as described in some of the articles in this special issue
of the WHO South-East Asia Journal of Public Health6,1518.
However, most of these diseases share common socioeconomic
determinants. These include difficult access to health services;
poverty; and poor housing, sanitation and water supplies.
Efficient, effective and sustainable prevention and control
of vector-borne diseases requires not only the application of
biomedical tools but also interventions to address those factors
that are beyond the domain of the health sector.
Outbreaks of dengue, chikungunya and Japanese encephalitis
are becoming common, possibly related to increasing population
movement, globalization of trade and urbanization without
adequate measures to prevent vector breeding. In addition
to effective systems for surveillance and rapid response,
multisectoral collaboration and community participation are
needed to prevent and control outbreaks of these diseases.
The parasitic vector-borne diseases kala-azar, lymphatic
filariasis, schistosomiasis and malaria are being targeted for
elimination at least in some countries. Some key challenges
to be addressed to accelerate progress towards elimination are
common to these diseases. Among them is the need to scaleup further the use of existing strategies, including integrated
vector management,19 and put in place innovative delivery
mechanisms to help ensure that everyone at risk or with
the disease can easily access evidence-based interventions.
Strong political will, sustainable financing and community
participation are essential. Investments are needed to
generate strategic information for decision-making, improve
procurement and supply chain management and develop and
maintain the right mix of expertise at different levels of the
health system to reach the goal of elimination.
While success in malaria control is noted globally,5 including
in Asia Pacific,20 and in Sri Lanka21, the pathway to accelerate
malaria control towards elimination is being seriously
threatened by vector resistance to insecticides and parasite
resistance to drugs. Insecticide resistance is widespread;
globally it is now reported in nearly two thirds of 97 countries
with ongoing malaria transmission. It affects all major vector
species and all classes of insecticides.22 The emergence of
artemisinin resistance in some areas in the Greater Mekong
subregion is a major threat to the progress in malaria control
and elimination.2325 Recently a molecular marker associated
CONCLUSION
Vector-borne diseases are major public-health problems in
the South-East Asia Region. While progress is notable, much
more needs to be done to eliminate lymphatic filariasis,
kala-aazar, schistosomiasis and malaria and to prevent reintroduction of transmission in areas freed from these diseases.
Well-coordinated multisectoral actions as well as active
participation of individuals, families and the communities at
risk are necessary to eliminate these diseases and to contain
the spread of dengue, chikungunya and Japanese encephalitis.
Additional tools, innovative delivery mechanisms, political
will and sustainable financing are essential to achieve universal
coverage to control and, whenever feasible, eliminate vectorborne diseases. World Health Day 2014 is another opportunity
to call for action against vector-borne diseases.
Rajesh Bhatia, Leonard Ortega,
A P Dash, Ahmed Jamsheed Mohamed
Department of Communicable Diseases,
New Delhi, India
Address for correspondence:
Department of Communicable Diseases,
Mahatma Gandhi Marg, New Delhi 110 002, India.
Email: bhatiaraj@who.int
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Gupta I, Chowdhury S. Economic burden of malaria in India: the need
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How to cite this article: Bhatia R, Ortega L,

Dash AP, Mohamed AJ. Vector-borne diseases in South-East
Asia: burdens and key challenges to be addressed. WHO SouthEast Asia J Public Health 2014; 3(1): 24
Perspective
DOI: 10.4103/2224-3151.115828
Expediency of dengue illness classification:

the Sri Lankan perspective
Hasitha Tissera1, Jayantha Weeraman1, Ananda Amarasinghe1,
AnandaWijewickrama2, Paba Palihawadana1, LakKumar Fernando3
Epidemiology Unit, Ministry

of Health, Sri Lanka; 2Infectious
Disease Hospital, Ministry
of Health, Sri Lanka; 3Centre
for Clinical Management of
Dengue/DHF, District General
Hospital Negombo, Ministry
of Health, Sri Lanka
DENGUE CLASSIFICATION
South-East Asia is the region with the highest burden of
dengue,1 and has been in the forefront of the development
of case classification and management.2 Historically, dengue
was considered an incapacitating but largely non-fatal illness.
During the late 1950s, outbreaks of fatal haemorrhagic fever
in children in Thailand and several other South-East Asian
countries changed this perception.3-6 Clinical information
gathered during these early outbreaks was the basis for dengue
clinical classification published in the 1975 World Health
Organization (WHO) guidelines, which were subsequently
updated in 1997.7,8 Dengue illness was classified as two distinct
clinical entities: dengue fever (DF) and dengue haemorrhagic
fever (DHF). In this classification, the main pathophysiological
change differentiating DHF from DF in clinically suspected
febrile patients is evidence of progressive and selective plasma
leakage lasting 2448 hours (the critical period) denoted by
haematological, radiological and clinical evidence in that order
of appearance. It is important to note that this classification
served a dual purpose; surveillance and clinical management.
The guidelines for prevention and control of dengue and
DHF published by the WHO South-East Asia Regional Office
(SEARO) in 2011 further revised the 1997 classification. In
this revised classification, DHF was subdivided into non-shock
and shock replacing Grades I and II and Grades III and IV,
respectively. In addition, unusual manifestations seen among
only a minority of patients with severe organ involvement,
such as liver, kidney, brain or heart (isolated organopathy),
associated with dengue illness were classified as expanded
dengue syndrome or unusual manifestations.9
To address concerns, particularly in clinical settings, regarding
application of the 1997/2011 WHO classification, the WHO
Special Programme for Research and Training in Tropical
Diseases (WHO TDR) classification was proposed in 200910
and apparently further updated in 2012.11 This classification
defines three different levels of clinical dengue illness:
Dengue, Dengue with Warning Signs and Severe Dengue. A
study done in Sri Lanka in 2011,12 which used the 2009 WHO
TDR classification because it was more user friendly, found
that the majority of DF patients had warning signs. This
finding indicates that the warning signs are rather nonspecific.
According to the WHO TDR classification, patients with
warning signs require strict observation; since these patients

Dr Hasitha Tissera, Epidemiology
Unit, Ministry of Health,
231 De Saram Place,
Colombo 01000, Sri Lanka
Email: chepid@sltnet.lk,
dr_korelege@yahoo.co.uk
form the majority, compliance with the WHO TDR guidance

would probably overburden clinical facilities. Furthermore, in
the 2009/12 WHO TDR classification clinical accumulation
of fluid is categorized as a warning sign. However, this
physical sign typically presents late and, by the time it is
clinically detectable, the patient may already have progressed
to impending shock. This predicament has possibly created
confusion among clinical practitioners in many countries
including Sri Lanka. Therefore, we note that the 2009/12 WHO
TDR classification has not given clinicians the anticipated ease
of application for successful case management.
Two perspective articles were published recently, entitled
Dogma in classifying dengue disease,13 and Dengue:
syndromic basis to pathogenesis research, inutility of the 2009
WHO case definition.14 The authors argued over a number
of important issues pertaining to dengue illness classification
faced today. From a clinical standpoint it is essential to make
all efforts to reduce substantially the morbidity, complications
and mortality whatever the classification used. An informal
expert consultation on case management of dengue was held
in August 2013 in Colombo, Sri Lanka organized by the WHO
SEARO with the participation of country representatives
and experts from the region. The overall objective of the
meeting was to appraise the current status of the use of case
classifications in the region. Here, we briefly describe the best
use of these classifications and their challenges in application
in the Sri Lankan perspective.
Tissera et al. : Dengue illness classification in Sri Lanka
THE SRI LANKAN EXPERIENCE

Dengue was first serologically confirmed in Sri Lanka in 1962,
with the first outbreak reported in1965.15 Thereafter, multiple
outbreaks of DF were reported with only occasional reporting
of DHF, a potentially life-threatening condition. DHF was first
reported as a public health problem in Sri Lanka in 1989.16,17
Since early 2000, progressively larger epidemics of dengue
with more cases of DHF have occurred at regular intervals.18
A major upward shift to a high incidence of dengue has been
reported since 2009, with a markedly high DHF proportion of
1015%.19
Classification of dengue illness is important for surveillance
and clinical diagnosis and management. The main objective
of surveillance is to have a sensitive tool to identify possible
dengue cases early for public health intervention. In Sri Lanka,
an integrated surveillance system of communicable diseases
includes dengue and has island-wide coverage through
trained and dedicated clinical and public health staff. National
surveillance data are based on timely, high-yield reports that
capture symptomatic dengue patients classified by use of the
1997/2011 system. The highest-ever total of 44461 dengue
cases (220 cases/100 000 population) was notified in 2012,
approximately a quarter of whom were children younger than
15 years.
Over the past several years a number of activities were initiated
in Sri Lanka to strengthen and standardize early detection and
management of DHF. The key activities were: development
and dissemination of national guidelines; training of all levels
of clinical staff based on these guidelines; institutionalization
of mandatory patient monitoring charts; capacity building by
establishing high-dependency units in major hospitals; and
regular clinical and death audits. Furthermore, two centres of
excellence were recently established to allow closer observation
of children and adults undergoing treatment; hands-on training
for clinical staff; and research.
In Sri Lanka, DHF is reported among all age groups from most
parts of the country. DHF cases are more common in urban
areas with hyperendemic transmission and tend to be younger
than DF patients (Epidemiology Unit, unpublished data). We
encounter two conflicting clinical practice scenarios. Most
practising clinicians actively look for plasma leak among
potential leakers (patients with fever beyond two days with a
platelet count dropping towards and below 100000 mm3) and
provide fluid therapy judiciously, based on the haemodynamic
status of each patient. A minority of clinicians largely depend
on warning signs as predictors of severe disease, diagnose
severity according to clinical end-points and manage cases
accordingly. Most clinicians have realized the importance of
detecting plasma leak that is preceded by a drop in platelet
count around the time of defervescence. This observation has
helped in early differentiation of DHF, thereby minimizing
disease severity and the occurrence of complications needing
adjunctive therapy. Notably, in a minority of patients with no
comorbidities, coinfections or unusual manifestations such
as massive bleeding (without leaking), the case-fatality rate
remains proportionately higher. This high fatality probably
reflects late detection of plasma leakage and therefore delayed

initiation of appropriate fluid therapy. This observation supports
what Scott Hastead 14 has referred to as clinicians having
varying degrees of experience, training and clinical skills that
probably influence the disease outcome. We believe Sri Lanka
has invested wisely to reach the lowest-ever case-fatality rates
of 0.28% in 2013 (from 5% in 1996) against a background of a
very high dengue incidence. In our opinion, lowering mortality
is a clinicians top priority and has been handled effectively in
Sri Lanka in recent years. Despite this success, some clinicians
continue to struggle to classify dengue illness effectively for
case management.
The 1997/2011 WHO classification identifies DF and DHF
as two distinct entities; by contrast, the 2009/12 WHO TDR
classification considers that dengue is one disease entity with
different clinical presentations and often with unpredictable
clinical evolution and outcome.
In all parts of Sri Lanka, dengue illness is now considered as
a differential diagnosis in patients presenting with acute onset
of fever with or without classical features of dengue. When
there is a mandatory complete blood count done on day 3 of
illness onwards, the appearance of leukopenia and subsequent
thrombocytopenia aids the diagnosis.20,21 Among other criteria,
warning signs of severe illness10 are considered when admitting
patients to hospital from day 3 onwards. The relation between
the drop in platelet count towards and below 100000 mm3 with
concurrent and consistent haemoconcentration evidenced by a
rapid rise in haematocrit towards 20% from the baseline appears
to be unique to DHF and helps to distinguish DHF from DF
and other acute febrile illnesses.2 This is the major advantage of
the 1997/2011 WHO classification, which has helped to guide
clinicians to manage patients without allowing complications
of severe dengue to arise, making DHF a predictably treatable
illness. Furthermore, it is noteworthy that a substantial
proportion of patients who develop potentially severe features
do not show any of the warning signs described in 2009/12
WHO TDR classification during the febrile phase.
Heavy reliance on warning signs in anticipation of worsening
clinical status without a proper monitoring regime has
repeatedly been found to result in unwarranted consequences.
As rightfully mentioned by Halstead, not all patients as well
as treatment centres do equally well. Having reviewed the
1237 dengue-related deaths reported over the past decade in
Sri Lanka, we are yet to find many cases where the primary
cause of death was not related to prolonged and repeated
shocks as a consequence of delayed and inappropriate
treatment or fluid overload due to over treatment with
intravenous fluids without proper monitoring (Epidemiology
Unit, unpublished reports). We have observed that the 2009/12
WHO TDR classification provides severity-based end-points
(whether natural or iatrogenic) and enables better classification
of clinically severe cases. The progressive nature of plasma
leak in DHF warrants close clinical and laboratory evaluations
and proactive action.2,9,22 Therefore, we reiterate that the main
challenge for clinicians is timely decision-making to guide
management to handle the fluctuating spectrum of clinical
syndrome using the classifications appropriately.
Tissera et al. : Dengue illness classification in Sri Lanka
The intention of this Perspective was not to do an exhaustive

comparison of the two classifications. No doubt, in terms
of surveillance as well as diagnosis and management both
classifications have their own advantages and disadvantages.
Both classifications were born and do exist under the auspices
of the WHO. However, countries with limited logistics and
human resources struggle to identify what is best for their own
use. It is now time to create a formal platform for both groups
to sit around one table together with representatives from
countries and develop a common guideline classifying dengue
illness best applicable to all. Validation of these classifications
as a tool for clinical management should be focused to study
the impact of their use in changing the course of the disease
and its related outcome.
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How to cite this article: Tissera H, Weeraman J,

AmarasingheA, Wijewickrama A, Palihawadana P, Fernando
L. Expediency of dengue illness classification: the Sri Lankan
perspective. WHO South-East Asia J Public Health 2014; 3(1):
57.
Source of Support: Nil. Conflict of Interest: None declared.
Contributorship: All authors have contributed to this paper and have read
and approved the final version submitted.
Review
DOI: 10.4103/2224-3151.115828
Highly infectious tick-borne viral diseases:

Kyasanur forest disease and Crimean
Congo haemorrhagic fever in India
Devendra T Mourya, Pragya D Yadav, Deepak Y Patil
Abstract
Ticks are distributed worldwide and can harbour and transmit a range of pathogenic
microorganisms that affect livestock and humans. Most tick-borne diseases are
caused by tick-borne viruses. Two major tick-borne virus zoonotic diseases,
Kyasanur forest disease (KFD) and CrimeanCongo haemorrhagic fever (CCHF),
are notifiable in India and are associated with high mortality rates. KFD virus was
first identified in 1957 in Karnataka state; the tick Haemaphysalis spinigera is the
main vector. During 20122013, cases were reported from previously unaffected
areas in Karnataka, and newer areas of Kerala and Tamil Nadu states. These
reports may be the result of improved active surveillance or may reflect altered
virus transmission because of environmental change. CCHF is distributed in Asia,
Africa and some part of Europe; Hyalomma spp. ticks are the main vectors. The
existence of CCHF in India was first confirmed in 2011 in Gujarat state. In 2013, a
non-nosocomial CCHF outbreak in Amreli district, as well as positive tick, animal
and human samples in various areas of Gujarat state, suggested that the virus is
widespread in Gujarat state, India. The emergence of KFD and CCHF in various
Indian states emphasizes the need for nationwide surveillance among animals
and humans. There is a need for improved diagnostic facilities, more containment
laboratories, better public awareness, and implementation of thorough tick control
in affected areas during epidemics.
Maximum Containment Laboratory,

Microbial Containment Complex,
National Institute of Virology,
Pune, Maharashtra, India
Dr DT Mourya, Director, National
Institute of Virology, 20-A,
Ambedkar Road, Pune-411001,
India
Email: directorniv@gmail.com
Key words: CrimeanCongo haemorrhagic fever, India, Kyasanur forest disease,

tick-borne diseases, ticks
Introduction
Globally, ticks are the important arthropod vectors for
transmission of numerous infectious agents and are responsible
for causing human and animal diseases.1 Various wild and
domestic animals are reservoir hosts for tick-borne pathogens
of livestock, pets and humans.2 Ticks are obligatory bloodsucking ectoparasites that infest mammals, birds, reptiles and
amphibians.3 Eighty per cent of the worlds tick fauna are hard
ticks and the remaining 20% are soft ticks. However, only 10%
of the total hard and soft tick species are known to be involved
in disease transmission to domestic animals and humans.3 Ticks
suck host blood during their lengthy attachment period (714
days); this may extend, depending on the association of the tick
species and host.3 Tick-borne diseases are prevalent only in
specific risk areas where favourable environmental conditions
exist for individual tick species.3 Worldwide increases in the
incidence of tick-borne diseases have been reported.4,5 Human

tick-borne diseases have been recognized since the discovery
of Lyme borreliosis, which is transmitted by Ixodid ticks.6
Rocky Mountain spotted fever, caused by Rickettsia rickettsia,
is transmitted by Dermacentor spp. in the United States of
America (USA). There are several other rickettsial infections
like rickettsioses and Boutonneuse fever (caused by Rickettsia
conorii found in Europe), transmitted by Rhipicephalus
sanguineus and other tick species. Generally, tick-borne
viral diseases manifest three different clinical conditions:
encephalitis, haemorrhagic fevers, and acute febrile illness.
Among viral infections, European tick-borne encephalitis and
the severe Russian springsummer encephalitis are transmitted
by Ixodid spp.7,8
Hyalomma anatolicum anatolicum and Haemaphysalis
spinigera are the two important species of ticks present in
India, which are responsible for causing the fatal tick-borne
Mourya et al.: Tick-borne viral diseases in India
Figure 1: The distribution of predominant Hyalomma anatolicum anatolicum and Haemaphysalis spinigera tick species of ruminants in India.
Table 1: Association of virus isolation from ticks (Hyalomma and Haemophysalis) and arboviral zoonotic diseases
(KFDV and CCHFV) of India
Virus name
Family/Genus
Tick species
CCHFV
Bunyaviridae/
Nairovirus
Hyalomma
marginatum; isolated
from many Ixodid
spp.
KFDV
Flaviviridae/
Flavivirus/
Haemaphysalis
spinigera; many
other Ixodid spp.
Natural vertebrate
Geographical
host
distribution in India
Hare
Gujarat, India
monkeys
(Semnopithecus
entellus, Macaca
radiata), rodents,
shrews, bats
viral diseases of CrimeanCongo hemorrhagic fever (CCHF)

and Kyasanur forest disease (KFD), respectively.9,10 The tick
species are widely distributed in different parts of world,
including India (see Figure 1 and Table 1).11,12
The highly infectious nature of KFD and CCHF causes
sporadic outbreaks among humans. These viruses have
Karnataka, India
First isolation in India

2011: Hyalomma
anatolicum pool of ticks
collected from domestic
animals from Gujarat
state, India
1957: langur monkey
(Semnopithecus entellus)
moribund adult organs
and tissues, 27/03/1957;
Kyasanur Forest near
Baragi village, India
emerged in comparatively new areas, revealing gaps in

many areas in understanding these diseases.13,14 This paper
focuses particularly on the Indian scenario of KFD and
CCHF infections, clinical and epidemiological features of the
diseases, active surveillance programmes among humans and
animals, the role of ticks as vectors, and current policies for
management of their control and for raising public awareness.
Highly infectious tick-borne

viral diseases in India
1.
Kyasanur forest disease
The KFD virus (KFCV) is a member of the genus Flavivirus

and family Flaviviridae. It was first recognized in 1957, when
an illness occurred concomitantly in monkeys (Semnopithecus
entellus and Macaca radiata) and in humans.15 The virus was
initially suspected as a Russian springsummer (RSS) complex
of viruses, since isolates from monkeys and human showed
relatedness to this virus.16
Mode of transmission of KFD virus
KFDV is transmitted to the wild monkeys Semnopithecus
entellus and Macaca radiate, through the bites of infected
H.spinigera ticks.17 After infection, KFDV is transmitted to
other ticks feeding on the infected animals. Infection causes
severe febrile illness in some monkeys. When infected
monkeys die, the ticks drop from their body, thereby generating
hotspots of infectious ticks that further spread the virus (Table
1). The genus Haemaphysalis includes 177 species. The ticks
are small (unfed adults <4.5 mm long), brownish or reddish,
and eyeless, and have very short mouthparts. They are easy
to differentiate from other genera by the characteristic lateral
projection of a palpal article 2 beyond the margins of the
basis capituli. All Haemaphysalis spp. are three-host ticks.
H. spinigera is the main vector of KFD, which is endemic
in Karnataka state, India.11 A large number of isolations have
been obtained from ticks, and H. spinigera contributed about
95% of these isolations. This is the predominant tick species
found in the forest. Among other susceptible species of
Haemaphysalis, in addition to H. spinigera, are H. turturis, H.
papuana kinneari, H. minuta, H. cuspidata, H. bispinosa, H.
kyasanurensis, H. wellingtoni and H. aculeate. Transmission
of KFDV in the laboratory has been demonstrated in a number
of Haemaphysalis and Ixodes species.1827
Humans become infected through the bite of infected unfed
nymphs, which appear to be more anthropophilic than mature
ticks.28 Ticks have also been found to transmit this virus
transstadially, thus also acting as a reservoir for the virus. In
Karnataka state, the activity of nymphs is very high during
November to May, correlating with a higher transmission rate
of KFD at this time of year. Adult fed female ticks lay eggs,
which hatch to larvae under the leaves. They further infest
small mammals and monkeys, as well as accidentally infesting
humans, and feed on their hosts. Subsequently, they mature
to nymphs, and the cycle is repeated. Nymphs and adults also
transmit the disease to rodents and rabbits by bite, and this
rodenttick cycle continues for more than one life-cycle.29
The finding that immature stages of H. spinigera infest a variety
of hosts, such as birds, monkeys, rodents, cattle and buffaloes,
and that these hosts are highly susceptible to the virus, suggests
that this species of tick might indeed be an important vector for
the disease.18,29
Although human-to-human transmission is not known, more
than 100 human cases have been reported in the past while
working on the virus. During a recent outbreak of KFD (2013)
10
in Bandipur Tiger Reserve forest, it was found that animal

handlers became infected while handling sick monkeys.10
Owing to the large number of KFD laboratory-associated
infections at the National Institute of Virology (NIV), Pune,
work on this virus was stopped for 30 years; however NIV
started working on the virus again after establishment of a
Biosafety Level-3 (BSL-3) laboratory.29
Geographical distribution of KFD virus in
India and its detection in newer areas
After the discovery of KFD, it was mainly confined to three
taluks (Sagar, Shikaripur and Sorab) of the Shimoga district of
Karnataka, until 1972. Thereafter, foci were reported from four
additional areas, namely Chikmagalur, Dakshina Kannada,
Udipi and Uttar Kanada districts of Karnataka state.30 For a long
time, KFD was thought to be endemic in the Shimoga district.
However, serological evidence obtained in the past during
different studies, suggests that KFD virus or related viruses
are present in other areas of India, which include parts of the
the Saurashtra region in Gujarat state, forested regions west of
Kolkata, West Bengal state, and the Andaman Islands.31,32
Since 1957, the estimated incidence of KFD in India has
been 400500 cases per year. The epidemic period begins in
November or December and peaks from January to April, then
declines by May and June.33 Between 2003 and March 2012,
there were 3263 reported human cases and, of these, 823 were
laboratory confirmed. Large numbers of human infections were
reported in 20032004, but a significant decline occurred in
2007 and again in 20102011.10,33 The frequency of cases can
be correlated with the number of confirmed KFD-infected nonhuman primates. As far as spread in new areas is concerned, an
outbreak of KFD was reported for the first time in December
2012 in Chamrajanagar district of Karnataka.10 In 2013, KFDV
was detected in autopsy of dead monkeys in Nilgiris District,
Tamil Nadu and in a human case from Wayanad district, Kerala
(Figure 2).10 Already in 2014, an outbreak of KFD has been
confirmed by screening human samples, monkey necropsy
samples and tick pools from the Kannangi and Konandur areas
in Thirthahalli taluk. Data indicate that, this year, the main
focus activity was in Shimoga District (NIV unpublished data).
In earlier years, the geographic area affected was small and the
number of cases was relatively low, while, with the increase
in the number of foci, the incidence has increased. These facts
suggest that constant changes in the ecobiology, including
deforestation and new land-use practices for farming and
timber harvesting, might have led to the spread of this disease
to newer localities.
Phylogenetic relation and ancestry of KFD virus in India
The positive-sense RNA genome of the KFDV is about 11kb
in length and encodes a single polyprotein that is cleaved posttranslationally into three structural (C, M and E) and seven
non-structural (NS1, NS2a, NS2b, NS3, NS4a, NS4b and
NS5) proteins. Evolutionary studies undertaken earlier for
KFDV, based on Bayesian molecular clock analysis (partial
E and NS5 gene sequences of ~50 KFD viruses), revealed a
rate of evolution of ~6.4104 substitutions/site/year with
Figure 2: Pictorial presentation of KFD activity in Karnataka, Kerala and Tamil Nadu and CCHF positivity in Gujarat State.
the divergence of KFDV estimated to have occurred 62 years

ago.34 However, a recent study based on analysis of full-length
sequences (KFDV n =3 and Alkhurma haemorrhagic fever
virus n=18 a variant of KFDV in Saudi Arabia) revealed
a slower rate of evolution (9.2105 substitutions/site/year)
and a much older ancestry of KFDV.34,35 Though the number
of KFDV isolates that were available at the time of the
study was limited, it appears that the analysis of full-length
genomes might have provided a more accurate estimate of
an older ancestry and also suggests that the evolution of tickborne viruses was more gradual than that of rapidly evolving
mosquito-borne viruses.35 Phylogeography studies for KFDV
are also important to genetically characterize the recently
circulating KFDVs and understand the dispersal pattern of the
virus within Karnataka and to newer geographical areas.
Clinical signs and symptoms
In humans, the incubation period of KFD is estimated to
be about 2 to 7 days after tick bites or exposure. The onset
is sudden, with chills followed by severe frontal headache.
Fever soon follows headache and rapidly rises to 104F. This
raised temperature is continuous and lasts for 512 days, or
even longer. There is severe myalgia, which is reminiscent of

dengue. Body pains are of high intensity at the nape of the neck,
lumbar region and calf muscles. Diarrhoea and vomiting occur
by the third or fourth day of illness. Bleeding from the nose,
gums and intestines begins as early as the third day, but the
majority of cases run a full course without any haemorrhagic
symptoms. Gastrointestinal bleeding is evidenced by
haematemesis or fresh blood in the stools. Some patients have
persistent cough, with blood-tinged sputum and occasionally
substantial haemoptysis. Physical examinations during the first
few days of illness reveal an acutely ill, febrile patient with
a severe degree of prostration. There is usually conjunctival
suffusion and photophobia. The cervical lymph nodes are
usually palpable, as are the axillary epitrochlear lymph nodes
in some cases. A very constant feature is the appearance of
papulovesicular lesions on the soft palate, but no skin eruption
has been noted. The convalescent phase of the disease is
prolonged. Often, the disease runs a biphasic course; the second
phase occurs after a febrile period of 1 to 2 weeks. The fever
lasts from 2 to 12 days (Table 2). It is initiated by headache and
by this time abnormalities of the central nervous system are
generally present. Neck stiffness, mental disturbance, coarse
tremors, giddiness, and abnormality of reflexes are noted.29,30
11

Table 2: Clinical phases of Kyasanur forest disease virus and Crimean-Congo hemorrhagic fever virus infection and
tests used for diagnosis.
Disease
KFD
CCHF
Phase of
illness
Acute phase
Post onset
days
27 days
Convalescent
phase
812 days
Acute phase
17 days
Convalescent
phase
712 days
months can
extend up to
4 month
Diagnostic test
IgM ELISA, Virus
isolation (In vitro and
In vivo), RT-PCR and
Real-Time RT-PCR
IgM ELISA
RT-PCR and RealTime RT-PCR (1 to
10 days), IgM ELISA
(4 days-4 months),
Virus isolation (In
vitro): 1 to 7 days
IgM ELISA, IgG
ELISA (7 days
onwards)
Clinically, KFD resembles Omsk hemorrhagic fever (OHF),

which occurs in the Omsk Oblast in Siberia. The other tickborne viral disease antigenically related to KFD and OHF is
tick-borne encephalitis.29
Case definition
Owing to the variability in clinical illness associated with KFD
infection, and the lack of data available on clinical diagnosis of
KFD, it is essential to emphasize the importance of laboratory
confirmation of the disease. The following case definitions are
proposed:
Case definition: a patient of any age presenting with acute
fever, headache and myalgia, and a history of exposure to ticks
and/or a visit to a forest area and/or living in, a KFD-endemic
area, particularly forest in Karnataka.33
Suspected case: a patient, within a radius of 5 km surrounding
the villages reporting recent monkey deaths or laboratoryconfirmed KFD cases, with sudden onset of high fever and one
of headache or myalgia.33
Probable case: a clinically compatible illness that does not
meet the SOPs for a confirmed definition, but with one of the
following:
epidemiological link to a documented exposure to a KFDaffected area (one or more of the following exposures
within the 3 weeks before onset of symptoms);
positive result on testing of clinical serum specimens
using the immunoglobulin M (IgM) enzyme-linked
immunosorbent assay (ELISA).
Confirmed case: a confirmed case of KFD is defined as a case
that fulfils the criteria for a probable KFD case and, in addition,
it should cover any of the following:
exposure to secretions from a confirmed acute or
convalescent case of viral haemorrhagic fever (VHF)
within 10 days of that persons onset of symptoms;
12
Disease signs and

Symptoms
Fever, cephalalgia,
myalgia, diarrhea,
cough, hepatomegaly,
splenomegaly, epistaxis,
bradycardia, oral and
intestinal hemorrhage,
meningoencephalitis
Fever, myalgia,
arthralgia, dizziness,
malaise, mucosal
hemorrhage, hemorrhagic
rash, multi-organ
failure, disseminated
intravascular
coagulopathy
Hematologic
Case
changes
fatality
Leukopenia,
210%
thrombocytopenia,
neutropenia,
eosinopenia, elevated
liver enzymes
Leukocytopenia,
360%
thrombocytopenia,
increase clotting
times, increased
pro-inflammatory
cytokines/
chemokines, elevated
liver enzymes
isolation of KFDV in cell culture or in a mouse model,

from blood or tissues;
detection of KFDV-specific genetic sequence by reverse
transcription-polymerase chain reaction (RT-PCR) or realtime RT-PCR from blood or tissues.
Diagnosis
In the KFD-endemic area of Karnataka state, India, the
differential diagnosis should include consideration of
influenza, typhoid and rickettsial group of fevers, for example,
Q fever and mite-borne typhus in mild cases, and malaria and
leptospirosis in moderate to severe cases.
Hospital laboratory testing: The following tests should be
performed on blood samples from enrolled patients, according
to standard hospital procedures:
complete blood count (CBC): total leukocytic count (TLC)/
differential leukocytic count (DLC), haemoglobin level,
and platelet counts;
liver function tests (aspartate aminotransferase (AST)/
alanine aminotransferase (ALT), serum bilirubin, alkaline
phosphatase);
serum electrolytes, blood urea, serum creatinine;
smear for malaria parasite or malaria rapid diagnostic test.
Standardized, detailed SOPs should be provided to each of the
hospital wards and laboratories, to ensure proper collection of
each of the specimens. Personal protective equipment should be
used by the collecting technician or care provider in all cases.
Blood samples should be collected from the hand or antecubital
fossa by the treating physician, by venipuncture with an aseptic
techniquee. For surveillance purposes, this should be done on
two separate occasions initially at the time of enrolment/
admission, and then 10 days after initial specimen collection or
at the time of discharge from the hospital (if less than 10 days).
In cases of fatality, the second specimen should be collected at
the time of death.
Diagnostic laboratory testing: For a long period, there were

no studies done on KFD; hence, hemagglutination inhibition
(HI), hemagglutination (HA), complement fixation and in vivo
inoculation of patients sera into suckling mice were the tests
of choice for diagnosis. During KFDV infection, the level of
viraemia reaches up to 3106 within 36 days and remains
high for as long as 1014 days of infection.7 Therefore, the
period of higher viraemia coincides with the time at which
patients usually report to hospital and collection of a blood
sample for laboratory diagnosis. Therefore, an early and
effective diagnosis strategy is essential.
After establishment of the first BSL-3 laboratory of India
at NIV,Pune, real-time RT-PCR, RT-PCR and detection
of IgM and IgG antibodies by ELISA were developed and
standardized.36 KFDV can be isolated from the blood of
patients (in acute phase 25 days), positive tick pools, or the
blood or viscera of monkeys by inoculation into infant mice, or
in vitro using Vero E6, BHK-21 or chick embryo cells. In all
these systems, infant mice are found to be the most susceptible
for virus isolation. KFD anti-IgM antibodies can be detected
using ELISA during the acute phase (4 days onward) (see
Table2).29 The front-line test for KFD is real-time RT-PCR
and RT-PCR from blood/serum of humans, blood and viscera
of infected monkeys, or tissues of ticks.36 According to what
is known, real-time RT-PCR can detect the virus in human
samples after onset of febrile illness up to the 10th day (NIV
data). Clear information about the KFD viraemia phase, the
interrelationship of IgM and IgG antibodies, and the duration
of persistence of these antibodies in naturally infected patients
remains to be understood (Table 2). Suspected samples
should be shipped according to international regulations for
the shipment of infectious agents, following triple container
criteria.37
Treatment
No specific treatment for KFD is available; however, supportive
therapy is important. This includes maintenance of hydration
and the usual precautions for patients with bleeding disorders.
Guidelines for management of KFD cases
In recent years, state public health agencies in the affected
districts have made efforts to ensure adequate staff and
infrastructure at primary health-care (PHC) and secondarylevel health facilities, to provide health care to critically ill
patients, undertake training of staff, and minimize the frequency
of transfer of trained staff. The role and responsibilities of
health-care providers at different levels of health facilities
are explained, and medical officers are trained to identify the
suspected KFD cases. Government has made provision for
well-equipped ambulances for transfer of critically ill patients
from community to PHC or from PHC to secondary health-care
facilities. For better organization of the health-care-delivery
system, mapping of primary, secondary and tertiary care health
facilities in high-risk areas has been made available. KFD cases
are recorded annually, thereby monitoring the annual disease
burden at all the health facilities, for better understanding
and preparedness for KFD disease. Continuous information,

education and communication activities with regard to early
recognition of suspected KFD cases are carried out among
newly recruited medical officers and other relevant populations.
State government educates the villagers and tourists who visit
the forest in Karnataka state about using repellent and gum
boots and having prior vaccination. Whenever monkey deaths
are reported, rapid action is taken to transmit information to
health officers and veterinary staff for necropsy of monkeys,
collection of specimens for diagnosis of monkey samples, and
proper disposal of dead monkeys. If a monkey is found positive
for KFDV, vaccination of human subjects should be carried out
in those areas. Education has been provided in local languages
every year. As soon as suspected cases are notified they are
referred to NIV, Pune for investigation and confirmation.
Improper storage of vaccine and lack of maintenance of the
cold chain result in ineffectiveness of the vaccine and could
be another reason for the emergence of KFD despite routine
vaccination. The trend of increasing numbers of patients
infected with KFD in Karnataka state warrants development
of a new vaccine either recombinant, or a virus-like-particlebased vaccine which will help in controlling the disease.33
Prevention
The formalin-inactivated KFDV vaccine produced in chick
embryo fibroblasts is currently in use in the endemic areas
in Karnataka state of India.38 The vaccine was found to be
immunogenic, potent, stable and safe. The production of
inactivated vaccines carries the inherent risk of utilizing large
quantities of potentially highly pathogenic viruses and the
possibility of incomplete inactivation of viruses. In addition,
vaccines based on inactivated viruses as antigens have shown
a certain level of adverse reactions, especially in children,
and this has to be carefully balanced with their efficacy and
durability.38
Control
Infected nymphs and larvae are shed in the forest, mainly by
the monkeys, rats, shrews, porcupines, squirrels, and probably
a few birds that form enzootic foci. Destruction of infected
ticks would necessitate control of ticks throughout the entire
forested area, but is not technically and economically feasible.
This is the main reason why, once focus of this disease becomes
established in any biotope, it cannot be eliminated easily.
As association of human infections in the vicinity of dead
monkeys has been shown, and the use of spray insecticides has
been recommended in a 50-m radius around a dead monkey.
However, although recommendations have been made for
spraying of insecticides around the place of monkey death, it
is technically difficult in certain inaccessible areas to transport
the large volumes of water needed for the spray. Economic and
logistical problems associated with regular insecticide spray
in a large area makes implementation of a control programme
difficult. Under these circumstances, the prevention of tick
bites by the use of repellents should be considered.29
13
2.
CrimeanCongo haemorrhagic fever
The CrimeanCongo haemorrhagic fever virus (CCHFV) is

also considered as an important zoonotic virus, owing to its
wide distribution and ability to cause disease in humans, where
it causes a high mortality rate. Secondly, it has the potential
to cause nosocomial cases/outbreaks. CCHF was recognized
for the first time in 1944, in the West Crimean region of the
former Soviet Union, during a large outbreak, and the virus
was subsequently isolated in 1956 from a human case.3942 It is
a member of the genus Nairovirus of the family Bunyaviridae.
The average case-fatality rate is 3050%; this varies between
5% and 80 % in various outbreaks, as reported earlier.43
Mode of transmission of CCHF virus
Humans become infected through tick bites, by contact with
a CCHF-infected patient during the acute phase of infection,
or by contact with secretions, blood or tissues from viraemic
livestock.44 Risk groups include individuals who are exposed
to ticks (mainly farmers, shepherds and veterinarians), and
persons who come in close contact with CCHF patients.
Thus, in hospital settings, family or nosocomial outbreaks are
observed. Observation of CCHF transmission in India during
the year 2011 showed it was mainly nosocomial, and started
with an index case history of tick bites and close contact with
animals.44 During June 2012, another episode of nosocomial
infections recorded from Ahmadabad city resulted in two
fatalaties.9 The history of exposure revealed that the treating
physician had an accidental contact with the patient (the index
case, resident of Bawla Taluka, Ahmadabad), who had similar
symptoms of haemorrhagic fever and had died a week earlier.
During the CCHF outbreak of 2013 in Karyana village, Amreli
district, the main reason for transmission of virus was infected
Hyalomma ticks infested on domestic animals. Once a human
was infected, the disease was transferred to other close family
relatives who either accompanied the infected individual to
hospital, lived in the same house, attended the funeral of a
person who had died due to CCHF, or came in contact with
infected body fluids.9
CCHFV circulates in nature in the enzootic tickvertebrate
tick cycle.45 Ticks of the Hyalomma genus have been reported
to be associated with the incidence of the disease and found to
play a key role in transmission of CCHFV to mammals.4650 The
CCHF cases coincide with the life-cycle of Hyalomma ticks,
and infection mainly occurs during the period when immature
ticks are active. High tick activity is associated with warm
winters and hot summers. The predominance of tick species
as vectors of CCHFV differs geographically and includes
H. anatolicum subspecies (H. anatolicum anatolicum), which
are distributed throughout Eurasia, while in the northern
half of Africa H. marginatum subspecies (H. marginatum
marginatum, H. marginatum rufipes, H. marginatum turanicum
and H. marginatum isaaci) predominate. Hyalomma species
of ticks are medium to large sized, with long hypostomes and
eyes located in sockets. They are mainly found in semi-arid
zones, and infest domestic and wild mammals as well as birds.
Of the 25 known Hyalomma spp., 15 are important vectors of
infectious agents of veterinary and public health importance.51
Among these, Hyalomma anatolicum anatolicum is important,
14
and this species has wide distribution in India.52 Nymphs and

unfed adults remain hidden in the dry and winter season in
crevices in stone walls, stables and weedy or fallow fields. The
life-cycle involves three hosts. This is medically important,
since, during the developmental cycle, ticks infest a variety
of hosts smaller to larger mammals, birds or reptiles. They
effectively withstand diverse habitats ranging from warm,
arid and semi-arid, harsh lowland, and long dry seasons.51 H.
anatolicum anatolicum is known to transmit virus to humans.53
CCHFV has a wide host range and can cause a transient
viraemia in many wild, domesticated and laboratory mammals;
antibodies against CCHFV have been detected in the sera of
variety of animals.44,5456 Viraemia does not develop in birds;
however, migratory species could carry infected ticks and play
a role in disseminating the virus over long distances.57
Geographical distribution of CCHF virus in India
CCHF is transmitted to humans and animals by the bite of
Ixodid ticks, mainly those of the Hyalomma genus. Thus,
the geographic distribution of CCHF is closely related to the
global distribution of Hyalomma spp. ticks. CCHFV has been
reported in over 30 countries covering Africa, South-Eastern
Europe, the Middle East and Western Asia.5865
India has always been considered at high risk for CCHF,
owing to its borders with affected countries such as China and
Pakistan. Because of the long association of India with these
adjoining countries and the possible trade of animals across
the border, the risk of CCHFV being passed to the Indian
subcontinent was recognized. The virus was first isolated from
ticks in Pakistan in the 1960s and the first reported human case
occurred in Rawalpindi in 1976.66,67 Since then, many sporadic
outbreaks have occurred in Pakistan every year, resulting in
high case fatality.68,69 In March 1998, an outbreak with 19
cases and 12 deaths (case-fatality rate 63.2%) was reported
from Takhar Province in the northern part of Afghanistan.70
Since this episode, Afghanistan has seen many outbreaks of
CCHF in subsequent years.71 In Iran, CCHF was first isolated
in 1978 and the disease re-emerged in 1999, with high case
fatality.72,73 In China, CCHF was first isolated in 1965 from a
human case and later, in 1984, from H. asiaticum ticks from
the same region of Xinjiang province in north-western China,
which is considered to be the most CCHF-affected area in the
country.74,75
Until 2011, the existence of CCHF was not known in India,
apart from some serological evidence recorded in the past.76
Serological evidence of the presence of CCHF in India was
reported by screening for HI antibodies in animal sera from
Jammu and Kashmir, the western border districts, southern
regions and Maharashtra state.76,77 Shanmugam et al. had
reported the presence, in 1973, of CCHFV-specific antibody
in nine human samples from Kerala and Pondicherry and
in goats from South India.77 All these studies were based on
serological findings only; no virus isolation could be achieved
and hence no clear evidence of this virus could be obtained.
During December 2010, just prior to the CCHF outbreak, blood
samples were collected by NIV, Pune, to examine livestock
from abattoirs in the northern adjoining state of Rajasthan
and some more distant areas of Maharashtra and West Bengal

states, for the presence of CCHFV-specific IgG antibodies.
Serum samples of buffalo, goat and sheep from Sirohi district,
in southern Rajasthan, were found to be positive for IgG
antibodies against CCHFV.44
The presence of CCHF disease was confirmed for the first
time in India during a nosocomial outbreak, in Ahmadabad
district, Gujarat state.44 Samples from three suspected cases,
83 contacts, Hyalomma ticks and livestock were screened for
CCHFV by real-time RT-PCR; of these, samples from two
medical professionals and the husband of an index case were
positive for CCHFV. About 17.0% of domestic animals from
Kolat, Ahmadabad were positive for IgG antibodies, while only
two cattle and a goat showed positivity by real-time RT-PCR.
Surprisingly, in the adjoining village of Jivanpara, 43.0% of
domestic animals (buffalo, cattle, sheep and goats) showed IgG
antibodies but only one of the buffalo was positive for CCHFV.
The H. anatolicum anatolicum ticks were positive by PCR and
virus isolation. Retrospective screening of suspected human
samples revealed that the virus was present in Gujarat state,
during the year 2010, earlier than this outbreak (see Figure 2).44
After its confirmation in India, sporadic cases of CCHF were
reported in 20112012.78 During the period of 23 June to 25
July 2013, a cluster of suspected VHF cases were reported in
Karyana village, Amreli district and, simultaneously, sporadic
cases were recorded from Surendra Nagar, Patan district and
Kutch district, Gujarat state.9 Owing to high alertness over
2 months, a total of 198 human samples were processed by
real-time RT- PCR and 19 samples were found to be positive for
CCHFV. Human suspected cases from Amreli, Kutch, Patan,
Rajkot and Surendranagar were found to be positive for CCHF
viral RNA. IgG antibody positivity was recorded in animals
from Karyana, Nilwada and Khambhala village from Amreli
distrct and Kundal village, Ahmadabad district. Surveillance
of anti-CCHF IgG in domestic animals showed a number of
animals from 15 districts that were positive (see Figure 3)
(NIV, unpublished data). This emphasizes the necessity of
continuous monitoring and screening of syndrome-based cases
for CCHF.
Figure 3: Pictorial presentation of different outbreaks and spread of CCHF in Gujarat State.
15
Ancestry of CCHF virus in India

Sequence-based molecular characterization of the Indian
CCHFV has shown that the virus possesses the functional
motifs known to occur in the S, M and L gene segment products,
as in other CCHF viruses. The complete genome was found
to be 19.2 kb in length. The CCHFV strains cluster into 67
distinct groups; West-Africa in group I, Central Africa in group
II, South-Africa and West Africa in group III, Middle-East and
Asia in group IV, Europe in group V and Greece in group VI.
Group IV may split into two distinct groups, Asia 1 and Asia 2.
The S segment of the six Indian CCHFVs showed 99.8%
nucleotide identity. Notably, both tick isolates shared 100%
nucleotide identity with one of the Indian human isolates
of 2011. Phylogenetic analysis based on the S segment
demonstrated that the Indian CCHFV isolates formed a distinct
cluster in the AsianMiddle East group IV of CCHF viruses.
The S segment was closest to a Tajikistan strain TADJ/HU8966
of 1990 (98.5% nucleotide identity) and was of South-Asia 2
type, while the M segment was of type M2. Both M and L
segments were closest to an Afghanistan strain Afg09-2990
of 2009 (93% and 98% nucleotide identity) respectively.
Complete genome analysis of Indian CCHFV isolates not only
revealed high genetic diversity but also showed recombination
and reassortment, which resulted in more complicated
evolutionary routes of the virus than mutation-based selective
forces.7983 The molecular clock of Indian isolates has revealed
the ancestry of these viruses is not very recent and dates back
to about 33 years, on the basis of the S segment, whereas it is
about 15 years based on the M segment.84
Clinical signs and symptoms
The initial nonspecific symptoms of CCHF can mimic other
common infections that occur in India, which may lead to
misdiagnosis. The delay of proper treatment and precautionary
measures may result in outbreaks, including nosocomial
outbreaks of this high-risk group of viruses.13,14,52 In India, this
disease needs to be differentiated from other infections such
as dengue, leptospirosis, rickettsiosis, brucellosis, Q fever and
other haemorrhagic fevers. Patient history is very informative,
especially when tick bite or travel to currently known endemic
areas in Gujarat is evident.
The clinical signs and symptoms are observed between 1 and
3 days (maximum 9 days) after a tick bite; however, when
infection is contracted from direct contact with viraemic
livestock or CCHF patients, these signs and symptoms may be
seen from 5 to 6 days later (maximum 13 days). They include
abrupt high fever, severe headache, malaise, nausea, vomiting,
diarrhoea and sore throat. Typically, the disease follows a fourphase course: incubation, pre-haemorrhagic and haemorrhagic
phases, and convalescence.13,14 Laboratory investigations
during the first 5 days of the CCHF disease mostly show
leukopenia, thrombocytopenia, elevated liver enzymes and
prolonged blood coagulation times. In most cases, platelets
20109/L or less, AST 700U/L or more, ALT 900 U/L or
more, partial thromboplastin time 60s or more, and fibrinogen
110 mg/dL or less are suggestive of a fatal outcome.43,44 High
viral load is also associated with a fatal outcome.85 In severe
16
cases, approximately 5 to 7 days after the onset of the

disease, haemorrhagic manifestations are observed mainly
petechiae, epistaxis, haematomas and vaginal bleeding. Death
usually occurs between 5 and 7 day of illness, while survivors
show progressive improvement (see Table 2). The disease
is milder in children and in secondary or tertiary cases.43,44
Haemophagocytosis is also one of the consistent features in
many cases; however, increased serum ferritin levels caused by
haemophagocytosis is also one of the consistent features related
to the severity of disease. The average period of incubation is
around a week. The first phase includes a few days of fever,
tiredness, headache and muscle pain, followed by a long
asymptomatic period. After that phase, the first signs that the
central nervous system has been compromised start appearing,
including meningitis, encephalitis and myelitis, which can
lead to neurological sequelae and, in a few cases, even death.
Information on the time of appearance of symptom of VHF has
varied, ranging between 1 and 21 days after exposure to the
virus. Symptoms also depend on the viral species involved and
may include fever, tiredness, dizziness, muscle pain, weakness
and exhaustion. In more serious cases, there is bleeding under
the skin or in internal organs, or bleeding out of the mouth,
eyes, ears and vagina. Patients with serious illness can show
signs of shock or coma, involving neurological symptoms like
delirium and convulsions.43,44
After a tick bite, the incubation period is of short duration
(37 days). The pre-haemorrhagic period is characterized by
sudden onset of fever, headache, myalgia, dizziness and further
symptoms of diarrhoea, nausea and vomiting. Hyperaemia of
the face, neck and chest; congested sclera; and conjunctivitis
are also noted. The haemorrhagic period is short, rapidly
progresses and typically begins at the third to fifth day of the
illness. The haemorrhagic signs vary from petechiae to the
appearance of large haematomas on the mucous membranes
and skin. Bleeding, commonly from the nose, gastrointestinal
system, urinary tract, respiratory tract and other sites including
the vagina; gingival bleeding; cerebral haemorrhage; and
bleeding from unexpected sites has been reported. The
convalescence period begins 1020 days after the onset
of disease. It is characterized by labile pulse, tachycardia,
temporary complete loss of hair, polyneuritis, difficulty in
breathing, poor vision, loss of hearing and loss of memory.85,86
Case definition: Defining a case is an important aspect of
a surveillance system. The case definition of the disease
will be more accurate when it is combined with laboratory
confirmation with clinical manifestations.13,45
The following are the case definitions for CCHF infection:
Suspected case: a patient with abrupt onset of high fever
>38.5C and one of the following symptoms: severe headache,
myalgia, nausea, vomiting, and/or diarrhoea and a history of tick
bite within 14 days prior to the onset of symptoms; or history
of contact with tissues, blood, or other biological fluids from a
possibly infected animal (e.g. abattoir workers, livestock owners,
veterinarians) within 14 days prior the onset of symptoms; or
health-care workers in health-care facilities, with a history of
exposure to a suspected, probable, or laboratory-confirmed
CCHF case, within 14 days prior to the onset of symptoms.
Probable case: a probable CCHF case is defined as a suspected

CCHF case fulfilling the following additional criteria:
thrombocytopenia <50000cells/mL and two of the following
haemorrhagic manifestations: haematoma at an injection
site, petechiae, purpuric rash, rhinorrhagia, haematemesis,
haemoptysis,
gastrointestinal
haemorrhage,
gingival
haemorrhage, or any other haemorrhagic manifestation in the
absence of any known precipitating factor for haemorrhagic
manifestation.
Confirmed case: a confirmed CCHF case is defined as a case
that fulfils the criteria for probable CCHF and, in addition,
is laboratory confirmed with one of the following assays:
detection by ELISA or immunofluorescence assay of specific
IgM antibodies against CCHFV, or a 4-fold increase in specific
IgG antibodies against CCHFV in two specimens collected in
the acute and convalescence phases, or detection by RT-PCR
of CCHF viral RNA in a clinical specimen, confirmed by
sequencing of the PCR product or CCHFV isolation.13,45
Diagnosis
Haemorrhagic fevers are contracted through contact with the
blood of infected animals, and the bite of infected ticks (CCHF
and KFD) and mosquitoes (dengue fever). Some of these
fevers can be transmitted from person to person. Laboratory
diagnosis of the disease is established by molecular methods,
while IgM and IgG antibodies become detectable by indirect
immunofluorescence assay or ELISA after the fifth day (see
Table 2).8789 However, there are reports that in severe cases
no antibody response is observed. Real-time RT-PCR for rapid
diagnosis of CCHFV infections is the test of choice in the acute
phase, and for ticks.90,91 The isolation of CCHFV requires a
high-containment BSL-4 laboratory, while viral RNA detection
combined with serology for laboratory diagnosis in BSL-3- or
BSL-2-compliant laboratories can be carried out following
good microbiological practices with standard protocol. The
Gujarat Government has planned to upgrade laboratories to
provide CCHF diagnosis, with proper biosafety precautions
and handling of these samples, after training and acquisition of
all the required biosafety equipment.
Treatment
So far, there is no specific treatment for CCHF. A vaccine
based on formalin-inactivated suckling mouse brain, which is
not yet approved by the Food and Drug Administration of the
USA (FDA) , has been used in Bulgaria and the former Soviet
Union.92 Since no specific treatment is available, supportive
treatment includes careful fluid and electrolyte balance,
monitoring and replacement with platelets, fresh frozen plasma
and erythrocyte preparations.93 The effect of ribavirin is still
controversial;9397 the drug has not been approved for the
treatment of CCHF by the FDA, but is, at present, the only
antiviral agent with promising effect, if administered before the
fifth day of the disease. It was observed that CCHF cases in India
supported the use of ribavirin.98 Ribavirin is contraindicated in
patients with chronic anaemia and haemoglobin levels below
8 g/dL, and in patients with severe renal impairment (creatinine
clearance <30mL/min). The drug may accumulate in patients
with impaired renal function. If ribavirin is administered,

patients should be carefully monitored during therapy for
signs and symptoms of toxicity, such as anaemia. Patients with
hypotension or haemodynamic instability should be managed
following standard guidelines for the treatment of shock, which
include resuscitation, fluid supplements (crystalloids/colloids)
and ionotropic support. In suspected secondary bacterial
infection, patients should be treated according to standard
guidelines/practice
for
community-acquired/nosocomial
infections. CCHFvenin, an immunoglobulin preparation
particularly from the geographical areas where this disease is
endemic, may be useful by the intravenous route for treatment
of patients with severe CCHF.9397
Guidelines for management of CCHF cases
In the hospital setting
The following precautions are recommended:13
isolate the patient in a room that is separate from other
patients in the hospital;
medical staff handling the patient should wear gloves and a
gown, to avoid direct contact with the patient;
after handling the patient, medical staff should thoroughly
wash their hands, as well as any other parts of their body
that came into contact with the patient, using soap and
water;
clinical procedures that are likely to cause spraying of
bodily fluids should be avoided, or only performed by
medical staff wearing a face shield, or a mask and eye
goggles;
bleach can be used for disinfection. A 1:100 dilution of
bleach should be used to clean surfaces, medical equipment,
and bedding and clothes. A 1:10 dilution of bleach should
be used to clean up bodily fluids. Alternatively, 5% Lysol
may be used.
In the family/community setting
Family members and friends who had direct contact with
the patient should be monitored for 14 days, for onset of a
febrile illness.
Dead body disposal
Rubber gloves or double surgical gloves should be used
for handling the dead body. The persons handling the dead
body in hospitals should also wear a mask and use personal
protective equipment.
The dead body should be sprayed with 1:10 liquid bleach.
It should then be wrapped with a winding sheet, which is
then sprayed with bleach solution.
The wrapped and bleached body should be placed in a
plastic bag, which is then sealed with adhesive tape before
transport.
The ambulance/transport vehicle should also be disinfected
after use.
17
Prevention
The main means of CCHF outbreak control, namely breaking
the transmission chains by avoiding/minimizing exposure to
the virus-infected material, is recommended for prevention.
Barrier nursing techniques are essential while treating
confirmed and suspected cases of CCHF. Close contacts of the
infected patient should be followed up with daily temperature
recording and monitoring of symptoms for at least 15 days
after the putative exposure. Health-care workers should take all
the necessary precautionary measures to prevent occupational
exposure.
Control
After confirmation of the CCHF outbreak in Gujarat state, a
highly efficient network of hospital reporting of admissions of
suspected cases, and help in monitoring the contacts and family
members was activated. Animal diseases health officials and
national vector-borne diseases (NVBCD) officials are on alert
for sampling of ticks and domestic animal samples from the
area of any suspected case in Gujarat state. With the diagnostic
support of NIV, Pune in the last 3years, every suspected case has
been referred to NIV for a quick diagnosis, to avoid the spread
of infection.9,44,57,78 An awareness programme is conducted in
different government and private hospitals, for reporting and
sending samples to NIV, Pune for confirmation. The strategic
actions taken by the state government included active human,
animal and entomological surveillance. Whenever any deceased
CCHF-positive patient is reported, immediate surveillance is
conducted for members of the community, for unusual fever
symptoms, as well as IgG antibody screening of domestic
animals and viral RNA detection in infested ticks. Isolation and
treatment of cases following universal precautions is carried
out, with contact tracing and monitoring of contacts, spraying
cattle in the affected area with anti-tick agents, spraying human
dwelling with residual sprays, and communicating the risk to
the public. Owing to proper precautions and quick preventive
measures, avoidance of nosocomial infection in humans is
optimized.13,14,98
The individuals in outbreak areas who are vulnerable to tick
bites, or exposed to infected animals or animal tissues, or
health-care and laboratory workers are considered to be at risk
of contracting CCHF. Thus, control measures should be mainly
focused on tick control in outbreak areas and on personal
protective measures for persons caring for CCHF patients.97101
Prevention and control with regard
to disease-affected animals:
segregate the animal from other livestock;
undertake tick control in infected animals, in consultation
with the animal husbandry department;
cattle sheds should be properly disinfected;
if milking an animal, the milk should not be used for human
consumption;
18
if animals are slaughtered, proper disposal of carcasses

should be performed;
the left-over feed should be sprayed with 3% bleach and
should be disposed of, to ensure that other animals do not
feed on it;
these procedures should be followed for at least 2weeks
and blood samples should be drawn and confirmed to be
free of viraemia
Tick bites are best prevented by people avoiding tick-infested
areas or by wearing long trousers that are tucked into boots. Tick
bites can be prevented by application of a topical repellent to
exposed skin and treatment of clothing with insecticide, which
gives nearly 100% protection. Dipping is the primary method
of tick control for livestock and has been found to be highly
effective for controlling several tick-borne diseases. Spraying
is another method used to apply the chemical acaricides that
kill ticks.99101 However, resistance of ticks to acaricides poses
an increasing risk to livestock.
Discussion
According to a recent study from the Zoological Society
of London, United Kingdom, along with researchers from
Georgia and New York, USA, India is considered a hot
spot for emerging infectious disease, on a global map.102
In recent years, vector-borne diseases have emerged as a
serious public health problem in countries of the South-East
Asia, including India. Many emerging zoonoses have spread
globally at the humananimal interface.103 Risk factors for
emergence reside in multiple sectors. India has extremes of
climatological and geographical conditions: temperatures that
vary from extremely low to high, temperate regions and desert,
thick evergreen forest, and areas of high rainfall. Increased
population, urbanization, international travel, change in
agricultural practices, environmental factors, change in
lifestyle, deforestation, close contact of animals, and a porous
international border make this country a high-risk area for
outbreaks of emerging and new diseases.102
Vector-borne zoonoses now occur in epidemic form on an
almost annual basis, causing considerable morbidity and
mortality.104 All these have impact not only on public health
but also on the livelihood and economy of affected countries.
A network of laboratories, trained laboratory staff, more highcontainment diagnostic laboratories, surveillance programmes,
modern equipment and trained medical professionals are
required in order that the country is prepared to deal with this
kind of emergency situation. KFD was originally assumed to
be restricted only to Karnataka state, but there is now evidence
of its spread; similarly, CCHF is not restricted to one district
but human positivity has now been recorded in seven districts.9
The recent sero-survey study by NIV, Pune, has revealed that
domestic animals are positive for anti-IgG antibody in at least
15 districts of Gujarat state (NIV unpublished data). Though
the main endemic foci are in Gujarat state, CCHF has been
suspected in other parts of the country, based on earlier serology
data.76,77 Strengthening of public health system networking for
reporting and circulating information, with participation and

education of the general public in the country, is required to
deal with these deadly diseases.
8.
9.
Conclusion
KFD and CCHF are both of high importance for public health
in India, as cases are observed almost every year in Karnataka
and Gujarat states, respectively. It is important that the
health system should be able to distinguish these tick-borne
haemorrhagic diseases from other diseases, which have diverse
and often overlapping, clinical presentations. In general, as
the incidence of tick-borne diseases increases in any area,
surveillance in other/adjoining geographic areas should also
be expanded. Keeping in view the current status, the Indian
Council of Medical Research (ICMR) has taken the initiative
to survey to determine the probability of the existence of KFD
in states adjoining Karnataka. Similarly, a joint initiative has
been taken up by ICMR and the Indian Council of Agricultural
Research (ICAR) to conduct a survey of IgG antibodies
against CCHF in domestic animals in different states of India.
In view of the One health concept put forward by WHO, it
is proposed to establish a joint ICMR and ICAR committee
on zoonoses, to create facilities for an ICMRICAR centre of
excellence on zoonoses, which will be upgraded to a National
Institute of Zoonoses. This institute will be dedicated to
research and development in the areas of zoonotic diseases
and will significantly contribute towards early diagnosis and
control of re-emerging and newly emerging zoonotic diseases.
Acknowledgements
10.
11.
12.
13.
14.
15.
16.
17.
18.
We gratefully acknowledge the encouragement and support

extended by Dr VM Katoch, Secretary, Department of Health
Research, Ministry of Health and Family Welfare, New
Delhi. We also gratefully acknowledge the cooperation of
the Directorate of Health Services, Government of Gujarat,
Integrated Disease Surveillance Programme, and authorities
of National Vector Borne Disease Control Programme and
the State Health Department, Karnataka, and Virus Diagnostic
Laboratory, Shimoga, Karnataka.
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prevent arthropod-related casualties. J. Travel Med. 1998;5:21720.
Ho-Pun-Cheung T, Lamarque D, Josse R, et al. Protective effect of
clothing impregnated with permethrin against D. reticulatus and D. Bull.
Soc. Pathol. Exot.1999;92:33740.
Ergonul O, Whitehouse CA. Risk groups and control measures for
crimean-congo hemorrhagic fever. In: Ergonul O, Whitehouse CA.
Editors. Crimean-Congo hemorrhagic fever: a global perspective.
Dordrecht: Springer, 2007. pp. 273-280.
Wiwanitkit V, Singh MY. Emerging infectious diseases in India. New
York: Nova Science Publishers, 2009.
Greger, M.The human/animal interface: emergence and resurgence of
zoonotic infectious diseases.Crit. Rev. Microbiol.2007;33:243299.
Kilpatrick AM,Randolph SE. Drivers, dynamics, and control of emerging
vector-borne zoonotic diseases. Lancet.2012;380(9857):1946-55.
How to cite this article: Mourya DT, Yadav PD, Patil DY.
Highly infectious tick borne viral diseases: Kyasanur forest
disease and Crimean-Congo hemorrhagic fever in India. WHO
South-East Asia J Public Health 2014; 3(1): 821.
Contributorship: : DTM and PDY contributed to the study design and
drafted the manuscript as the lead writers. PDY collated and summarized
the collected data and DYP carried out extensive systematic review of the
literature about Kyasanur forest disease and CrimeanCongo haemorrhagic
fever on different databases, and helped in preparing the draft. All the
authors were involved in revising the manuscript.
21
Review
DOI: 10.4103/2224-3151.115828
Current status of dengue and

chikungunya in India
Dayaraj Cecilia
Abstract
National Institute of Virology,

Maharashtra, India
Dengue, a Flavivirus and chikungunya, an Alphavirus, transmitted by Aedes

mosquitoes, are a cause of great concern to public health in India. Every year,
thousands of individuals are affected and contribute to the burden of health care.
Dengue outbreaks have continued since the 1950s but severity of disease has
increased in the last two decades. Chikungunya outbreaks started in the 1960s
and dwindled to sporadic cases until a resurgence in 2006. Based on the data
of National Vector Borne Disease Control Programme (NVBDCP), the number of
cases reported in 2013 was about 74454 for dengue with 167 deaths and 18639
for chikungunya. The number of cases reported is increasing, probably because
of the availability of IgM detection kits produced and distributed by National
Institute of Virology through NVBDCP and better reporting. In the absence of wellstructured epidemiological studies, this review attempts to summarize reports on
dengue and chikungunya outbreaks from various regions of India. For dengue,
young adults are the major group affected; the severity of disease in India is still
lower than that reported elsewhere in South-East Asia; and paediatric cases of
dengue haemorrhagic fever have a high mortality. For chikungunya, all age groups
are affected but severe manifestations are more often seen in children. Persisting
arthralgia, neurological syndromes and non-neurological manifestations are
recorded. Changes in the genotype and mutations in the genome have been
detected for both dengue and chikungunya viruses. The review ends with a short
summary of the most recent vector-control studies.

Dengue Group, National Institute of
Virology 20-A, Dr Ambedkar Road,
Pune-411001, Maharashtra, India
Email: cecilia.dayaraj@gmail.com
Key words: dengue, chikungunya, India, symptoms, outbreaks, evolution
INTRODUCTION
Dengue and chikungunya are two mosquito-borne viral diseases
of great public health concern in India. Dengue virus (DENV)
and chikungunya virus (CHIKV) are transmitted by the same
species of mosquito, Aedes aegypti and share spatiotemporal
territories. Both viruses are known to cause acute febrile illness
with almost identical symptoms in the early phase of infection,
although the clinical profiles differ as the infection progresses.
DENV belongs to the Flaviviridae family and CHIKV belongs
to the genus Alphavirus of Togaviridae. Before the genome
organization and replication strategy was discovered the two
viruses were placed in arboviruses, group-A and group-B, by
virtue of being arthropod-borne viruses and having singlestranded positive-sense RNA genomes. Both viruses are
believed to have originated in Africa about 200300 years ago
22
as shown by molecular clock analysis. However, for DENV,

the Malay Peninsula is also considered as a possible place of
origin.1
GLOBAL DISTRIBUTION
Dengue
The name dengue originated from the Swahili word for bonebreaking fever or the word for the walk of a dandie in
Spanish. The first probable case of dengue fever (DF) was
recorded during the Jin Dynasty (265420 AD) in China. The
first recognized epidemicsoccurred almost simultaneously in
Asia, Africa and North America in the 1780s, shortly after the
identification and naming of the disease in 1779 by Benjamin
Cecilia: Dengue and chikungunya in India
Rush.2 The presence of four serotypes has become one of the

complex challenges presented by dengue. Protective immunity
against the infecting serotype is lifelong but lasts for only
34 months against the other serotypes. A second infection
after this period often results in severe disease. In the early
1900s, spread of dengue was explosive and accompanied
the movement of people across continents because of the
slave trade and the two World Wars; India was one of the
major areas affected.3 Presently, about 40% of the worlds
population is at risk and there are 50100 million cases every
year. An estimated 500000 people with severe dengue require
hospitalization each year and about 2.5% of those affected
die.4 In the last few years, dengue has re-emerged in the United
States of America and has made inroads into Europe.5 In India,
dengue is widespread and endemic in most major cities.6
Chikungunya
Chikungunya was first detected in 1952 in Makonde, United
Republic of Tanzania (formerly Tanganyika) and derives its
name from kungunyala, the Swahili word for the contorted
posture of patients because of their arthritic symptoms. It was
first described by Robinson and Lumsden in 1953.7 Epidemics
were subsequently noted in the Philippines (1954, 1956 and
1968), Thailand, Cambodia, Viet Nam, India, Myanmar and
Sri Lanka.8In India, major epidemics of chikungunya were
reported in 1963 in Kolkata, in 1965 in Pondicherry (formerly
Pondicherry), Tamil Nadu, Andhra Pradesh, Madhya Pradesh
and Maharashtra and again in 1973 in Maharashtra.9Thereafter,
sporadic cases continued to be recorded in Maharashtra during
1983 and 2000.10 Since 2003, there has been a resurgence of
chikungunya outbreaks in the islands of the Pacific Ocean,
including Madagascar, the Comoros, Mauritius and Reunion
Island.11In January 2006, there was a very large epidemic in
Reunion Island followed quickly by the one in India.12 Almost
1.3 million suspected chikungunya fever cases were reported
in India.13 Resurgence of chikungunya has been attributed
to various factors including globalization, increase in the
mosquito population, loss of herd immunity and the mutation
A226V in the E1 gene causing a significant increase in CHIKV
infectivity for Ae. albopictus.11
DISTRIBUTION IN INDIA
Since 2007, diagnosis and data assimilation for dengue and
chikungunya in India have been facilitated by the National
Vector Borne Disease Control Programme (NVBDCP). The
programme has 347 sentinel centres in 35 states and 14 apex
referral laboratories, which are supplied with DENV- and
CHIKV-specific IgM detection kits produced by the National
Institute of Virology (NIV).
Goa, Gujarat, Haryana, Karnataka, Kerala, Madhya Pradesh,

Maharashtra, Punjab, Rajasthan, Tamil Nadu, Uttar Pradesh,
West Bengal, Chandigarh, Delhi and Puduchery. During 2010
2012, dengue encroached into the remaining states. Figure-1
shows the distribution of dengue cases among the states of
India in 2013.
Although the number of dengue cases has shown a steady rise
with every passing year, the mortality has reduced (Figure-2).
The overall mortality rate of 1.2% in 2007 dropped to 0.25%
in 2013. This reduction is probably the result of the cumulative
effects of better patient management, increased diagnostic
capabilities and better reporting. Compared with the rest of
South-East Asia, the number of dengue shock syndrome (DSS)
cases in India remains low.
The execution of well-designed epidemiological studies has
been difficult. We carried out a pilot age-stratified, crosssectional dengue prevalence study in collaboration with
Vadu Rural Health Programme, KEM Hospital Pune. Dengue
prevalence was determined in two villages that differed in the
level of urbanization and population density. A significantly
higher seropositivity of 58.5% for DENV was found in the
urbanized village, compared with 41.2% for the rural village.15
Daman & Diu, 61
Puduchery, 2215 Arunachal Pradesh, 0

Andhra Pradesh, 910
D&N Haveli, 190

Chandigarh, 107
A& N Island, 67
Bihar, 1246
Chattisgarh, 52
Goa, 198
Assam,
4526
Delhi, 5574
Gujarat, 6170
Uttrakhand, 54
Haryana, 1784
West Bengal, 5920

Uttar Pradesh, 1409
Tripura, 0
Himachal Pd., 86
J & K, 1837
Jharkhand, 161
Tamil Nadu, 6122

Karnataka, 6408
Sikkim, 38
Rajasthan, 4413
Kerala, 7911
Punjab,
4114
Orissa, 7132
Maharashtra,
5432
Madhya Pd., 1255
Meghalaya, 46
Nagaland, 0
Manipur, 9
Mizoram, 7
Figure 1: Distribution of dengue cases in Indian states in 2013 (based

on NVBDCP data)6
80000
1.40
70000
1.20
60000
1.00
50000
0.80
40000
0.60
30000
0.40
20000
Dengue
0.20
10000
0.00
The history of dengue outbreaks in India has been recently

reviewed.14 More recent and systematic data are now available
because of the NVBDCP. The data on the web site of NVBDCP6
and earlier publications by NIV3 show that dengue has been
endemic in 16 states since the beginning: Andhra Pradesh,
2007
2008
2009
2010
No. of cases
2011
2012
2013
% Mortality
Figure 2: Total dengue cases reported to NVBDCP (left axis) and

percentage mortality (right axis) in India, 20072013
23
in Delhi, a mortality rate of 6.6% was reported in DHF/DSS

patients from a single hospital where the mean age was 25.6
years.21 Another study, in Mumbai in 2003, reported three
deaths in 38 DHF/DSS cases in the paediatric intensive-care
unit with a mean age of 4.9 years.22 Therefore, it is evident that
to get accurate data, well-designed epidemiological studies in
demographically defined populations are required.
2000
1800
1600
1400
1200
1000
800
600
400
Chikungunya
200
0
J
No tested
No positive
Figure 3: Seasonality of dengue during 20052010 in Pune city15
There have been a few longitudinal studies based on single/

multiple hospital data. A study on samples received at the
All India Institute of Medical Sciences, New Delhi, during
20032005 reported 44.56% positivity in 1820 samples. The
maximum number of cases belonged to the 2130 years age
group and the peak was in October. Co-circulation of all four
serotypes was observed in 2003 and emergence of DENV-3 as
the dominant serotype in 2005.16 Another study from a tertiary
care hospital in Delhi covering 7 years (20022008), reported
30.15% positivity in 7846 samples and circulation of all four
serotypes in 2003 followed by DENV-3 in 20042006, DENV2 in 2007 and DENV-1 in 2008.17 We carried out a longitudinal
study for a period of 6 years (20052010) in Pune city involving
24 private and government clinics/hospitals.15 On testing 5106
samples we observed a positivity of 48.45%. The 2130 years
age group was most affected by dengue throughout the 6
years. The cumulative number of cases observed per month
during the 6-year period showed that the largest numbers were
observed in the month of October with a positivity of 57.9%
(Figure-3). All four serotypes were found to be circulating in
Pune. Each year was characterized by the predominance of one
of three serotypes. DENV-1 was dominant in 2005 and 2007,
DENV-2 was dominant in 2008 and DENV-3 was dominant in
2009. In 2010 both DENV-2 and DENV-3 were co-dominant.
DENV-4 was poorly represented with just one case each in
2009 and 2010; both cases were dengue haemorrhagic fever
(DHF).18 Based on the symptoms presented the cases, were
classified into DF, DHF or DSS according to World Health
Organization (WHO) 2007 criteria. During the 5-year period,
90.5% (n=2239) of the patients were classified as DF and 9.5%
(n=235) cases were categorized as DHF. Year-wise analysis
revealed that the proportion of DHF cases was about 20%
in 2005, 2006 and 2008; the proportion dropped to 6.8% in
2007, 2009 and 2010.19 This fall probably reflected improved
diagnosis and better reporting of non-hospitalized dengue
cases. DHF was seen with low severity despite the circulation
of multiple serotypes.
There have been isolated reports on mortality in paediatric
DHF/DSS cases which are much higher than the cumulative
mortality reported by NVBDCP. Cherian et al.20 reported a casefatality rate of 26.3% in a study that included 19 children older
than 1 year in 1990 in the North Arcot district and the adjoining
areas of Tamil Nadu and Andhra Pradesh. In the 1996 outbreak
24
The first recorded chikungunya outbreak was in Kolkata in

1963. This was followed by epidemics in Tamil Nadu, Andhra
Pradesh and Maharashtra in 196465 and in Barsi in 1973.23
CHIKV then seems to have disappeared from India. The virus
re-emerged in 2006 after a gap of 32 years and caused an
explosive outbreak affecting 13 states. The states first affected
were Andhra Pradesh, Karnataka, Maharashtra, Madhya
Pradesh, Tamil Nadu, Gujarat and Kerala. All ages and both
sexes were affected. The virus isolates belonged to the African
genotype different from the viruses circulating in 19631973,
which belonged to the Asian genotype.12,23 The A226V shift
in the E1 protein that was detected with progression of the
epidemic in Reunion Island was absent in all of the Indian
isolates. The A226V mutation was found to occur only in the
2007 isolate from India.24
In 2008 almost 100 000 people in different villages of
Kasargodu district, Kerala were affected by chikungunya. This
was followed by a large outbreak in Tirunelveli district, Tamil
Nadu in 20092010. The CHIKV isolate was found belong to the
Eastern Central Southern African genotype (E1:226A). During
20092010, cases were also reported from Maharashtra.23 In
the subsequent years, CHIKV spread to other states: Goa,
Orissa, Rajasthan, West Bengal, Andaman & Nicobar Islands
and Puducherry.13 The year 2011 was exceptional in that cases
were reported from all states except Punjab, Dadra and Nagar
Haveli and Lakshadweep. Lakshadweep had a chikungunya
outbreak only in 2007. Distribution of cases in 2013 is shown
in Figure 4.
West Bengal, 646
A& N Island, 202 Delhi, 18 Puduchery, 146
Tamil Nadu, 859

Rajasthan, 76
Orissa, 35
Madhya Pd., 139

Kerala, 219
Maharashtra,
1432
Andhra Pradesh,
4827
Assam, 742
Karnataka, 5295
Goa, 1049
Gujarat, 2890
Jharkhand, 61
Figure 4: Distribution of chikungunya cases in Indian states in 2013

(based on NVBDCP data)13
India reported 1.3 million cases in 2006 but no data on

mortality were available except for two reports one on a
subset of patients and one deductive. In one report, among
90 laboratory-confirmed chikungunya cases hospitalized in
Ahmadabad, 18 deaths were recorded of which 15 were aged
60 years or older and five had comorbidities.25 The other report
was deductive; based on death records during previous years
in Ahmadabad, the excess deaths that occurred during the
outbreak period was attributed to CHIKV and a mortality rate
of 4.9% was reported.26
SYMPTOMS
Dengue
DENV causes self-resolving DF in the majority of cases,
characterized by severe body ache, retro-orbital pain, headache
and at times rash, abdominal pain and nausea. According
to the new terminology recommended by WHO in 200915
dengue cases can be classified into dengue without warning
signs, dengue with warning signs (abdominal pain/persistent
vomiting/mucosal bleed/increase in HCT with decrease in
platelet count) and severe dengue (severe plasma leakage,
severe bleeding and severe organ involvement.
Several groups have tried to identify prognostic symptoms
for progression to severe disease. During a 5-year study
conducted by our group on clinical profiling of patients;
joint pain, retro-orbital pain and itching were seen in a
significantly higher proportion of DF cases. The clinical
triad of abdominal pain, rash and conjunctival congestion
was found to be a possible prognostic marker of progression
towards severe disease due to the strong association of these
symptoms with DHF cases. Melaena and haematemesis were
the most common haemorrhagic manifestations in DHF. Liver
involvement, which has been well documented in DHF, was
evident in about 85% of the DHF patients tested.19 Similar
observations were reported from Delhi,28 Kerala29 and West
Bengal.30 Althoughdengueis considered a non-neurotropic
virus, neurological complications have been reported in
dengue cases. The neurological manifestations of dengue
infection can be grouped into three categories: neurotropic
effect of the virus encephalitis, meningitis, myositis and
myelitis; systemic complications encephalopathy, stroke,
hypokalaemic paralysis and papilloedema; and postinfection
acute disseminated encephalomyelitis, encephalomyelitis,
myelitis, neuromyelitis optica, optic neuritis and GuillainBarr syndrome.31,32
Chikungunya
Symptoms generally start 47 days after the mosquito bite. The
acute phase is characterized by painful polyarthralgia, high
fever, asthenia, headache, vomiting, rash and myalgia. In the
chronic phase, incapacitating arthralgia persists for months.
Neurological syndromes in cases from Ahmadabad and Pune
included encephalitis, encephalopathy and myelopathy or
myeloneuropathy. Non-neurological systemic syndromes
included renal, hepatic, respiratory, cardiac and haematological
manifestations together with atypical manifestations including
lymphadenopathy, oral ulcers and encephalitis.33,34 Optical

abnormalities have also been associated with CHIKV
infections.35,36
Children are at maximum risk for severe manifestations of
the disease. Some of the clinical features in children include
neurological manifestations, i.e. seizures, altered levels of
consciousness, blindness due to retrobulbar neuritis and
acute flaccid paralysis.37 Another report on CHIKV infection
in infants younger than 12 months old indicated that the
most characteristic features of the infection in infants were
acrocyanosis, symmetrical superficial vesicobullous lesions
and erythematous asymmetrical morbiliform rashes.38 CHIKV
infection in neonates is very rare, one case presented with severe
thrombocytopenia and features of multisystem involvement.39
Vertical transmission of CHIKV from mother to child has been
documented.40
VIRUS EVOLUTION
Dengue
When dengue first emerged in India during 195060s, the
disease was mild despite circulation of all four serotypes.
The disease profile changed and greater severity was reported
from the late 1980s. The circulation of serotypes in different
parts of the country and changes in the circulating serotypes
in consecutive years has been reviewed recently.41 The Indian
isolates obtained over a span of 50 years by NIV were sequenced
and analysed with global data.4244 The phylogenetic analysis
of the E gene sequence revealed that the Indian viruses formed
clusters that were temporally distinct. For all four serotypes,
the viruses circulating in India in the 1950s and causing mild
disease were either replaced or evolved into lineages/genotypes
with greater virulence and/or transmissibility. Genotype shifts
for DENV-2 (American to Cosmopolitan) and DENV-4
(genotype V to I) and lineage changes for DENV-1 (India III
to India I and II of American African genotype) and DENV-3
(F to A, B, C and D of genotype III) were observed.9 Genotype
III of DENV-3, which originated in India, is more virulent and
has caused haemorrhagic outbreaks in many countries. DENV4 serotype seems to have its origin in India. The evolution
of genotype I of DENV-4 in India could be associated with
an event of recombination of a genotype V Indian isolate of
1961 with a genotype I Sri Lankan isolate of 1978. Complete
genome sequence analyses have confirmed these results for
DENV-145and DENV-2.46
Chikungunya
The evolutionary timescale of CHIKV was estimated to be in
the last 300 years under a constant-population relaxed-clock
model. Phylogenetic analysis based on partial sequences of
NS4 and E1 genes showed that all earlier isolates (19631973)
were Asian genotype, whereas the 2006 and 2000 isolates were
African genotype. The progenitor of the 20052007 viruses
was found to have existed around 9 years ago and may have
originated from Uganda.47 The Indian 2006 isolates were closer
25
to the Reunion islands isolates (99.9% identity) than to the

2000 isolate, confirming involvement of the Reunion virus in
the outbreak. The A226V shift observed with the progression
of the epidemic in Reunion Island was absent in the Indian
isolates47 but was present in isolates obtained from 2007
onwards in different parts of India: Tamil Nadu (20092010),
Kerala (2009)48 and Orissa (2010).49
VECTOR
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4.
Ae. aegyptiis the principal vector for both DENV and

CHIKV. DENV is maintained in a humanmosquitohuman
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involves non-human primates and a number of forest-dwelling
mosquitoes. It is not clear how the virus is maintained in
Asia. Transovarial transmission (TOT) has been reported for
DENV.50,51 However, for CHIKV all the earlier studies have
shown absence of this phenomenon.52 There are some scanty
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How to cite this article: Cecilia D. Current status of dengue

and chikungunya in India. WHO South-East Asia J Public
Health 2014; 3(1): 2227.
27
Original research
DOI: 10.4103/2224-3151.115828
Vector-borne diseases in central India,

with reference to malaria,filaria,
dengue and chikungunya
Neeru Singh1, Manmohan Shukla2, Gyan Chand1,
Pradip V Barde1, Mrigendra P Singh2
Abstract
Background: Vector-borne diseases (VBDs) caused by parasites and viruses
are a major cause of morbidity and mortality in Madhya Pradesh (MP), central
India. These diseases are malaria, lymphatic filariasis, dengue and chikungunya.
Epidemiological information is lacking on different VBDs that are commonly
prevalent in rural-tribal areas of MP, except on malaria.
Methods: The studies were carried out at the request of Government of Madhya
Pradesh, in three locations where many VBDs are endemic. Data on malaria/filaria
prevalence were collected by repeatedly undertaking cross-sectional parasitological
surveys in the same areas for 3 years. For dengue and chikungunya, suspected
cases were referred to the research centre.
Results: Monitoring of results revealed that all the diseases are commonly
prevalent in the region, and show year-to-year variation. Malaria slide positivity
(the number of malaria parasitaemic cases, divided by the total number of blood
smears made) was 18.7% (190/1018), 16.4% (372/2266) and 20.4% (104/509)
respectively in the years 2011, 2012 and 2013. There was a strong age pattern
in both Plasmodium vivax and P. falciparum. The slide vivax rate was highest
among infants, at 5% (odds ratio [OR]=3.8; 95% confidence interval [CI]=1.5
to 9.4; P<0.05) and the highest slide falciparum rate was 20% in children aged
14 years (OR=2.0; 95% CI 1.5 to 2.7; P<0.0001). This age-related pattern was
not seen in other VBDs. The microfilaria rate was 7.5%, 7.6% and 7.8% in the
years 2010, 2012 and 2013, respectively. Overall, microfilaria rates were higher
in males (8.7%) as compared to females 6.4% (OR=1.5; 95% CI=1.1 to 2.0;
P<0.01). The prevalence of dengue was 48% (dengue viruses 1 and 4 DENV-1
and DENV-4), 59% (DENV-1) and 34% (DENV-3) respectively, in the years 2011,
2012 and 2013 among referred samples, while for chikungunya very few samples
were found to be positive.
Regional Medical Research Centre

for Tribals (Indian Council of
Medical Research), Jabalpur
Madhya Pradesh, India
2
National Institute of Malaria
Research Field Station, Jabalpur,
Regional Medical Research
Centre for Tribals Campus,
Jabalpur, Madhya Pradesh, India
1

Dr Neeru Singh, Regional Medical
Research Centre for Tribals (Indian
Council of Medical Research),
Nagpur Road, Post Garha, Jabalpur
482003, Madhya Pradesh, India.
Email: neeru.singh@gmail.com;
rmrctjabalpur@rediffmail.com
Conclusion: Despite recent advances in potential vaccines and new therapeutic

schemes, the control of VBDs remains difficult. Therefore, interruption of
transmission still relies on vector-control measures. A coordinated, consistent,
integrated vector-management approach is needed to control malaria, filaria,
dengue and chikungunya.
Key words: Chikungunya, dengue, filaria, malaria, Madhya Pradesh, vectorborne diseases
28
Singh et al.: Vector-borne diseases in central India
Introduction
Vector-borne diseases (VBDs) caused by parasites and viruses
are major cause of mortality and morbidity across the world,
especially in tropical and subtropical low- and middleincome countries. Malaria, lymphatic filariasis, dengue and
chikungunya are important VBDs, with a major contribution to
the overall global disease burden every year.
Malaria is a major public health problem, causing 207 (range
135 to 287) million cases and 0.627 (range 0.473 to 0.789)
million deaths throughout the world in 2012.1 One hundred
and four countries and territories are endemic for malaria, and
India alone contributes about 50% of the 2 million reported
cases in the World Health Organization (WHO) South-East
Asia Region.1 The majority of malaria cases and deaths in
India are reported from Chhattisgarh, Jharkhand, Madhya
Pradesh, North Eastern States, Orissa and Rajasthan.2 There
are six efficient vectors of malaria, of which three are common
in central India, namely Anopheles culicifacies, A. stephensi
and A. fluviatilis.3,4
Lymphatic filariasis is endemic in 81 countries in tropical and
subtropical regions of Asia, Africa, central and south America
and Pacific Island nations, with more than 120 million people
infected and 1.34 billion people at risk of infection.5,6 An
estimated 25 million have genital disease and 15 million have
lymphoedema or elephantiasis caused by Wucheraria bancrofti
or Brugia malayi.7 India alone contributes 40% of global cases
of lymphatic filariasis.6 In India about 600 million people,
residing in 250 districts, are at risk.8 There are about 31 million
microfilaria carriers and 23 million chronic clinical cases.9
Lymphatic filariasis is caused mainly by W. bancrofti (>99%)
and transmitted by mosquito Culex quinquefasciatus.
Dengue fever is a most important re-emerging arboviral
disease, causing an estimated 390 million infections every
year worldwide, of which nearly 100 million require medical
attention,10 and more than 500000 require hospitalization.11 It
is estimated that 34% of the global cases are from India10 and
the country is known to be endemic, with all four serotypes
(DENV-1, DENV-2, DENV-3 and DENV-4) circulating
throughout the year in different parts.12 Aedes aegypti is
regarded as the principal vector for this virus in India.13
Chikungunya virus (CHIKV) is a mosquito-transmitted singlestranded RNA alpha virus belonging to the family Togaviridae.
There is historical evidence that CHIKV originated in Africa
and subsequently spread to Asia.14 A characteristic feature of
CHIKV is that it causes explosive outbreaks, before apparently
disappearing for a period of several years to decades. In 2005,
the disease re-emerged in the Indian Ocean, after 32 years, and
over 1.3 million cases of chikungunya are estimated to have
occurred in India.15 The disease is overshadowed by dengue,
which has similar symptoms and is transmitted by same vector;
as a result chikungunya is neglected because the symptoms are
milder in comparison to dengue.
This study aims to describe the characteristics of VBDs that are

commonly prevalent in central India, to help policy-makers to
commence appropriate, evidence-based strategies for curbing
these diseases. The results reported fill some knowledge gaps
with regard to the burden associated with these VBDs in
Madhya Pradesh.
MATERIALS AND METHODS

The study has the approval of the ethics committee of the
Regional Medical Research Centre for Tribals (RMRCT),
Jabalpur.
Study area
Madhya Pradesh is situated in the centre of India and
comprises 50 districts. At the request of the Government of
Madhya Pradesh, the studies on malaria, lymphatic filariasis
and dengue were carried out in the districts of Anuppur,
Panna and Narsinghpur respectively (see Figure 1). Statewide analysis of chikungunya was also carried out. RMRCT,
Jabalpur is the WHO collaborative centre for the health of the
indigenous population and the National Vector Borne Disease
Control Programme (NVBDCP) designated apex referral
laboratory for dengue and chikungunya, for Madhya Pradesh
and Chhattisgarh.
Anuppur district
Anuppur is located at 23.1N 81.68E, with an average
elevation of 505m. The district is about 300 km from RMRCT,
Jabalpur, has an area of 3701 km2 and one third of the area is
under forest. The population of the district is 749237, of whom
48% are ethnic tribes.16 The villages are located off road and
the terrain is inaccessible. The study area is on the border of
the Bilaspur and Korea districts of Chhattisgarh state. Most
tribal villages are formed of three to eight scattered hamlets,
encircled by perennial streams and their tributaries. These
streams supports numerous breeding sites for A. culicifacies
and A. fluviatilis, throughout the year. The inhabitants of the
villages are of the primitive Baiga tribe and the local economy
is mainly forest based. The area is under two rounds of indoor
residual spray (IRS) with dichlorodiphenyltrichloroethane
(DDT) for vector control. The inhabitants spend most of their
time outside their dwellings and sleep outdoor during hot and
humid seasons, or in agricultural fields for crop protection. In
all, 12 cross-sectional parasitological surveys were carried out
for malaria during 20112013, covering all seasons i.e. spring
(February to March), summer (April to June), monsoon (July to
September), post monsoon (October to November) and winter
(December to January). Spleen examination was carried out
in children aged between 2 and 9 years, with or without fever,
using Hacketts method.17
29
Figure 1: Map of India (A) and Madhya Pradesh (B), showing study districts Anuppur (C), Panna (D) and Narsinghpur (E)
RMRCT: Regional Medical Research Centre for Tribals, Jabalpur
Panna district
Madhya Pradesh state
Panna is located at 24.27N 80.17E, with an average elevation

of 410 m. Panna district is highly endemic for filarisis and
about 200 km from RMRCT, Jabalpur. Panna has an area of
7135 km2, of which 49% is under forest. The population of
the district is 1 016 520, of whom about 88% live in rural
areas (only 15.4% ethnic tribe) and they are engaged mainly
in agricultural activities. From 2004, mass drug administration
(MDA) started in the district, and by June 2013 eight rounds
were completed. Microfilaria surveys were carried out in
randomly selected villages that historically had clinical cases
related to filarial disease. Among these, sentinel villages under
NVBDCP were also surveyed. A total of three surveys were
carried out in the years 2010, 2012 and 2013.
Blood samples of patients in Madhya Pradesh state with

suspected chikungunya during 2011 to 2013 were referred to
RMRCT for laboratory testing.
Narsinghpur district
Narsinghpur is located at 22.95N 79.2E, with an average
elevation of 347m. The district has an area of 5125.55 km2, with
a population of 1091854 and is about 90 km from RMRCT,
Jabalpur. Forest covers 26.6% of the geographical area and the
inhabitants of the study area belong to a low socioeconomic
group and are employed in agricultural practices. Blood
samples from patients with suspected dengue in Narsinghpur
during 2011 to 2013 were referred to RMRCT for laboratory
testing.
30
Sample processing for malaria,

filaria, dengue and chikungunya
For malaria, thick and thin blood smears were made from all
fever cases and cases with a history of fever in the past 14
days, after obtaining written informed consent. Blood smears
were stained with Jaswant singh and Bhattacharji stain18 and
examined under a microscope as described earlier.9,19 Treatment
was provided as per national drug policy on malaria, i.e.
artemisinin-based combination therapy (ACT) + primaquine
for Plasmodium falciparum and chloroquine + primaquine
for P. vivax.20 Pregnant women and infants were not given
primaquine.21 Before undertaking this investigation, data from
the district in previous years were obtained from the district
malaria officer Anuppur, along with details of the insecticide
used for spray and the population covered (see Table 1).
For lymphatic filariasis, blood slides were prepared by
conducting night blood surveys between 8 pm and 11 pm,
from a randomly selected population; 40L of blood was
taken from a finger prick and a thick smear was prepared and

Table 1: Epidemiological situation of malaria in Anuppur district and the population under DDT spray (2011 to 2013)
Year
Target population
2011
2012
2013
681862
764511
779801
Population
Sprayed with DDT
126431
156014
174178
BSE
Positive
Pf
Pv
ABER
API
SPR
SFR
81868
85734
76331
1211
834
846
650
520
447
561
314
399
12.01
11.21
9.79
1.78
1.09
1.08
1.48
0.97
1.11
0.79
0.61
0.59
Source: District malaria officer, Anuppur district.

ABER: Annual Blood Examination Rate; API: annual parasite incidence; BSE: blood slide examined; DDT: dichlorodiphenyltrichloroethane;
Pf: Plasmodium falciparum; Positive: positive for malaria; SFR: slide falciparum rate; SPR: slide positivity rate.
stained as described earlier.22 Treatment to microfilaria carriers

was provided by the district medical officer, as per NVBDCP
guidelines.
For dengue, the blood samples from suspected patients were
collected by the treating physician and referred to the laboratory
in the cold chain, with information in a predesigned format.23
All the samples collected after the fifth day of illness were
tested for the presence of DENV-specific immunoglobulin
M (IgM), by enzyme-linked immunosorbent assay (ELISA),
using a kit developed by the National Institute of Virology
(NIV), Pune, India as per the manufacturers protocol. The
samples collected in the acute phase of illness (in the first 5
days) were tested either for the presence of nonstructural (NS1)
protein by using the dengue day 1 diagnostic test (DENGUE
DAY1 TEST, J Mitra and Co. Pvt. Ltd. New Delhi, India) and/
or by nested reverse transcription polymerase chain reaction
(nRT-PCR),24 with minor modification.25 The PCR products
were sequenced to identify genotypes, using the basic local
alignment search tool.25
For diagnosis of chikungunya, samples were referred from
all over the state. These samples were tested for the presence
of CHIKV IgM antibodies, using a kit manufactured by NIV,
Pune. The samples collected in the acute phase of illness were
subjected to RT-PCR, as described by Naresh et al. (2007).26
A few, randomly picked, dengue-negative samples were also
tested for the presence of CHIKV IgM and the PCR products
were sequenced.
Data analysis
The demographic and clinical information of patients was
double-key entered into Microsoft Excel 2007. All records were
validated and all inconsistencies and differences were resolved
before analysis. Statistical analyses were performed using
STATA 12 for Windows (StataCorp LP, Texas, United States of
America). Categorical data are presented as frequency counts
(%) and compared using the 2 or Fishers exact statistic as
appropriate. Odds ratios (ORs) and 95% confidence intervals
(CIs) were also presented for 22 contingency tables. The
significance level was considered alpha = 0.05 and at 95%
confidence level.
Study definitions
The slide positivity rate (SPR) was defined as the number of
malaria parasitaemic cases, divided by the total number of
blood smears made. The slide falciparum rate (SFR) and slide
vivax rate (SVR) were defined as the number of falciparumand vivax-infected cases respectively, divided by the total
number of blood smears made. The microfilaria rate was
calculated as the number of microfilaria-positive cases out of
the total number of blood smears examined.
RESULTS
Malaria slide positivity was 18.7% (190/1018), 16.4%
(372/2266) and 20.4% (104/509) respectively in the years
2011, 2012 and 2013. The age-specific and species-specific
data on malaria are shown in Table 2. Both P. vivax (16.1%;
107/666) and P. falciparum (82.3%; 548/666) were prevalent
in all age groups, with a few cases of mixed infection with
P. vivax and P. falciparum (1.2%; 8/666). Only three cases of
P. malariae were found. Young children between 1 and 4 years
of age showed the highest rate of parasite positivity. A decrease
in malaria positivity was recorded in relatively older children
in the age groups >4years to 8 years and >8 years to 14 years.
An additional decrease in malaria positivity was seen in older
children and adults (>14 years). Further analysis revealed
that the SVR was highest in infants (<1 year; OR = 3.8;
95% CI=1.5 to 9.4) when compared with adults (P<0.05).
However, the SFR was highest in young children >1 year to 4
years (OR=2.0; 95% CI=1.5 to 2.7) as compared to adults
(P<0.0001). The gametocyte rate was 20.8%, 21.1%, 11.9%,
10.6% and 4.2% in the age groups <1 year, >1 year to 4years,
>4 years to 8 years, >8 years to 14 years, and >14 years,
respectively. In adults, the gametocyte rate was significantly
lower than in other age groups (see Table 2).
Analysis of the distribution of malaria cases by species of
parasite and season revealed (data not shown) that P. falciparum
was the dominant species in all surveys. The SFR was highest
(25%) in the post-monsoon season (OR=3.1; 95% CI=2.0 to
4.9), followed by winter (24%; OR=2.9; 95% CI=2.1 to 4.0),
and lowest in monsoon (10 %). Year-wise analysis revealed
that SPR and SFR increased from 18.7% and 14.9% in 2011
to 20.4% and 19.1% in 2013, though the difference was not
statistically significant. The proportion of P. falciparum
increased from 80% in 2011 to 93% in 2013 (OR=1.3, 95%
CI=1.0 to 1.8). The prevalence of splenomegaly was 35.5%
(338/950) in 2012, which increased to 40.6% in 2013 (67/165).
The average spleen enlargement was 1.82.
For lymphatic filariasis, 3016 individuals were screened during
three surveys carried out in Panna district (see Table 3). The
microfilaria rate was 7.5%, 7.6% and 7.8% respectively in the
31

Table 2: Malaria positivity in the study area of Anuppur district (20112013), according to age and species
Age group
(years)
+ve/BSE (SPR)
Pf (SFR)
Pv (SVR)
PfG rate
1
>14
>48
>814
>14 years
31/141 (22.0)
110/459 (24.0)
162/807 (20.1)
228d/1289 (17.7)
135/1097 (12.3)
24 (17.0)
90 (19.6)
134 (16.6)
188 (14.6)
120 (10.9)
7 (5.0)
20 (4.4)
28 (3.5)
37 (2.9)
15 (1.4)
20.8
21.1
11.9
10.6
4.2
Malaria
2.0 (1.3 to 3.1)b
2.2 (1.7 to 3.0)c
1.8 (1.4 to 2.3)c
1.5 (2.2 to 1.9)b
1 (reference)
Odds ratio (95% CI)

P. falciparum
P. vivax
1.7 (1.0 to 2.7)a 3.8 (1.5 to 9.4)a
2.0 (1.5 to 2.7)c 3.3 (1.7 to 6.5)b
1.6 (1.2 to 2.1)b 2.6 (1.4 to 4.9)a
1.4 (1.1 to 1.8)b 2.1 (1.2 to 3.9)a
1 (reference)
1 (reference)
PfG
6.0 (1.5 to 24.0)b
6.1 (2.1 to 17.9)c
3.1 (1.1 to 8.9)a
2.7 (1.0 to 7.6 )a
1 (reference)
+ve: malaria parasitaemic cases; BSE: blood slide examined; CI: confidence interval; odds ratio: odds ratio; Pf: Plasmodium falciparum; Pfg rate:
Plasmodium falciparum gametocytes rate; Pv: Plasmodium vivax; SFR: slide falciparum rate; SPR: slide positivity rate; SVR: Slide vivax rate.
a
P<0.05.
b
P<0.01.
c
P<0.0001.
d
3 Plasmodium malariae.
Table 3: Microfilaria rates from Panna district (20102013)

Year
2010
2012
2013
Odds ratio (95% CI)
Male
+ve/screened
Female
+ve/screened
36/394
56/659
66/759
15/281
25/416
33/507
Microfilaria positivity rate (95% CI)

Male
Female
9.1 (6.5 to 12.4)
5.3 (3.0 to 8.6)
8.5 (6.5 to 10.9)
6.0 (3.9 to 8.7)
8.7 (6.8 to 10.9)
6.5 (4.5 to 9.0)
1 (reference)
1.5 (1.1 to 2.0)a
+ve: microfilaria positive; CI: confidence interval.

a
P<0.01.
Table 4: Dengue cases detected from Narsinghpur district in 2013
Age groupa (years)

015
1625
2645
46 and above
+ve/sample tested
9/32
9/28
23/54
7/26
Positivity rate (95% CI)

28.1 (13.8 to 46.8)
32.1 (15.9 to 52.3)
42.6 (29.2 to 56.8)
26.9 (11.6 to 47.8)
Odds ratio (95% CI)

1.1 (0.3 to 3.4)
1.3 (0.4 to 4.2)
2.0 (0.7 to 5.7)
1 (reference)
CI: confidence interval.

a
Age of one patient is not known.
years 2010, 2012 and 2013. Both sexes were infected but the
overall microfilaria rate was higher in males (8.7%) as compared
to females (6.4 %). This difference was statistically significant
(OR=1.5; 95% CI=1.1 to 2.0; P<0.01). Monitoring of drug
distribution and compliance revealed that coverage was 43%
and the compliance rate was 19%.
For dengue, 31 samples were referred from Narsinghpur
district in 2011, of which 48% were positive (DENV-1 and
DENV-4). In 2012, a total of 123 samples were referred and,
of these, 59% were positive (DENV-1), while in 2013, 141
samples were tested, of which 34% were positive (DENV-3).
Further analysis revealed that adults in the age groups 2645
years had the highest numbers of dengue cases, as compared
to other age groups, although this was not statistically
significant (see Table 4). It was interesting to note that about
5% of dengue-positive cases were admitted to the tertiary care
government hospital at Jabalpur (referral hospital) in 2011 and
2012 when DENV-1 and DENV-4 were detected, while 50%
of dengue patients were admitted to tertiary care for treatment
when DENV-3 was detected. Analysis further revealed that
32
the DENV-1 (genotype III) in 2011 and 2012 and DENV-3

(genotype III) in 2013 were circulating in the area.
For CHIKV infection, out of 364 tested samples, 20 were found
to be positive. Nine samples were found positive by nRT-PCR.
The sequencing and phylogenatic analysis revealed that the
virus belonged to the East Central South African genotype. In
the years 2011 and 2012, all the positive cases reported were
from Jabalpur district, whereas in 2013, two chikungunya
cases were detected in the samples referred from Mandsaur
district of west Madhya Pradesh, while two cases were among
travellers returning from the southern part of India.
DISCUSSION
The morbidity and mortality associated with VBDs pose a
growing problem for global public health. Studies such as the
current one are crucial for understanding the dynamic nature of
malaria, lymphatic filariasis, dengue and chikungunya, in this
extremely heterogeneous epidemiological landscape.
The risk of malaria within the country varies dramatically, as

several distinct malaria ecotypes exist. Forest malaria is a wellcharacterized ecotype associated with high transmission of
malaria.4 In this study area, malaria transmission is perennial,
with both P. vivax and P. falciparum present in all surveys.
More than 45% of cases were reported in children aged less
than 8 years and 34% cases were reported in children aged
between 8 years and 14 years. Only 20% of infections were
found in older children and adults. The number of malaria
cases and age groups indicated that the risk for the age group
under 8years was two times greater than in older age groups,
as recorded earlier.4 There is evidence that, as transmission
intensity increases, the age of peak morbidity decreases.27,28
Interestingly, a recent study reported a shift in the mean age
of malaria cases after introduction of intervention measures
in Orissa (long-lasting insecticidal nets [LLINs] + ACT).29
In spite of high malaria positivity, the insecticide-treated nets
(ITNs)/LLINs are not distributed, nor is the area sprayed with
synthetic pyrethroid. Only two rounds of DDT were sprayed,
and resistance to this insecticide is common among vectors.30
It is worthwhile to mention that tremendous progress has been
made in some countries in reducing malaria-related morbidity
and many countries are striving for elimination of malaria.31
Amidst this progress, a major challenge is in forested areas,
which are not approachable throughout the year and which
are dominated by socioeconomically disadvantaged people of
tribal origin.32 These high-risk populations may carry infection
from their workplace to their villages,33 or may be at higher risk
of infection because of behavioural factors. Moreover, a large
proportion of people are sleeping in the forest unprotected,
particularly during October to December, when falciparum
transmission is highest.34 Although the feeding behaviour
of vectors was not studied in this area, earlier studies have
revealed that vectors bite both indoors and outdoors.4 Malaria
control remains difficult if foci are located in forested areas,
owing to the complexities of human behaviour and of scaling
up malaria-control measures. Several independent studies
have reported that the incidence of malaria in the country is
grossly underestimated.35,36 This is mainly due to lack of proper
surveillance, particularly in remote areas.
Lymphatic filariasis is in the elimination phase in several
countries, including India. However, the rates of microfilaria
recorded in this study showed that this area is still highly endemic
for filariasis after the eighth round of mass drug administration.
Records revealed that four rounds of mass drug administration
were carried out with diethylcarbamazine (DEC) alone, with
a further four rounds with DEC + albendazole. Available
literature reveals that five or more rounds of a good compliance
rate of mass drug administration reduce the microfilaria rate to
below 1%, where it is expected that transmission ceases.37,38
Overall, the microfilaria rate of Panna district is 1%,
according to the state VBD control programme. However,
foci and hot spots for filaria are still present, from where it can
spread to areas that are currently free of filaria transmission.
To stop transmission, the mass drug administration should be
with DEC +albendazole, with more than 60% compliance.
The present study shows the need to improve the delivery
system of drugs and to strengthen information, education and
communication (IEC) and behaviour-change communication

(BCC) for better drug compliance.39
Moreover, Panna district is also endemic for malaria19 and,
recently, 16 samples were referred for dengue, of which 56%
were positive for DENV-3.
Dengue is the fastest re-emerging arboviral infection transmitted
by Aedes mosquitoes.40 The four antigenically distinct
dengue viruses (DENV-1 to -4) cause a wide range of signs
and symptoms, with marked differences in clinical severity,
ranging from asymptomatic infections to undifferentiated
fever, dengue fever, dengue hemorrhagic fever and dengue
shock syndrome.40 The four serotypes of DENV showed wide
variation over time in epidemiology and clinical presentation.
Moreover, besides differences in serotypes, other factors such
as sequence variation and primary and secondary infections
are known to influence the clinical manifestations.41 The
incidence of dengue is increasing worldwide, in terms of both
the number of reported cases42 and the number of countries
where the disease is emerging or re-emerging.10 There are
many reasons for the increase in reported cases: the spread of
disease is enhanced by frequent international travel, thereby
increasing the movement and exposure of viraemic people;
increasing urbanization, which favors manmosquito contact;
and, above all, ineffective vector-control measures.43 It is
worth mentioning here that Narsinghpur is not only endemic
for dengue; evidence of lymphatic filariasis was also found in
this district, which was non-endemic earlier.22
Historically, CHIKV too has been documented to be circulating
in central India for over half century and the virus was isolated
from both human and mosquitoes from Nagpur city in 1965.44
The present study, conducted over the last 3years, confirms the
circulation of CHIKV in the central part of India. Although this
study has the limitation of small sample size and a low number
of referred samples, it underlines that the ECSA genotype of
CHIKV is in circulation in Madhya Pradesh; it is important to
monitor the virus activity, as CHIKV is known to spread very
fast, especially in immunologically naive populations, and can
cause long-lasting arthritis resulting in clinical complications.
To conclude, malaria, lymphatic filariasis, dengue and
chikungunya are all transmitted by mosquitoes and, in areas
where more than one disease is endemic, these diseases
can be potentially controlled by the same interventions or
strategies.45 Despite recent advances for potential vaccines
and new therapeutic options, the control of VBDs remains
difficult.40 Therefore, interruption of transmission still relies
on vector-control measures. This suggests the need for a
better coordinated, multi-disease strategy for vector control,
wherever these diseases are endemic.45 Vector control through
the use of physical, biological and chemical methods is an
important component of prevention of VBDs. However, these
methods face several obstacles, in particular the development
of insecticide resistance in the vectors and the drastic reduction
of chemicals available for public health. WHO encourages
adoption of the integrated vector-management strategy, which
is a rational decision-making process for optimal use of
available resources. One of the key features of integrated vector
33
management is capacity-building at the operational level, to

plan, implement, monitor and evaluate vector control and its
epidemiological and entomological impact. To improve the
coverage and utilization of interventions, a regularly updated,
interactive, comprehensive and sustained national advocacy
(IEC/BCC) campaign is required.
Acknowledgements
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34
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support under the Indian Council of Medical Researchs VDL
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How to cite this article: Singh N, Shukla M, Chand G, Barde

PV, Singh MP. Vector-borne diseases in central India, with
reference to malaria,filaria, dengue and chikungunya. WHO
Source of Support: State Tribal Welfare Department, Government of
Madhya Pradesh; Department of Health Research, Government of India;
Ministry of Health and Family Welfare and Indian Council of Medical
Research, New Delhi, India. Conflict of Interest: None declared.
Contributorship: NS conceived the idea; NS, GC and PVB designed
the study and prepared the manuscript; MS, GC and PVB did field and
laboratory investigations; MPS did the data analysis and interpretation of
results. All authors read and agreed upon the manuscript.
35
Original research
DOI: 10.4103/2224-3151.115828
Co-circulation of dengue virus

serotypes with chikungunya virus in
Madhya Pradesh, central India
Pradip V Barde1, Mohan K Shukla1, Praveen K Bharti1,
Bhupesh K Kori1, Jayant K Jatav2, Neeru Singh1
Abstract
Background: Dengue and chikungunya present with very similar signs and
symptoms in the initial stage of illness and so it is difficult to distinguish them
clinically. Both are transmitted by Aedes aegypti and Aedes albopictus mosquitoes.
This study was conducted with the aim to explore the co-circulation of dengue and
chikungunya viruses in central India.
Materials and methods: Samples from suspected dengue cases were subjected
to dengue immunoglobulin M (IgM) enzyme-linked immunosorbent assay (ELISA)
and dengue-negative samples were tested with chikungunya-specific IgM ELISA.
The samples collected in acute phase of illness were tested by nested reverse
transcription polymerase chain reaction (nRT-PCR). Chikungunya virus (CHIKV)
sequences were analysed to determine their genotype.
Regional Medical Research Centre

for Tribals (ICMR), Jabalpur,
Madhya Pradesh, India.
2
Netaji Subhash Chandra Bose
Medical Collage, Jabalpur,
Madhya Pradesh, India.
1

Dr N Singh, Regional Medical
Research Centre for Tribals (Indian
Council of Medical Research),
Nagpur Road, Post Garha,
Jabalpur 482003, Madhya Pradesh,
India.
Email: neeru.singh@gmail.com;
rmrctjabalpur@rediffmail.com
Results: Of 138 samples screened for dengue, 21 (15.2%) were positive, and of
119 samples screened for chikungunya, 13 (10.9%) were positive. Dengue viruses
1 and 4 were found co-circulating with chikungunya virus in Jabalpur, central
India. The chikungunya virus detected belonged to the East Central South African
genotype.
Conclusion: Accurate and timely diagnosis would help in patient management
and use of resources. It is advocated to simultaneously test samples for these two
diseases in endemic areas. This will also aid in understanding the epidemiology
of chikungunya.
Key words: Central India, chikungunya, co-circulation, dengue
Introduction
Arthropod-borne viral infections cause major disease burden in
tropical and subtropical countries worldwide. The incidence of
dengue has increased more than 30-fold in the last 50 years.1 It
is estimated that about 100 million dengue cases and over 390
million infections occur worldwide annually.1,2 India contributes
about 34% of these cases.2 Four antigenically related serotypes
of dengue virus (DENV), with different genotypes, are known
to be circulating in India.3 All four serotypes can cause simple
febrile illness (DF), which may lead to more complex clinical
outcomes such as dengue hemorrhagic fever (DHF), dengue
shock syndrome (DSS) or death.4 Chikungunya re-emerged in
2005, after a gap of 32 years, with about 1.4 million cases, and
36
continues to circulate in India,4 with a predominance of the East

Central South African genotype of virus.5, 6 Dengue-confirmed
and chikungunya-suspected cases have been reported from
this part of the country in the recent past.4 Infection with the
chikungunya virus is generally self-limiting but in a few cases
it may cause severe incapacitating arthralgia in small joints,
lasting up to 6 months or more.4
DENV and CHIKV are both transmitted by Aedes aegypti
and Aedes albopictus mosquitoes. In the initial stage of
illness, both diseases present with a similar set of clinical
symptoms, such as sudden onset of high-grade fever, muscle
and joint pain, headache, nausea and vomiting, and rash,4
making differential diagnosis difficult clinically. Chikungunya
Barde et al.: Co-circulation of dengue and chikungunya viruses
has low/no mortality, whereas for dengue, mortality may go

up to 35% in outbreak situations and serious cases, though
early referral and good management can reduce this. In the
absence of any licensed vaccine for either of these diseases,
timely intervention by prompt accurate diagnosis, along with
mosquito control, are the best tools for controlling or avoiding
outbreaks in endemic areas.
Ethical approval
Samples were referred to this virology laboratory for diagnosis
of diseases and thus considered as part of the public health
response; nonetheless, the project Establishment of Grade II
Virology Laboratory had ethical clearance from the institution
ethics committee of RMRCT, Jabalpur, India.
Chikungunya can spread with ease and causes a high

percentage of clinical cases with a very high attack rate in an
immunologically naive population.7 However, chikungunya
is overshadowed by dengue in outbreak situations and in
dengue-endemic areas.8 Diagnosis of chikungunya is equally
important, as it would help to estimate the disease burden
and, in turn, help with designing intervention strategies. Cocirculation and coinfections of these two viruses are reported.5
This study sought to confirm the co-circulation of the two
viruses in central India, using serological and molecular tools.
Samples and testing

This year-round (April 2011 to March 2012) study was
conducted in Madhya Pradesh. Blood samples of patients
reporting to health-care units of Jabalpur and the adjoining
14 districts, with symptoms of dengue and chikungunya,
as defined by NVBDCP,4 were collected by clinicians and
referred for diagnosis to the virology laboratory of RMRCT,
along with clinical and demographic information in the World
Health Organizations (WHOs) predesigned format.9 Upon
receipt, serum was separated by brief centrifugation at 4oC
and was preferably tested on same day by immunoglobulin M
(IgM) enzyme-linked immunosorbent assay (ELISA) or nested
reverse transcription polymerase chain reaction (nRT-PCR).
Materials and Methods

The virology laboratory of the Regional Medical Research
Centre for Tribals (RMRCT), Jabalpur is recognized as the
Apex Referral Laboratory by the National Vector Borne Disease
Control Program (NVBDCP) for dengue and chikungunya, for
Madhya Pradesh and Chhattisgarh.
The testing sequence for the samples is shown in Figure 1.

All the samples were tested by dengue-IgM-specific ELISA;
DENV-ELISA-negative samples were tested by chikungunya
IgM ELISA, using kits manufactured by the National Institute
Total
sample
n=138
Acute phase
sample n=25
DEN nRT-PCR
DENV IgM
ELISA n=138
n=19
Positive
n=119
Negative
n=06
Positive
n=19
Negative
CHIK RT-PCR
n=19
CHIK IgM
ELISA n=119
n=06
Positive
n=113
Negative
n=09
Positive
n=10
Negative
Figure 1: Flowchart depicting the methodology of processing the samples

ELISA: enzyme-linked immunosorbent assay; CHIKV: chikungunya virus; DENV: dengue virus; IgM:
immunoglobulin M; nRT-PCR: nested reverse transcription polymerase chain reaction
37
of Virology, Pune, India, as described by manufacturer. A

subset of samples, which were collected in the acute phase of
illness, were also subjected to DENV nRT-PCR,10 for detection
of DENV RNA and the DENV serotype. Of these, samples for
which the DENV nRT-PCR result was negative were subjected
to CHIKV-specific RT -PCR,11 with minor modifications. The
PCR products were extracted and sequenced as described
earlier.12 The sequences were analysed for their homologies,
using the basic local alignment search tool, and representative
sequences were submitted to GenBank. The partial nucleotide
sequence of CHIKV envelop gene 1 (E1) was compared with
14 sequences of CHIKV strains from the National Center for
Biotechnology Information (NCBI) database from Asia and
Africa. Multiple sequence analysis was done using CLUSTAL
W software and the p-distance Neighbor Joining phylogenetic
tree was generated using Molecular Evolutionary Genetics
Analysis (MEGA), version 5, with application of 1000
bootstrap replicates.13
The data were double-key entered into Microsoft Excel.
Single-sample proportion testing and logistic regression were
done using SPSS version 20.
Results
One hundred and thirty-eight samples from 15 districts of
Madhya Pradesh were screened for dengue (see Figure 1). Of
these, 63 (46%) patients were from rural areas; 85 (62%) were
male and 53 (38%) were female. The results for age, sex and
screening tests for diagnosis of dengue and chikungunya are
given in Table 1. A total of 15.2% (21/138) were positive for
dengue and 10.9% (13/119) were positive for chikungunya.
Single-sample testing confirmed that there was no significant
difference between these two proportions (P=0.117).
Most of the patients, where infection was suspected 112
(81%) had fever (100103oF) for more than 2days, with
associated symptoms such as headache, body ache, joint pain,
fatigue and nausea. Hepatomegaly was seen in 18 (13%) cases.
The platelet count was available for 42 patients, of whom 26%
had thrombocytopenia (platelet count <105/mm3). No cases of
DHF, DSS or death were noted. Statistical analysis revealed
no significant difference in initial symptoms such as fever in
confirmed cases of dengue and chikungunya.
Out of 138 samples tested, 21 (15.2%) were found to be positive
for dengue, from four districts, namely Jabalpur (DENV-
1 and DENV-4), Katni (DENV-4), Panna and Narsinghpur

(DENV-4). Of the 21 dengue-positive cases, 15 were only
IgM ELISA positive, two were only RT-PCR positive and four
samples were positive on both tests.
The nRT-PCR and sequencing results confirmed that DENV-1
(n=1) and DENV-4 (n=6) were circulating in and around
Jabalpur, central India. Most of the confirmed cases of dengue
and chikungunya were detected in the monsoon and postmonsoon periods.
DENV-1 was first identified in central India and the sequence
showed that it was closely related to the DENV identified from
New Delhi (JF 815209.1). DENV-4 identified in this study
had sequence homology with DENV-4 identified in 2010
(GenBank: JF929180).12
Out of 119 dengue-negative samples, 13 (10.9%) were positive
for chikungunya. All chikungunya-positive samples (n=13)
were from Jabalpur district. Six samples were IgM ELISA
positive and nine were RT-PCR positive; of these, two samples
were positive on both tests. The phylogenetic analysis carried
out using nucleotide sequences established that CHIKV from
Jabalpur belonged to the East Central South African (ECSA)
genotype (see Figure 2), with close sequence homology with
isolate from Delhi (GenBank: JN048826).
It was noted that, in the case of dengue, the positivity was higher
among males (16/85; 19%) as compared to females (5/53; 9%),
though the difference was not statistically significant. In the
case of chikungunya, no such difference was observed. After
adjusting for the sex of cases, the positivity of dengue was
significantly higher among adults (age 16 years and above)
when compared to children (15 years; odds ratio [OR]=31.1;
95% confidence interval [CI]=6.8 to 142.8; P<0.01) but in
the case of chikungunya, this difference was not significant
(OR=1.5; 95% CI=0.44 to 5.5; see Table 1).
Discussion
DENV-3 was detected during an outbreak that occurred
at Jabalpur in 1966.14 However, dengue and chikungunya
remained neglected diseases in this part of country, with very
few studies focusing on these infections.4,12,15 Because of the
emergence of different serotypes and their genotypes, dengue
epidemiology is continually changing, posing challenges to
clinicians and health authorities. CHIKV re-emerged in 2005,
Table 1: Age and sex distribution of the suspected and confirmed cases of dengue and chikungunya
Age group
(years)
0 to 15
16 and above
Total
Suspected casesa
M
54
31
85
F
38
15
53
T
92
46
138
Dengue positive
by sex
M
F
0
2
16
3
16
5
Dengue positive by
screening method
ELISA nRT-PCR
T
2
nil
2
17
6
23
19
6
21b
Chikungunya
positive by sex
M
F
4
5
3
1
7
6
Chikungunya positive
by screening method
T
ELISA RT-PCR
3
6
9
3
3
6
6
9
13b
ELISA: enzyme-linked immunosorbent assay; F: female; M: male; nRT-PCR: nested reverse transcription polymerase chain reaction; T: total.
a
Dengue-negative (n=119) samples were tested for chikungunya by ELISA and 19 by RT-PCR.
b
Four samples of dengue and two samples of chikungunya were positive by both tests.
38
India-06-HQ702750
64 India-11-JQ740183
India-10-JN048826
94
India-11-JX911895
India-06-FJ000068
83
68 Reunion-06-AM258993
Central Africa-84-HM045784
100
99 India-63-EF027140
Thailand-58-HM045810
Thailand-95-HM045787
84
92
Indonesia-10-AB678693
ECSA Genotype
Asian Genotype
} West African Genotype

Onyong-nyong-96-AF079456 } Outgroup
Senegal-66-AF192891
0.25
0.20
0.15
0.10
0.05
0.00
Figure 2: Phylogenetic tree of chikungunya viruses generated by the NJ method, using the p-distance model based on the partial nucleotide
sequence (266bp) of the E1 gene. Tree showing chikungunya virus detected in this study () belonging to East Central South African genotype.
Each strain is labelled with the country and year of isolation followed by GenBank accession number. Onyongnyong virus was used as the
outgroup
after a gap of almost 32 years, and made its presence felt in

India with more than one million cases.4 However, after the
epidemic, the medical fraternity neglected CHIKV infections,
probably because chikungunya is considered to be a disease
with mild morbidity and no mortalities. In contrast, dengue
is a disease with significant morbidity and mortality and is
endemic in the country.2 As reported earlier,4 and also seen in
this study, the initial symptoms of chikungunya are similar to
those of dengue and both are transmitted by same vectors Aedes
aegypti and Aedes albopictus. Probably because of the severity
of dengue, both clinicians and public health officials focus on
this disease, and samples are sent to laboratories with requests
for diagnosis of dengue only. The present study demonstrates
that DENV and CHIKV are co-circulating in Jabalpur, and
there is no significant difference in the positivity for the two
diseases. Although this study has a limited number of samples,
it emphasizes the importance of chikungunya diagnosis, as
there is no significant difference in the positivity of samples
for the two diseases.
Serological tests (ELISA) have demonstrated the presence
of dengue and chikungunya from central India in the recent
past.4,12,15 With establishment of the Viral Diagnostic Laboratory,
it was possible to provide molecular diagnosis of DENV, with
identification of the serotype, and to conduct characterization
studies on CHIKV, which lead to identification of DENV
serotype 1 and CHIKV ECSA genotype (see Figure 2).
It is known that, before 1973, the Asian genotype was
circulating in India and was subsequently replaced by the
ECSA genotype.4,5 This study documents, for the first time,
circulation of the ECSA genotype in this part of India. It will be
interesting to isolate and further characterize these circulating

viruses for better epidemiological understanding.
In an endemic area like India, where multiple DENV serotypes
are circulating with CHIKV, the possibility of concurrent
infection occurs.4 An earlier study reported the presence
of DENV serotype 4 in central India;12 detection of another
serotype (DENV-1) is alarming. There is some evidence
that infection with multiple DENV serotypes, or coinfection
with other pathogens, may produce a severe outcome of the
disease.16,17 An early and accurate diagnosis can help clinicians
to decide the course of treatment.
The presence of IgM for DENV and CHIKV can only be
detected around the fifth day of infection; the tests such as
nonstructural protein (NS1) detection for DENV and RT-PCR
for both these viruses to detect virus antigen/RNA should be
preferred. As apparent in the present study, although based
on a small sample size, the early symptoms cannot clinically
distinguish between dengue and chikungunya; thus, we
advocate early and simultaneous testing of samples for DENV
and CHIKV.
Acknowledgements
The authors are grateful to the Secretary to the Government
of India, Department of Health and Research, Ministry of
Health and Family Welfare, and The Director-General, Indian
Council of Medical Research, for financial support under the
project Establishment of Grade II Virology Laboratory.
The financial support and the kits provided by the National
39
Vector Borne Disease Control Programme, New Delhi, India

is acknowledged. Help from Dr RK Sharma for statistical
analysis and technical help from Virology Laboratory staff
of the Regional Medical Research Centre for Tribals is also
acknowledged
2.
3.
4.
5.
6.
7.
8.
9.
10.
40
12.
13.
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Gubler DJ. Epidemic dengue/dengue hemorrhagic fever as a public

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Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI. The
global distribution and burden of dengue. Nature. 2013;25:5047.
Chakravarti A, Arora R, Luxemburger C. Fifty years of dengue in India.
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India, Ministry of Health & Family Welfare. National Vector Borne
Disease Control Program. New Delhi: Directorate General of Health
Services. http://nvbdcp.gov.in - accessed 27 February 2014.
Chahar HS, Bharaj P, Dar L, Guleria R, Kabra SK, Broor S. Coinfections with chikungunya virus and dengue virus in Delhi, India.
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Bedno S, Burke H, Dumilla AM, Konde J, Njenga MK, Sang R, Breiman
RF. Seroprevalence of Chikungunya virus (CHIKV) infection on Lamu
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docstoc.com/docs/33070597/Guidelines-for-Treatment-of-DengueFeverDengue-Haemorrhagic - accessed 27 February 2014.
Lanciotti RS, Calisher CH, Gubler DJ, Chang GJ, Vorndam AV. Rapid
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Naresh Kumar CV, Anthony Johnson AM, Sai Gopal DV. Molecular
characterization of chikungunya virus from Andhra Pradesh, India &
phylogenetic relationship with Central African isolates. Ind Jour of Med
Res. 2007;126:534540.
Barde PV, Godbole S, Bharti PK, Chand G, Agarwal M, Singh N.
Detection of dengue virus 4 from central India. Ind Jour of Med Res.
2012,136, pp. 491494.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S.
MEGA5: Molecular Evolutionary Genetics Analysis using maximum
likelihood, evolutionary distance, and maximum parsimony methods.
Mol Biol Evol. 2011;28:27319.
Rodrigues FM, Pavri KM, Dandawate CN, Banerjee K, Bhatt PN. An
investigation of the aetiology of the 1966 outbreak of febrile illness in
Jabalpur, Madhya Pradesh. Ind Jour of Med Res. 1973;61:146270.
Ukey P, Bondade S, Paunipagar P, Powar R, Akulwar S. Study of
seroprevalence of dengue Fever in central India. Indian J Community
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Baba M, Logue CH, Oderinde B, Abdulmaleek H, Williams J, Lewis J,
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960329. doi:10.1155/2012/960329.
How to cite this article: Barde PV, Shukla MK, Bharti PK, Kori
BK, Jatav JK, Singh N. Co-circulation of dengue virus serotypes
with chikungunya virus in Madhya Pradesh, central India. WHO
Source of Support: The study was funded by the Indian Council of
Medical Research (ICMR), under ICMRs Viral Diagnostic Laboratory
network project, and the Directorate of National Vector Borne Disease
Control Program, New Delhi provided kits for diagnosis of dengue and
chikungunya. Conflict of Interest: None declared. Contributorship: PVB
and NS designed the study and did literature search and writing. BKK and
PVB did data collection, data analysis, data interpretation and writing. JKJ
did sample collection, clinical diagnosis and treatment. PVB and MKS did
data analysis and interpretation (ELISA, nRT-PCR). MKS and PKB did
data analysis and interpretation (sequencing and sequence analysis) and
writing. All authors read and agreed upon the manuscript.
Original research
DOI: 10.4103/2224-3151.115828
Barriers to malaria control in rural southwest Timor-Leste: a qualitative analysis

Penny E Neave1, Maria L Soares2
Abstract
Department of Community Health

Development, Auckland University
of Technology, New Zealand
2
Childfund, Rua Governador,
Laserda de Maia, Vila
Verde, Dili, Timor-Leste
1
Background: Malaria is an important health problem in Timor-Leste. Although

funding has been provided to reduce the burden of this disease, few studies have
investigated whether this has improved malaria-related knowledge, management
of symptoms, and treatment in rural communities. The aim of this study was to
explore the perceptions and practices undertaken in relation to all aspects of
malaria control by members of two rural communities in Timor-Leste.
Methods: A qualitative study was undertaken in two rural hamlets in Timor-Leste.
Research methods included transect walks, focus groups and semi-structured
interviews. Content analysis was used to identify themes.

Penny Neave, AUT University,
Akoranga Drive, Northcote,
Auckland, New Zealand.
Email: pneave@aut.ac.nz
Results: The location of the hamlets near rice fields, leaking taps, inadequate
water supplies and dumping of waste from the local hospital provided opportunities
for mosquitoes to breed. Most participants were aware of the link between
mosquitoes and malaria, but a lack of control over their environment was a major
barrier to preventing malaria. The distribution of bed nets had occurred once, and
was the only intervention undertaken by the National Malaria Control Programme.
However, limiting the distribution of bed nets to pregnant women and children
aged under 5 years had resulted in some focus group respondents believing that
only those in these groups could be affected by malaria. Self-diagnosis and home
treatment were common. Treatment for unresolved infections depended on access
to transport funds, and belief in the power of traditional healers.
Conclusion: Improvements in infrastructure, empowerment of rural communities,
and better access to treatment are recommended if the incidence of malaria is to
be reduced throughout the country.
Key words: Access to treatment, empowerment, malaria, sanitation, Timor-Leste.
Introduction
Malaria is endemic throughout Timor-Leste, and over three
quarters of the population live in areas of high transmission.1
The majority (81%) of infections are caused by Plasmodium
falciparum and 19% by Plasmodium vivax.1 Although the
parasite prevalence may be in the range of 19%,2 there are local
and seasonal variations.3 Underreporting of cases, particularly
in rural areas, makes an accurate estimation of the incidence of
this disease problematic.2
There are nine species of anopheles mosquito that can transmit
malaria to humans in Timor-Leste. The two most common
are Anopheles barbirostris and Anopheles vagus genotype B.
The former breeds in large permanent bodies of water with
permanent vegetation.3 The preferred breeding habitats of

the latter are fresh and brackish swamps, and small plastic
containers, tyres and concrete drains.4
With the help of international funding, Timor-Lestes Ministry
of Health established the National Malaria Control Programme
in 2003. Interventions undertaken were both top-down (led
by government agencies) and bottom up (community led).
Among the former interventions, one priority was to establish
and strengthen health services that had suffered significant
disruption during the war with Indonesia. Others included the
wide distribution of bed nets to pregnant women and children
aged under 5years, and providing school- and communitybased education about malaria.
41
Neave et al.: Malaria in Timor-Leste
As part of its bottom up approach, the Ministry of Health

Integrated Community Health Services (SISCa) was
introduced throughout Timor-Leste. With a slogan of from,
with and to the community, the aim was to mobilise
community members to access basic healthcare services, with
the help of health volunteers working in the community.5
Only two previous studies have investigated how malaria is
managed in Timor-Leste following the implementation of the
National Malaria Control Programme.6,7 One of these focused
predominately on the use of bed nets,6 and the other discussed
the implementation of the grant given by the Global Fund to
Combat AIDS, Tuberculosis and Malaria.7 The latter study
reported that there had been an increase in knowledge about
malaria transmission in the country, and greater awareness of
the need for maintaining high levels of sanitation.7 However,
it is not known whether these improvements have been
experienced throughout the country. The aim of this study was
to explore the perceptions and practices undertaken in relation
to all aspects of malaria control by members of two rural
communities in Timor-Leste.
methods
Ethical approval to carry out the study was obtained from the
Auckland University of Technology Ethics Committee, and
accepted by the District Health Service Ethics Committee in
the area of Timor-Leste in which the study was conducted.
All study participants gave written informed consent before
participating.
The exact location of the study is not provided, to ensure
anonymity of the respondents. It was set in two hamlets in a
rural area of south-west Timor-Leste. One was approximately
8km, and the other 12km away from the nearest health clinic,
where individuals with suspected malaria could be tested and
receive treatment. One researcher chose the area in which to
carry out the study, based on her familiarity with this district.
This researcher was native to Timor-Leste, spoke Tetum (the
national language) fluently, was familiar with local customs
and had previously worked on malaria-control campaigns
in the country. Previous work undertaken by this researcher
in this region had suggested that knowledge of malaria in
the community was poor, but regional reported malaria data
suggested that the incidence rate was lower in this area than in
other districts in the country.
Before data collection commenced, meetings were arranged
with national, regional and local government officials, to gain
support for the study. They provided details of local health
volunteers, and the head of each hamlet, who would be asked
to facilitate the research.
Transect walks
To evaluate the potential for mosquito breeding in the
community, transect walks were carried out with the assistance
of a guide, who also answered questions. Transect walks are
journeys taken through a community, and can be used to explore
local sanitation conditions. During the walk, photographs were
42
taken of the local environment and the bedrooms of some

houses, to demonstrate how bed nets were hung and their state
of repair. Maps of each hamlet were drawn, showing potential
mosquito breeding sites.
Focus group discussions

Focus groups were organized in each hamlet. Health volunteers
informed community members about the study and encouraged
participation. Interested participants contacted the hamlet
leader or health volunteer, and their contact details were passed
to the researcher. Each was given a week to decide whether
they wished to take part.
Semi-structured interviews
The hamlet leaders (one from each hamlet) and the traditional
healer from one hamlet were invited to take part in semistructured interviews. The other hamlet did not have a
traditional healer working there.
Topics covered in the interviews and focus groups comprised:
knowledge about malaria transmission and symptoms; actions
taken to diagnose and treat malaria; and knowledge about the
national malaria-control programme.
Interviews were recorded using a digital recorder, with the
exception of the interview with one head of hamlet, who
requested written notes to be taken instead. Focus groups and
interviews were carried out in Tetum, transcribed verbatim and
translated into English by one of the authors.
For the analysis, the data from the transect walks, focus groups
and semi-structured interviews were categorised into five main
themes, using content analysis: malaria transmission sites in
each hamlet; knowledge of malaria transmission; prevention
of mosquito bites; symptoms of malaria; and appropriate
treatment. All responses that corresponded to one of these
themes were collated by one author, and reviewed by the other
to ensure agreement.
Results
Transect walks, focus groups and semi-structured interviews
were carried out in July 2012 and each lasted about an hour.
One focus group was conducted in the local school, and the
other in the home of the hamlet head. One was attended by
three women and four men and the other was attended by five
women and two men. Study participants were subsistence
farmers, or individuals who gained an income from selling
firewood or from making and selling traditional clothes. Three
semi-structured interviews were conducted and these were
carried out in respondents homes.
The age of the participants of this study ranged from 20 to
70 years. One village had approximately 60 households, and
the other about 80 households. Most family houses consisted
of three bedrooms. The average number of occupants per
household in the first hamlet was 4.5 and in the second hamlet
was 5.3.
Sites suitable for malaria transmission

Rice fields
From the transect walks, it was observed that, in both hamlets,
rice fields were located close to households. Slow-moving
water, algae and small irrigation channels connecting river
water to these channels provided sites for mosquitoes to
breed. The village guide explained that some farmers irrigated
their rice field during the night, when many mosquitoes were
prevalent.
Lack of suitable water supply and drainage systems
In the first hamlet, water provided for the community ran from
a communal tap continuously, as it could not be turned off,
although the head of one hamlet explained he had made repeated
requests for the tap to be mended. In the second hamlet, one
well served nearly 400 people. Many individuals from both
hamlets used the river, a distance of several kilometres away,
to wash clothes or collect water. The transect walks revealed
that irrigation channels along the river path provided sites for
mosquitoes to breed, and on the banks of the river there were
pools of stagnant water.
Some houses lacked toilets, necessitating the use of outdoor
areas near to mosquito-breeding sites.
Disposal of rubbish
In the first hamlet, some households used a nearby rubbish tip.
Others buried their rubbish or burned it. However some noncombustible items, such as cans and bottles, provided sites for
mosquitoes to breed. Rubbish was scattered along the side of
the road, by community members and by residents of other
hamlets, as well as by the local hospital, which used an area
near to one of the hamlets as a dumping site for hospital waste.
Many participants explained that an initiative to clean the local
environment must be made directly from the hamlet head.
Without this, no action would be taken. This was confirmed by
the heads of each hamlet.
Knowledge about malaria transmission

Some focus group members referred to their lack of education
to justify why they did not know in detail how malaria was
transmitted, but all respondents recognized the importance
of avoiding mosquitoes and were aware of the link between
stagnant water and malaria.
The traditional healer attributed spiritual reasons for malaria
infections, which he said resulted from current or past misdeeds,
or not caring for an ancestor. He considered pregnant women
as being particularly susceptible because they had stopped
menstruating.
Prevention of mosquito bites

Common measures to prevent mosquito bites were killing
them by hand, covering of the body in the evening, or burning
tyres, dry cassava and cow dung to create smoke. Some people
who could afford to do so would also purchase anti-mosquito
creams and mosquito coils, although the sporadic income that
many received meant that creams and mosquito coils could not
be used throughout the year.
Nets had been given free of charge to pregnant women and
children aged under 5years, in both hamlets, 2 or 3years
previously, and the hamlet heads had played a role in their
distribution. Some families who received more nets than others
had shared them with others.
The distribution of bed nets was the only awareness
participants had of the National Malaria Control Programme.
All participants understood that sleeping under nets would
help to protect against being bitten by mosquitoes. However,
limiting the distribution of bed nets to pregnant women and
children under 5years of age had, unintentionally, resulted
in some focus group respondents believing that only those in
these groups could be affected by malaria. Others, as well as
the head of one hamlet, recognized that other family members
could also become ill with malaria, and argued that nets should
have been distributed more widely.
Despite wanting more nets, there was an acknowledgement
among participants that there was a lack of space to hang them.
Most houses contained three bedrooms but were occupied by
four to seven people.
There was some confusion about whether and how often nets
should be washed. Some repaired holes in nets, but others
threw them away if they became torn or damaged.
Symptoms and diagnosis

Most participants could name some common symptoms of
malaria. Others, including one of the hamlet heads, claimed
not to know the symptoms, as they did not believe they had
personal experience of these.
There were some discussions among participants about
whether it was possible to self-diagnose malaria from clinical
symptoms. Some believed they could self-diagnose, while
others recognized that a blood test was necessary for an
accurate diagnosis:
We got this disease but we dont know, therefore we go to the
hospital to get it tested . . . if we stayed at home then we didnt
know, so go to hospital to get blood tested then we will know .
. . if its malaria disease (focus group respondent).
Treatment seeking
Initial treatment of malaria-type symptoms would most
typically be carried out by the individual. Eating boiled
papaya leaves with noodles was popular, as it was believed
that the bitter taste would be effective. Some would purchase
analgesics or antibiotics from the nearby shop (within walking
distance) if they could afford it. No participant mentioned a
hospital visit as a first course of action.
43
If symptoms persisted, the options available were either to

visit the local hospital (where treatment was provided free
of charge) or to seek help from a traditional healer. A lack of
available cash for transport (the cost ranged from between
US$2 and US$4) was the reason voiced by many, including
hamlet heads, to explain why the latter action might be taken.
Access to money was described as particularly difficult at times
of the year when there were few crops to sell. The heads of
the hamlets had made unsuccessful requests to regional health
officers for a mobile clinic to make regular visits, and/or for a
local hospital to be built.
Not all respondents believed that traditional healers had a role
to play in the treatment of malaria. However, a few said that
some hospital doctors they had received treatment from did
believe in the power of traditional healers. They might advise
patients to visit one if their symptoms did not resolve in a
few days after treatment had started, so that spiritual barriers
that might be preventing its success could be overcome. The
spiritual healer confirmed he had been asked by a male nurse
to treat his wife, who had been admitted to hospital but had
not recovered. He also explained that people might come from
other hamlets to be treated by him, and that they might pay him
between US$2 and US$5.
Treatment by the traditional healer involved carrying out a
ceremony while sharing food and cigarettes, or killing animals:
Malaria can be treated through bringing betel nuts and giving
them to the spirit of the dead, then it will get healed. Kill a
chicken and feed the spirit of the dead people, then we will not
get it again (traditional healer).
Discussion
The aim of this study was to investigate knowledge, attitudes
and practices relating to malaria transmission, symptoms and
treatment in one small rural area of Timor-Leste after the
implementation of malaria programmes carried out in this
country to reduce the burden of this disease. The qualitative
methodology employed allowed exploration of concepts that
might be a barrier to malaria control. Further research using
quantitative methodologies would be necessary to determine
whether the results could be extrapolated to other rural
populations. Interviewing a range of respondents enabled a
diversity of views to be included, while the use of a transect
walk by a research team member with malaria expertise meant
that an independent evaluation could be made of the potential
for mosquitoes to breed in the vicinity.
Rather than poor knowledge about malaria transmission,
a lack of control over managing the sanitation in their local
environment appeared to be the predominant factor that
limited the ability of respondents to protect themselves
against mosquito bites. Specific problems mentioned were
the dumping of rubbish by the local hospital, for example of
receptacles in which mosquitoes could breed, and the lack of
response to repeated requests for improved water supplies. The
poor sanitary conditions were confirmed during the transect
walks. While Martins and colleagues have noted that some
success has been made by the first Global Fund grant to reduce
44
malaria-related morbidity and mortality in Timor-Leste,7 the

results of the research presented here suggest that a priority
for the country is still the strengthening of infrastructure,
the provision of waste disposal services and improved water
supply, including to remote rural areas. Interventions focusing
on increasing malaria-related knowledge without providing the
means to prevent mosquito bites are unlikely to be effective.
Only bed net distribution was mentioned as an intervention
by the National Malaria Control Programme, as well as the
fact that this had taken place on one occasion with no followup. Many respondents recognized the usefulness of bed nets,
and this is in line with the findings of Lover and colleagues.6
The confusion about who malaria could affect, an unintended
consequence of targeting pregnant women and children
aged under 5years, was also noted by Lover et al.6 Ongoing
educational sessions with local communities may overcome
this confusion, and could also be used to provide information
about the requirements for washing nets. A lack of trust of
outsiders may make this difficult. Although the researcher who
carried out the fieldwork was born in Timor-Leste, she noted
that several respondents described her amongst themselves
as an outsider or foreigner, and were reluctant to discuss
issues freely. The heads of hamlets could be a useful interface
between community members and health workers from outside
these areas, to ensure that information is understood and
trusted. There is also a need to involve community members
more in efforts to reduce malaria. Despite being aware of the
risks within their local environment, respondents appeared to
be reliant on interventions from outside, and no respondent
mentioned any bottom-up approaches to malaria control,
despite these being a specific aim of the National Malaria
Control Programme. Efforts to reduce the incidence of
malaria in other areas of the same region have shown that full
community engagement and commitment is a key component
to success,8,9 and could be replicated in Timor-Leste.
Responses to questions about the most effective diagnosis
and treatment of malaria also suggested perceptions of
powerlessness among some respondents. Some could not
seek a parasitological diagnosis and drug treatment because
of a lack of funds. Thus, the provision of free diagnostic tests
and treatment for malaria, implemented in Timor-Leste in
2007, remains outside the scope of people who are not able to
access it. However, the traditional healer mentioned that some
people would access his treatments by paying similar sums of
money to those they would spend on biomedical treatment.
Thus, financial difficulties alone could not explain why some
people resorted to supernatural treatments for malaria, and two
parallel beliefs in malaria etiology appeared to be common.
The finding that a belief in supernatural causes of malaria was
reported to be held by some medically trained staff highlights
the need to reinforce the importance of medical treatment with
these individuals, and, in particular, the need for laboratory
confirmation of suspected malaria. This is in order that other
causes of presenting symptoms can be ruled out, or treated.
Timor Leste is still in the malaria control phase.1 Thus,
the priority is to reduce the morbidity and mortality caused
by this disease, by preventive measures, accurate diagnostic
testing and treatment.9 The results of this study suggest that
there is still much progress to be made in rural areas. With

respect to prevention, bottom-up approaches could focus
more on enabling the community to take control of improving
sanitation within their local environment, ensuring they
understand the rationale for targeting particular groups with
bed nets, and explaining how nets can be maintained correctly.
Preventing rubbish entering the hamlets from other areas, and
providing access to accurate diagnostic tests and treatment,
as well as ongoing training of clinicians are important topdown priorities.
References
1.
2.
3.
4.
5.

report_2012/report/en/ - accessed 27 February 2014.
de Almeida A, et al. Malaria epidemiology in the Democratic Republic
of East Tim or. Asian Pacific Journal of Tropical Medicine. 2010;3:283287.
Bragonier R, et al. Rainy-season prevalence of malaria in Bobonaro
district, East Timor. Annals of Tropical Medicine and Parasitology.
2002;96(7):739-743.
Cooper RD, et al. Malaria vectors of Timor-Leste. Malaria Journal.
2010;9:40. doi:10.1186/1475-2875-9-40.
Timor Leste, Mnistry of Health. SISCa- Servisu Integradu da Saude
communitaria (Integrated Community Health Services). 2009. www.
6.
7.
8.
9.
10.
basicsorg/documents/13-SISCa-Guidilines.pdf - accessed 27 February

2014.
Lover AA, et al. An exploratory study of treated-bed nets in TimorLeste: patterns of intended and alternative usage. Malaria journal.
2011;10:199.
Martins JS, Zwi AB, Kelly PM. Did the first global fund grant (2003
2006) contribute to malaria control and health system strengthening in
Timor-Leste. Malaria Journal. 2012;11: 237.
Hung LQ, et al. Control of malaria: a successful experience from Viet
Nam. Bulletin of the World Health Organization. 2002;80(8):660-66.
Kaneko A. A community-directed strategy for sustainable malaria
elimination on islands: short-term MDA integrated with ITNs and robust
surveillance. Acta tropica. 2010;114(3): 177-183.
World Health Organization Overview of malaria elimination. Geneva:
WHO, 2013. http://www.who.int/malaria/areas/elimination/overview/
en/ - accessed 27 February 2014.
How to cite this article: Neave PE, Soares ML. Barriers to

malaria control in rural south-west Timor-Leste: a qualitative
analysis. WHO South-East Asia J Public Health 2014; 3(1):
4145.
Source of Support: Maria Soares received a scholarship from the
New Zeland AID Programme. Conflict of Interest: None declared.
Contributorship: PEN jointly conceived the study, advised on the study
design, jointly carried out data analysis and co-wrote the paper. MLS jointly
conceived the study, contributed to formulating the study design, carried out
the fieldwork and contributed to writing the paper.
45
Original research
DOI: 10.4103/2224-3151.115828
Dengue fever in a rural area of West Bengal,

India, 2012: an outbreak investigation
Dilip K Biswas1, Rama Bhunia2, Mausumi Basu3
Abstract
Deputy Chief Medical Officer of

Health-II, district Purba Medinipur,
West Bengal
2
Lady Duffrin Victoria Hospital,
Kolkata, West Bengal
3
Department of Community
Medicine, Institute of Post
Graduate Medical Education
and Research, (IPGME&R)
Kolkata, West Bengal, India
1
Background: During September 2012, an increased number of fever cases was

reported from Ramnagar-II block, Purba Medinipur district. This study investigated
the outbreak, with the following objectives: to describe the distribution of fever
cases, to determine the risk factors and to recommend preventive measures.
Materials and Methods: The clinical features, date of onset and outcome of
all cases of fever were listed. Blood specimens were collected from affected
patients and sent for serological examination. An epidemic curve was plotted and
environmental and entomological surveys were carried out.
Results: There was a total of 100 cases, of which 56% (56/100) were men. Among
the four villages studied, the highest number of cases was from Gopalpur 37%
(37/100), followed by Badalpur 26% (26/100); 19% (19/100) of cases had a history
of migration from dengue-endemic areas. The majority of cases were in age group
1545 years 52% (52/100), followed by the age group >45 years 28% (28/100).
All the cases had history of fever (100%), followed by myalgia 82%, headache
78%, and retro-orbital pain 73%. The outbreak started on 7 September 2012,
peaked on 18 September, then gradually declined and no further cases were noted
after 28 September 2012. Seventy-nine per cent (79/100) of cases were NS1 test
positive (non-structural antigen-1) and 72% (13/18) cases were positive on a
dengue monoclonal antibody (IgM) capture enzyme-linked immunosorbent assay
(MAC-ELISA) test. All recovered except one (case-fatality ratio: 1%). The values
for Household Index, Container Index and Breteau Index of the four villages were:
Badalpur, 3%, 10% and 5%; Gopalpur, 13%, 23% and 18%; Ramchandrapur, 9%,
11%, and 13%; and Tajpur, 2%, 2% and 2%.

Dr Dilip Kumar Biswas,
Welcome Housing, 228 Ashokegarh,
Kolkata-700108, West Bengal, India
Email: dilipbiswas29@gmail.com
Conclusion: The outbreak was probably due to dengue fever. The study led to a
recommendation to destroy water containers and use mosquito nets. The outbreak
was controlled.
Key words: dengue, outbreak, rural area, West Bengal
Introduction
Dengue is a mosquito-borne viral disease found in tropical
and subtropical regions.1 Over 2.5 billion people, 40% of
the world population, are at risk of dengue fever.2 According
to the National Vector Borne Diseases Control Programme
(NVBDCP), the number of cases in India has escalated
steadily, from 3306 in 2001 to 50 222 in 2012; deaths have
risen from 53 in 2001 to 242 in 2012.3 In West Bengal, 3306
confirmed dengue cases were reported from 1 January 2012 to
30 September 2012, of which nearly 2000 cases were recorded
from the Kolkata Metropolitan Corporation areas.4 Dengue
46
fever and dengue haemorrhagic fever are prevalent in urban

areas, as Aedes aegypti mosquito, the vector of dengue (family:
Culicidae; genus: Aedes, subgenus: Stegomyia; species:
Aedes aegypti), usually breeds in urban and peri-urban areas.5
Outbreaks of dengue fever have also been reported from rural
areas of India.6
The rapid growth of industries and building activities,
improvement of transport facilities such as railway and roads,
increased movement of people from urban to rural areas, and
environmental changes have all favoured the spread of dengue
in rural as well as urban areas.7, 8 An increase in the number
Biswas et al.: Dengue outbreak in West Bengal, India
of fever cases was reported from Ramnagar-II block of Purba

Medinipur district on 7 September 2012. This investigation
was carried out with the following objectives: (i) to confirm
the existence of an outbreak; (ii) to describe the outbreak
in relation to time, place and person; (iii) to determine the
etiology of the outbreak; and (iv) to recommend measures to
control the outbreak.

Ethical permission was not required for this research, since it
was an outbreak investigation. The data were analysed using
coded numbers instead of individual names.
Descriptive epidemiology
Health workers informed the researchers about a sudden
increase of fever cases that occurred during September 2012, in
four villages, namely Badalpur, Gopalpur, Ramchandrapur and
Tajpur, under Ramnagar-II block of Purba Medinipur district,
West Bengal. Febrile illness was associated with myalgia,
arthralgia, headache, retro-orbital pain, rash and haemorrhagic
manifestations suggestive of dengue fever. Dengue fever
(suspected dengue case) was defined as acute febrile illness of
27 days duration, with two or more of the following: headache,
retro-orbital pain, myalgia, arthralgia, rash, haemorrhagic
manifestations, or leukopenia; and a confirmed case of
dengue was also associated with one or more of the following:
supportive serology (reciprocal haemoagglutinationinhibition
antibody titre, comparable immunoglobulin G (IgG) enzymelinked immunosorbent assay (ELISA) titre, or positive
monoclonal IgM antibody capture (MAC-ELISA) test in a
serum specimen from the late acute or convalescent phase.9
Clinically suspected dengue cases were tested with a rapid
test kit such as NS1 antigen (nonstructural antigen 1 rapid
diagnostic) test kit. Since a dengue referral laboratory was not
available at the outbreak district, blood samples were also sent
to Midnapore Medical College Hospital for MAC-ELISA test,
for confirmation of dengue virus. Use of the NS1 ELISA and
IgM ELISA (MAC ELISA) tests was recommended by the
West Bengal Government for confirmation of dengue at public
health laboratories.
Data collection and analysis

Trained health workers worked with the primary investigator
to collect data in a predesigned format. They conducted houseto-house surveys to identify fever cases in the affected villages
and also looked for any affected patients from the four villages
admitted at the Ramnagar-II Block Primary Health Centre
and Contai Subdivisional Hospital. These two hospitals were
the referral hospitals for these villages. The proportion of
cases by age group and sex was calculated. The outbreak was
described in terms of time, place and person, and an epidemic
curve was drawn to observe the dynamic of the outbreak. It
was recognized that the movements of villagers to the dengueendemic area might spread the outbreak.
Entomological investigation
A demographic map of the study villages and surveyed houses
was prepared. An entomological investigation was carried
out to understand the density of vectors responsible for viral
transmission. A larval survey was conducted by searching
mosquito breeding sites inside and outside houses, using the
single larval survey (SLS) technique.10 Larvae were identified
by visual inspection of their appearance and movement in
water, by the district public health specialist/epidemiologist.
Analysis and calculation of the standard Aedes larval indices,
such as House Index (HI), Container Index (CI) and Breteau
Index (BI), were carried out, to estimate the prevalence and
infestation level of vectors in the locality.
A value of HI greater than 5% and/or of BI greater than 20%
for any locality are indications that the locality is prone to
dengue.12 For epidemiological purposes, the HI indicates
potential spread of virus through an area once an infected case
becomes established. Lawns and grounds around the houses
were considered as peri-domestic sites. Unused wells, tree
holes, discarded tyres, empty coconut shells, broken earthen
pots, plastic cups and packets, etc. were considered as breeding
sites.
Environmental study
The investigation team observed the sanitation practices, watercollection habits, water containers for mosquito breeding,
mosquito breeding sites, drainage systems and personal
protection measures against mosquitoes. The environmental
investigation was carried out with the help of records of
temperature, rainfall and humidity, from the meteorological
department.
RESULTS
The affected block is one of the coastal blocks of the district.
The total population of these affected villages was 5381. They
were mainly farmers and labourers by occupation and some
of them moved for work to dengue-endemic areas and visit
their houses frequently. A total of 100 affected patients were
identified in the four villages, of which 56% (56/100) were
men. There was no history of dengue cases over the previous
5years. The highest number of affected patients was reported
from the village of Gopalpur 37% (37/100), followed by
Badalpur 26% (26/100), and 19% (19/100) of affected patients
had a history of migration from dengue-endemic areas.
The majority of cases 52% (52/100) were in the age group of
1544 years, while only 3% (3/100) of cases were aged under
5years (see Table 1). The outbreak started on 7September 2012,
peaked on 19 September 2012 and declined gradually. There
was no reported case after 28 September 2012 (see Figure1).
All 100 cases had fever. Other signs and symptoms were:
myalgia (82 patients), headache (78), retro-orbital pain (73),
breathlessness (47), vomiting (47), diarrhoea (17), abdominal
pain (16), skin rash (14), bleeding manifestations (e.g. nose
or gum bleeding, petechiae or easy bruising) (6), and altered
47

Table 1: Distribution of suspected cases of dengue fever, by age and sex, at Ramnagra-II block, Purba Medinipur
district, West Bengal, India, during September 2012
Badalpur
Age group
(years)
Male
14
514
1544
>45
Total
Gopalpur
Total
Female
(%)
1
2 (8)
0
2 (8)
7
14 (54)
2
8 (31)
10
26 (26)
1
2
7
6
16
40
Male
1
2
11
4
18
Total
Female
(%)
0
1 (3)
6
8 (22)
8
19 (51)
5
9 (24)
19
37 (37)
Ramchandrapur
Total
Male Female
(%)
0
0
0 (0)
2
1
3 (21)
5
1
6 (43)
2
3
5 (36)
9
5
14 (14)
Notification
Tajpur
Male
Female
0
2
7
4
13
0
2
6
2
10
Total
(%)
0 (0)
4 (17)
13 (57)
6 (26)
23 (23)
Total
(%)
3
17
52
28
100
Control measure taken
35
No. of cases
30
CFR=1
25
20
15
10
5
30.9.12
28.9.12
26.9.12
24.9.12
22.9.12
20.9.12
18.9.12
16.9.12
14.9.12
12.9.12
10.9.12
8.9.12
6.9.12
4.9.12
Date of onset
Figure 1: Epidemic curve of outbreak of suspected dengue fever at four villages of Ramnagar-II block, Purba Medinipur district, West Bengal,
India during September 2012; CFR: case-fatality ratio
cognitive function (2). Three patients had complications, of

which one had multi-organ failure and two had pneumonia.
All the patients recovered, except one female patient aged 43
years. The case-fatality ratio (CFR) was therefore 1%.
Laboratory tests
Of 100 affected patients, 79% (79/100) were positive for NS1
antigen test and 18 blood specimens were sent for MACELISA test, of which 72% (13/18) were tested positive.
Entomological survey
A total of 989 water-holding containers from the four villages
were searched for breeding sites of Aedes larvae, both indoors
and outdoors. Of these, 208 houses in Badalpur, 468 houses
in Gopalpur, 172 houses in Ramchandrapur and 289 houses in
Tajpur were surveyed. An average of 8% (89/1137) of houses
48
showed the presence of Aedes aegypti larvae. The average HI,

CI and BI were calculated in the four villages; they were 8.0%,
13.1% and 9.5% respectively, with ranges of 2% to 13%, 2%
to 23% and 2% to 18% respectively. The maximum HI, CI and
BI values were observed in Gopalpur village, and were 13%,
23% and 18% (see Table 2).
Environmental study
During the researchers visit, it was observed that water
accumulated in drums, drains, ponds and other containers
of water. The inhabitants used to take tea in plastic and
earthen pots and throw these used pots away in their yards.
Water accumulated in these containers, after rain. Water also
accumulated in broken flower vases, earthen pots, coconut
shells and tyres, which favoured mosquito breeding. After
careful examination, these coconut shells, tyres, earthen pots,
flower tubs and plastic containers were found to be positive
for Aedes aegypti larvae. There was no scarcity of water in

Table 2: Entomological survey at four villages of
Ramngar-II block, Purba Medinipur, West Bengal, India,
during September 2012
Villages
Gopalpur
Ramchandrapur
Badalpur
Tajpur
House Index
(%)
13
9
3
2
Container
Index (%)
23
11
10
2
Breteau
Index (%)
18
13
5
2
the villages, but water for cattle was collected and stored in
earthen pots without a cover. Mosquitoes were found to be
breeding there. The relative humidity and temperature of the
district was 7590% and 2737C respectively, in the month
of September. The total rainfall in the district during September
2012 was 302mm.13
DISCUSSION
This epidemiological investigation showed that the outbreak
was probably dengue fever. Young and active age groups were
most affected, and those with a history of migration from
dengue-endemic areas. Environmental conditions and larval
indices favoured an explanation of Aedes aegypti and dengue
virus transmission.
Small water containers such as plastic tea cup, water bottles,
chips packets, tyres, coconut shells, earthen pots, etc. were
present in these villages, which favored mosquito breeding.
Newly constructed buildings and concrete roads in the villages
indicated urbanization. There was no scarcity of water in the
villages, but water for cattle was collected and stored water in
earthen containers without cover, and mosquitoes bred there .
The BI was less than 50% in all four villages. So, a high risk of
transmission was not considered. On the other hand, the BI was
<5% in three out of four villages, which was not considered a
low risk of transmission. Similarly, the HI of Gopalpur village
was >10%, which was considered a high risk of transmission.
However the HI was not <1% in the other three villages, so this
could not be considered a low risk of transmission.14
Though dengue outbreaks had previously been reported from
urban areas, in the recent past outbreaks had also been reported
from semi-urban and rural areas of North India,15 South India,16
Western India,17 and West Bengal,18 as well as in this outbreak.
In this study, most of the patients were men and young, in the
age group of 1545 years; this finding was similar to that of
a study in Upadi district,15 but dissimilar to another study at
Kanyakumari of Dharmapuri district,6 where more women and
children (615 years) were affected.
It was also evident that movement of villagers to dengueendemic areas had contributed to this outbreak, which was
consistent with the findings of other studies.6,1 6
In this study, 72% (13/18) of affected patients were positive

on the MAC-ELISA test, whereas a study at two villages at
Dharampuri district revealed that 42% (13/31) and 27%
(14/52) tested positive, respectively.6 Climatic factors such as
temperature, humidity and rainfall would have contributed to
the abundance of Aedes mosquitoes and virus transmission.19
The spread of dengue fever in the villages needed preventive
actions. The health authority, along with local administration,
took joint initiatives to increase awareness of dengue fever and
its signs and symptoms, and early referral of severe cases to
hospital was conducted. Vector-control measures were carried
out, especially reduction of breeding sources by destroying
unnecessary and discarded water containers. The communities
were also taught about personal protective measures against
mosquito bites. It is suggested that regular training of health
workers, social workers (ICDS workers), panchayat workers,
local nongovernment organization workers and other
departments, on dengue and other vector-borne diseases, will
reduce the incidence of outbreaks in the future.
Limitations
A pupal index survey was not carried out and involvement
of a qualified entomologist would have added value to the
investigation. Larvae were identified by visual inspection alone
and not confirmed by a laboratory. A dengue-referral laboratory
was not available at the district and the nearest laboratory
facilities (at Midnapore and the School of Tropical Medicine,
Kolkata) were 150175km away from the place of outbreak.
The logistic challenges meant that, out of 100 affected patients,
the MAC-ELISA test was only done for 18.
CONCLUSION
It was revealed from the epidemiological, entomological and
serological investigations that suspected fever outbreaks were
probably due to dengue virus infection. Adverse meteorological
conditions and unplanned urbanization favoured the breeding
of Aedes mosquitoes in the study villages. Involvement of
government sectors and community youth groups to clean
up the discarded tyres and containers in the neighbourhoods,
and raise awareness among the villagers addressed the dengue
outbreak.
Acknowledgements
The authors would like to acknowledge Dr Sukumar Das, Ex
Chief Medical Officer of Health, Purba Medinipur district, for
his kind permission to conduct the study. They also acknowledge
the health workers of Ramnagar-II block for helping with data
collection and Dr TK Pathak, Associate Professor, Department
of Microbiology, Midnapore Medical College and Hospital,
Minapore, for helping with serological tests.
49
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How to cite this article: Biswas DK, Bhunia R, Basu M.

Dengue fever in a rural area of West Bengal, India, 2012: an
outbreak investigation. WHO South-East Asia J Public Health
2014; 3(1): 4650.
Contributorship: DKB conceived the study with data collection, data
entry, analysis and manuscript writing; RB was involved in designing the
study, with editing and critical editing; MB was involved in editing, revision
and critical editing the study. All authors read and finally approved the final
manuscript. DKB is the guarantor of the paper.
Original research
DOI: 10.4103/2224-3151.115828
Dengue vectors in urban and suburban

Assam, India: entomological observations
V Dev1, K Khound2, GG Tewari1
Abstract
National Institute of Malaria

Research (Field Station),
Guwahati, Assam, India
2
National Vector Borne Disease
Control Programme, Government
of Assam, Guwahati, Assam, India
1
Background: Dengue is rapidly becoming established in north-east India and

spreading, on account of rapid urbanization and population movement, with
reported morbidity and attributable death cases. This study aims to determine the
seasonal abundance of Aedes (Stegomyia) albopictus and Aedes (Stegomyia)
aegypti in Guwahati metropolis and suburban settlements; to characterize the
breeding resources for these mosquitoes; and to ascertain the status of their
susceptibility to adulticides and larvicides.
Methods: Mosquito larval surveys were carried out in different localities in both
Guwahati city and adjoining suburbs from January to December 2013, to determine
the seasonal abundance of disease vectors and their breeding preferences.
The insecticide susceptibility status of mosquito adults and larval populations of
both Aedes aegypti and Aedes albopictus was ascertained, using World Health
Organization standard diagnostic concentrations and test procedures.

Dr V Dev, National Institute of
Malaria Research (Field Station),
Guwahati 781022, Assam, India.
Email: mrcassam@hotmail.com
Results: The study revealed that both Aedes aegypti and Aedes albopictus are
widely abundant in Guwahati city and suburbs, and breeding in a wide variety of
resources. Aedes albopictus, however, was the predominant mosquito species
in suburbs, breeding preferentially in flower vases, cut-bamboo stumps and leaf
axils. Aedes aegypti was the most common in the city, breeding predominantly in
discarded tyres, cement tanks and used battery boxes. Both Aedes aegypti and
Aedes albopictus were resistant to dichlorodiphenyltrichloroethane (DDT; 4%), but
susceptible to malathion (5%), and exhibited a varied response to pyrethroids.
However, larval populations of both these mosquito species were susceptible to
larvicides, including malathion (1.0 mg/L), temephos (0.02 mg/L) and fenthion
(0.05 mg/L), at much lower dosages than diagnostic concentrations.
Conclusion: Given the seasonal abundance and case incidence in city areas,
it is highly probable that Aedes aegypti is the predominant mosquito vector
transmitting dengue virus. The study results have direct relevance for the state
dengue-control programme, for targeting interventions and averting outbreaks and
spread of disease.
Key words: Aedes aegypti, Aedes albopictus, Assam, dengue, insecticide
susceptibility status, mosquito breeding habitats, north-east India, seasonal
abundance
Introduction
There has been dramatic increase in dengue cases globally
and nearly half of the worlds population is estimated to be
living at risk of the disease.1 The World Health Organization
(WHO) estimates that there are 50 to 100 million cases
every year in tropical and subtropical countries.1 Dengue is
endemic in India, with reported disease outbreaks in large
metropolis cities.24 However, with increased urbanization and

population movement, the disease is reportedly spreading to
other metropolitan areas or cities that were hitherto free from
disease.57 The state of Assam, situated in north-east India,
reported 237 confirmed cases of dengue for the first time in
2010, and subsequently there was a significant increase in 2012
and 2013, with 1058 and 4526 cases recorded, respectively.3
Of the total confirmed cases for each year in the state, the
51
Dev et al.: Dengue vectors in Assam, India
majority (7090%) were recorded in the largest metropolitan

area, Guwahati city. The actual disease burden is estimated to
be much higher, with many cases undiagnosed and additional
cases reported in public/private sectors.
Aedes aegypti (renamed as Stegomyia aegypti) and Aedes
albopictus (renamed as Stegomyia albopicta) are reportedly
prevalent in the north-east region of India, which offers ideal
conditions for proliferation of these mosquito vectors and the
spread of disease.5 Recent occurrences and increased case
incidence of dengue in north-eastern states warrant detailed
investigations of the seasonal prevalence of these two mosquito
species, to improve understanding of their bionomics, for
formulation of suitable interventions at specific places and
times. There have been sporadic informal reports of mosquito
surveys in north-eastern states, but no data on the relationship
of seasonal abundance and the member species composition of
the Aedes albopictus subgroup.810
This study aims to determine the seasonal abundance of Aedes
albopictus and Aedes aegypti in Guwahati metropolis and
suburban settlements; to characterize the breeding resources
for respective species; and to ascertain their susceptibility to
adulticides and larvicides.
Study site, topography and climate

Guwahati city (261110 N, 91453 E), situated on the
southern bank of the mighty river Brahmaputra (54m above
sea level), is a fast-growing metropolis in Assam state and a
gateway to the north-east of India for economic activities. It is
the largest city in north-east India, spread over 264km2, with
a population of 1.5 million, and is a principal centre of socialcultural, political, industrial, trade and commerce for the entire
north-east of India. The study site comprised Guwahati city and
its adjoining suburban Sonapur block (see Figure 1). The city
is densely populated, and grouped into four zones (East, West,
South and Capital zone), under the jurisdiction of Guwahati
Municipal Corporation for administrative purposes. Typically,
the general population live in houses/apartment complexes
made of brick and cement but drainage is still open in many
areas. There is a piped water supply in most areas of the city,
yet many households store potable water in cement tanks or
plastic/tin containers for domestic use. In Sonapur block
(population 0.19 million), however, housing is mixed, with
many structures made of split bamboo with thatched roofing,
often with an attached cattle shed. This block is sparsely
populated, with large tribal concentrations and vast forest cover.
In this region, most of the year is hot and humid and, during
Mean mosquito breeding indices (range)
City Zone
No. of dengue
cases
HI
CI
BI
West Zone
238
13.86
(0.0430)
34.76
(5.1961.5)
55.31
(8160)
East Zone
2863
12.36
(3.2228.5)
36.67
(13.4380)
31.34
(20.1957.1)
Capital Zone
819
14.40
(2.1727.5)
23.39
(1.0738.4)
40.43
(2.1762.5)
South Zone
201
No data
No data
No data
20.41
(4.3440)
26.39
(2.8560)
62.05
(4.341200
Sonapur block
Figure 1: Diagrammatic sketch map of Guwahati city and adjoining suburban Sonapur block, showing mosquito larval survey locations (yellow
circles) in different zones. Aedes aegypti is the predominant mosquito species in the city (total cases = 4121) and Aedes albopictus in the
suburban Sonapur block (total cases = 2). Inset is the map of India showing location of the study site, and table giving distribution of dengue
cases in different zones and corresponding entomological indices of disease vectors. HI:House/premise Index, CI: Container Index; BI: Breteau
Index.
52
the summer (April to September), the monthly mean maximum

and minimum temperatures range from 30C to 34C and 20C
to 25C respectively. For rest of the year (October to March),
the monthly mean maximum and minimum temperatures range
from 24C to 32C and 9C to 22C respectively. The rainy
season is extended, with pre-monsoon showers during April to
June, followed by heavy downpours during July to September;
in the post-monsoon months (October to March), the rainfall is
comparatively less. The relative humidity is high (>70%) for
most of the year and the total annual rainfall ranges from 1.5m
to 2m and many areas get inundated due to flash flooding.
Methods
The study protocol was approved by the Institutional Scientific
Advisory Committee and bears the project ID No. NIMR/
IDVC/2011/139; household heads provided informed verbal
consent.
Entomological sampling techniques

Larval breeding surveys
To determine the seasonal abundance of Aedes albopictus and
Aedes aegypti and species-specific breeding habitats, mosquito
larval surveys were conducted in different localities in both
Guwahati city and the adjoining suburban Sonapur block, during
January to December 2013 (see Figure 1). Different breeding
resources were searched in various localities, including market
places, houses (exterior premises only), nurseries, industrial
areas and other landmark locations, such as the railway yard,
city zoo and airport. All possible mosquito breeding resources,
namely discarded tyres, flower vases, coconut shells, cutbamboo stumps, and plastic/tin/earthenware containers were
searched for larval/pupal breeding, in both urban and suburban
settings. Larval collections were made, aided by a dipper (200
mL capacity) in tyres and cement tanks, and by direct pipetting
of larvae and pupae from cut-bamboo stumps, leaf axils and
small plastic/tin/earthenware containers of <200 mL capacity.
Collections of immature populations, including larvae and
pupae, from each type of container were kept separately in
small water-filled containers, until emergence, for accurate
species identification. Adult mosquitoes were identified
using available taxonomic keys and related publications, and
seasonal abundance was monitored by conventional indices,
i.e. the House/premise Index (HI), Container Index (CI) and
Breteau Index (BI).
(but not all) have been recorded in India; however, there are
no data on the abundance of member species of this subgroup
specific to north-eastern states. Mosquitoes were identified
using taxonomic keys primarily based on male genitalia for
claspette, a species-specific diagnostic character.12
Insecticide susceptibility status

The insecticide susceptibility status of mosquito adults as
well as larval populations of both Aedes aegypti and Aedes
albopictus was ascertained using WHO standard diagnostic
dosages and test procedures.13,14 Batches of unfed, 23-dayold female mosquitoes (emerged from field-collected larval
populations) were introduced into holding tubes for 1 h and
then transferred into the exposure tube and placed vertically
for 1 h to the test insecticides, namely organochlorine (4 %
dichlorodiphenyltrichloroethane [DDT]), organophosphorous
(5% malathion), and synthetic pyrethroids (0.75% permethrin,
0.05% deltamethrin). Knocked-down and dead mosquitoes
were recorded after this time (1 hKD) before being transferred
into the holding tubes. A mosquito was recorded as knockdown if it was lying on its back or side and was unable to
maintain flight after a gentle tap. Mortality was recorded 24 h
after exposure (24 hM). Each test was replicated five to eight
times (1020) mosquitoes per replicate. Appropriate controls
were tested as described above, with a batch of 10 unfed
females per replicate against each insecticide. The experiments
were completed at ambient room temperature of 272C and
relative humidity of 7080%. Ten per cent sugar-soaked cotton
was provided to the females during the 24-h holding period.
Following the WHO test protocol,14 two to four batches
of third- or fourth-instar larvae (2040 per replicate) were
evaluated against larvicides, namely fenthion (0.05 mg/L),
malathion (1.0 mg/L) and temephos (0.02 mg/L). The first
filial generation of each mosquito species was exposed to
serial dilutions of discriminating dosages. The number of dead/
moribund and alive mosquito larvae post 24-h exposure was
recorded, keeping appropriate control for corrected percentage
mortality. Data from larval bioassays were subject to probit
analysis, using SPSS software version 22 for determining the
50% and 95% lethal concentrations (LC50 and LC95), with
95% confidence intervals.
Results
Entomological observations
Species composition of the Aedes

(Stegomyia) albopictus subgroup
Seasonal abundance of Aedes aegypti and Aedes albopictus
Aedes (Stegomyia) albopictus is a species subgroup, members

of which are known to coexist in south-east Asia, and are
implicated in transmission of dengue and chikungunya/
arboviruses.11 These include Aedes albopictus (Skuse), Aedes
downsi (Bohart and Ingram), Aedes flavopictus (Yamada),
Aedes novalbopictus (Barraud), Aedes patriciae (Mattingly),
Aedes pseudalbopictus (Borel), Aedes seatoi (Huang) and
Aedes subalbopictus (Barraud). Some of these member species
Monthly data on the houses/premises inspected and containers

searched for seasonal changes in breeding indices, including
HI, CI and BI are given in Table 1. Based on monthly breeding
surveys, it was observed that during the winter season (January
to March), the majority of the containers searched were dry
(82.4%), and of those recorded wet (17.6%, 532/3013), all
were devoid of mosquito breeding. During the remainder of
the season (April to December), 27% (2039/7651) of wet
53

Table 1: Monitoring seasonal abundance of Aedes albopictus and Aedes aegypti mosquito breeding, dengue vector
mosquito species in Guwahati metropolis and suburbs, Assam, India
HI (number of positive premises/
number inspected 100)
Month,
2013
January
February
March
April
May
June
July
August
September
October
November
December
Number of
positive
premises
0
0
0
4
12
14
19
14
22
31
8
14
Number of
premises
inspected
44
141
212
119
107
122
133
103
231
195
43
65
CI (number of positive containers/

number searched 100)
Number of
positive
containers
0
0
0
6
65
42
65
40
60
77
25
28
HI
0
0
0
3.4
11.2
11.5
14.3
13.5
9.5
15.9
18.6
21.5
Number of
containers
searched
97
172
263
205
192
140
285
226
237
587
75
92
CI
0
0
0
2.9
33.8
30.0
22.8
17.6
25.3
13.1
33.3
30.4
BI (number of positive containers/

number of premises inspected
100)
Number of
Number of
positive
premises
BI
containers
inspected
0
44
0
0
141
0
0
212
0
6
119
5.0
65
107
61.0
42
122
34.4
65
133
48.8
40
103
38.8
60
231
25.9
77
195
39.5
25
43
58.1
28
65
43.0
HI: House/premise Index, CI: Container Index; BI: Breteau Index.
100
Mosquito breeding indices
90
80
70
60
50
40
30
20
10
0
Jan
Feb
Mar
Apr
May
Jun
Jul
Aug
Sep
Oct
Nov
Dec
2013
HI
CI
BI
Figure 2: Seasonal cumulative larval breeding indices of Aedes aegypti and Aedes albopictus mosquito species in Guwahati city and adjoining
suburbs, Assam, India. HI: House/premise Index, CI: Container Index; BI: Breteau Index
containers searched were positive for Aedes immature stages;

however, monthly entomological indices, i.e. HI, CI and BI
ranged from 3.4 to 21.5, 2.9 to 33.8, and 5.0 to 61.0 respectively
(see Figure2). At the onset of the rainy season in April, the HI
was observed rising gradually and peaked during November
and December (post-monsoon season). Similarly, the CI
combined for both Aedes aegypti and Aedes albopictus was
observed rising from 2.9 in April and then fluctuated between
13.1 and 33.8 for rest of the season. There was a parallel rise in
BI, from 5.0 in April to 61.0 in May and it then varied between
25.9 and 58.1 during June to December. During April to
December, of a total of 2039 breeding sources searched in both
urban and suburban areas, 408 (20%) containers were positive
for mosquito breeding. Of these, 172 (8.43%) and 167 (8.19%)
containers were positive for Aedes albopictus and Aedes aegypti
54
respectively, and the remaining 69 (3.38%) were positive for

mixed breeding comprising both species (see Table 2). Aedes
albopictus, however, was first detected at the beginning of April
and Aedes aegypti was first recorded in May. The CI, however,
for each mosquito species, and the extent of mixed breeding,
varied during the months investigated. The CI ranged from
1.70 to 28.12 and 0.52 to 26.67 for Aedes albopictus and Aedes
aegypti respectively, and for mixed breeding it varied from 1.05
to 9.78 for the months observed. Both these mosquito species
are morphologically separated by the presence of a distinct
lyre marking covered with white scales on the scutum (Aedes
aegypti) or a prominent median stripe of white scales on the
scutum (Aedes albopictus). Both varieties of Aedes aegypti,
i.e. mosquitoes with dark scales (type form) and pale scaled
mosquitoes (variety queenslandensis) were recorded breeding

Table 2: Seasonal container positivity of Aedes albopictus and Aedes aegypti, dengue vector mosquito species in
Guwahati metropolis and adjoining suburbs, Assam, India
Month, 2013
January
February
March
April
May
June
July
August
September
October
November
December
Total
a
Total rainfall
(mm)
0
11.4
21.7
94.7
464.3
336.5
260.6
135.4
122.7
214.6
0
0
1661.9
Total number of
wet containers
searched for
mosquito
breeding
97
172
263
205
192
140
285
226
237
587
75
92
2571
Number (%)
of containers
positive for
mosquito
breeding
0
0
0
6 (2.92)
65 (33.85)
42 (30.00)
65 (22.80)
40 (17.69)
60 (25.31)
77 (13.1)
25 (33.3)
28 (30.43)
408 (15.9)
Number (%) of containers positive for

species
Ae. albopictus
Ae. aegypti
Mixed
Number of
reported
dengue
casesa
0
0
0
6 (2.92)
54 (28.12)
12 (8.57)
45 (15.78)
25 (11.06)
12 (5.06)
10 (1.70)
5 (6.67)
3 (3.26)
172 (6.7)
0
0
0
0
1 (0.52)
30 (21.43)
17 (5.96)
15 (6.63)
27 (11.39)
41 (6.98)
20 (26.67)
16 (17.39)
167 (6.5)
0
0
0
0
10 (5.20)
0
3 (1.05)
0
21 (8.86)
26 (4.42)
0
9 (9.78)
69 (2.7)
0
0
0
0
1
0
2
75
1635
1395
827
188
4123
Data based on reported cases in the study area (source: State Health Directorate of Assam).
in Guwahati city; the latter was the predominant collection in

pre-monsoon and monsoon months (April to September), and
the former was the exclusive collection during post-monsoon
months (October to December).
Breeding habitat surveys
During April to December 2013, of a total 2039 containers
searched for mosquito breeding, 17.95% (260/1448) and
25.04% (148/591) were positive in urban and semi-urban areas
respectively. Both Aedes aegypti and Aedes albopictus were
observed breeding in a variety of natural and artificial habitats
(see Figure 3). Aedes albopictus was recorded breeding in tyres,
cut-bamboo stumps, plastic/tin containers, flower vases and
leaf axils, in both urban and suburban areas but the CI varied
between habitats and ecotype (see Table 3). It was relatively
less abundant in city areas in all habitats, and in coconut shells
it was observed only in suburbs. It was, however, the exclusive
collection in flower vases and leaf axils in both in urban and
suburban areas, and was predominant in plastic/tin containers
(CI = 8.7) in urban areas, compared to Aedes aegypti (CI =
3.9). Aedes aegypti, on the other hand, was the most common
species in the city, predominantly breeding in discarded tyres
(CI = 15.3), and was the exclusive collection in cement tanks
(CI = 43.7) and used battery boxes (CI = 14.3). Mixed breeding
of both mosquito species was largely recorded in tyres in both
urban and suburban areas, in which Aedes aegypti and Aedes
albopictus occurred in approximately 60:40 proportions, and
occasionally in cut-bamboo stumps, plastic/tin containers and
coconut shells, during the months investigated
Species composition of the Aedes
(Stegomyia) albopictus subgroup
Mosquito adult males that emerged from larval collections from
various breeding resources in different localities were dissected
for male terminalia/claspette, a species-specific diagnostic
Figure 3: Breeding habitats of Aedes aegypti and Aedes albopictus

in Guwahati city and adjoining suburbs, Assam, India. Upper left: a
discarded tyre, a preferred breeding source for Aedes aegypti in urban
areas (written permission to reproduce this image was provided by
the individual portrayed); upper right: a cut bamboo stump, a breeding
source for Aedes albopictus in rural areas; lower left, a leaf axil, a
breeding source for Aedes albopictus; lower right: a flower vase, a
preferred breeding habitat for Aedes albopictus
characteristic of the Aedes albopictus subgroup. During April

to December, 290 male mosquitoes were dissected for male
genitalia, all of which were confirmed to be true morphotype
Aedes (Stegomyia) albopictus (Skuse), as they possess (i) a
claspette mushroom like with numerous scales and several
widened specialized setae on the mesal aspect, and a few
widened specialized curved setae on an apical angle of the
expanded distal part; and (ii) a tergum IX, with a conspicuous
horn-like median projection. Thus, it is concluded that Aedes
albopictus is the only member species of the Aedes albopictus
subgroup that is prevalent in Guwahati and suburbs.
55

Table 3: Major breeding habitats and relative abundance of Aedes albopictus and Aedes aegypti in Guwahati
metropolis and adjoining suburbs, Assam, India, April to December 2013
Breeding habitat
Tyres
Bamboo stumps
Tin/plastic
containers
Flower vases
Leaf axils
Cement tanks
Battery boxes
Coconut shells
Ecotype
Urban
Semi-urban
Urban
Semi-urban
Urban
Semi-urban
Urban
Semi-urban
Urban
Semi-urban
Urban
Semi-urban
Urban
Semi-urban
Urban
Semi-urban
Number of wet
containers
searched for
mosquito
breeding
799
194
75
132
334
50
154
202
35
7
16
2
28
1
7
3
Number (%)
of containers
positive for
mosquito
breeding
172 (21.5)
72 (37.1)
13 (17.3)
37 (28.0)
46 (13.8)
10 (20.0)
14 (9.1)
26 (12.9)
4 (11.4)
2 (28.6)
7 (43.7)
0
3 (10.7)
0
1 (14.3)
1 (33.3)
Number of containers positive for species

(Container Index)
Aedes
albopictus
Aedes aegypti
Mixed
breeding
17 (2.1)
21 (10.8)
11 (14.7)
35 (26.5)
29 (8.7)
10 (20.0)
14 (9.1)
26 (12.9)
4 (11.4)
2 (28.6)
0
0
0
0
0
1 (33.3)
122 (15.3)
25 (12.9)
0
0
13 (3.9)
0
0
0
0
0
7 (43.7)
0
4 (14.3)
0
0
0
33 (4.1)
26 (13.4)
2 (2.7)
2 (1.5)
5 (1.5)
0
0
0
0
0
0
0
0
0
1 (14.3)
0
Table 4: Insecticide susceptibility status of Aedes aegypti and Aedes albopictus, dengue mosquito vector species in
Assam, India, July to October 2013
Number of
mosquitoes
exposed (number
of replicates)a
70 (5)
Number (%) of
mosquitoes
knockdown in 60
minutes
1 (1)
Number (%) of
mosquitoes
dead post 24h
exposure
2 (2)
Aedes albopictus
60 (5)
7 (12)
8 (13)
Malathion (5%)
Aedes aegypti
Aedes albopictus
70 (5)
80 (6)
69 (99)
78 (98)
70 (100)
80 (100)
S
S
Deltamethrin (0.05%)
Aedes aegypti
101 (8)
96 (95)
81 (80)
Aedes albopictus
100 (7)
100 (100)
100 (100)
Aedes aegypti
110 (6)
28 (25)
24 (22)
Aedes albopictus
101 (8)
88 (87)
97 (96)
VR
Insecticide (diagnostic
concentration)
DDT (4%)
Permethrin (0.75%)
Mosquito species
Aedes aegypti
Susceptibility
status
R
R: resistant (mortality <80%); VR: verification required (mortality 8197%); S: susceptible (mortality 98100%).
a
Mortality in control replicates was <5%.
susceptible to deltamethrin: 1hKD=100%, and for permethrin

1hKD ranged from 57% to 100% and 24 hM was <97%; thus,
the susceptibility status was borderline (verification required)
according to the given WHO criterion.
Insecticide susceptibility status of

mosquito adult and larval populations
Adult bioassay
The results of the susceptibility test of Aedes aegypti and
Aedes albopictus females to various insecticides are presented
in Table 4. Both Aedes aegypti and Aedes albopictus were
resistant to DDT (4%), with a mortality of <80%, but
fully susceptible to malathion (5%) at the given diagnostic
concentrations. However, both these species exhibited a varied
response to pyrethroids (deltamethrin and permethrin). Aedes
aegypti was observed to be resistant to deltamethrin (0.05%)
as well as permethrin (0.75%), but Aedes albopictus was
56
Larval bioassay
Larval samples of both Aedes aegypti and Aedes albopictus
were susceptible to all three larvicides, including malathion
(1.0 mg/L), temephos (0.02 mg/L) and fenthion (0.05 mg/L),
at much lower dosages than given diagnostic concentrations.
For larvicide assay of Aedes aegypti, the LC50 to LC95
values for malathion were 0.0199mg/L to 0.0707mg/L, for
temephos 0.000059mg/L to 0.000317mg/L, and for fenthion

Table 5: Summary statistics of susceptibility test results of mosquito larvae of Aedes aegypti and Aedes albopictus to
various larvicides in Assam, India, June to July 2013
Larvicide
(diagnostic
concentration,
mg/L )
Malathion (1.0)
Temephos (0.02)
Fenthion (0.05)
Number
of larvae
assayed
Regression
equation
Pearson X2
goodness of fit
LC50 (95% confidence

interval), mg/L
LC95 (95% confidence

interval), mg/L
Aedes aegypti
280
y=4.91 + 2.85x
0.029
Aedes albopictus
160
y=5.48 + 3.1x
0.410
Aedes aegypti
200
y=9.67 + 2.28x
0.010
Aedes albopictus
120
y=20.52 + 4.5x
0.427
Aedes aegypti
160
y=28.76 + 10.91x
0.204
Aedes albopictus
160
y=17.61 + 7.27x
0.192
0.0199
(0.0138 to 0.0271)
0.01747
(0.01292 to 0.02108)
0.000059
(0.000018 to 0.000183)
0.000027
(0.000023 to 0.000031)
0.00226
(0.00216 to 0.00283)
0.00374
(0.00340 to 0.00404)
0.0707
(0.0474 to 0.1562)
0.0518
(0.0415 to 0.0764)
0.000317
(0.000128 to 0.5883)
0.000058
(0.000047 to 0.000083)
0.00294
(0.00272 to 0.00342)
0.00579
(0.00519 to 0.00699)
Mosquito species
LC50: concentration that is lethal to 50% of the population. LC95: concentration that is lethal to 95% of the population.
0.00226mg/L to 0.00294mg/L, respectively. For Aedes

albopictus, the LC50 to LC95 values for malathion were
0.01747mg/L to 0.0518mg/L, for temephos 0.000027mg/L
to 0.000058 mg/L, and for fenthion 0.00374 mg/L to
0.00579mg/L respectively (see Table 5).
Dengue is spreading rapidly and becoming established in

north-east India, owing to socioeconomic and developmental
changes, with a dramatic increase in urbanization and
population movement, and an increase in reported morbidity
and attributable death.3,5 In the state of Assam, although most
cases have been recorded in Guwahati city itself, confirmed
cases have also been reported from other district towns,
supported by serological evidence for circulating strains
of dengue virus.5,15,16 In 2013, 91% (4121/4526) of the total
reported dengue cases were recorded in Guwahati city alone
and only two cases in the suburban Sonapur block. The cases
were, however, unevenly distributed in different zones of the
city, with large concentrations in the East zone, Capital zone,
West zone and South zone, in decreasing order (see Figure 1).
with increased case incidence, although correlation with CI

and the number of cases was very weak (r=0.248, P=0.455;
see Table 2). Similarly, correlation of dengue cases with HI
(r = 0.348, P=0.218) and BI (r=0.230, P=0.557) were
also insignificant statistically. Given the variable distribution
of confirmed dengue cases in different zones of the city, and
the data analysed for mosquito breeding indices for respective
zones, the CI was observed to be the highest in the East zone,
corresponding to a record number of cases, but correlation
was very weak (r = 0.43) and there was negative correlation
for HI (r = 0.891) and BI (r = 0.90). Aedes albopictus, on
the other hand, was the predominant mosquito species in the
semi-urban area, breeding in variety of habitats, preferentially
in flower vases, cut-bamboo stumps and leaf axils. With only
two dengue cases recorded in the suburban Sonapur block, it
is highly unlikely that Aedes albopictus is an efficient vector.
Instead, it is argued that, with increased urbanization and
depletion of forest cover, Aedes aegypti is reportedly invading
the suburbs and other town areas in the state, competitively
displacing Aedes albopictus, as evidenced by higher relative
abundance in tyres in both urban and suburban areas (see Table
3).5 Similar observations have also been documented in other
countries of south-east Asia.17
The present study has revealed that both Aedes aegypti and
Aedes albopictus (the only member species of the Aedes
albopictus subgroup) are widely abundant in Guwahati city
and suburbs, breeding in a wide variety of resources (see
Table 3). The seasonal prevalence of both mosquito species
occurs from the onset of rains in April until December, and
the mosquito breeding indices varied between the months
observed (see Figure 2). Aedes aegypti was the most common
species in urban areas, breeding predominantly in discarded
tyres; it seemingly outnumbered Aedes albopictus, evidenced
by the CI, and was recorded exclusively in cement tanks
and used battery boxes (see Table 3). Interestingly, a CI
of 0.52 (for Aedes aegypti), and combined CI of 5.20, was
associated with the first reported dengue case in May, and
high values of CI for Aedes aegypti were maintained in the
city premises during July to December, which corresponded
Even though both Aedes aegypti and Aedes albopictus are the
suspected vectors and implicated in dengue transmission in
the north-east region of India, given the seasonal abundance
and case incidence in city areas, it is highly probable that
Aedes aegypti is the predominant mosquito vector transmitting
dengue virus. With the increasing distribution range of Aedes
aegypti and evidence of virus activity, it is projected that
dengue will emerge as a major public health issue in northeast India. However, the role of Aedes albopictus in dengue
transmission in this region needs to be elucidated. Given the
fact that populations of both mosquito species were resistant
to DDT, and showed a variable response to pyrethroids,
malathion should be the insecticide of choice for control.
Similar study results have been reported in Thailand, where
populations of Aedes aegypti have been found to be resistant
to both deltamethrin and permethin, evidenced by underlying
Discussion
57
biochemical mechanisms.18,19 For anti-larval operations, even

though larval populations of both species were susceptible
to all three larvicides, malathion (1.0 mg/L), temephos (0.02
mg/L) and fenthion (0.05 mg/L), repeated applications seemed
inappropriate given the diversity of breeding resources and
selection pressure for resistance. Apart from the variable
response of mosquito adults to pyrethroids, similar study results
have been reported for mosquito adult and larval population
in other regions of India, including Delhi and Jharkhand.2022
However, continuous monitoring of insecticide susceptibility
against dengue vectors is imperative for effective control
and containment of disease spread. To overcome insecticide
resistance, an appropriate mix of technologies, including
application of bio-larvicides, namely, Bacillus thuringiensis
israelensis (Bti) and insect growth regulator compounds;
sustained efforts for community awareness; and community
participation to prevent mosquito breeding, enforced by civic
bye-laws, should all be considered.23
This study has provided data on the prevalence of both disease
vectors and some bionomic characteristics, but lack of data on
the pupae-per-person index in the given locality remains the
limitation of the study. The pupal/demographic survey has been
proven to be an effective tool for assessing risk and targeting
the most productive containers for reducing operational costs,
and has been duly endorsed by WHO.2426 There is scope for
further research on the subject to generate similar data for other
districts/states of north-east India, with particular reference
to identification of high-risk areas, vector incrimination and
seasonal infectivity of dengue, as well as chikungunya virus
infection and co-infection of various dengue serotypes.2729 The
study results have direct relevance for the state dengue-control
programme, for targeting interventions and averting outbreaks
and spread of disease.
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project staff for technical assistance. Thanks are also due NR
Choudhury, district officer for data access on reported cases
and coordinated efforts for vector breeding surveillance, and to
the India Meteorological Department, Guwahati, for providing
meteorological data.
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and Nagaland. J Commun Dis. 1996;28:5658.
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manifestations associated with dengue virus infection in Nagaland. J
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Insectcide susceptibility status of certain populations of Aedes aegypti
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India. J Vector Borne Dis.2011;48:116118.
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W, Wai KT, Tyagi BK, Kroeger A, Sommerfeld J, Petzold M. Eco-biosocial determinants of dengue vector breeding: a multicountry study in
urban and periurban Asia. Bull World Health Organ. 2010;88:173184.
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AC,Barbazan P,Cote M,Midega J,Sanchez F,Manrique-Saide
P,Kroeger A,Nathan MB,Meheus F,Petzold M. Reducing costs and
operational constraints of dengue vector control by targeting productive
breeding places: a multi-country non-inferiority cluster randomized
trial. Trop Med Int Health.2009;14(9):11431153.
Fock DA. A review of entomological sampling methods and indicators
for dengue vectors. Geneva: World Health Organization, 2003.
Document No. TDR/IDE/Den/03.1. http://whqlibdoc.who.int/ hq/2003/
TDR_IDE_DEN_03.1.pdf - accessed 28 February 2014.

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Fock DA, Alexander N. Multicountry study of Aedes aegypti pupal

productivity survey methodology: findings and recommendations.
Geneva: World Health Organization, 2006. Document No.TDR/IDE/
DEN/06.1.
Mourya DT, Thakare JP, Gokhale MD, Powers AM, Hundekar Sl,
Jaykumar PC. Isolation of chikungunya virus from Aedes aegypti
mosquitoes collected in the town of Yawar, Pune district, Maharashtra
state, India. Acta Virol. 2001;45:305309.
Chandrakant L, Pradhan SK. Emergence of chikungunya virus in Indian
subcontinent after 32 years: a review. J Vector Borne Dis. 2006;43:151
160.
Dutta P, Khan SA, Khan AM, Borah J, Chowdhury P, Mahanta J. First
evidence of chikungunya virus infection in Assam, Northeast India.
How to cite this article: Dev V, Khound K, Tewari GG. Dengue

vectors in urban and suburban Assam, India: entomological
observations. WHO South-East Asia J Public Health 2014; 3(1):
5159.
Source of Support: This study was funded by the Indian Council of
Medical Research, New Delhi (File No.5/8-7 (306) V-2011-ECD-II).
This submission has been reviewed by the Institute Publication Screening
Committee and bears the approval No. 03/2014. Conflict of Interest: None
declared. Contributorship: VD developed the concept proposal, conducted
overall supervision, data collation and analysis, and drafted the manuscript;
KK coordinated the study, provided intermediate supervision and developed
portions of the manuscript; GGT undertook data collection, intermediate
supervision, data compilation, mosquito dissections and identification. All
authors have read the final version and approved it for submission.
59
Original research
DOI: 10.4103/2224-3151.115828
An evaluation of the surveillance system

for dengue virus infections in Maldives
Aishath Aroona Abdulla1, Fathimath Rasheeda2, Ibrahim
Nishan Ahmed3, Maimoona Aboobakur4
Abstract
Senior Medical Officer,

Indira Gandhi Memorial Hospital,
Mal, Maldives;
2
Public Health Program Officer for
Surveillance, Center for Community
Health and Disease Control,
Ministry of Health and Family,
Maldives;
3
Senior Public Health Program
Officer for Surveillance, Center for
Community Health and Disease
Control, Ministry of Health and
Family, Maldives;
4
Director, Public Health Programs,
Center for Community Health
and Disease Control, Ministry of
Health and Family, Maldives.
1
Background: Dengue is endemic in Maldives. The largest epidemic to date was

in 2011. This study evaluates the surveillance system for dengue during 2011,
identifies gaps and suggests ways to improve.
Methods: This evaluation of the national surveillance system for dengue was done
in September to October 2012, using an evaluation tool based on United States
Centers for Disease Control and Prevention (US CDC) guidelines. Staff involved
in surveillance of different levels, and doctors expected to notify, were interviewed,
and surveillance data from the Health Protection Agency (HPA) were compared by
use of an independent database of the countrys national referral hospital in Mal,
Indira Gandhi Memorial Hospital (IGMH), to assess sensitivity and timeliness.
Results: National surveillance is conducted by HPA, which collects information
daily from a network of health facilities. Standard case definitions were published,
but they were not easily accessible to clinicians. The quality of data was acceptable.
Information is disseminated as annual communicable disease reports to health
facilities and uploaded onto the official website. The timeliness of reporting was
good (median 2 days). However, the usefulness for early warning of outbreaks
was limited, owing to central and peripheral resource limitations. Data were useful
for planning. Sensitivity was 0.54. Acceptability by clinicians was poor, owing to the
lack of feedback reaching them. The reporting rate was high from the paediatric
ward in IGMH (85%), where the responsibility of notifying was also assigned to
ward in-charge and support staff, but it was extremely low from the medical ward
(1.7%), where only doctors were given the responsibility.

Dr Aishath Aroona Abdulla,
Epidemiologist, Health Protection
Agency, Ministry of Health and
Family, Maldives, Roashanee
Building, Mal, Maldives.
E-mail: aroona@health.gov.mv,
iaroona@hotmail.com
Conclusion: This evaluation shows the performance of the dengue surveillance

system was good overall. However, clinicians need more regular feedback. The
performance could be improved significantly by written protocols, legislature
and assigning the responsibility of surveillance in hospitals to ward managers in
addition to doctors.
Key words: dengue, dengue haemorrhagic fever, doctors role, dengue shock
syndrome, evaluation, surveillance, Maldives
Introduction
Dengue is a mosquito-borne disease with significant morbidity
and mortality. Over 40% of the worlds population is currently
at risk from dengue. The World Health Organization (WHO)
currently estimates that there may be 50100 million dengue
infections worldwide annually. Dengue is found in tropical
and subtropical countries worldwide, mostly in urban and
60
semi-urban areas. Severe dengue is a leading cause of serious

illness and death among children in some Asian countries.
There is no specific treatment to cure dengue, but with early
detection and good clinical management, the case-fatality rate
can be reduced to less than 1%. Vector control, environmental
management and community mobilization are important for
effective prevention and control. Surveillance is crucial for
early detection of outbreaks and timely control.1
Abdulla et al.: Dengue surveillance in Maldives
Maldives is a small country, with a population of about

330000 dispersed over 194 inhabited islands.2,3 The central
public health authority the Health Protection Agency (HPA)
is responsible for surveillance as well as public health services,
interventions and planning for disease control and health
promotion. Surveillance is conducted by the Communicable
Disease Surveillance Unit of the Communicable Disease
Division.
Dengue was first reported in Maldives in 1979, as the first
dengue outbreak. Thereafter, outbreaks were reported
intermittently. Dengue is now an endemic disease in Maldives,
with perennial occurrence and seasonal peaks during the
months of June to August each year. It was the fourth most
commonly notified disease in 2011. After a major outbreak
in 1998 and 1999, surveillance for dengue began in the year
2000. Case-based data were collected and are available from
2005.46
The objectives of the dengue surveillance are to characterize
seasonal patterns of dengue infections, to detect epidemics
and take control measures, and to plan and prioritize efforts to
control the disease in Maldives. The last epidemic in June 2011
was the worst experienced, with 2909 cases and 12 deaths.
However, the case-fatality rate was maintained low at 0.4%,
with good clinical management nationwide.5,6 There was some
criticism regarding the inadequacy of public health measures
related to this outbreak. The surveillance system of Maldives
had not been formally evaluated in the recent past.
This study was conducted to evaluate the surveillance system
during the year of the epidemic, identify gaps in the surveillance
system, and suggest ways to improve the functioning of the
system.
Methods
A qualitative evaluation of the national-level indicator-based
surveillance system for dengue infections was conducted in
September to October 2012, using an evaluation tool based on
the United States Centers for Disease Control and Prevention
(US CDC) Updated guidelines for evaluating public health
surveillance systems.7 This study reports on the following
attributes:
data quality assessed by the completeness of core data
fields and proportion of duplicates and proportion of
confirmed cases, i.e. positive predictive value calculated
using the proportion of patients diagnosed with dengue
fever (DF), dengue haemorrhagic fever (DHF) and
dengue shock syndrome (DSS), with clinical or laboratory
confirmation;
simplicity assessed by method of notification;
sensitivity the proportion of individuals given the final
diagnosis of DF, DHF or DSS from the national-level
referral hospital Indira Gandhi Memorial Hospital (IGMH)
that were detected by the surveillance system;
acceptability assessed by the reporting rate and views of
doctors;
timeliness assessed by the time taken from the date of

onset to date of notification; the ideal assessment by time
from the date of consultation to the date of inclusion in the
database could not be done because the date of receipt of
notification to HPA and date of entry into the database were
not recorded.
A semi-structured questionnaire consisting of 16 main questions
was used. Staff involved in surveillance at different levels of the
surveillance system were interviewed. This included a policylevel person, a staff member of the Communicable Disease
Surveillance Unit, a staff member of the Medical Records
Unit of IGMH, and a laboratory staff member of IGMH. To
assess sensitivity and timeliness, data on dengue patients
reported to HPA from IGMH were accessed with the necessary
permissions and compared with data in an independent patient
database maintained by the Medical Records Unit of IGMH for
the hospitals use. Data for a one-month period in May in 2011
were selected for comparison because, as this was the month
before the epidemic was declared, there were more cases, while
it was hoped to reduce bias from increased reporting after
official declaration and media publicity. Daily inpatient lists
compiled by nurses were compared with the list of reported
cases prepared by the hospital Medical Statistics Unit. Doctors
in hospitals in Mal and Hulhumal were interviewed using a
separate questionnaire to assess the acceptability of the system
and identify how data are collected at the hospital level (see
Supplementary Online Annex 3 for questionnaire).
Results
The national surveillance system for dengue covered
a population of approximately 317000, scattered over
approximately 200 inhabited islands as estimated for 2011.
Approximately one third of the population lives in the capital
Mal. There are 21 administrative divisions (20 administrative
atolls and Mal city).2 HPA collects information from a
network of atoll hospitals and from the tertiary hospital and
other hospitals and clinics in Mal. The flow of data is shown
in Figure 1.
Standard case definitions were used and a case definition
booklet was published in 2008 and disseminated,8 but case
definitions were not easily accessible by the users (reporting
clinicians) at the time of the evaluation. Objectives were
defined for the communicable disease surveillance system, but
surveillance staff were not aware of any written documentation
of the objectives.
The surveillance system for dengue is mainly indicator based.
Aggregate data in the form of daily counts and individual casebased information are collected. Information is collected on a
daily basis from all health facilities, using a real-time online
software database (SIDAS), fax and email (see Table 1).
Who notifies?
Although there are no written procedures or legislation
indicating who is responsible for notifying, it is expected that
the forms will be completed by treating clinicians. Usually
61
Councils,
Ministry of
Health,
stakeholders,
public , WHO
Occurrence of
DF /DHF/DSS cases
Case goes to health

facility
Case
confirme
by treating doctor
Feedback and dissemination of information for public health action
Reporting sources
Health cent res, health posts; hospitals
atoll, regional, IGMH, ADK; clinics
(MNDF, private), laboratories; doctors,
nurses, health workers, clinical support
staff (ward clerks, cl inical assistants),
laboratory technicians
Reporting :
sending notifications
confidentiality
maintained
Data recipients
Primary level
Health centre in charge
Data management
(from secondary level
and above)
collection
Secondary level
Atoll (13)/regional (6)/tertiary
hosp ital medical records or PHU
entry
editing
storage
analysis
report generation
Tertiary level
HPA s urveillance unit
report dissemination
confidentiality
maintained
Figure 1: Data flow through the national surveillance system of Maldives

ADK : ; DF: dengue fever; DHF: dengue haemorrhagic fever; DSS: dengue shock syndrome; HPA: Health Protection Agency; IGMH: Indira
Gandhi Memorial Hospital; MNDF: Maldives National Defense Force; PHU: Public Health Unit; WHO: World Health Organization.
62

Table 1: Methods of receiving notifications during the month of May 2011
Method
Web entered directly or onto
Excel sheets uploaded
Email
Fax
Number (%) in May 2011

95 (36.7)
142 (54.8)
22 (8.5)
Telephone
Post
Total
None in May
None (not used)
259 (100%)
Remarks
From atoll and regional hospitals
From IGMH
Hulhumal, Villingili private hospitals (ADK) and clinics
Other centres sometimes fax data when they have disruption
of internet connection or software malfunction. Owing to
internet problems, all reports from K Atoll1 (Thulhusdhoo is the
administrative centre) are generally faxed, despite having access to
the SIDAS system
Deaths were informed by telephone as well one in February, two
in June.
K Atoll is where the capital Mal is situated. However, for administrative purposes, the islands of Mal, Hulhumal and Villingili
are under Mal city and suburbs, while the island of Thulhusdhoo is the administrative centre for the rest of the atoll.
these are doctors, except in islands where primary health-care

workers are the only clinicians. In many peripheral hospitals,
clinical assistants or ward clerks complete forms, and doctors
sign them. In the wards of IGMH, forms are completed by
doctors. In the paediatric ward, in-charge nurses and ward
clerks are also given the responsibility of ensuring notification,
and assist in completing forms. In the medical ward of IGMH,
the entire responsibility of notification is left to doctors. At
the time of the evaluation, all hospitals, health centres and
clinics (government owned and private) had been instructed
to report cases of dengue infections. The central-level policy
is that responsibility has been given to institutional, rather than
individual health-care providers. However, at the reporting
level, clinicians and hospital staff were of the opinion that that
it is the responsibility of doctors.
What information is collected?

Case-based information was collected, relevant to person,
place and time, case classification, diagnosis (DF, DHF and
DSS), and laboratory confirmation. There were some gaps in
the notification forms, which did not cover outcome (death or
discharged) clearly, and indicator of disease burden (whether
outpatient or admitted). However, the practice of informing
all deaths from dengue by telephone to the surveillance unit
was maintained. The field for address was also not worded to
capture the address of residence, which is important for control
measures. Box 1 details the information collected by the
notification form. The notification forms had slight variations
from one hospital to another, despite a template being provided
in the case definition booklet,8 as hospitals printed their own
forms.
Receiving and storing data

An online electronic system, the WHO South-East Asia
Regional Office Integrated Data Analysis System (SIDAS),
is used though the surveillance network. Data can be entered

offline and uploaded, and thus can be used at peripheral
locations. Trained medical records officers or community
health workers enter data into SIDAS from atoll hospital level,
where internet facilities are available. A SIDAS user manual is
available at all atoll hospital surveillance units, and centrally
for reference.9
Security of the system, and patient confidentiality, are protected
by password-protected access to the SIDAS system. The
data-entry officers at the statistics units in atoll and regional
hospitals, and surveillance officers at HPA, who enter and edit
data, are provided a username and password by HPA. However,
the system is not sensitive to IP address, and can be accessed
from any computer by a person with an authorized username
and password. This allows it to be used by individual healthcare providers to report data online. However, this facility is
not used, as it may threaten data quality and confidentiality,
because of the lack of restrictions to edit and access individual
patient data on the system. Therefore use of SIDAS is restricted
to atoll-level and central-level data entry by HPA. The same
username and password give access to entering new data as
well as accessing and editing individual patient information.
The present system saves each patients name, age, sex and
address, but no telephone contact number. As there is no
stigma associated with dengue infection, patient confidentiality
may not be a major problem at present. However, the easy
availability of identifiable names and addresses with little
restriction could threaten individual confidentiality.
This system is used for all notifiable infectious diseases,
including tuberculosis, but excluding HIV and sexually
transmitted infections, as they require a higher degree of
confidentiality of patient information.
Data management and analysis

Data can be edited at atoll level and at central level by HPA.
The approved users can also edit patient information online or
locally and upload into the system, and, conversely, download
63

Box 1:
Information collected in the communicable disease
notification form
Name of patient, age and sex, (hospital registration
number added by hospitals)
Address, separate fields for:
atoll
island
and two addresses:
permanent address
temporary address (in the island where the patient is
hospitalized). This is printed as Address in Mal in
reporting forms of IGMH.
(The instructions in the form do not specify to record the
address where the patient lived at the time of contracting
the disease.)
Date of onset of illness (not printed in IGMH form)
Date of admission (for admitted patients)
Date of consulting the doctor (for outpatients)
Names of the doctor who diagnosed, the doctor who
referred, and, finally, the doctor or person reporting (3
separate fields)
Diagnosis 2 fields:
preliminary or clinical diagnosis
confirmed diagnosis supported by laboratory tests
Case classification: suspected/probable/confirmed (not
printed in IGMH form)
Condition of the patient
Comments
Reporting persons name and signature and date.
(Forms in IGMH and Hulhumale hospital specify this
field as reporting doctor.
The fax number of CCHDC is given at the bottom of
the form for faxing reports. Two names and land phone
numbers of contact persons to be called in non-official
hours are also given in the form. However, the staff at
CCHDC has changed, and this is not updated on the
reporting forms.
The reporting hospital or institution is not included in
the template, but identified by the logo at the top of the
form, as individual hospitals prints their own forms.
blank templates and updated Excel spreadsheets to the local

computer. Editing is generally done following cross-checking
of the address of residence, or when the diagnosis or case
classification is revised following revised reports by notifying
health-care providers. Patients initially diagnosed with DF may
later be diagnosed as having DHF or DSS. Cross-checks for
64
data quality are only done on address at island level (required

for prevention activities), for patients from atolls outside main
cities, as the population is too high in Mal and main city
islands to trace addresses. Data were analysed manually.
Dissemination
Surveillance information is disseminated as annual
communicable disease surveillance reports. The surveillance
unit attempts to produce more frequent reports, such as biweekly reports, but their ability to keep up with this is highly
limited. The reports were uploaded onto the Ministry of Health
website, but the majority of doctors interviewed were not aware
of this. Atoll-level public health or medical record units analyse
and prepare annual reports, which focus more on the regional
hospitals own patient data than peripheral data (information
from three surveillance unit staff in regional hospitals).
Resources
HPA had two full-time surveillance officers and a programme
manager for the unit. They were overworked, and could not keep
up with targets. The estimate according to past performance
is that about six officers are required for efficient functioning
of the unit, including active surveillance for dengue and other
priority communicable diseases, analysing regularly for timely
detection of outbreaks and appropriate dissemination of data
for action. Atoll- and regional-level units have varying staff
numbers in hospital medical record units, usually between
one and three staff. Public health activities are carried out
by primary health-care workers, who have a diploma-level
training. The equipment required, such as computers and
communication equipment, were available. However, there
were limitations in the SIDAS software used, particularly for
data analysis, as it could only analyse proportions, it cannot
generate graphs or maps, and alert functions cannot be set-up.
Also, internet and internal network connections are not stable,
particularly in the atolls. The maximum outage was when
some atolls were unable to upload data online for a period of
about two weeks, owing to a malfunction of the online SIDAS
system. In such a case, the atoll stations maintain reporting by
faxing information to HPA.
Characteristics of the
surveillance system evaluated
Quality of data
The quality of data was generally acceptable but there were
some gaps. There are 11 mandatory core data fields (see
Box1); if these are not complete, the software is designed
to not save the case details. However, the core field date of
onset was incomplete for 69% of entries. These data have
been saved, by saving a default system date for the incomplete
cases. Therefore, the date of consultation or admission, which
was duly completed, was used for analyses.
Core data fields that may be inaccurate include: address

of residence, date of onset of illness, and surveillance case
classification, as their interpretation was left to the person
completing the form. Addresses of residence were verified
for cases from atolls, but not for cases from Mal, Addu and
Fuvamulah. Fifty-three per cent of patients were notified from
Mal. Clinical outcome was not included in the core data field.
A data field named Clinical condition was used in the system,
but doctors were not clear what was required from this field.
According to surveillance staff, it was meant to record whether
a patient died, recovered or was very sick.
Data are checked for duplicates and cleaned, and laboratory
confirmations and outcomes updated by the medical records
units of hospitals and the surveillance unit in HPA. There
were only 16 repetitions out of 2680 cases entered in the last
database by 13 October 2011 (0.06%).
Dengue was diagnosed mainly clinically and the case definition
was not strictly followed. Therefore, the positive predictive
value was 0.58, calculated using the proportion of patients
diagnosed with DF, DHF and DSS with clinical or laboratory
confirmation. Laboratory confirmation was not available for
the majority (91%) of patients, as dengue serology was often
not tested, particularly in Mal. This is because serology
is neither a requirement for treating dengue, nor the most
useful confirmatory test according to the case definition. The
confirmatory tests such as polymerase chain reaction (PCR),
virus isolation and quantitative dengue serology tests required
by the WHO case definition are not available in Maldives. In
order to detect circulating dengue virus (DENV) serotypes
during an epidemic, the surveillance unit obtains samples from
a cluster of 1020 patients and tests them from a reference
laboratory in another country the Armed Forces Research
Institute of Medical Science (AFRIMS), Thailand. Only
DENV-1 virus serotype was detected during the 2011 epidemic,
from nine samples obtained. This was not a new serotype to
Maldives, and had been detected in previous years as well.
Usefulness
The dengue surveillance data are useful to detect outbreaks
of dengue, but the usefulness in early detection was highly
limited at the time, owing to the absence of an automated early
warning of outbreaks and the difficulty of the surveillance unit
checking the dengue data of all atolls on a daily basis.
The data have provided some useful information, including
detecting the seasonal pattern of dengue infections, and
localizing pockets of outbreak, particularly construction
sites in Mal, that require preventive measures. It has helped
in quantifying the burden of disease in various areas for
planning resources, policy decisions and concentrating efforts
in improving clinical treatment. Thus, it seems to meet most
of the objectives of the surveillance system, except that of
providing early warning of outbreaks. Seroprevalence studies
have not been done to date.
Simplicity and flexibility

Dengue surveillance is part of the infectious disease surveillance
system. Data flow from the peripheries to HPA is relatively
simple using the online SIDAS database. However, it is not
so easy to verify data from the reporting person. The island of
residence of an identified case could be verified without much
difficulty, unless the individual lived in a major city (Addu
City, Fuvamulah or Mal). However, as IGMH enters data into
a different format and emails them, this added to the workload
of both IGMH and the surveillance unit at HPA, as these data
accounted for more than half of the notifications.
The doctors interviewed had different experiences. As clinical
assistants or ward clerks, who are non-medical support staff,
complete the forms for most doctors, these doctors found the
process simple, as they only needed to write the diagnosis and
sign the form. The two doctors interviewed from the medical
unit in IGMH completed forms themselves, and found it a
little cumbersome. This sometimes resulted in postponing
notification. The forms are in a format that requires most of the
requested information to be written; this resulted in variation
in information such as diagnoses, which affected the quality
of data.
As data analysis is not possible using the SIDAS system, the
data files have to be downloaded and analysed separately,
using MS Excel, and there is no automatic early warning built
in. This presents an additional burden to the surveillance unit.
The surveillance system is flexible enough to accommodate
changes in case definition. However, adding more data fields,
or tiers, and more complex analyses, such as analysis of data
by incidence rather than case numbers, and disease burden
analyses, are not yet possible.
Sensitivity
Sensitivity was 0.54 for inpatient notifications (n=154). The
breakdown by diagnosis showed that reporting rates were
similar for DF (40%) and DHF (38%), while 100% of DSS
cases were reported, reflecting the higher tendency to report
severe illness. Forty-one outpatient cases of DF and DHF
were reported. However, unreported outpatients were not
documented, so it was not possible to calculate sensitivity for
outpatients.
The system had not been adequately sensitive in detecting
outbreaks early, as experienced in the epidemic declared
from 1June, which could have been detected about three
weeks earlier (in the week of 814 May), and even as early as
February for control measures, as seen in the weekly time trend
graph (see Figure 2). There is no automatic alert to warn of
an outbreak. Surveillance staff had to look at disease patterns
manually by creating graphs each time. They were not used to
checking on a regular basis until after the epidemic occurred.
Since then, dengue data have been updated and checked for
outbreaks on a weekly basis. There was no formal event-based
surveillance system during this period.
65
Figure 2: Weekly dengue cases reported from Maldives in 2011, overlaid on trends for 2009 and 2010
Acceptability
A total of 126 centres were required to report dengue infections;
8.9% of health stations did not notify at the time of the study,
owing to unavailability of staff. Acceptability to the clinicians
reporting was poor. The doctors interviewed were not aware
of the usefulness and functionality of the surveillance system.
They felt that prevention activities were not carried out with
urgency, and were rather delayed at the time of the study.
They were not aware of surveillance reports uploaded on the
Ministry of Health website.10 Reporting rates from paediatric
versus medical inpatient units showed that 85% of paediatric
patients were reported in May, while only one adult patient
(1.7%) was reported. The paediatric unit treated almost twice
as many patients with dengue infections as the medical unit.
The majority of doctors interviewed claimed that they are
too busy and have to prioritize other work, such as patient
management, over reporting. Sometimes they forget to
report. In all units other than internal medicine, support staff
such as clinical assistants or ward clerks help in initiating
and completing reporting forms, while doctors only write
the diagnosis. This includes the paediatric ward and general
outpatient department. Medical officers in the emergency room
said that reporting is often not done there, where it is too busy
to report outpatients, and it is assumed that inpatients will be
reported during their stay. In medical wards, doctors carry out
the entire process.
Surveillance staff at IGMH Medical Records Unit claimed
that the workload was too much to keep up with. They also
claimed that clinicians do not report on time. They found
66
patients admitted with dengue from daily census sheets that

were not reported, but were not actively requesting clinicians
to report them. Surveillance staff at the central level were also
overworked, but very dedicated, and did their best to keep up.
None of the doctors interviewed, whether local areas or from
another country, were aware of the epidemiological reports.
Most thought that surveillance data were not published. Atoll
hospitals, public health units and councils were yet to be added
to the mailing list for receiving epi-reports.
Timeliness
It is expected that an outbreak will be investigated within two
weeks of first being reported.11 The average time from onset
of illness to reporting during the month of May 2011, before
the epidemic was declared, was 3days (median 2days). For
the month of June, the mean time was 10 days. More recently,
in September, after the frenzy of the epidemic had calmed
down, the average and median time from onset to reporting
was 4days. This would be acceptable given the natural history.
However, it may still not be accurate, as the majority of data
for onset of illness were missing (70% for May and 59%
for September 2011). The average time between the date of
consultation and date of reporting was half a day for May and
2 days for September; 56% and 30% of data were missing
for May and September respectively. The most appropriate
measure for timeliness (difference between the date of seeking
treatment and the date of entering the case in the surveillance
database) could not be calculated, as the date of receipt to

HPA and date of entry were not noted. The large proportion
of missing data also reduces the representativeness of this
calculation. Dissemination of data for action was also very
late, with a gap of 5 months for the last report.
The delay in detection and declaration of the outbreak suggests

the advisability of setting alert levels and incorporating an
automated alert in the system. If this is not possible, staff
should continue to check dengue trends at least on a weekly
basis. Since the epidemic, central-level staff now continue to
check on dengue trends on a weekly basis.
Discussion
The dissemination of reports needs to be improved, in order to

gain acceptability and improve reporting rates. Reports should
be shared on a regular basis, with reporting institutions, atoll
public health units and councils, in addition to policy-makers
at the Ministry of Health.
The quality of data showed significant gaps in date of onset,

and addresses showed some inaccuracy. This may have been
due to the fact that, at that time, health facilities printed and
used their own notification forms. The forms in IGMH did not
have date of onset printed on them; thus, this field would be
unlikely to be completed for over a half of the notifications
received from IGMH. The fields for recording address in
notification forms was difficult for the reader to understand
there were two addresses permanent address and Address
in Mal or address in island, and these varied across forms
in different facilities. Also, as the population of Maldives is
highly mobile, and patients are referred from various places,
there were confusions in noting address, unless the patient
or accompanying person was directly asked for it. Therefore,
it was suggested that this field should be revised to address
of present residence, with instructions to ask directly for
the address of residence at the time the patient became ill. It
was suggested that the field with the confusing term clinical
condition was replaced by outcome. The case definitions
were not utilized, despite the fact that booklets had been
printed. Case definitions should be more widely available to
reporting clinicians, by displaying the dengue case definition
as posters in wards.
The reporting rate of 54% of inpatients from IGMH was mainly
due to the poor reporting from the medical ward. The marked
difference between medical and paediatric wards showed that
delegating responsibility to nurses and clinical support staff
helped to improve the reporting rates greatly, compared to
giving the responsibility solely to the doctors. As many doctors
claim that they are too busy and have to prioritize other work,
such as patient management, over reporting, our opinion is that
the institutional responsibility policy helps to maintain some
degree of reporting, as other hospital staff are also given the
role of initiating the process of notification. We emphasize
the need to have good written protocols defining staff and
institutional roles and responsibilities that are available and
accessible to the surveillance staff and clinical staff expected
to notify diseases. This is particularly important because of the
high turnover of clinicians in Maldives. After the epidemic, as
instructed by HPA, the hospital medical records staff also began
the practice of calling wards to retrieve dengue notifications
that doctors had missed the previous days.
The unusual timeliness with a median time of only 2 days in
May may reflect some inaccuracy of recording the date of
onset, as dengue would generally be diagnosed about 35 days
from the onset of fever.11 The high variation with a delay of 10
days may be a bias induced by the increased workload during
the peak of the epidemic, as the time reduced during the later
months.
In conclusion, Maldives has a well-functioning surveillance

system for dengue. However, this study identified some gaps
that should be improved in order to improve the sensitivity,
acceptability and usefulness of the system, particularly in
detecting outbreaks early.
After sharing the findings and recommendations of this
evaluation with HPA, some changes were made to the
surveillance system. Case definitions for DF, DHF and DSS
were updated, in keeping with the WHO Regional Office for
South-East Asia 2011 guidelines,11 printed and sent out to all
health facilities to display in the doctors rooms and wards,
and also posted on the Ministry of Health website. The
communicable disease notification form was revised to enable
collection of mandatory information with greater ease, and
included answers that could be selected by tick-marks rather
than writing, with specific instructions for completion. The
new template was pre-tested, finalized and sent to all health
facilities, and uploaded onto the Ministry of Health website,
with instructions to use only this template and no other forms.
The surveillance unit in HPA has communicated with WHO
to improve the SIDAS online data-management system.
Discussions are under way to improve laboratory surveillance.
HPA is also in the process of compiling a legal regulation
for disease surveillance under the Public Health Protection
Act 7/2012, and guidelines for disease surveillance to be
used by health-care facilities. These will define the roles and
responsibilities of health facilities, as well as clinical, support,
medical records and public health staff, in the process of
disease surveillance.
Staff capacity-building by expanding HPA and training for
atolls is being conducted, and further training is planned to
improve the functioning of the system.
Acknowledgements
Our heartfelt appreciation for their time and support in
conducting this evaluation go to: Ms Geela Ali, Permanent
Secretary of Health, Ministry of Health and Family for
granting permission to conduct this evaluation and providing
vital information by interview; the Director Public Health
Programs, Head of Communicable Disease Division for
granting permission to interview staff and access the
surveillance system for conducting this study; and all those
who participated in this evaluation by interviews, including
staff of the surveillance unit at CCHDC, medical records
67
staff of IGMH and Hulhumal Hospital and doctors working

in wards, emergency rooms and out-patient departments of
IGMH and Hulhumal hospital.
7.
8.
References
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2.
3.
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6.
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World Health Organization. Dengue and severe dengue. Fact sheet no.
17, March 2014. Geneva: WHO, 2013. http://www.who.int/mediacentre/
factsheets/fs117/en/index.html - accessed 19 March 2014.
Republic of Maldives, Ministry of Planning and National Development.
Analytical report 2006: population and housing census 2006. Male:
MOP&ND, 2006.
Republic of Maldives, Ministry of Health and Family. The Maldives
health statistics 2009. Male: MOH&F, 2009.
Regional Technical Advisory Group (RTAG) on Dengue: report of the
second meeting. Bali, Indonesia, 2729 November 2012. New Delhi:
WHO-SEARO, 2012.
Republic of Maldives, Epidemiology and Disease Surveillance Unit.
Dengue epidemiological report 29th September 2011. Male: CCHDC,
2011.
Republic of Maldives, Minsitry of Health. Annual communicable
disease report 2011.Male: Center for Community Health and Disease
Control, 2011.
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11.
Guidelines Working Group. Updated guidelines for evaluating

public health surveillance systems: recommendations from the
Guidelines Working Group. Morbidity and Mortality Weekly Report.
2001;50(RR13):135.
Republic of Maldives, Minsitry of Health and Family. Case definition
for notifiable disease in Maldives 2008. Male: Centre for Community
Health and Disease Control, 2008.
SIDAS: an instant reference for atoll users - instructions manual. New
Delhi: WHO-SEARO, 2007.
Republic of Maldives, Minsitry of Health and Gender. Male: MOH&G.
http://www.health.gov.mv - accessed 20 March 2014.
World Health Organization, Regional Office for South East Asia.
Comprehensive guidelines for prevention and control of dengue and
dengue haemorrhagic fever. Revised and expanded. New Delhi: WHOSEARO, 2011.
How to cite this article: Abdulla AA, Rasheeda F, Ahmed IN,

Aboobakur M. An evaluation of the surveillance system for
dengue virus infections in Maldives. WHO South-East Asia J
Public Health 2014; 3(1): 6068.
Contributorship: AAA is the principal author who designed, collected data
for, and wrote the major part of the report, MA contributed to data collection
and writing the report, FR contributed to a significant part of data collection
and some analysis, INA contributed to data analysis.
Research brief
DOI: 10.4103/2224-3151.115828
Atypical presentation of visceral

leishmaniasis (kala-azar)
from non-endemic area
Yatendra Singh, Paramjeet Singh, Subhash Chandra Joshi, Mohammad Khalil

Department of Medicine,
Government Medical
College, Haldwani, India
Abstract
Leishmaniasis is a major public health problem in various part of world; it has also
emerged in new geographic areas and host populations. Visceral infection can
remain subclinical or become symptomatic, with an acute, subacute or chronic
course. Kala-azar, or visceral leishmaniasis (VL), presents as fever, pancytopenia
and hypergammaglobulinaemia. The presence of splenomegaly is characteristic
of VL. It may be absent in immunocompromised patients, who may present
atypically. Absence of splenomegaly is rare in immunocompetent patients, though
it may occur in the early stages. Atypical presentations can be challenging to the
clinician. This paper presents an atypical presentation of kala-azar, with multiorgan failure in the absence of splenomegaly or fever.

Dr Yatendra Singh, Room no. 32
Sr Hostel Government Medical
College, Haldwani 263139, India
Email: dryatendra84@yahoo.com
Key words: kala-azar without splenomegaly, multi-organ failure, pancytopenia,

visceral leishmaniasis
Introduction
Leishmaniasis is a vector-borne zoonosis with variable clinical
presentations, in the form of visceral, cutaneous (of localized
or diffuse types) and mucocutaneous types, depending upon
the Leishmania species and immune responses of the hosts.
Visceral leishmaniasis (VL) is endemic in various parts of India,
mainly Bihar, West Bengal and Orissa, as well as neighbouring
countries such as Nepal and Bangladesh. Recent increases
in the number of cases have been reported from nonendemic
areas of India.1 Atypical presentation of VL in an nonendemic
area can lead to a diagnostic dilemma. This paper reports VL
in a patient from a nonendemic region of India, who presented
with pancytopenia and multi-organ failure in the absence of
splenomegaly or fever.
Case History
The patient gave written informed consent for publication.
The patient was a 32-year-old woman, who did not smoke or
consume alcohol and who worked as a labourer in her native
region, Uttarakhand, India. She was admitted to hospital with
a 4-week history of weakness, vomiting, abdominal pain,
progressive dyspnoea, loss of appetite and weight loss. She was
severely anaemic and two units of packed red blood cells had
been transfused prior to admission. Intravenous ceftriaxone
at 1g twice a day had been administered by her general
practitioner for the past 5 days, but brought no symptomatic
relief. No significant past history was present. She had never
visited any area endemic for VL.
On physical examination, the patient was tachypnoeic and
tachycardic, with mild jaundice and severe pallor. Abdominal
examination revealed mild hepatomegaly, with tenderness in
the right hypochondrium. The remaining systemic examination
was normal. A chest radiograph was normal. Ultrasonography
of the abdomen revealed early medical renal disease and mild
hepatomegaly.
Laboratory investigations revealed that haemoglobin
was 38 g/L and normocytic normochromic anaemia with
pancytopenia was observed on peripheral smear examination;
total serum bilirubin was 54.72mol/L and serum creatinine
was 291.7mol/L. The transaminases were raised (serum
glutamic oxaloacetic transaminase [SGOT] 766IU, serum
glutamic pyruvic transaminase [SGPT] 555IU). Total
serum proteins were 65g/L and albumin was 15g/L. Others
tests, including arterial blood gas analysis, were in the normal
range. Tests for enteric fever, dengue, malaria, HIV and viral
hepatitis (A, B, C and E) were negative. The thyroid profile,
69
Singh et al.: Atypical presentation of visceral leishmaniasis
iron profile and vitamin B12 values were normal. Antinuclear

antibodies (ANA), cytoplasmic and perinuclear antineutrophil
cytoplasmic antibodies (c-ANCA and p-ANCA) and direct
Coombs tests were negative.
The patient had a working diagnosis of pyrexia with
pancytopenia, so Napiers aldehyde test was done and found
to be positive. To confirm the diagnosis of VL, a rK39
strip test and bone marrow examination were carried out.
The rK39 immunochromatographic strip was positive for
anti-K39 antibody. Intracellular and extracellular amastigotes
(LeishmanDonovan bodies) were visualized directly in
Giemsa-stained bone-marrow aspirate.
The patient was started on amphotericin B, at a dose of 0.5 mg/
kg/day after 1week and this was continued for 3weeks. By the
seventh day of treatment, she had improved symptomatically
as well as biochemically. Three units of whole blood were also
transfused to maintain her haemoglobin levels. At discharge,
the spleen tip was just palpable and the liver was not palpable.
The patient is under regular follow-up and is asymptomatic.
Discussion
VL ranges over the intertropical zones of America and
Africa, and extends into temperate regions of South America,
Southern Europe and Asia. There are an estimated 12 million
cases worldwide, with one and a half to two million cases
occurring each year.2 Ninety per cent of the VL cases in the
world are in Bangladesh, India, Nepal, Sudan and Brazil. VL
is a chronic infectious disease caused by Leishmania donovani
and characterized by irregular fever, hepatosplenomegaly,
weight loss, pancytopenia and hypergammaglobulinaemia.
There is infiltration of the reticuloendothelial system with
amastigotes, which gives rise to the clinical and biochemical
features. Splenomegaly is an important feature of the clinical
presentation, owing to the hyperplasia of the reticuloendothelial
cells that are filled with parasites. In one series, splenomegaly
was reported to be present in 100% of patients,3 but it may
be absent in immunocompromised patients, such as those
who are HIV positive, renal transplant recipients, those with
haematological malignancies and those on long-term steroids.
Rarely, it may be absent in acute cases, or in the early stages
of the disease.4,5
Milder forms of liver involvement occur in 17% of individuals
with VL,6 and are structurally and functionally reversible
after treatment. Pathophysiologically, liver involvement in
VL is typically self-limiting and involves a mononuclear celldominated granulomatous inflammation mediated by cytokines,
chemokines and reactive oxygen and nitrogen species.7 Several
authors have described renal pathological changes in VL.8,9
The main pathophysiological mechanism responsible for
renal impairment in VL probably includes the deposition of
immune complexes. The most frequent pathologies found are
proliferative glomerulonephritis and interstitial nephritis. The
development of acute kidney injury is an important clinical
complication in individuals with VL, which appears to increase
the mortality rate in this group of patients.10 The patient in this
study had both hepatic and renal involvement.
70
VL misdiagnosed as connective tissue disorders is well

reported in the literature . Haematological abormalities found
in systemic lupus erythematosus, namely anaemia, leukopenia
or lymphocytopenia and thrombocytopenia due to the presence
of auto-antibodies, can also be found in kala-azar.Leishmania
donovaniinfection induces nonspecific and specific antibody
production, much of which is probably due to parasite-released
substances, which act as B-cell mitogens. As a consequence of
B-cell hyperactivity,Leishmania donovaniinfection may cause
hypergammaglobulinaemia and production of auto-antibodies
such as ANA.1113 This may cause confusion in diagnosis. For
this reason, a careful clinical approach is required to reach a
definitive conclusion. For similar reasons, the patient in this
study was also investigated for these biochemical markers and
antibodies.
Conclusion
The case is presented to highlight the atypical presentation of
VL in a nonendemic region where the index of suspicion is
low. The patient presented with pancytopenia and multi-organ
failure, in the absence of splenomegaly and fever, which is an
unusual presentation of kala-azar.
Delayed diagnosis due to atypical manifestations can lead to
fatal outcomes for patients. Instead of relying solely on the
classical clinical features of VL, simple laboratory findings
like pancytopenia, altered albumin/globulin ratio and positive
aldehyde and rK39 strip tests can help make an early diagnosis,
even in atypical cases, thereby reducing the mortality of VL.
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Rheumatol. 2003;22:4525. Epub 2003 Oct 31.
Casato M, de Rosa FG, Pucillo LP, Ilardi I, di Vico B, Zorzin LR,et al.
Mixed cryoglobulinemia secondary to visceral Leishmaniasis. Arthritis
Rheum. 1999;42:200711.
How to cite this article: Singh Y, Singh P, Joshi SC, Khalil M.

Atypical presentation of visceral leishmaniasis (kala-azar) from
non-endemic area. WHO South-East Asia J Public Health 2014;
3(1): 6971.
Source of Support: Nil. Conflict of Interest: Nil.Contributorship: YS
introduction and discussion; PS introduction and discussion; SCJ case
history; MK data collection.
71
Research brief
DOI: 10.4103/2224-3151.115828
Profile of dengue infection in

Jamnagar city and district, west India
Krunal D Mehta1, Prakash S Gelotar1, Swati C Vachhani1,
Naresh Makwana2, Mala Sinha1
Department of Microbiology, Shri

MP Shah Government Medical
College, Jamnagar, India
2
Department of PSM, Shri MP
Shah Government Medical
College, Jamnagar, India
1
Abstract
Background
India is one of the countries in the World Health Organization South-East Asia
Region that regularly reports outbreaks of dengue fever (DF)/dengue hemorrhagic
fever (DHF). As effective control and preventive programmes depend upon
improved surveillance data, this study was carried out to report the seroprevalence
of dengue virus infection in an area around Jamnagar city, Western India.
Methods
The laboratory records of clinically suspected dengue patients from July 2008
to June 2011 were analysed retrospectively for the results of immunoglobulin
M (IgM) anti-dengue antibodies, tested by dengue monoclonal antibody (IgM)
capture enzyme-linked immunosorbent assay (MAC ELISA). Variations in disease
incidence by sex, age group and season were assessed.

Dr Krunal D. Mehta, Department
of Microbiology, Shri MP Shah
Government Medical College,
Jamnagar, Gujarat, India
Email: krunaldmehta@yahoo.co.in
Results
A total of 903 serum samples were tested, of which 253 were positive. The majority
were males (72%) and in the age group of 1630 years. The incidence of dengue
peaked in October and slowly tapered by December.
Conclusion
Dengue cases were higher during September to December, in the post-monsoon
season. This observation is useful for planning special preventive strategies. The
study draws attention to the susceptibility of the male, young adult age group.
Key words: Dengue, India, seasonal variation, vector
Introduction
In recent years, dengue has become a major global public
health concern. Approximately 2.5 billion people, living
mainly in urban areas of tropical and subtropical regions, are
estimated to be at risk of acquiring dengue infection.1 In India,
unplanned urbanization and migration of the population from
rural to urban areas with lack of proper sanitation facilities are
important factors that have resulted in an increased burden
of dengue in recent times.2 In the last decade, outbreaks and
deaths have been reported from northern states of Haryana,
Punjab and Uttar Pradesh; southern states of Andhra Pradesh,
Tamil Nadu and Karnataka; western states of Gujarat and
Rajasthan; and the eastern state of West Bengal. The casefatality rate has been less than 1% in recent years,3 but a
72
major outbreak associated with haemorrhagic manifestations

occurred in Calcutta in 2004.4 Since there is no specific
treatment or vaccine for dengue, prevention and control of
the disease mainly depend upon epidemiological surveillance
that provides reliable estimates of the disease, thereby helping
implementation of effective vector-control measures. This
retrospective study was carried out to assess the seasonal
variation in dengue cases in a tertiary care hospital, and health
centres in the surrounding district, to inform control measures
and preventive programmes.

This was a retrospective analysis of routine laboratory
diagnostic work; thus, ethical approval was not necessary.
Mehta et al.: Dengue in west India
Age and sex data on all patients who presented with signs and
symptoms of fever, headache and joint pain that were suggestive
of dengue virus infection, dengue haemorrhagic fever (DHF)
or dengue shock syndrome (DSS), at the Government Hospital,
Jamnagar, Gujarat, India, or at the primary and community
health centres in Jamnagar district between July 2008 and June
2011 were recorded. World Health Organization (WHO) criteria
were followed for inclusion or exclusion of a case of dengue
infection.5 Serum samples were tested for the presence of antidengue immunoglobulin M (IgM), using dengue monoclonal
antibody (IgM) capture enzyme-linked immunosorbent assay
(MAC ELISA) kit of the National Institute of Virology, Pune,
India.
Data on the beginning and end of the annual monsoon season
in Jamnagar district were taken from the sample-collection
register for dengue, available from the Department of
Microbiology, GG Hospital, Jamnagar, Gujarat, India.
RESULTS
A total of 903 acute-phase blood samples were collected
from clinically suspected cases of dengue virus infection. Out
of these, 253 samples (28%) were positive for dengue virus
infection. Fig. 1 shows that there were few dengue cases from
January to July each year; the incidence started to increase in
August to September, peaked in October and slowly tapered
by December, This shows a seasonal trend of dengue, which
correlates with the monsoon season in west India, and is from
the end of July to the start of November each year. The most
affected age group was 1630 years (125/253, 49%), followed
by 015 years (81/253, 32%), 3145 years (36/253, 14%), 46
60 years (10/253, 4%), and 60 years (1/253, 0.4%). Out of
the total 253 laboratory-confirmed dengue cases, 182 were in
males (72%) and 71 were in females (28%).
2008
DISCUSSION
In the past decade, dengue has been occurring regularly in
India, with periodic surges in the number of cases.6 Analysis of
the year-wise distribution of dengue cases revealed an unsteady
increase in the number of dengue patients over the past few
years. This may be partially attributed to the rapid unplanned
urbanization, with unchecked construction activities and poor
sanitation facilities contributing fertile breeding grounds for
mosquitoes; it is also true that an increased alertness to the
disease among the medical fraternity, following the initial
epidemic and the availability of diagnostic tools in the hospital,
has contributed to the increased detection of cases.7 To identify
the seasonal variation of the disease, analysis of the data on
a monthly basis was carried out. A gradual increase in cases
was noted from August, with a peak in September and October,
over each of the 4years studied. The correlation between
occurrence of dengue and the monsoon season is clearly evident
in this study, and is further supported by similar findings from
Kerala,8 Ludhiana,9 and Karachi.10 This may be because this
season is very favourable for breeding of the vector, i.e. Aedes
aegypti and Aedes albopictus.14 The presence of some dengue
IgM-positive cases even during dry months, as seen in this
study, probably reflects the year-round activity of the mosquito
vector. The year-round occurrence of dengue infection, with a
peak in the rainy season, is consistent with reported patterns
of dengue transmission.11 This seasonal outbreak of disease
transmission is very important at a local level, for effective
control measures, and emphasizes that preventive measures
against dengue infection should come into full swing during
water stagnation periods after the initial bouts of rainfall and at
the end of the monsoon period.
In this study, 28% of symptomatic patients were serologically
positive for dengue infection. The proportion of dengue cases
2009
2010
2011
Number of postivie cases
35
30
25
20
15
10
5
0
Jan
Feb
Mar
Apr
May June
July
Aug
Sept
Oct
Nov
Dec
Figure 1: Month-wise distribution of dengue cases

Note: the monsoon season in west India is from the end of July to the start of November each year.
73
Mehta et al.: Dengue in west India
for the age group 1630 years was highest, similar to the results
noted in a study by Kumar et al.;7 the order of prevalence was
followed by the age group 015years. However, in several
international studies, dengue has been reported to be mainly
a paediatric public health problem.12,13 Dengue infection
occurred in most active age groups, i.e. children and adults,
who were out of the house most of the time, either playing or at
work. This observation is noteworthy, because true endemicity
of dengue is reached when adult infection declines and only
the new entrants into the population, i.e. children, are affected
more by the disease.8 In the present study, males were found to
be more affected than females.
From the high incidence of dengue IgM seropositivity, it
appears that dengue is fast emerging as a major health concern
in this part of India. In the absence of specific treatment for
dengue, management is mainly supportive; further, there are
no vaccines currently available in market, thus early diagnosis
and vector control is the only method by which dengue can be
controlled.
The number of dengue cases was higher during September

to December in the post-monsoon season; this information is
useful for planning special preventive strategies. The study
draws attention to the male, young adult age group. The results
of this study indicate that dengue infection is unlikely to wane,
but is going to stay and will play havoc if immediate control
measures are not taken. There is an urgent need for a long-term
vector-control strategy, to prevent outbreaks. At the same time,
this will solve the problem of other mosquito-borne diseases
like chikungunya, Japanese encephalitis, malaria and filaria.
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Bennett SN, Holmes EC, Chirivella M, Rodriguez DM, Beltran M,
Vorndam V, Gubler DJ, McMillan WO. Selection-driven evolution of
emergent dengue virus. Mol Biol Evol. 2003 Oct;20(10):165058.
India, Ministry of Health and Family Welfare. Dengue cases and deaths
in the country since 2007. New Delhi: National Vector Borne Disease
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Control Programme, Directorate General of Health Services, 2013.

http://www.nvbdcp.gov.in/den-cd.html - accessed 24 February 2014.
National Institute of Communicable Diseases. CD Alert.Dengue/
Dengue Haemorrhagic Fever, Delhi, India. 2004;8:24.
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fever: diagnosis, treatment, prevention and control. 2 nd ed. Geneva:
WHO, 1997. pp. 1223.
Singh B. Dengue outbreak in 2006: failure of public health system?
Indian J. Community Med. 2007;32:99100.
Kumar A, Rao CR, Pandit V, Shetty S, Bammigatti C, Samarasinghe
CM. Clinical manifestations and trend of dengue cases admitted in a
tertiary care hospital, Udupi district, Karnataka. Indian J Community
Med. 2010;35:38690
Kavitha R. Dengue fever: the rise and the establishment of a new
disease in Kerala, India with special references to the capital,
Thiruvananthapuram. J Acad Clin Microbiol. 2007;9:6570.
Lal M, Aggarwal A, Oberoi A. Dengue fever: an emerging viral fever in
Ludhiana, North India. Indian J Public Health. 2007;51:1989.
Khan E, Siddiqui J, Shakoor S, Mehraj V, Jamil B, Hasan R. Dengue
outbreak in Karachi, Pakistan, 2006: experience at atertiary care center.
Reiter P. Climate change and mosquito-borne disease. Environ Health
Perspect. 2001 Mar;109(Suppl 1) :14161.
Shah GS, Islam S, Das BK. Clinical and laboratory profile of dengue
infection in children. Kathmandu University Med. J. 2006;13:404.
Anderson KB, Chunsutiwwat S, Nisalak A, Mameen P, Libarty D,
Rothman AL. Burden of symptomatic dengue infection in children at
primary school in Thailand: a prospective study. Lancet. 2007;369:1452
59.
Yukiko Higa. Dengue vectors and their spatial distribution. Trop Med
Health. 2011 Dec;39(Suppl 4):1727. http://www.ncbi.nlm.nih.gov/
pmc/articles/PMC3317606/ - accessed 24 February 2014.
How to cite this article: Mehta KD, Gelotar PS, Vachhani SC,
Makwana N, Sinha M. Profile of dengue infection in Jamnagar
city and district, west India. WHO South-East Asia J Public
Health 2014; 3(1): 7274.
Contributorship: KDM concept and design of study, data collection and
data analysis; PSG data collection; SCV data entry; NM analysis of
data, discussion writing; MS analysis of data. Acknowledgements: The
authors thank all the GG civil hospital, Jamnagar Clinic staff for providing
support for recruitment of patients and collection of samples, and also
acknowledge the Department of Microbiology, Shri MP Shah Government
Medical College, Jamnagar, for extending support for the study.
Policy and practice
DOI: 10.4103/2224-3151.115828
Mass primaquine preventive treatment

for control of Plasmodium vivax malaria
in the Democratic Peoples Republic
of Korea: a country success story
Shushil Dev Pant1, Kim Yun Chol3, Yonas Tegegn2,

Partha Pratim Mandal1, Ri Kwang Chol3
Office of the WHO Representative,

14-Munsudong, Pyongyang,
Democratic Peoples Republic of
Korea
2
Office of the WHO Representative,
Bangkok, Thailand
3
Ministry of Public Health,
Democratic Peoples
Republic of Korea
Abstract
In 1998, the resurgence of Plasmodium vivax malaria in the Democratic Peoples
Republic of Korea quickly increased to an epidemic, with 601013 cases reported
during 19992001. The introduction of mass primaquine preventive treatment
(MPPT) in 2002 was followed by a rapid reduction of malaria disease burden. The
intervention has been well accepted by the community. Doctors were part of a strong
functional health system with the ability to deliver interventions at the household
level. MPPT was considered for control of malaria after a study conducted in two
neighbouring endemic villages (ris) involving 320 healthy adults demonstrated that
presence of parasitaemia was significantly lower among those receiving MPPT
than those who did not. Similarly, in a mass blood survey conducted in the study
sites during May, 2002 involving 5138 persons in study and 4215 in comparison
areas, the total positive results were 710 times rarer in the treatment group
both before and after the malaria transmission season. In addition, the number
of malaria cases in the MPPT treatment ris was strikingly lower than control ris in
every month during the malaria transmission season of 2002. The prevalence of
G6PDD deficiency in DPR Korea is low, haemolytic events are rare and deaths
due to MPPT have not been reported. MPPT in itself is a powerful intervention
and the decision to deploy it depends on the epidemiology of malaria, urgency of
malaria control and resources available in the country.

Dr Shushil Dev Pant, Office
of the WHO Representative,
14-Munsudong, Pyongyang,
Democratic Peoples Republic of
Korea. Email: pants@who.int
Key words: Malaria, Democratic Peoples Republic of Korea, mass primaquine

preventive treatment, Plasmodium vivax
Background
The resurgence of Plasmodium vivax malaria in the Democratic
Peoples Republic of Korea followed the outbreak in 1998,
when 2100 malaria cases were reported. This outbreak occurred
after the country had been malaria free for more than 25 years.1
At the time, there was no outbreak-response plan, and limited
national expertise had been retained for malaria programme
management. Entomologists, microscopes, and people with
the skills to read malaria slides were scarce. There were limited
resources and capacity to scale up vector-control interventions.
In the absence of a rapid and appropriate response, the outbreak
soon spread nationwide. A total of 601013 cases were reported
over 19992001. Most of the people affected were adults
and only 712% of cases were children aged under 15years.
Agriculture workers were the predominant occupational group
affected. However, no mortality associated with malaria was

reported.2
In this setting, the World Health Organization (WHO) assisted
the Ministry of Public Health to introduce mass primaquine
preventive treatment (MPPT), starting with pilot studies
in 2002. The decision to deploy MPPT was also strongly
influenced by the encouraging experiences of other countries
that had prevalent P. vivax infection, with dual strains of short
and long incubation periods notably neighbouring China,
where about 30 million people were treated between 1973
and 1983.3 Introduction of MPPT in the Democratic Peoples
Republic of Korea contributed to significant reduction of P.
vivax malaria in subsequent years. This review describes the
evolution of the intervention and its contribution to malaria
control in the country.
75
Pant et al.: Mass presumptive primaquine treatment in DPR Korea
Materials and methods

International publications citing studies or reviews of diseasecontrol programmes in the Democratic Peoples Republic
of Korea are limited. This paper aims to share the countrys
success story, based on the limited documentation available.
The majority of references for development of the document
came from the assignment reports of the WHO malaria experts.
These experts worked in the country and were supported to
review the epidemiology of malaria after its resurgence there;
to design the study to assess the effectiveness of MPPT; to
develop the plan of implementation; and to monitor the progress
made in malaria control from 1998 to 2012. Information shared
during detailed discussion with the manager of the National
Malaria Programme and malaria experts in the country has also
been used as reference to enrich the document. Where possible,
the information provided by the national programme has been
verified against the documents in WHO archives. Publications
from neighbouring countries and experiences of countries that
have also successfully implemented MPPT to control malaria
have also been included, to improve understanding of the
MPPT concept, in an attempt to make this document more
comprehensive and useful for policy decisions.
The hypothesis: MPPT reduces

malaria transmission
Malarial infections in the Democratic Peoples Republic of
Korea during January to April (winter) are dormant and rarely
reported. In addition, the vectors of malaria begin to hibernate
from the end of November and mosquitoes are rarely spotted
until the end of April. Thus, malaria transmission is extremely
rare during winter months.2
According to the Ministry of Public Health, based on a research
conducted in 2000, P. vivax malaria parasites that are prevalent
in the Democratic Peoples Republic of Korea exhibit two
different durations of incubation period. For 2030% of the
P. vivax infections the incubation period is 23 weeks, while
for 7080% of infections it is 612 months.4 The report of this
research has not been shared, but the national programme is
confident of the reliability of the data. However, in the absence
of means for parasite genotyping, these conclusions are open
to debate.
Infections with short-incubation parasites manifest in the same
transmission season and the majority of infections (caused by
long-incubation parasites) are therefore asymptomatic in the
respective winter and manifest at the beginning of malaria
transmission season (May to August). In other words, in a

given year, 7080% of reported cases were infected in the
previous year and 2030% of cases are new infection or relapse
of the short-incubation type. Infections with long-incubation
parasites, and cases that will relapse in the transmission season,
were dormant during the immediate preceding winter.
Mass treatment with primaquine during winter will thus
reduce the number of individuals in the community who are
harbouring hypnozoites, thereby reducing the local parasite
reservoir. Despite an increase in vector density and human bite
rate in June to August, most anopheles bites are non-infectious.
As a result, the entomological inoculation rate becomes low
and malaria transmission decreases.[5]
Study of the hypothesis

A study was conducted in 2001 to test the above hypothesis.
The study aimed to evaluate the effectiveness of MPPT in
reducing reinfection or the relapse rate among treated and
non-treated cases.6 Two neighbouring endemic villages (ris)
were selected as the treatment and control sites. A total of 320
healthy adults without patent disease or contraindications to
primaquine administration (pregnancy, patients with lupus,
arthritis, leukaemia or hepatitis, or with a history of haemolysis/
hypersensitivity after taking primaquine) were selected for the
treatment arm. Other details of the characteristics of the sample
are not documented. Each case in the treatment arm received
15mg primaquine per day for 14 days in the month of March.
They were followed up for parasitaemia in subsequent months.
The results were compared with 320 adult controls who did
not receive primaquine. Owing to limited laboratory capacity,
the cases could not be reclassified into new, recrudescence or
relapse.
Table 1 shows the results of the prospective study. The
presence of parasitaemia was significantly lower (P<0.0001)
among those receiving MPPT. The study demonstrated strong
evidence that MPPT was an effective intervention to reduce
malaria transmission.
Piloting of MPPT in malaria

transmission areas
MPPT was introduced during February to April 2002 in seven
malaria-endemic counties of five provinces. The counties
selected for the piloting were: Kangnam, Sukchon, Sonchon,
Sinchon, Hwangju, Anbyon and Panmum.7 Malaria outbreaks
Table 1: Study of the effectiveness of primaquine prophylactic treatment for reducing reinfection or relapse
Infections detected during follow-up
Number
Malaria
cases
Relapse/
reinfection
rate, %
April
May
June
July
August
September
October
Primaquine
320
2.9
None
320
98
36.0
24
34
28
Regimen
Month, 2001
Relative risk = 10.9 (95% confidence interval=5.6 to 21.2, P<0.0001, Yates corrected 2 test).
76
were reported from all of the ris of the seven counties in

the preceding year. For a pilot study, each selected county
was further divided into treatment ris (total 91 ris in seven
counties) and control ris (total 85 ris in seven counties). In
the Democratic Peoples Republic of Korea, the villages are
isolated and cross-border contamination of control areas is
unlikely. Children under the age of 5years, pregnant women,
and patients with lupus, arthritis, leukaemia, hepatitis, or a
history of haemolysis/hypersensitivity after taking primaquine
were excluded from MPPT. In treatment ris, primaquine was
administered to all eligible 391357 inhabitants. The control ris
were represented by 421875 people above the age of 5years.
season of 2002, as shown in Table 3; the totals in this table also

show that there are 90% fewer cases of malaria in treatment ris
compared to control ris.
Assessment of side-effects and safety

The prevalence of glucose-6-phosphate dehydrogenase (G6PD)
enzyme deficiency in the Korean peninsula has historically
been reported as low. According to a WHO report, the trait of
G6PD deficiency has a prevalence between 0.5 and 2.9 % in
Korea; however the source of this information is not quoted
directly in the WHO report.8 In 2002, a study was conducted in
the Democratic Peoples Republic of Korea to assess the safety
of different durations and doses of primaquine treatment.7 The
first group (10022 persons) received primaquine 0.25mg/kg/
day for 7 days and a secondr group (10033 persons) received
primaquine 0.5mg/kg/day in two divided doses for 14days.
The overall reported rate of side-effects was slightly lower in
the first group (4.8%) as compared to the second one (6.5%).
No severe side-effects or deaths were reported.
In 2002, the government conducted a mass blood survey in the

study sites during May (5138 persons in study areas, 4215 in
comparison areas) and September (3716 persons in study areas,
2994 persons in control areas). The result from the survey are
shown in Table 2. The total number of positive results was 710
times lower in the treatment sample both before and after the
malaria transmission season. The results of the assessment also
concluded that the likelihood of being infected with malaria in
MPPT areas was 417 times lower than in untreated areas (see
Figure 1).7
In 2002, at the onset of MPPT, a total of 391357 people from

91 ris of seven malaria counties were targeted for MPPT. The
intervention was undertaken from 18 April to 3 May 2002.
Nearly 400000 follow-up cards to record probable sideeffects were printed in Korean language and distributed to ri
levels. These cards were filled in for each individual receiving
The total number of malaria cases in the pilot areas was studied
every month after the introduction of MPPT. The number of
cases of malaria in the treatment ris was strikingly lower than in
the control ris in every month during the malaria transmission
Table 2: Slide-positive rate (SPR) amongst primaquine-treated and control population

Population
May 2002
September 2002
Slides examined
Slides positive
SPR (%)
Slide examined
Positive
SPR (%)
Treated
5 138
0.04
3 716
0.03
Control
4 215
14
0. 33
2 994
11
0.37
1000
900
800
700
600
500
400
300
200
100
0
Kangnam
Sukchon
Sonchon
Sinchon
Study
Hwangju
Anbyon
Panmun
Control
Figure 1: Malaria incidence per 100000 population in study and control sites
77

Table 3: Malaria cases and incidence by counties among treatment and control ris, 2002
County
Ris
Pop
May
June
July
Aug
Sept
Oct
Nov
Dec
Jan
Feb
Total
Malaria
incidence
per 1000a
Kangnam
Treatment
33 030
12
0.36
Control
27 581
17
76
58
42
34
15
242
8.2
Treatment
86 000
10
51
24
101
1.12
Control
87 000
104
451
654
529
490
32
2 266
25.6
Sonchon
Treatment
54 470
13
13
19
58
1.04
Control
74 250
136
367
566
439
141
11
1 664
22.2
Sinchon
Treatment
72 857
13
19
57
239
158
24
511
6.7
Control
56 455
52
705
1 207
936
490
76
3 479
60.0
Treatment
74 030
11
14
39
16
89
1.20
Control
83 670
241
307
312
322
119
14
1 316
15.5
Treatment
40 970
33
35
37
131
2.8
Control
51 964
68
257
407
368
169
74
14
1 359
22.4
Treatment
30 000
45
56
61
142
148
42
501
15.1
Control
40 955
646
584
979
834
699
166
16
3 930
91.4
Sukchon
Hwangju
Anbyon
Panmun
Malaria incidence was calculated by using the total population of the village as denominator.
Delivery of MPPT
primaquine treatment, by their respective doctors. An analysis
of the content of these cards revealed that the prevalence of
various side-effects was very low and did not exceed 4%. Most
importantly, no cases of severe haemolysis were reported, as
shown in Table 4.10 Cases with suspected haemolytic symptoms
discontinued the drugs and were referred to higher centres for
treatment. All of them recovered in the subsequent 35 days
and were excluded from future rounds of MPPT. The national
programme has confirmed that no death related to MPPT has
been reported in the country so far.
Table 4: Prevalence of side-effects among persons
treated with primaquine, 2002
Side-effects
Number of
people with
symptoms
Proportion of
side-effects (%)
Headache
4 291
32.1
Epigastric pain
2 451
18.3
Nausea and vomiting
1 801
13.5
Dizziness
1 753
13.1
Anorexia
1 702
12.7
254
1.9
Changed urine color

Black-coloured urine
Others
Total
78
15
0.1
1 098
8.2
13 365
100.0
Encouraged by the results of the studies on the effectiveness

and safety of MPPT, the national programme implemented
MPPT every year from 2002 to 2007. MPPT was completed
each year before April. Owing to limited resources, the country
could not conduct the mass campaign in 2008, 2011 and 2012.
In every ri of the Democratic Peoples Republic of Korea, there
is at least one ri hospital with about 610 doctors. The health
care of all members of a unit of about 150250 households
(HH) is a primary responsibility of each doctor.
A task force plans and delivers MPPT in each ri. The task force
consists of a supervisor from province or county level and all the
HH doctors of the target ri. Volunteers from the community are
an integral part of the planning and delivery process. The HH
doctors/volunteers visit house to house, to identify and record
inhabitants eligible for the mass treatment in the respective
year. The target excludes children aged under 5 years, pregnant
women, people with a history of side-effects with primaquine,
and people with a history of liver or blood disorder. Prior to
implementation of MPPT, HH doctors/volunteers were trained
on recording and reporting, calculation of dose, ensuring drug
compliance and monitoring of side-effects of the drugs.
A daily primaquine dose of 0.25mg/kg was administered after
breakfast for 14 consecutive days,10 under direct observations.
Before ingestion of the daily dose, the doctors inquired about
the symptoms of side-effects of the drugs and looked for any
signs of haemolysis. Any such observation was recorded and
all individuals with suspected haemolytic or any other serious
side-effects were immediately excluded from treatment and
referred for appropriate care.
It was a major challenge to break a 7.5 mg primaquine tablet to

provide a dose of 0.25mg/kg/day to a child. However, the HH
doctors and volunteers tried to adhere to the national guideline
as far as practical.
The proportion of people completing a full course of
primaquine in the mass campaign was always over 94%; it was
difficult to achieve 100% coverage of the targeted population,
as individuals with suspected haemolytic symptoms were
excluded from further treatment. In addition, there was
a difference between baseline data and the actual size of
household numbers, owing to death or migration of members.
Impact of MPPT
The burden of malaria began to decline after introduction of
MPPT in 2002. The total number of cases was reduced by 80%
following two round of MPPT in 2002 and 2003. A similar
trend was observed in the subsequent years. Compared to
2001, the total malaria burden had decreased by 90% in 2012.
An increase in the number of malaria cases was observed when
MPPT could not be conducted in a particular year. Details of
the impact of MPPT during 20022012 are shown in Table 5.
Presumptive treatment with chloroquine for all fever cases
also contributed to reduction of malaria transmission. In an
effort to confirm cases before treatment, expansion of malaria
microscopy centres started from the year 2001, and capacitybuilding in malaria microscopy was a high priority for the
government. Up to 2004, 4060% of suspected malaria cases
were tested annually and those with a positive result received
radical treatment. The microscopy confirmation improved
to 7090% among suspected cases in subsequent years.
However, data on the accuracy of the results of microscopy are
not available. A drug-effectiveness study conducted in 2005
and 2012 confirmed that chloroquine is effective against the
existing P. vivax strain prevalent in the Democratic Peoples

Republic of Korea .
In addition, during 20022009, there were attempts to improve
coverage of vector-control interventions. Owing to limited
resources, the interventions were only rolled out to selected
areas and were inadequate to control malaria transmission
in the country. DDT was used from 2001 to 2003 and only
10000 people benefited from indoor residual spraying.7 There
are reports that bed nets (insecticide treated and untreated)
were also widely used; however, there are no data available
on coverage and use to make conclusions on the effect the nets
had to contain the outbreak. Communities were encouraged
to reduce vector breeding sites and burn moxa (mugwort,
Artemisia vulgaris, Artemisia leaf) to repel mosquitoes away
from the communities. In the absence of data and studies on
the effectiveness of traditional vector-control interventions, it
is difficult to measure their contribution to reducing the burden
of malaria.
With support from the Global Fund Round 8 Malaria grant,
711960 long-lasting insecticidal nets have been distributed
to malaria-affected communities in the Democratic Peoples
Republic of Korea from 2010 to 2012. During the same period,
more than 450000 households and 90000 agriculture and
night-time workers have been protected with insecticide-treated
clothes each year. The pyrethroid group of insecticides was
preferred for ease of operation, and because they are effective
against malaria vectors. Malaria microscopy services have been
expanded to 1023 centres and about 90% of suspected cases
are being confirmed. The contribution these efforts have made
to reduce malaria transmission is under study. Table 5 also
demonstrates that the number of malaria cases increased in the
years MPPT was not conducted (2008, 2011, 2012). Irrespective
of the coverage of other malaria-control interventions, MPPT
is essential to reduce the burden of malaria disease in the
Democratic Peoples Republic of Korea.
Table 5: Reduction in the number of malaria cases after introduction of MPPT

Percentage decrease of
case burden compared
to previous year
241000
19
19
425475
60559
80
75
Number of cases treated

with MPPT
Cases of malaria
reported
2001
296540
2002
396644
2003
2004
392829
33803
89
44
2005
449700
11507
96
66
2006
378366
9353
97
19
2007
4904261
7436
97
21
2008
23409
92
215 (increase)
2009
826344
16679
94
29
2010
968818
15392
95
2011
17518
94
14 (increase)
23537
90
26 (increase)
2012
a
Percentage decrease of
case burden compared
to 2001
Year
MPPT not conducted in this year.
79
Conclusion
3.
MPPT is a success story of the Democratic Peoples Republic

of Koreas programme to control P. vivax malaria. Since the
introduction of the intervention, a drastic decrease in malaria
burden has been observed in the country. A strong health
system is essential for proper planning of the mass campaign,
with monitoring and achievement of high coverage, and for
drug compliance and monitoring of the side-effects. Inadequate
resources interrupted MPPT in 2008, 2011 and 2012, and an
increase in malaria cases was observed in each of these years.
Further resources need to be mobilized to ensure continuity of
MPPT to achieve further gains in malaria control.
The contraindications and compliance to the long regimen of
primaquine treatment are the major limitations to the ability of
MPPT to have an impact. MPPT needs to be complemented
by other interventions to eliminate P. vivax among individuals
with contraindications to primaquine treatment. At the same
time, resistance of the local P. vivax strain to primaquine needs
to be studied at intervals, to ensure the intervention is effective.
The urgency of malaria control, as well as the resources
available in the country and ethical issues related to mass
primaquine administration, need to be carefully considered
before a decision is made to implement MPPT.
References
1.
2.
80
Chol PT, Suwannapong N, Howteerakul N. Evaluation of a malaria

control project in DPR Korea, 2001-2003. Southeast Asian J Trop Med
Public Health. 2005 May; 36(3):56571.
Kondrachine AV. Malaria control in DPR Korea: assignment report:
3-25 July 2001. New Delhi: World Health Organization, Regional Office
for South-East Asia, 2001.
4.
5.
6.
7.
8.
9.
10.
Hsiang MS1, Hwang J, Tao AR, Liu Y, Bennett A, Shanks GD, et al.
Mass drug administration for the control and elimination of Plasmodium
vivax malaria: an ecological study from Jiangsu province, China. Malar
J. 2013 Nov 1;12:383.
Nguyen Hoan Phu. Malaria Mass Prophylaxis with Primaquine in DPR
Korea: assignment report 17 April 15 June 2002. New Delhi: World
Health Organization, Regional Office for South-East Asia, 2002.
Kondrashin AV, Baranova AM, Sergiev VP. Widespread use of
primaquine for control of Plasmodium vivax epidemics in a population
with varying degrees of G6PD deficiency. Med Parazitol (Mosk). 2010
Oct-Dec;(4):248.
Arbani PR, Schapira A. Mission report to DPR Korea. New Delhi: WHO
Regional Office for South-East Asia, 2002.
Pinyowiwat V. Malaria control in DPR Korea: experiences on
primaquine prophylaxis. New Delhi: WHO Regional Office for SouthEast Asia, 2003.
WHO Working Group. Glucose-6-phosphate dehydrogenase deficiency.
Bulletin of the World Health Organization. 1989; 67: 601611.
Outcome and impact of mass chemoprophylaxis with primaquine on
Vivax malaria in the DPR Korea, Assignment Report: 1 30 June 2007,
Dr AV Kondrashin, WHO Short-term consultant. New Delhi, 2007.
Ministry of Public Health, DPR Korea. National malaria treatment
guideline. 2002
How to cite this article: Pant SD, Chol KY, Tegegn Y, Mandal
PP, Chol RK. Mass primaquine preventive treatment for control
of Plasmodium vivax malaria in the Democratic Peoples
Republic of Korea: a country success story. WHO South-East
Asia J Public Health 2014; 3(1): 7580.
Policy and practice
DOI: 10.4103/2224-3151.115828
Monitoring the durability of long-lasting

insecticidal nets in field conditions in Nepal
J Hii1, GD Thakur2, BR Marasini2, YR Pokhrel2, MP Upadhyay2,
KRRijal3, NR Adhikar3, SK Pant4, L Ortega5, N Singh5, P Ghimire5
School of Public Health, Tropical

Medicine and Rehabilitation
Sciences, James Cook University,
Australia, 2Epidemiology and
Disease Control Division,
Department of Population Health,
Kathmandu, Nepal, 3Kantipur
College of Medical Sciences,
Kathmandu, Nepal, 4VectorBorne Disease Research and
Training Center, Department of
Population Health, Hetauda, Nepal,
5
Country Office and South-East
Regional Offices, World Health
Organization, Nepal and India
1
Abstract
Understanding and improving the durability of long-lasting insecticidal nets (LLINs)
in the field is critical for the success of malaria prevention using mosquito nets,
as well as contributing to procurement decisions based on the number of years
of protection, rather than the current practice of unit cost. Using the recently
published guidelines from the World Health Organization (WHO) some progress
has been made in the monitoring and assessment of performance of nets in the
field. This paper describes the protocol of an ongoing retrospective study of the
attrition rate, physical integrity and bioefficacy of three polyester LLIN products
that were distributed during 2010 to 2013 in Nepal. It is hoped that robust and
auditable data on net survival (physical integrity and bioefficacy) of these three
brands in different environments will assist the Nepal National Malaria Control
Programme in planning future LLIN-replacement strategies, including behaviourchange communication about LLIN care and maintenance. The advantages and
disadvantages of prospective and retrospective cross-sectional approaches
are discussed, including appropriate strategies to validate the timing for mass
distribution of nets. Similar studies should be done in other countries to (i) track
LLIN durability to support management of resupply, and (ii) inform procurement
decisions at the global level. New, more predictive, textile laboratory testing is also
urgently needed.

Dr Jeffrey Hii, School of Public
Health, Tropical Medicine and
Rehabilitation Sciences, James Cook
University, QLD 4811, Australia.
Email: hiijk1@gmail.com
Key words: Bioefficacy, long-lasting insecticidal nets, malaria, malaria control,

malaria transmission, physical integrity
BACKGROUND AND RATIONALE

The National Malaria Control Programme in Nepal is using
indoor residual spraying (IRS) and long-lasting insecticidal
nets (LLINs) to reduce the transmission of malaria, with the
long-term goal of malaria elimination, in line with World
Health Organization (WHO) recommendations,13 and the
regional malaria-control strategy.4 Distribution and promotion
of the use of LLINs is an integral component of the National
Malaria Control Programme. Since 2005, 3.3 million LLINs
have been distributed with support from the Global Fund.5
The national LLIN distribution policy 2005 recommended one
LLIN per household in endemic districts in stratum 1; this was
later changed in 2009 to one LLIN for two persons. By the
end of 2013, the estimated LLIN coverage was 100% of target
population in high- and moderate-risk areas. The procurement
and distribution of LLINs in Nepal was mainly managed

by Population Services International (PSI-Nepal), and all
other activities of malaria prevention and control activities
are implemented by the Epidemiology and Disease Control
Division (EDCD). Since 2007, WHO has promoted universal
coverage with effective methods of vector control for everyone
at risk of malaria.1, 6 Recently, WHO has also recommended free
distribution of nets through mass campaigns, complemented
by continuous distributions through antenatal-care facilities
and child immunizations,7 in order to achieve and sustain the
goal for universal coverage. For procurement purposes, this
requires an overall ratio of one LLIN for every 1.8 people
in the target population; this is based on an allocation of one
LLIN per two persons, adjusted for the effect of odd-numbered
households.8 LLINs were developed in the 1990s and first
approved by the WHO Pesticide Evaluation Scheme in 2003.
81
Hii et al.: Durability of long-lasting insecticidal nets in Nepal
LLIN technology is based on the slow release of pyrethroid

insecticides, rendering them wash resistant and extending
insecticide residual effectiveness to at least 3years without the
need for retreatment.1,9
As the largest funder for malaria programmes, Global Fund
financing helped provide over 310 million LLINs for malaria
control between 2002 and 2012,10 resulting in a rapid increase
in bednet ownership and utilization (in addition to largely
used conventional nets) in the target population.11 However, a
critical question, which has direct implication for the success
of malaria control, remains: How long does an LLIN last
in serviceable condition, under field conditions? Current
budgeting for LLINs is based on an assumption that LLINs have
an average useful life of at least 3 years.1,9 However, there is a
significant paucity of information on LLIN survival time, the
variation in performance between LLINs of different textiles,
and the general environment in which the net is being used
(climate, housing, sleeping place and washing patterns). For
these reasons, a recent publication by WHO provided guidance
on how to estimate the longevity of nets using durability data
from the field.12
Villagers in Nepal generally wash clothes and LLINs with
detergent powder and soap and dry them in sunlight for
45 hours. In 2008, bioassays tests conducted in Dhanusha,
Kanchanpur, Kavre and Makwanpur districts, with LLINs
washed up to three times, showed 100% mosquito mortality.5
In 2009, bioassay tests carried out in Banke, Dang, Dhanusha,
Kanchanpur, Morang and Nawalparasi districts, on LLINs
washed not more than twice, also showed 100% mosquito
mortality. After the fourth washing, there was a sharp decline in
mortality to 42% in Kanchanpur district.5 The report concluded
that LLIN distributed in 2010 had many public comments like:
it was weak, not durable and not effective like previous LLIN.
In reality, there is considerable variation in LLIN durability in
relation to their conditions of use, for example, local washing
and drying techniques and storage. These factors may partly
explain the observed variations.13
Field data on LLIN survival are not currently available to
inform the National Malaria Control Programme on the timing
and nature of future LLIN replacement strategies, including
changing peoples behaviour with respect to care and repair
of nets, that is, avoiding holes and repairing them early to
prevent deterioration. Acknowledging this gap, the Ministry of
Health and Population requested WHO to give guidance on
this question, and to assist in the planning and implementation
of a retrospective study of LLINs that were distributed during
2010 to 2013.
This paper summarizes the protocol of this study and the
progress to date. As far as the authors are aware, this is the
second study of this type in the WHO South-East Asia Region.
Similar studies in other countries where the use of LLINs is
one of the key strategies for malaria prevention and control are
also advocated.
82
STUDY PROTOCOL:
OBJECTIVES AND METHODS
The objectives of this ongoing study are: (i) to assess the
physical integrity and bioefficacy of three polyester LLIN
products; (ii) to determine the attrition rate of LLINs and
factors that have contributed to attrition in four eco-zones since
2010; and (iii) to compare the use of LLINs distributed since
2010.
The study was conducted in 11 districts representative of the
four ecological zones, that is, (i) Terai plain rice (2districts);
(ii) Terai foothill (3 districts); (iii) Inner Terai forest fringe
(3districts); and (iv) hills and river valleys (3 districts).
Information on physical integrity (holes), bioefficacy and
attrition in local conditions was collected using a standardized
questionnaire, and analysed to allow the programmes to gather
scientific evidence related to the study objectives.
Using the method of Kilian for estimating the necessary
sample size,14 a sample of 40 LLINs per village development
committee (VDC) was considered sufficient. This was based
on the assumption of one measurement for each of the nets per
time point, an alpha error of 0.05, power of 80%, and standard
deviation of 8.0.
A total of 440 households were randomly selected from VDCs
of the above districts, with a range of 3050 households per
district. VDCs were selected on the basis of LLIN distribution
dates, having >50 households, and being representative of
the major ethnic tribes. Household rosters showing dates of
LLIN distributions, and GPS points available from PSI were
used to validate the identity of household locations including
interviews with household heads by district/health facility
staff. Households were randomly selected from this list prior
to the follow-up surveys; if the householder was absent, or if
the house was no longer in the VDC, the next house on the list
was selected.
After getting informed consent, the interview was conducted
and one randomly selected LLIN was collected and replaced
with a new LLIN. Each LLIN sampled was hung up from the
four corner points and examined. The size of holes, divided
into the categories <0.5cm, 0.52cm, 210cm, and >10cm
diameter; their position on the LLIN; and the number of holes
in each category were recorded. Hole categories are designed
to be easily and accurately measured under field conditions and
were weighted as 1, 23, 196 and 578, respectively. The number
of holes in each category was multiplied by the category weight
and expressed as a proportionate hole index (PHI).13
From each of the LLINs collected, four pieces 2525cm in size
were cut from four sides of the net as per WHO guidelines,13
using sharp scissors. For chemical assays, 10% of randomly
selected LLINs were selected; four subsamples per LLIN were
assembled as one sample, rolled up and placed in a new, clean
aluminium foil, labelled and stored at room temperature for
chemical analysis at Walloon Agricultural Research Centre,
WHO Collaborating Centre for Quality Control of Pesticides,

Gembloux, Belgium. Another two sets of four subsamples
were similarly rolled up in clean aluminium foils and tested
using standard WHO cone bioassay methods, at the Vector
Borne Disease Research and Training Centre Hetauda and
Kasetsart University, Thailand.
STUDY IMPLEMENTATION: UPDATE

The study was approved by the National Health Research
Council, Kathmandu, Nepal. Villagers are informed about the
aims and objectives of the study through house-to-house visits.
Information on various aspects of the study was read in the
local language and written consent was obtained from each
household before the start of the interview.
An orientation workshop was conducted to finalize the survey
protocol with EDCD, Kantipur College of Medical Sciences
research team, and enumerators. A precoded, structured
questionnaire was adapted from the WHO guidelines,13
pretested and adjusted for any issues arising from the piloting
in Kavre and Sindhupalchowk districts. Data collection
commenced in December 2013. The information collected
through survey questionnaires and reports of cone bioassay
and chemical analysis13 will be entered in a Microsoft Access
database and analysed using SPSS statistical software.
The field survey in 11 districts representing four different
ecological zones were completed; 440 LLINs (4 triplicate
pieces from 440 nets) were collected by the end of January
2014. The LLIN pieces are undergoing bioassay at the Vector
Borne Disease Research and Training Centre, Hetauda and
Kasetsart University, Thailand, and the chemical content of
10% of the samples representing different locations, brands and
years of distribution are being tested at the WHO collaborating
centre in Belgium. The results from the analysis are expected
to be available soon, and will provide the National Malaria
Control Programme with scientific evidence for policy review.
In view of the huge investments on LLINs for malaria control,

amounting to USD500 million every year,11, 15 and the fact
that, with the exception of IRS, there is no other malaria vectorcontrol tool that could be easily scaled up to help accelerate
progress in malaria control towards elimination, a similar
study should be carried out in other countries, to track LLIN
durability. This would support management of resupply, and
inform, at global level, procurement decisions, in conjunction
with urgently needed new, more predictive textile laboratory
testing. It should be noted that there is an urgent need for the
development and validation of novel vector-control strategies,
since LLINs and IRS are not sufficient to combat outdoor and
early-biting transmission of malaria, which is a major concern
in South-East Asia.
Acknowledgements
The authors acknowledge Nepal Health Research Council for
permission to conduct the study, TGF / PSI- Nepal for funding
the study channeled through WHO Nepal, MoHP/DOHSNational Malaria Program for programmatic support for the
study and WHO for technical support.
REFERENCES
1.
2.
3.
4.
5.
DISCUSSION AND RECOMMENDATIONS

In this study protocol, the following possible limitations were
considered: (i) the survival of LLINs cannot be estimated in
most settings; (ii) LLINs available may be a biased sample, as
worn-out LLINs may no longer be present; (iii) a significant
and unknown portion of the local population has moved into
or out of the study area; (iv) the number of opportunities for
follow-up are limited; (v) labels on LLINs fade or are lost
over time, making identification difficult; and (vi) recall by
users of what happened more than 12 months previously may
be unreliable. However, prospective studies obviate some of
the disadvantages listed above, compared with retrospective,
cross-sectional studies.13 Protocol development for comparing
different products is required to test the true performance
of some brands, which may reach 4 years or more in some
environments.14 This may include the one or more products
that are already in large-scale use in that setting, together with
some selected alternatives (e.g. some of those that bid for the
last tender but were not selected).
6.
7.
8.
9.
10.
World Health Organization. Global malaria programme: insecticide

treated nets: a position statement. Geneva: WHO, 2007. http://www.
who.int/malaria/publications/atoz/itnspospaperfinal.pdf - accessed 17
March 2014.
Roll Back Malaria. The global malaria action plan for a malariafree world. Roll Back Malaria Partnership, 2008. http://www.
rollbackmalaria.org/gmap/gmap.pdf - accessed 17 March 2014.
World Health Organization. Indoor residual spraying: an operational
manual for indoor residual spraying (IRS) for malaria transmission
control and elimination. Geneva: WHO, 2013.
The revised malaria control strategy 2006 2010. New Delhi: WHOSEARO. Document no. SEA-MAL 243 (Rev 1).
Nepal, Ministry of Health and Population. Nepal malaria strategic plan
20112016. (Revised version-December 2011). Teku, Kathmandu:
MOH&P, Department of Health Services, Epidemiology and Disease
Control Division, 2011. http://apmen.squarespace.com/storage/ countrypartner/Nepal%20Strategic%20Plan%202011-1016.pdf accessed 17
March 2014.
United Nations. Secretary-Generals message on world malaria day.
25 April 2012. http://www.un.org/sg/statements/index.asp?nid=6023 accessed 17 March 2014.
World Health Organization. WHO recommendations for achieving
universal coverage with long-lasting insecticidal nets in malaria control,
September 2013. Geneva: WHO, 2013. http://www.who.int/malaria/
publications/atoz/who_recommendation_coverage_llin/en/ - accessed
17 March 2014.
Kilian A, Boulay M, Koenker H, Lynch M. How many mosquito nets
are needed to achieve universal coverage? Recommendations for the
quantification and allocation of long-lasting insecticidal nets for mass
campaign. Malaria J. 2010;9:330.
World Health Organization. Guidelines for laboratory and field
testing of long-lasting insecticidal nets. Geneva: WHO, 2013.
Document no. WHO/HTM/NTD/WHOPES/2013.3. www.who.int/iris/
bitstream/10665/80270/1/9789241505277_eng.pdf - accessed 17 March
2014.
Global Fund to Fight AIDS, TB and Malaria. Strategic investment for
Impact: global fund results report 2012. Geneva: GFATM, 2012.
83

11.
12.
13.
14.
15.
84

report_2012/report/en/ - accessed 17 March 2014.
World Health Organization. WHO Guidance note for estimating the
longevity of long-lasting insecticidal nets in malaria control. Geneva:
WHO,
2013.
http://www.who.int/malaria/publications/atoz/who_
guidance_longevity_llins/en/ - accessed 17 March 2014.
World Health Organization. Guidelines for monitoring the durability
of long-lasting insecticidal mosquito nets under operational
conditions. Geneva: WHO, 2011.
http://whqlibdoc.who.int/
publications/2011/9789241501705_eng.pdf - accessed 17 March 2014.
Kilian A. Estimating the potential gains and savings from increased
mosquito net durability. Networks document, Networks, September
2011.
World Health Organization. WHO global malaria programme: a system
to improve value for money in LLIN procurement through market
competition based on cost per year of effectuive coverage. Concept
Note. Geneva: Global Malaria Programme. http://www.who.int/malaria/
publications/atoz/gmpllin_effective_coverage_concept_note.pdf
How to cite this article: Hii J, Thakur GD, Marasini BR,

Pokhrel YR, Upadhyay MP, Rijal KR, Adhikar NR, Pant SK,
Ortega L, Singh N, Ghimire P. Monitoring the durability of
long-lasting insecticidal nets in field conditions in Nepal. WHO
Source of Support: This study was financially supported by the World
Health Organization and the Global Fund. Conflict of Interest: None
declared. Contributorship: JH and LO designed the study, with inputs
from PG, who coordinated the field and laboratory activities and drafted the
manuscript. GDT and BRM facilitated the training workshop and ethical
review; YRP, MPU, KRR, NRA, SKP and NS supervised the field studies
with the assistance and inputs from students of Kantipur College of Medical
Sciences. All authors contributed to the final version of the text and have
read and approved the manuscript.
Policy and practice
DOI: 10.4103/2224-3151.115828
Malaria elimination in Sri Lanka: what

it would take to reach the goal
Risintha Premaratne1,Leonard Ortega2,
Navaratnasingam Janakan3, Kamini N Mendis4
Abstract
Anti-Malaria Campaign,
Narahenpita, Colombo 5, Sri Lanka;
2
World Health Organization SouthEast Asian Regional Office, New
Delhi, India; 3Country Office of
the World Health Organization,
Sri Lanka, Bauddhaloka Mawatha,
Colombo 7, Sri Lanka; 4141 Jawatta
Road, Colombo 5, Sri Lanka
1
Fifty years after narrowly missing the opportunity to eliminate malaria from Sri
Lanka in the 1960s, the country has now interrupted malaria transmission and
sustained this interruption for more than 12 months no indigenous malaria
cases have been reported since October 2012. This was achieved through a
period overlapping with a 30-year separatist war in areas that were endemic for
malaria. The challenge now, of sustaining a malaria-free country and preventing
the reintroduction of malaria to Sri Lanka, is examined here in the context of rapid
postwar developments in the country. Increased travel to and from the country to
expand development projects, businesses and a booming tourist industry, and the
influx of labour and refugees from neighbouring malarious countries combine with
the continued presence of malaria vectors in formerly endemic areas, to make
the country both receptive and vulnerable to the reintroduction of malaria. The
absence of indigenous malaria has led to a loss of awareness among the medical
profession, resulting in delayed diagnosis of malaria despite the availability of
an extensive malaria diagnosis service. Highly prevalent vector-borne diseases
such as dengue are competing for health-service resources. Interventions that
are necessary at this critical time include sustaining a state-of-the-art surveillance
and response system for malaria, and advocacy to maintain awareness among
the medical profession and at high levels of government, sustained funding for the
Anti-Malaria Campaign and for implementation research and technical guidance
on elimination. The malaria-elimination effort should be supported by rigorous
analyses to demonstrate the clear economic and health benefits of eliminating
malaria, which exceed the cost of a surveillance and response system. An annual
World Health Organization review of the programme may also be required.

Kamini N Mendis, 141 Jawatta
Road, Colombo 5, Sri Lanka.
Email: kaminimendis@gmail.com
Key words: delay in diagnosis, elimination, imported malaria, malaria, prevention

of reintroduction, receptivity, South-East Asia, Sri Lanka, vector-borne diseases,
vulnerability
Introduction
Sri Lankas protracted history of malaria is studded with some
landmark events in global public health, such as the severe
malaria epidemic of the 1930s, which led to an estimated
5.5 million cases and 80 000 reported deaths;1,2 and near
elimination of malaria during the Global Malaria Eradication
Programme of the 1960s,1 which reduced the number of cases
from 91990 in 1953 to a mere 17 in 1963, with many of these
being imported infections (see Figure 1). In the past decade,
the national malaria control programme of Sri Lanka, the
Anti-Malaria Campaign (AMC), has, once again, achieved a
steady reduction in malaria transmission rates in the country.

These have been sustained for more than 10years over a period
that spanned a 30-year separatist war that raged in the north
and east of the country areas that were previously highly
malarious.3 There have now been no indigenous malaria cases
in the country among its 20 million inhabitants for over a year
(see Figure 1).
This time, the opportunity to eliminate the disease from
Sri Lanka presents itself against a background of postwar
developments in the country that impose high risks for malaria
resurgence; a global momentum to eliminate malaria; the
85
Premaratne et al.: Malaria elimination from Sri Lanka
who had contracted malaria overseas, and the vast majority

of the rest was of Pakistani and Indian origin (see Figure3).
SriLankan peacekeeping forces returning from service in
malaria-endemic countries, irregular migrants, business
travellers and boat people voyaging the Indian Ocean and
making landings in Sri Lanka have been the main contributors
to imported malaria being reported with increasing frequency
in Sri Lanka over the past few years (see Table 1).
2 2 11
11
10
Figure 1: The reported annual incidence of malaria since 1999
presented with the annual malaria incidence in the period 1949
1969 to illustrate the near elimination in the earlier years and the
resurgence that followed
17
59
odds of a persisting vulnerability and receptivity to malaria
in the country; and enormous challenges of sustaining a focus
on a disease that is no longer endemic . This paper critically
examines the prospects of eliminating malaria from Sri Lanka,
and the even greater challenge of preventing its reintroduction
to the country.
Sri Lankan
Indian
Ugandan
Indonesian
Tajik
Challenges for sustaining interrupted

transmission and preventing reintroduction
While intense surveillance-based operations of case detection,
management, entomological surveillance and vector control
have contributed to interrupting local transmission in the
country since October 2012, postwar developments continue
at an accelerated pace. These have resulted in an influx of
tourists; imported labour from malaria-endemic countries
particularly India and China; refugees from neighbouring
endemic countries; Sri Lankan expatriates returning home;
and nationals travelling for business or leisure, all of which are
bringing a steadily increasing proportion of imported malaria
cases into the country (see Figure 2). In 2013, nearly 60% of
imported malaria was among travellers of Sri Lankan origin
Pakistani
Burmese
English
Korean
Ukraine
Figure 3: Number of patients with imported malaria in Sri Lanka in

2013, by nationality
Table 1: Occupational categories of imported malaria

cases among foreign and national patients, Sri Lanka
2013
Occupation category
Armed forces/police
Sri Lankan
nationals
4
Business/trade
20
Seaman
13
Technician/skilled labourer
Manual labourer
Figure 2: The number of microscopically confirmed malaria cases

reported from Sri Lanka (indigenous and imported), 20082013
86
Foreign
nationals
Professional
Student
Tourist
Pilgrim
Asylum seeker
19
Social worker
1
59
36
Since the end of the separatist war, Sri Lanka has been on a
steep development trajectory with the building of new air and
sea ports, including in areas that were previously endemic
for malaria; the construction of several highways traversing
the country; increasing global business investments; and a
rapidly growing tourist industry, all of which are associated
with increased travel of foreign nationals; and introduction
of foreign labour into the country, increasing the number of
imported malaria cases. Ongoing construction projects are
leading to the creation of new vector breeding sites, including
in previously endemic areas.
Meanwhile, the principal vector of malaria, Anopheles
culicifacies, and secondary vectors such as A. subpictus,
are as prevalent in the country as previously (see Figure 4).
Furthermore, A. culicifacies has reportedly diversified its
breeding habitats from previously clear, unpolluted slowflowing waters to more polluted and still sources of water.4
Although evidence is unavailable on current vectorial capacities
of these mosquito species, their prevalence implies a continuing
high receptivity to malaria in previously endemic areas. This,
when combined with the increasing reports of imported malaria
from diverse parts of the country, almost certainly points to a
sustained high risk of malaria reintroduction unless rigorous
measures are taken to prevent it.
Compounding these risks are some inevitable challenges

associated with sustaining health services and surveillance
for a non-prevalent disease. Clinical awareness of malaria has
plummeted to the extent that in 2012 there was an unacceptable
delay in the diagnosis of patients with malaria (see Figure 5). In
nearly half of indigenous cases, and 66% of imported malaria
patients, five or more days elapsed from the time the patient
sought treatment until a malaria diagnosis was made; in 10%
and 20% of these patients respectively, it took more than 10
days for a malaria diagnosis to be made. An external evaluation
of the malaria-elimination programme in 2013 found that,
although diagnostic services for malaria are adequately and
widely distributed in all parts of the country, rates of referral
by medical practitioners for a malaria diagnosis remain
persistently low.5 As a result, the disease had even progressed
to severe and complicated malaria in some patients. Despite
this, zero malaria mortality has been sustained in the country
since 2007 owing to a high standard of clinical management of
severe malaria patients.
Figure 5: Number of days from onset of illness to blood testing

for malaria among indigenous (yellow) and imported (red) malaria
patients in Sri Lanka in 2012
Figure 4: Geographical distribution of A. culicifacies (principal vector)

during the high-density season in Sri Lanka, 2013
Malaria control and elimination continues as a priority of

the Ministry of Health, with the directorate of the national
malaria control programme, the AMC, providing technical
guidance to the elimination programme. In the currently
decentralized health system, this programme is implemented
by the provincial ministries of health, through Regional
Malaria Officers. The malaria control programme in 2003,
and the elimination programme from 2008 onwards has
been supported additionally by three successive grants from
the Global Fund to fight AIDS, Tuberculosis and Malaria,
amounting to USD2077223, 2159122 and 2159122 for
the periods 2003 to 2008, 2005 to 2009 and 2009 to 2013,
respectively. Other vector-borne diseases such as dengue are
highly prevalent (see Figure 6) and currently feature as one of
the greatest public health challenges, competing fiercely for the
attention of public health services, including human resources,
at a provincial level.
87
reintroduction would help as an advocacy tool for the muchneeded continuation of national and international investments
for malaria elimination and prevention of reintroduction.
Figure 6: The reported annual number of malaria and dengue cases

in Sri Lanka 19992013
What does success depend on?

Sri Lanka has achieved and sustained interrupted malaria
transmission during the last stages of an intense separatist war
that gripped the country and its health services and economy.
Therefore, the goal of sustaining a malaria-free country after
the cessation of the war appears well within the capacity of its
health system, particularly with hindsight of a failed effort in
the 1960s.
Surveillance with 24-hour compulsory notification and rapid
response for malaria now needs to be the singular focus of
SriLankas elimination programme. Given the cost of malaria
to the country over the years,6 the effort and resource investment
required for a rigorous surveillance and response system would
be entirely justified. Ports of entry to the country by both
sea and air; building construction sites, such as those for the
accelerated building of highways; free-trade zones; new sea
ports and industrial parks; and other imported-labour-intensive
activities will need to be the focus of enhanced surveillance
for malaria. The necessary policy and strategy adjustments to
act within the recently adopted Sri Lanka National Migration
Health Policy7 will need to be developed to deal with the influx
of labour and migration from neighbouring highly malarious
countries. One example is to allow compulsory screening of
migrant labour.
Sustaining awareness of malaria among public-health medical
practitioners, through in-service training, and continued
collaboration with medical educators and professional medical
associations and colleges, should be a priority. A highquality malaria diagnostic service needs to be meticulously
maintained by the AMC, with a system of externally accredited
microscopists.
A focus on malaria elimination at the highest levels of
government is now needed, to seek the cooperation of sectors
beyond health, which govern and regulate major development
efforts in the country. Rigorous economic analysis to
demonstrate the cost effectiveness of preventing malaria
88
Reflection on the previous near-eradication effort of the 1960s

dictates two critical interventions to achieve and sustain
elimination of malaria. One is for the Ministry of Health to
ward off complacency and to refrain from shifting resources
from malaria to other high-burden vector-borne diseases
such as dengue. Sri Lankas recent experience with a failed
leprosy elimination serves as a stark reminder that proposals
on integration of malaria services with health services for any
other disease must not be considered for at least the next 5
years. In 1996, Sri Lanka reached the leprosy-elimination target
stipulated by the World Health Organization (WHO), of less
than one case per 10000 population, and, thereafter, supported
by eloquent policy arguments and a seemingly sound structural
basis for integration, district-level anti-leprosy services were
integrated into the general health services in 2001/20028 a
move that has resulted in a resurgence of leprosy. The AMC
needs, rather, to be reprogrammed, vastly strengthening its
entomological and infection and disease surveillance and
response arm; improving the quality of diagnostic services;
and shifting its geographical focus on the strict basis of
receptivity and vulnerability in different parts of the country.
The second is to sustain a focus on and investment in research
and technical guidance for malaria elimination and prevention
of reintroduction. Steps for this are already being taken at a
national level the Sri Lankan research funding agencies will
earmark modest funds for research on malaria for the next
several years. One of the many factors that are widely believed
to have contributed to the decline of malaria in Sri Lanka
during the past few decades is the deployment of evidencebased control operations by the AMC at all level of the health
system, supported by mobile malaria units, on the basis of an
extensive national research effort on malaria. Such a strong
research and technical basis would well serve the elimination
and prevention of resurgence of malaria now.
Discussion
The cost of malaria to Sri Lanka has been enormous over
centuries and would be more so now in the context of
globalization, competitive economies and higher standards
of living. Recent attempts to estimate the cost of malaria to
SriLanka,6,9,10 suggest massive economic benefit would be
gained by malaria elimination, even though the methodology
used in these studies barely broached the economic opportunities
lost to commerce, trade and tourism,11 or the cost of malaria to
human development,12, 13 making the estimated cost of malaria
to Sri Lanka a gross underestimate. Exactly 50 years after a
missed opportunity to eliminate malaria, the country stands
today at a pivotal point in its malaria history. The price of an
outstanding surveillance and response system which is now
essential, is not beyond the affordability of Sri Lankas health
system, which is known to deliver an equitable and effective
health service. Singapore, with similar environmental risks
for malaria as Sri Lanka, has sustained a malaria surveillance
and response system to keep the country malaria free, despite
large volumes of labour migration into the country and small
local outbreaks,14 which must reflect an assumption that the

investments are well below the cost of a malaria resurgence.
Although the WHO Region of South-East Asia , to which
SriLanka belongs, bears the second largest burden of malaria
in the world, second only to Africa, several countries within the
region have made significant achievements in either eliminating
malaria (Maldives in 1984) or, more recently, significantly
reducing their levels of endemicity (Bangladesh, Bhutan,
Nepal, and Timor-Leste).15 India and Myanmar still harbour
considerable case incidence rates of malaria, contributing the
most by far to the regions disease burden. Eliminating malaria
from Sri Lanka, and sustaining a malaria-free status, would
be an important regional milestone, serve as a much-needed
boost to the concerted global malaria-elimination efforts, and
help validate the sustained high investments for the global fight
against malaria. The corollary the cost of failure to achieve
and sustain malaria elimination in Sri Lanka would be far
greater than the mere return of malaria. It would place the
country at risk of artemisinin-resistant malaria, which has now
extended from its point of origin at the ThailandCambodia
border, reported in 2009 ,16 as far west as Myanmar. It would
also risk the country facing the globally growing problem of
insecticide resistance in vector mosquitoes, and thus confront
an escalating cost of malaria control, which would jeopardize
its development efforts.
Poverty of resources if often cited as a legitimate reason for
failure of disease-control efforts, alluding to muliple demands
on restricted health budgets and competing health priorities
as making such goals unachievable. Yet, having achieved and
sustained more than a year of arrested malaria transmission in
Sri Lanka, and bearing in mind that international support for
malaria elimination is accessible and forthcoming, this may
not be such a limiting factor at present. A failure to sustain
malaria elimination at this stage is more likely to reflect poor
judgement and planning on the part of health and national
authorities rather than of lack of resources. Some of SriLankas
characteristics, such as its island nature and thus not being
as prone to unregulated human migration as countries with
contiguous land borders; its land extent and terrain are not
unwieldy; it has a highly performing and equitable health
system; and it has a high literacy rate, are all factors that would
support the feasibility of achieving and sustaining malaria
elimination, despite the countrys intrinsically high receptivity
and vulnerability to malaria. Given the achievements so far, it
is imperative that national investment of resources and effort
continue unabated, and that the international support required
to sustain this achievement is forthcoming.
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Abeyasinghe R R, Galappaththy GNL, Gueye CS, Kahn JG, Feachem
RGA. Malaria control and elimination in Sri Lanka: documenting
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Gunathilaka N,Fernando T,Hapugoda M,Wickremasinghe
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in polluted water bodies in Trincomalee District of Sri Lanka. Malar
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country review: malaria control and elimination programme, 1828
February 2013.
Report of meeting on elimination of malaria from and preventing its reintroduction to Sri Lanka: identifying gaps in operational research. Anti
Malaria Campaign, Sri Lanka. 2013, 10 December 2013.
Sri Lanka, Ministry of Health. Sri Lanka national migration health
policy. Colombo: MOH, 2012. http://www.migrationhealth.lk/sri_
lanka_national_migration_health_policy.pdf - accessed 25 March 2014.
Report of the evaluation of the anti leprosy programme in Sri Lanka.
Fairmed Foundation, Sri Lanka, 2011.
Ruberu PS. Economic justification of intensive malaria control
programme in Sri Lanka 1977/81. (unpublished).
Attanayake N. Cost-effectiveness of anti-malaria activities in SriLanka.
PhD Thesis. London: London School of Hygiene and Tropical Medicine,
1994.
Gallup JL, Sacs JD. The economic burden of malaria. Harvard: Centre
for international Development, 1998. http://www.earth.columbia.edu/
sitefiles/file/about/director/ pubs/mal_wb.pdf - accessed 25 March 2014.
Fernando D, de Silva D, Carter R, Mendis KN, Wickremasinghe R.
A randomized, double-blind, placebo-controlled, clinical trial of the
impact ofmalariaprevention on the educational attainment of school
children. Am J Trop Med Hyg. 2006;74(3):38693.
Fernando D, de Silva D, Wickremasinghe R. Short-term impact of an
acute attack ofmalariaon the cognitive performance of schoolchildren
living in amalaria-endemic area of Sri Lanka. Trans R Soc Trop Med
Hyg. 2003;97(6):6339.
Ng LC, Lee KS, Tan CH, Oo PL, LamPhua SG, Lin R, et al.
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transmission in Singapore, 2009. Malaria Journal. 2010;9:305. http://
www.malariajournal.com/content/9/1/305 - accessed 25 March 2014.
Bhatia R, Rastogi RM, Ortega L. Malaria successes and challenges in
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Dondorp AM, Nosten F, Yi P. Das D, Phyo A, Tarning J, Lwin KM, et
al. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J
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How to cite this article: Premaratne R, Ortega L, Janakan N,

Mendis KN. Malaria elimination in Sri Lanka:what it would take
to reach the goal. WHO South-East Asia J Public Health 2014;
3(1): 8589.
Contributorship: RP reviewed and analysed the data from the AntiMalaria Campaign, LO reviewed and provided the malaria data from the
Asian region, JN provided the data on other vector-borne diseases in Sri
Lanka, KM drafted the overall paper. All authors reviewed and edited the
final text.
89
Policy and practice
DOI: 10.4103/2224-3151.115828
Containing artemisinin resistance

of Plasmodium falciparum in
Myanmar: achievements, challenges
and the way forward
Thar Tun Kyaw1, Thaung Hlaing2, Krongthong Thimasarn3, Khin Mon

Mon4, Gawrie N. L. Galappaththy3, Valaikanya Plasai5, Leonard Ortega6
Department of Health, Ministry of

Health, Myanmar; 2National Malaria
Control Programme, Ministry of
Health, Myanmar; 3Malaria Unit,
WHO Office of the Representative
to Myanmar; 4Former National
Malaria Control Programme
Manager, Ministry of Health,
Myanmar; 5independant consultant,
6
WHO Regional Office for SouthEast Asia, New Delhi, India
Abstract
Artemisinin resistance is a major threat to global malaria control and elimination
efforts. Myanmar detected the first indication of the resistance in 2009 in the
eastern part of the country, bordering Thailand. Since 2010, WHO has played
a vital role in ensuring that a comprehensive programme on the containment of
the resistance is in place. This paper documents achievement made in terms of
output, outcomes and early impact on malaria from July 2011 to December 2013.
It also identifies enabling factors to success and, most importantly, challenges
awaiting the national programme and its partners.
Key words: malaria, Myanmar, artemisinin resistance

Dr Krongthong Thimasarn,
Malaria Unit, WHO Office
of the Representative to
Myanmar, Myanmar.
Email: thimasarnk@who.int
Background
The malaria elimination goal, as recommended by the World
Health Organizations Global Malaria Programme (GMP)
relies heavily on the effectiveness of a few tools; among them
antimalarials. Artemisinin has been used widely in the Greater
Mekong Subregion (GMS) since 1995,1 and in Myanmar as
first-line treatment since 2002. 2 While the therapeutic efficacy
of artemisinin-based combination therapy (ACTs) remains at
satisfactory level globally, two locations in the world have
confirmed artemisinin resistance hotspots.3,4 Both foci are
located in the GMS, namely, the western border of Cambodia
and Thailand and the western border of Thailand bordering
Myanmars Tanintharyi and Bago regions and Mon state. In
Myanmar, evidence of suspected artemisinin resistance was
reported in 2009,5 and confirmed in 2011.6
To date, no next-generation antimalarials are on the horizon,
thus artemisinin resistance is a major threat to progress made
in the past decade, with possible serious global implications
for malaria elimination.7 The Myanmar national malaria
programme has joined the global community in the containment
of artemisinin resistance since April 2011 by initiating the
Myanmar artemisinin resistance containment (MARC). This
paper documents the process, current achievements, enabling
factors, as well as lessons learned during early implementation
of the programme.
90
MARC Strategic framework for artemisininresistance containment in Myanmar8

Efforts to contain the spread of artemisinin resistance in
Myanmar started since its first indication in 2009, even though
artemisinin resistance was not confirmed until 2011. WHO
Myanmars Malaria Unit has been one of the major forces
behind the initiation of artemisinin-resistance containment
in Myanmar since early 2010. With financial assistance from
the Bill and Melinda Gates Foundation (BMGF), the MARC
framework was developed in 2010 through consultation and
brainstorming sessions of the Malaria Technical and Strategy
Group (TSG), building on the CambodiaThai containment
project with the strategy developed in 2008.9 Later on, the
framework also benefited from technical guidance from
the Global Plan For Artemisinin Resistance Containment
(GPARC).4 The Myanmar Ministry of Health endorsed the
framework in April 2011, and activities started in July 2011.
MARC specific objectives are shown in Box 1.
At the outset, from July 2011 to 2012, financial resources for
MARC rolling out came primarily from the Three Diseases Fund
(3DF), which later became Three Millennium Development
Goals (3MDG) Fund in 2013. A total of US$ 9 million was
mobilized through the 3DF to roll out MARC from July 2011
to 2012 and another US$11 million from 3MDG for MARC
activities in 2013.
Kyaw et al.: Containment of artemisinin resistance in Myanmar

Box 1:
MARC Objectives
1) To improve access to and use of early diagnosis and
quality treatment according to the national treatment
guidelines.
2) To decrease drug pressure for selection of artemisinin
resistant malaria parasites by stopping the use of artemisinin monotherapies and sub-standard/fake drugs.
3) To limit the transmission of malaria by vector control
and personal protection.
4) To increase migrant/mobile population access to and
use of malaria diagnosis, treatment and vector control
measures including personal protection.
5) To support containment of artemisinin resistant parasites through advocacy and BCC/IEC.
6) To conduct studies, especially operational research to
support the development of evidence-based containment policies and strategies.
7) To provide effective management and coordination to
enable rapid and high-quality implementation of the
containment strategy.
MARC aims at delaying the spread of artemisinin-resistant

parasites, and reducing transmission, morbidity and mortality
of falciparum malaria. Out of 330 townships of Myanmar,
MARC targets 52 townships, 21 in Tier 1 (strong evidence of
suspected resistance), and 31 in Tier 2 (unclear evidence of
suspected resistance, but bordering Tier 1 area). Tier 3 refers
to areas endemic to Plasmodium falciparum with no evidence
of artemisinin resistance and limited contact with Tier 1 areas.
Eight implementing partners (IPs)aimplement MARC
activities with funding from 3DF. An additional four partnersb
implement MARC activities with either their own funding, or
other sources of funding. Key strategies include a multisectoral
approach and integrated interventions in scaling up of case
management, reduction of drug pressure, and improved access
to quality treatment and malaria prevention among targeted
population groups, particularly mobile populations. Because
MARC relies on a multisectoral approach, coordination among
implementing partners is vital to success. The TSG coordinates
among partners at higher levels, and at implementing level,
local committees. This mechanism ensures strong public
private partnership in MARC implementation.
IP in 20112012 included Community Development

Association, World Concerns, World Vision, Myanmar
Health Assistant Association, Myanmar Medical Association,
International Organization for Migration, Population Services
International, and WHO Myanmar. Two new IPs in 2013
includes Friend for Health and Medical Action Myanmar.
b
Medicin san Frontieres-Switzerland, Japan International Cooperation Agency, CPI/GHAP and USAID/PMI CAP-Malaria
a
MARC major activities and outputs, 20111013

Set up of screening points along the ThaiMyanmar and
MyanmarChina border areas to detect malaria among
migrants, and mobile malaria clinics to reach hard-to-reach
areas to improve access to quality treatment.
A monotherapy replacement programme using affordable
or free-of-charge quality ACTs through the private sector,
and publicprivate partnership.
Insecticide-treated nets and long-lasting insecticidal
nets (ITNs/LLINs), and, in certain areas, indoor residual
spraying together with personal protection measures to
limit transmission in containment areas.
Activities to advocate for the support of containment of
artemisinin resistance among partners and stakeholders.
These activities are for example, meetings with the affected
communities, other governmental agencies, and the private
sector, including private practitioners.
Therapeutic efficacy studies (TES) and day 3 parasitaemia
studies for evidence-based policy and strategic
development.
System strengthening for timely and improved information:
epidemiological and entomological surveillance. Surveys
of households, health facilities and private vendors.
Training activities to support the above activities:
microscopists at state or region level; BHS, VBDC staff;
volunteers at villages and at worksites for case detection
and treatment, as well as LLIN distribution.
Public-private partnerhsip initiation for: migrant mapping,
case management, LLIN/ITN distribution, and artemisinin
monotherapy replacement.
Documentation: information, education and communication
(IEC) material and behaviour change communication
(BCC) material for different target populations such
as private practitioners, volunteers, and the affected
community; guidelines for the treatment and prevention of
malaria among mobile/migrant populations; national drug
policy; and migrant mapping.
MARC achievements during 20112013
While it has been merely 30 months since the first
implementation of MARC, the project has achieved its two
goals. First, malaria mortality and morbidity has declined in
MARCs target areas in the two years (Table 1); and second,
TES results, as well as day 3 parasitaemia studies, detected
no new suspected resistance in Tier 3, but results in the
containment areas along the eastern border of Myanmar are
still inconclusive due to high population movement across this
border and inaccessibility in conflict areas.
Significant outcomes of MARC in containment areas since
July 2011:
improved access to quality diagnosis and treatment
through volunteers, both in villages and at worksites, as
well as a network of private physicians and clinics in the
52 townships;
91

Table 1: State and region wise malaria morbidity and mortality, Myanamar, 20081012
No.
MARC/
NonMARC
State/
Region
2008
2009
2010
2011
2012
Morbidity
rate*
Mortality
rate**
Morbidity
rate
Mortality
rate
Morbidity
rate
Mortality
Rate
Morbidity
rate
Mortality
Rate
Morbidity
rate
Mortality
Rate
Ayarwaddy
3.72
0.70
2.02
0.57
3.68
0.71
6.03
0.66
4.28
0.62
Bago
(West)
6.64
1.19
7.51
1.19
6.55
0.54
5.14
1.00
4.28
0.76
Chin
44.72
2.87
44.75
2.33
37.09
3.22
44.64
2.94
26.67
0.21
Magway
7.77
1.11
6.06
0.80
7.34
0.42
4.58
0.37
3.20
0.16
Mandalay
2.95
0.75
2.71
0.44
3.45
0.30
4.67
0.30
3.68
0.08
Rakhine
42.04
3.74
35.10
2.91
37.09
1.75
32.48
1.37
22.61
0.74
Sagaing
18.12
2.69
16.45
3.19
19.68
2.01
16.79
1.80
11.83
1.98
Shan
(East)
5.55
0.78
4.70
0.11
4.84
0.33
3.02
0.82
2.26
0.33
Shan
(North)
12.96
4.37
12.65
4.08
14.46
3.88
13.55
1.95
8.47
1.72
10
Shan
(South)
8.60
3.13
8.07
2.81
9.13
3.16
9.33
2.27
7.37
1.53
11
Yangon
1.25
0.22
0.61
0.20
0.59
0.22
0.51
0.07
0.41
0.03
9.73
1.54
8.39
1.38
9.53
1.08
9.36
0.90
6.62
0.70
6
7
8
Non-MARC
Non-MARC
Bago
(East)
11.62
1.47
9.68
1.46
9.25
0.76
10.36
0.89
6.17
0.77
13
Kachin***
23.18
7.18
45.20
6.91
70.09
5.80
34.58
4.75
22.85
2.43
Kayah
26.64
1.20
24.70
0.30
22.98
0.30
27.54
3.34
18.54
1.59
Kayin
12.37
3.93
12.75
2.02
14.13
2.46
16.50
3.22
9.90
2.05
16
Mon
9.14
1.71
8.24
2.17
8.98
1.67
9.84
1.14
8.29
0.70
17
Tanintharyi
24.30
4.48
21.22
3.50
24.12
3.74
46.41
3.35
30.71
1.57
MARC area
14.82
3.07
16.49
2.70
20.39
2.32
20.86
2.36
13.89
1.37
Nationwide
10.75
1.84
10.00
1.64
11.70
1.33
11.68
1.20
8.09
0.83
14
15
MARC
12
*Morbidity rate/1000 population

**Mortality rate/100 000 population
*** MARC covers all townships in the State/Regions mentioned except in Kachin. In the latter, four of 18 townships are covered. The four
townships contribute around 1/3 of total cases in the State.
increased coverage of personal protection through

increased use of LLINs, reintroduction of IRS and
improved knowledge of target populations through IEC
and BCC activities;
improved compliance of private sector to national drug
policy;
national drug policy, including a policy to ban artemisinin
monotherapy;
92
mapping of migrants at local level for microplanning of

malaria control;
standardized and computerized surveillance system
strengthened and expanded into township level in Tier 1;
a system for early detection of artemisinin resistance along
the border.
MARCs enabling factors

First, Myanmars NMCP was able to capitalize on the strong
networks of private physicians in Myanmar in the provision
of quality assured antimalarials. Second, not-for-profit local
professional organizations, such as Myanmar Health Assistant
Association in Myanmar and many others, have fostered the
control efforts. Third, external financial and technical supports
from numerous partners made it possible for the programme
to conceive and implement such an ambitious project. Finally,
strong political will to support malaria control and elimination
efforts of the Ministry of Health has played a vital role in
the success of MARC as well as regular malaria control
achievements.
Challenges in implementing MARC
While MARC has tremendous success since its inception in
April 2011, the programme continues to face challenges in the
coming years:
1. Civil unrest in some containment areas have limited access,
and imposed significant difficulties to its implementation.
It also contributed to high turnover of trained staff posted
in villages or work sites inflict additional cost of recruiting
and training of new ones.
2. Communication barriers due to cultural and language
difference between malaria service providers and recipients
have impeded the effectiveness of the programme.
3. Inadequate coordination at all levels, from national to state/
region, to township, and to village levels, as well as among
national level and sub-recipients, resulted in ineffective
management of programme activities.
4. Overlapping of areas of activity at lowest level of
implementation due to many IPs has caused confusion
among staff. Volunteers for case management in villages
and at worksites, for example, were implemented by
several partners, thus they faced different recruitment, job
descriptions, and training manuals and process.
5. While increased coverage of LLIN and ITN among target
populations is one of MARCs major objectives, these
are mobile population and migrants. This factor together
with outdoor transmission in the forest continues to pose
technical challenges to MARCs future achievement.
6. Smooth transition of MARC as project activities to become
an integral part of malaria control remains a challenge.
7. Enhanced economic opportunities due to several reasons,
including the supportive political environment in Myanmar,
the Mekong economic corridor, as well as the Asian
Economic Community (AEC), will contribute to increased
non-immune population movement into malarious areas,10
thus posing further challenges for artemisinin-resistance
containment in GMS.
8. Long and cumbersome processes of grant negotiation and
administration delayed the commencement of containment
activities by several months. Grant agreement signing, and
fund transferring require much attention and energy.
9. Donors were not adequately coordinated. This had led to

fragmentation of implementation and reporting, as well as
confusion among workers under different implementing
partners.
Conclusions and the way forward
Implementation of MARC started 30 months ago, focusing on
using a multisectoral and integrated approach in implementing
various antimalarial interventions in containment areas, and
with funding from 3DF, and later 3MDG. Several important
outcomes and two early impacts were achieved in containment
areas according to MARCs two goals: reduced morbidity and
mortality; and no further artemisinin resistance were detected
outside know foci.
It is imperative for all parties to embrace lessons learned,
both positive and negative. Successes from Myanmar that
can be repeated elsewhere are, for example, enhanced
publicprivate partnerships in implementation of malaria
activities, and replacement of artemisinin monotherapy due to
concerted efforts among multisectoral partners. How MARCimplementing partners overcame challenges encountered
during its 30-month implementation can also be beneficial
elsewhere.
From 2014 onwards, containment of artemisinin resistance
in Myanmar will become an integral part of the efforts under
the GMS regional artemisinin resistance initiative (RAI), with
funding from the Global Fund to Fight AIDS, Tuberculosis and
Malaria (GFATM) and BMGF. 3MDG will continue to provide
additional funding for artemisinin-resistance containment
activities in Myanmar beyond 2013, possibly until 2016,
focusing on two main activities: (1) improved access to
diagnosis and treatment to target populations in containment
areas; and (2) provision of locally appropriate vector control
measures and personal protection.
While it is good news that funds continue to pour into Myanmar,
multiple donors together with multiple implementing
partners requires careful planning and adequate coordination.
Maintaining what was achieved in the face of rapid changes in
administrative and finance mechanisms, as well as increased
technical issues, continues to pose challenges to Myanmar
NMCP and WHO. This phenomenon is not unique to Myanmar,
however.11 The donor community can work together to ensure
that the technical implementing partners are not unnecessarily
burdened by administrative requirements.
References
1.
2.
3.
Delacollette C, DSouza C, Christophel E, et al. Malaria trends and

challenges in the Greater Mekong Subregion. Southeast Asian J Trop
Med Public Health. 2009;40:674-91.
Myanmar, Ministry of Health. National strategic plan, malaria
prevention and control 2010-2015 (Annex 3). Yangon: Department of
Health, MOH , 2012.
Bustos MD, Wongsrichanalai C, Delacollette C, Burkholder B.
Monitoring antimalarial drug efficacy in the Greater Mekong Subregion:
an overview of in vivo results from 2008 to 2010. Southeast Asian J
Trop Med Public Health. 2013;44(Suppl. 1):201-230.
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4.
5.
6.
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8.
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World Health Organization. Global plan for artemisinin-resistance

containment (GPRAC). Geneva: WHO, 2011.
World Health Organization, Regional Office for South-East Asia. Report
of the workshop to review and plan therapeutic efficacy studies to monitor
P. falciparum and P. vivax resistance to anti-malarial drugs in the Greater
Mekong Sub-region. Mandalay, Myanmar, September 30-October 2,
2009. New Delhi: WHO-SEARO, 2010. Document No. SEA-MAL-263.
http://whothailand.healthrepository.org/bitstream/123456789/1015/1/
SEA-MAL-263-%20TES%20in%20Mandalay%202009.pdf accessed
28 March 2014.
Reviewing and planning therapeutic efficacy studies (TES) to monitor
antimalarial drug resistance in the Greater Mekong Subregion (GMS):
report of a workshop, Kunming, The Peoples Republic of China,
12-13 June 2012. New Delhi: WHO-SEARO, 2013. Document
No.
SEA-MAL-270.
http://whothailand.healthrepository.org/
bitstream/123456789/1460/10/SEA-MAL-270.pdf - accessed 28 March
2014.
Daniel JC. Drug-resistant malaria: a generation of progress in jeopardy.
Washington, DC: Center for Strategic & International Studies, 2013.
http://csis.org/files/publication/131107_ Daniel_DrugResistantMalaria_
Web.pdf - accessed 28 March 2014.
Myanmar, Ministry of Health Myanmar. Strategic framework for
artemisinin resistance containment in Myanmar (MARC), 2011-2015.
Yangon: MOH, 2011.
9.
10.
11.

Development of a strategy towards elimination of plasmodium
falciparum parasites with altered response to artemisinins: report of an
informal consultation, Bangkok, Thailand, 13-14 February 2008. New
Delhi: WHO-SEARO, 2008. Document No. SEA-MAL 257.
Myanmar, Ministry of Health Myanmar. Annual report 2011: vectorborne diseases control programme. Nay Pyi Taw. Yangon: MOH, 2013.
Rieffel L, Fox JW. Too much, too soon? The dilemma of foreign aid to
Myanmar/Burma. Arlington, VA: Nathan Associates Inc, March 2013.
How to cite this article: Kyaw TT, Hlaing T, Thimasarn K,

Mon KM, Galappaththy GNL, Plasai V, Ortega L. Containing
artemisinin resistance of Plasmodium falciparum in Myanmar:
achievements, challenges and the way forward. WHO SouthEast Asia J Public Health 2014; 3(1): 9094.
Contributorship: TTK provided information, TH provided information,
KT wrote the paper, KMM provided information, GNLG wrote the paper,
VP wrote the paper, LO reviewed the paper.
Policy and practice
DOI: 10.4103/2224-3151.115828
Economic burden of malaria in India:

The need for effective spending
Indrani Gupta, Samik Chowdhury
Abstract
About 95% of Indias population resides in malaria-endemic areas and, according
to government sources, 80% of malaria reported in the country is confined
to populations residing in tribal, hilly, difficult and inaccessible areas. Using a
nationally representative sample, this study has estimated the economic burden
of malaria in India by applying the cost-of-illness approach, using the information
on cost of treatment, days lost and earnings foregone, from the National Sample
Survey data. A sensitivity analysis was carried out, by presenting two alternative
scenarios of deaths. The results indicate that the total economic burden from
malaria in India could be around US$1940 million. The major burden comes from
lost earnings (75%), while 24% comes from treatment costs. Since mortality is low,
this is not a major source of economic burden of malaria. An analysis of the trend
and patterns in public expenditure by the National Vector Borne Disease Control
Programme shows a declining focus of the central government on vector-borne
diseases. Also, allocation of financial resources among states does not reflect the
burden of malaria, the major vector-borne disease in the country.
Institute of Economic
Growth, New Delhi, India
Professor Indrani Gupta, Health
Policy Research Unit, Institute
of Economic Growth, University
Enclave, Delhi 110007, India.
Email: ig.indrani@gmail.com,
indrani@iegindia.org
Key words: Economic burden, India, malaria, public spending
Introduction
In India, vector-borne diseases such as malaria, dengue,
chikungunya, Japanese encephalitis (JE), kala-azar and
lymphatic filariasis have considerable impact, in terms of
morbidity and mortality. The epidemiology of these vectorborne diseases varies considerably, on account of ecology,
vector bionomics, and economic, sociocultural and behavioural
factors.1 Residents of rural and tribal areas as well as urban
slums are most at risk from such diseases, which impact mostly
the poor and vulnerable sections of the population. Vectorborne diseases contribute to widespread disease, disability
and deaths in India, especially among the poor, who have
limited access to timely and effective treatment. Children and
pregnant women have low immunity to vector-borne diseases
like malaria, and are especially vulnerable, leading to maternal
deaths, stillbirths, and low birth weight in infants.
The major burden of vector-borne disease in India comes from
malaria; according to the Directorate of the National Vector
Borne Disease Control Programme (NVBDCP), about 95% of
the population in the country resides in malaria-endemic areas.
While severe a decade ago, there has been a declining trend in
the overall endemicity of malaria in the country, with a reported
number of cases in 2012 of around 1.06 million (provisional). 1
Despite the significant presence of vector-borne diseases in

India, there is a paucity of studies on the economic burden on
households and likely cost of these illnesses, using nationally
representative data. While there continue to be debates and
discussions around the prevalence, incidence and deaths from
malaria, the last health round (60th round) of the National
Sample Survey2 of India (NSS) which is a nationally
representative survey is yet to be utilized to understand the
treatment burden of malaria and the profile of those affected.
The NSS has the potential to independently validate the various
estimates of malaria burden. While limitations exist, they
exist for other surveillance data as well, and such a nationally
representative sample should be used for a better understanding
of the malaria situation in the country.
This paper, therefore, uses unit-level data from the NSS 60th
round on health, to analyse the direct and indirect costs of
malaria; specifically, the data are analysed to understand the
distribution of the burden of malaria across sex, residence
(rural/urban areas), education and consumption categories.
Subsequently, the analysis focuses on direct and indirect costs
of treatment for outpatients and hospitalizations. The NSS
60th round is useful in this context because, in addition to
costs of treatment, it also seeks responses on missed days of
work and earnings foregone. Alternative estimates of deaths
95
Gupta et al.: Economic burden of malaria in India
are used to calculate the burden from loss of earnings and years
of productive lives. While the survey pertains to 2004, the
estimates are used in conjunction with more recent estimates
of malaria cases in India, to assess the economic burden of the
disease on the country. The paper also highlights certain key
issues on the patterns in public financing of the NVBDCP in
general.
Malaria in India
The case-load of malaria in India has reduced and reported
deaths are declining, indicating declining endemicity. However,
the epidemiology of malaria remains complex, owing to the
geographical and ecological diversity. In the mid-1970s,
malaria re-emerged in India, with 6.4 million new cases in
1976,3 indicating the need for constant vigilance and prevention.
According to the NVBDCP,1 of the reported 1.06 million cases
in 2012, 50.01% are due to P. falciparum. Also, about 95% of
the countrys population resides in malaria-endemic areas, and
80% of malaria reported in the country is confined to regions
that have more than 20% of their population residing in tribal,
hilly, difficult and inaccessible areas. The most affected states
are the north-eastern ones: Andhra Pradesh, Chhatisgarh,
Gujarat, Jharkhand, Karnataka, Madhya Pradesh, Maharashtra,
Odisha, Rajasthan and West Bengal.
It is possible that the actual number of malaria cases is higher
because a large number of infected individuals might be seeking
treatment from private health providers, who do not report
to NVBDCP.4 Non-reporting of mortality causes a serious
problem with data on the medical cause of certification of death,
compounded by the lack of medical certification of deaths as
well as issues with the attribution of specific cause of death.3
Other analyses point out that it is indeed a challenge to estimate
the true case burden of malaria in India.5 A more recent article
indicates that global malaria mortality may be much higher
than previously estimated, especially among adults.6 For India,
a widely quoted study in The Lancet estimated that 205000
deaths per year could be attributed directly to malaria, with
lower and upper limits of 125000 and 277000, respectively.7
These figures differed significantly from the 2008 World
Health Organization (WHO) World malaria report,8 which
reported 15000 deaths per year due to malaria, and also from
the numbers reported by the NVBDCP. Research also confirms
that the majority of deaths from malaria were not in any formal
health-care facility, and therefore, would not be counted in any
reporting system.9 Finally, the analysis contended that cases
due to Plasmodium falciparummight represent only a fraction
of the total malaria disease burden in India.
Clearly, surveillance is a key area that needs further policy
focus to refine estimates of cases and deaths because the
economic burden of malaria is entirely driven by the case-load
and mortality.
Economic impact of malaria: global evidence

A number of studies have looked at the economic impact of
malaria globally. Some have estimated the impact of malaria
96
on economic growth and there is some evidence for a belief

that regions that have been able to reduce malaria have
subsequently registered higher economic growth.10 However,
numerous studies have focused on the economic burden on
households; for example, an early study from Malawi showed
that households with a very low income bore a disproportionate
share of the economic burden ofmalaria, with 32% of their
annual household income being lost as a result of the direct
and indirect costs of malaria, compared to only 4.2% for
households in the low- to high-income categories.11
Another study from Sri Lanka indicated that, although the
overall economic impact was limited,cases of malaria occurred
seasonally and were concentrated in an important agricultural
season. This season saw the bulk of the economic impact
in terms of loss in working days and loss in school days, in
addition to the usual direct costs.12
A study from Nigeria compared the financial and economic
costs of malaria with other illness episodes for households
in five malaria holoendemic rural communities. The findings
showed that the costs of treatment for malaria accounted for
almost half of expenditure on curative care costs incurred by
the households.13
However, despite a significant burden of malaria in India,
few studies have looked at the economic impact of malaria
on households, though there are some that have looked
at chikungunya14 and lymphatic filariasis.15 One paper
examined the effects of a large-scale eradication programme
that drastically reduced malaria over a short period of time.
The findings indicate that malaria eradication resulted in
improvements in income for males.16
While the consensus from such studies is that malaria imposes
significant burden on households, there is as yet no study that
has used a nationally representative database to assess the total
economic burden of illness and deaths from malaria in India.
METHODS
The study used NSS data for the last available health round
on India, which pertains to 2004. The NSS data contain
information on the direct costs of treatment for both outpatient
and hospitalization episodes in rural and urban areas
respectively. The survey also asks about the kind of illness
suffered by the respondent. While self-reported morbidities
may not be accurate generally, anyone who stated malaria as
his/her illness has certainly had a diagnosis. Thus, it is safe
to assume that the malaria numbers from the NSS are indeed
malaria, though the number could be higher due to lower
treatment-seeking behaviour in general.17
In the absence of more recent data, current available estimates
of cases and deaths are used for analysis and discussion of
economic burden. For the total number of deaths, data from
WHO and the more recent Lancet study were used for the
lower and upper range of possible deaths from malaria. The
direct and indirect costs for both inpatients and outpatients
were calculated from NSS data. Wherever required, the
weights given in the NSS data were used to estimate nationally
representative numbers. A cost-of-illness approach was used to

calculate the economic burden of malaria, using the information
on cost of treatment, days lost and earnings foregone, and the
present value of number of years of life lost due to malaria.
Since the NSS pertains to 2004, the gross domestic product
(GDP) deflator was used to arrive at expenditure figures for
2012, with the assumption that relative treatment costs remain
the same.
Since one component of the cost of illness is productive work
days lost, the analysis was restricted to adults only.
The stepwise methodology to calculate costs of illness from
malaria for adults is given next.
1. Total economic burden from malaria has three components:
treatment costs due to illness, productivity loss due to
foregone earnings emanating from lost days of work, and
the economic value of lost earnings due to death.
2. Two inputs are important in these calculations: the total
number of cases of malaria and total number of deaths due
to malaria. WHO estimates that in India about 11% of the
population is malaria free, 67% reside in low-transmission
areas (01 case per 1000 population), and the remaining
22% live in high-transmission areas (greater than 1 case per
1000 population). In all therefore, 89% of the population is
affected. Since the WHO estimates are ranges, (prevalence
of 01 and greater than 1), these were assumed to be 0.5
and 1 per 1000 or 0.05% and 0.1% in low- and hightransmission areas respectively.
3. For deaths, two alternative estimates are used: WHO
estimate of 15000 per year,18 and the upper range of deaths
from the Lancet study (277000). This is done to get a range
within which the true economic burden might lie. Thus,
two alternative estimates of economic costs are arrived at,
with two different assumptions regarding total deaths from
malaria, while the number of cases remains the same.
4. It is also assumed, based on the Lancet study, that 60%
of the total deaths are of adults (age 15years and above).
7
This number is independently validated from the NSS
study, which shows that slightly more than 60% of malaria
cases occurred among adults.
5. Treatment costs are calculated using the costs of outpatient
treatment and hospitalization from NSS 60th round. These
costs are re-estimated for 2012 by using a suitable deflator.
6. The total burden due to treatment costs is calculated by
using the unit costs of treatment, in conjunction with
estimated cases.
7. From NSS, the average earnings foregone are used to
arrive at the potential loss of earnings, in conjunction with
the total days lost due to illness and death
8. Assuming 45 years as the average age of death due to
malaria among adults, and an average age of retirement
as 60years, the potential number of life-years lost can be
calculated, and, using a discount rate of 5%, the present
value of earnings foregone can be estimated.
RESULTS
Profile of malaria-affected individuals
The data indicate that in 2004 there were a total of 2.4 million
cases of malaria (see Table 1). This is somewhat higher than
the NVBDCPs reported 1.92 million cases for 2004, and more
consistent with other views discussed above about the true
burden of malaria in the country. Other statistics indicate that
slightly more males are affected than females. The majority of
malaria cases are in rural areas (78%) and about 75% of the
cases occur among individuals who are illiterate or have less
education. The distribution across consumption quartiles is
somewhat more, even though the lowest quartile has 10% more
cases than the other three quartiles. Overall, of all ailments
reported, malaria comprised 2.5% and 1.9% of the cases in
rural and urban areas respectively.
Table 1: Profile of malaria-affected individuals
Characteristic
Sex, male
Residence, rural
Education
Illiterate
Primary and less
Consumption quartile
First
Second
Third
Fourth
Percentatge (total n=2396194)

54
78
48
27
33
23
24
22
Source: NSS unit level data, 60th round2
Table 2 presents the distribution of cases between the

Empowered Action Group (EAG) of states, comprising Assam,
Bihar, Jharkhand, Madhya Pradesh, Odisha, Rajasthan, Uttar
Pradesh and Uttarakhand versus other major states. The
EAG states are prioritized for special focus in government
programmes.
Table 2: Malaria cases across EAG and non-EAG states
Residence/states
Rural
Urban
Total
EAG
39.3
8.2
47.5
Non-EAG
38.4
14.0
52.4
Source: NSS unit level data, 60th round.2
While slightly higher for the EAG states, the case-load

between these two groups seems similar for rural India. In fact,
for urban India, the cases are significantly higher for the nonEAG states. Overall, 47.5% of the total cases occurred in the
EAG states. The EAG states comprise about 45% of Indias
population, and to that extent, the distribution seems logical.
However, if the fact that these are the socioeconomically
weaker states and contribute mostly to the adverse Millennium
Development Goal (MDG) outcomes is taken into account,
such a distribution of case burden becomes a cause for concern.
97
Treatment costs and loss of work

days and earnings due to malaria
Table 3 presents the average expenditure on malaria for
outpatient treatment and hospitalization, work days lost, and
loss of earnings, by residence and consumption quartiles.
Overall, an average of 175 rupees was spent for each outpatient
treatment and 75 rupees on each hospitalization for malaria
in 2004. The disease required more outpatient expenditure
generally, though hospitalization expenses in urban India were
relatively much higher than in rural India. While the average
work days lost was similar across residence, loss of earnings
was higher in urban areas. There also seems to be a positive
correlation between economic status and cost of treatment,
with higher quintiles spending more on malaria treatment.
Economic burden of malaria in India

Table 4 presents estimates of the economic burden of malaria
from treatment costs, the value of earnings foregone because of
work days lost, and the current value of lives lost.
The costs of illness for outpatient treatment, hospitalization
and other costs are based on the estimates given in Table 3, and
calculated for 2012 by applying the appropriate GDP deflator.
The relative costs have, therefore, been assumed to be the same
with respect to each other. The average total cost of treatment
was 475 rupees in 2012. Earnings loss per day were 213 rupees
and the total work days lost is assumed to the same (10 days),
derived from the NSS study.
The results indicate that the total economic burden from
malaria in India could be around US$1940 million and varying
the death rate does not make much difference. That is because
the major burden comes from lost earnings (75%), while the
remaining 24 % comes from treatment costs. Mortality and
value of lives foregone is not a major source of economic
burden of malaria. The results do not change much when
varying the total number of deaths. However, if the prevalence
figures were varied, the estimates would change dramatically,
though this exercise is not attempted here, owing to the lack of
data that might indicate the true prevalence and incidence of
malaria in the country. Clearly, if the prevalence was assumed

to be double, the loss of earnings would be a substantial part of
the total economic burden. Overall, while malaria may not lead
to many deaths, it imposes a great burden via illness and missed
days of work, which in turn has implications for households
welfare, and ultimately would also play out at the macro level
by impacting national productivity and income.
Public financing of vector-borne

disease control in India
High economic burden warrants significant spending on
prevention, control and treatment; this section attempts to
understand the level and patterns of public spending on the
malaria programme.
Public expenditure on malaria prevention and control forms
a part of the NVBDCP of the Government of India. The
NVBDCP is an umbrella programme for prevention and
control of vector-borne diseases, and is, in turn, a part of the
National Disease Control Programme (NDCP), which has
another five components dealing with leprosy, tuberculosis,
blindness, drug de-addiction and iodine deficiency. Currently,
the NVBDCP has a 43% share of expenditure under the
NDCP and malaria accounts for more than half of the central
government expenditure on vector-borne diseases.
The two sources of financing NVBDCP expenditure are the
Domestic Budgetary Support (DBS) and the Externally Aided
Component (EAC). While the DBS represents the central
government contribution, the EAC consists primarily of
funding from the Global Fund to Fight AIDS, Tuberculosis
and Malaria and the World Bank (GFATM). Figure 1 shows
the trend in allocation and actual expenditure on the NVBDCP.
The DBS and EAC have been supplementing each other since
19971998, which marked the initiation of the World Bankassisted Enhanced Malaria Control Project (EMCP). Other
than a brief period between 20052006 and 20082009, the
DBS has exceeded the EAC. This jump in EAC coincides
with the GFATM-assisted Intensified Malaria Control Project
(IMCP) in 94 districts of 10 states, along with the introduction
of rapid diagnostic test kits.19 Actual expenditure has trailed
budgetary outlay for the entire period and reached a peak
Table 3: Direct and indirect cost of illness from malaria, 2004

Categories
Sector
Rural
Urban
Quartiles
Poorest
Second
Third
Richest
All
Treatment cost (average per capita per month), rupees

Outpatient
Others (Transport,
Hospitalization
care
lodging etc)
Total
Work days
lost
Loss of earnings
(average per capita
per day), rupees
191
119
53
149
28
19
272
286
10
9
107
171
167
154
173
210
175
46
75
58
135
75
28
25
24
26
26
241
254
256
370
275
11
11
9
8
10
91
131
119
158
124
Source: NSS unit level data, 60th round.2
98
Total economic costs due to

malaria (millions of rupees)
Total economic costs due to
malaria (millions of US dollars,
US$1=60 rupees)
1935
1937
2010-11
2009-10
2008-09
Budget Allocation -- DBS
Budget Allocation -- EAC
Budget Allocation -- Total
Actual Expenditure
Figure 1: Budgetary allowance and expenditure under NVBDCP

DBS: Domestic Budgetary Support; EAC: Externally Aided Component.
Source: Strategic plan for malaria control in india, 2012201719
Note: scenarios I and II are based on alternative

estimates of deaths from malaria.
during 20082009, which was followed by a reduction in

budgetary outlay itself, in absolute terms. Comparing the
previous two plan periods (see Table 5), it is observed that the
aggregate approved outlay has grown by 27% between the two
plan periods, but actual expenditure has grown by only 13%.
Further, the rate of absorption measured by the proportion of
outlay actually spent has declined by more than 25 percentage
points between the two plan periods. This is important because
a major chunk of the plan expenditure is in the form of
direct transfer of central plan assistance to state/district-level
autonomous bodies/implementing agencies. Such a low rate of
utilization could be indicative of weak absorptive capacities,
as well as administrative issues. Whatever the reasons, lower
absorption leads to efficiency loss, and needs proper analysis.
Figure 2 shows the trends in plan expenditure on NVBDCP
by the central government. It is important to note that plan
expenditure comprised 96% of the total expenditure on the
programme in the year 20112012.21 Plan expenditure (the
blue line) demonstrates a clearly increasing trend over the
years, with a slight decline during 20072009. It has more than
doubled during the 10-year period. While this is encouraging,
when viewed in isolation, it says little about the significance
of this programme within the central government budget
for the health sector. To examine this, Fig. 2 also plots plan
expenditure on NVBDCP, but as a percentage share of total
plan expenditure of the Ministry of Health and Family Welfare

(MOHFW; the red line). It is observed that this share steadily
declines from 4% in 20022003 to 2.2% in 20112012.
When this trend is juxtaposed with the significant burden of
malaria analysed in the previous section, it emerges as a cause
for concern. In fact, plan expenditure on the NDCP as a share
of the total plan expenditure of the MOHFW has also registered
a decline from 9% in 20022003 to 5% in 20112012. This
is indicative of the general decline in health spending of the
government, which affects all public health programmes.22
Although health is constitutionally a state subject, the
central government provides technical, commodity (drugs,
insecticides and larvicides) and financial assistance to the
states and UTs. North-eastern States (Arunachal Pradesh,
Assam, Manipur, Meghalaya, Mizoram, Nagaland and Tripura)
have been provided 100% central assistance for programme
implementation since December 1994. Additionally, in 100
districts of eight states, namely Andhra Pradesh, Chhattisgarh,
Jharkhand, Gujarat, Madhya Pradesh, Maharashtra, Orissa
and Rajasthan, 1045 PHCs predominantly inhabited by tribal
people have been provided full support, including operational
expenses under the EMCP, with World Bank assistance, since
1997. The new World Bank-supported Malaria control and
kala-azar elimination project for a period of 5 years has also
been implemented since 20082009. The operational costs for
Table 5. Plan financing of anti-malaria programme
Plan expenditure on NVBDCP

Approved outlay (billion rupees)
Actual expenditure (billion rupees)
Expenditure as % of outlay
2006-07
116194
2007-08
116093
2005-06
115
2004-05
14
2003-04
Current value of lives lost (millions

of rupees)
2001-02
87739
2002-03
Value of earnings foregone

(millions of rupees)
2000-01
28340
1999-00
Total costs of treatment (millions of

rupees)
Scenario
II
1998-99
Scenario I
5.0
4.5
4.0
3.5
3.0
2.5
2.0
1.5
1.0
0.5
0.0
1997-98
Parameters
Rs Billion
Table 4: Economic burden of malaria under alternative

assumptions of mortality
Xth plan (20022007)

13.49
11.97
88.7
XIth plan (20072012)

31.9
19.53
61.2
Average annual growth (%)

27.3
12.6
Source: Health profile of India, 2012, Central Bureau of Health Intelligence.20
99
Plan Expenditure on NVBDCP

Expenditure on NVBDCP as % of Total Plan Expenditure of MOHFW
Figure 2: Trends in plan expenditure on NVBDCP

Source: Health profile of India, Central Bureau of Health Intelligence,
MOHFW, Government of India,20 and Demand for grant no 47,
MOHFW, Union Budget, Ministry of Finance, Government of India.21
implementation of the NVBDCP and certain commodities are

met from state funds. The centre also meets the requirement of
states during emergency situations. Being under the umbrella
of the National Rural Health Mission, the states are required to
submit their project implementation plan every year, which is
appraised in the MOHFW, and thereafter funds are allocated
under the NVBDCP.19
Figure 3 shows the distribution of central allocations for
NVBDCP for selected states with a share of malaria cases
greater than 1%, for the year 20102011. The percentage share
of malaria cases for the same year is also plotted alongside.
The states are ordered by their share in total allocation for the
NVBDCP.
States that receive the highest share of central allocation
for NVBDCP are Odisha, Assam, Jharkhand, Bihar and
Chattisgarh. If this is combined with the states share of malaria
cases, some interesting observations can be made. For more
than half of these states, the share of allocation falls short of the
share in malaria cases in the country. Especially significant are
the cases of Chattisgarh, Gujarat, Jharkhand, Maharashtra and
Odisha, which are also known to be the states with relatively
greater burden of malaria. This analysis raises the possibility
of reallocation of central resources and aligning these with
disease burden across states.
Comparing with the estimated economic burden calculated
from the cost-of-illness approach, in 2012, about 5410 million
rupees or US$86 million was spent on the entire vector-borne
disease programme of the country. While a major part of this
will be on malaria, the amount remains much lower than the
potential economic burden imposed by the disease, which is
around US$1940 million for only adults. There are significant
costs involved for treatment, as well as other social costs of
morbidity and deaths of children that have not been included
in the analysis.
100
5.0
Percent share of Allocation
Karnataka
Tamil Nadu
Gujarat
Manipur
Mizoram
0.0
Nagaland
2011-12
2010-11
2009-10
200809
2007-08
200607
200506
200405
200304
200203
0.0
10.0
Arunachal Pradesh
1.0
15.0
Rajasthan
2.2
Meghalaya
2.0
Maharashtra
1.9
Tripura
2.0
Andhra Pradesh
2.0
20.0
Madhya Pradesh
2.1
West Bengal
2.0
25.0
Uttar Pradesh
2.6
2.1
3.4
3.0
Bihar
3.0
3.2
30.0
Chhattisgarh
4.0
4.1
3.0 3.8
Assam
3.1
4.5
4.0
3.5
3.0
2.5
2.0
1.5
1.0
0.5
0.0
Jharkhand
3.1
3.3
Odisha
3.4
Percent
Rs Billion
5.2
3.9
5.0
Percent
6.0
Percent share of Malaria cases
Figure 3: Share of allocation under NVBDCP and malaria cases for

selected states, 20122011
Source: data on financial allocation from Lok Sabha
unstarred question No. 5008, dated on 2 September 2011;23
data on malaria cases from NVBDCP website.24
Overall, the expenditure analysis indicates that there is a need

to step up spending on malaria, which is very low compared
to the potential burden it is imposing in the country, and
possibly declining as a percentage of total health spending
in the country. Also, the distribution across states does not
seem commensurate with the disease burden, indicating the
possibility of improving resource allocation for spending to be
more effective.
CONCLUSIONS AND DISCUSSION

While a proper surveillance system would remain a key to
assessment of the economic impact of malaria and require
global cooperation and consensus regarding the methodology
of estimation,25 the analyses in this study, including the
estimates of cost of illness and deaths, yield useful insights
into the magnitude of the problem, and enable comparison with
current disease-control expenditures. The current surveillance
is clearly inadequate, since it mostly captures data from the
public sector. Also, the economic burden of malaria may be
much higher, especially since a significant percentage of the
population does not seek care. Under these circumstances,
these figures for economic burden should be treated as being
on the lower side; the true impact may be much higher, being
driven by cases of morbidity resulting in loss of productive
days, and treatment costs, rather than mortality. In particular,
the loss of work days is quite high for malaria and is likely
to impose a high economic impact at the household level as
well. The profile of those affected clearly indicates that such
work-day losses are going to be felt more severely by the most
vulnerable.
Funding will remain the most important policy concern for the
control, prevention and treatment of malaria. While domestic
funding for malaria is augmented by international funding from
sources like the GFATM and the World Bank, analysts have
pointed out that global funding has not been adequate so far
and it is unlikely that MDG goals to halve the disease burden by
2015 will be achieved without significant increases in funding.26
The gap in funding need remains a critical global concern and
it could be almost four times the funds currently available.
The Roll Back Malaria Partnership has developed The Global
Malaria Action Plan, which can be viewed as a document
around which other partners can coordinate their efforts. For
resource mobilization, a two-pronged strategy visualized by
GMAP includes setting up resource-mobilization processes
at country level, by developing a fully fledged country-level
financing plan, and coordination with international agencies
such as the World Bank and other partners.27.
Furthermore, even at the domestic level, actual expenditure has
fallen far short of approved outlay for vector-borne diseases.
Priority accorded to vector-borne disease seems to have
declined over the years, as evidenced by the declining share of
this component in the plan expenditure of the MOHFW. There
also seem to be horizontal imbalances in the distribution of
these funds across states, with states with higher prevalence
of malaria not necessarily receiving higher funding from the
central government
In addition to scaling up effective interventions, strengthening
health systems remain a cornerstone of a successful strategy
of malaria control. Interventions can be effective only if there
is an effective system of, for example, supply chain, human
resources and monitoring and evaluation. Strengthening
health systems, as well as scaling up interventions, would
require funding. While international funding has been a major
part of Indias funding for malaria, the country has to find
additional resources from its domestic sources for a sustainable
programme of control and elimination of malaria.
6.
7.
8.
9.
10.
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burden of malaria in India: the need for effective spending.
WHO South-East Asia J Public Health 2014; 3(1): 95102.
Contributorship: Both authors were responsible for conceptualization,
analysis and writing this paper.
Policy and practice
DOI: 10.4103/2224-3151.115828
Towards universal health coverage: an

example of malaria intervention in Nepal
Shiva Raj Adhikari
Abstract
A comprehensive and integrated assessment of health-system functioning
requires measurement of universal health coverage (UHC) for disease-specific
interventions. This paper aims to contribute to measurement of UHC by utilizing
locally available data related to malaria in Nepal. This paper utilizes the elements
of UHC as outlined by the World Health Organization (WHO). The concept of
UHC represents both improvements in health outcomes and protection of people
from poverty induced by health-care costs. Measuring UHC focusing on a tropical
disease highlights the progress made towards elimination of the disease and
exhibits health-system bottlenecks in achieving elimination of the disease. Several
bottlenecks are found in the Nepalese health system that strongly suggest the need
to focus on health-system strengthening to shift the health production function of
malaria intervention. The disaggregated data clearly show the inequality of service
coverage among subgroups of the population. Analysis of effective coverage of
malaria interventions indicates the insufficient quality of current interventions. None
of households faced catastrophic impact due to payment for malaria care in Nepal.
However, the costs of hospital-based care of malaria were not captured in this
analysis. The paper provides the current status of UHC for malaria interventions
and reveals system bottlenecks on which policy-makers and stakeholders should
focus to improve Nepals malaria control strategy. It concludes that financial
coverage of the malaria intervention is at an acceptable level; however, service
coverage needs to be improved.
Department of Economics,
Tribhuvan University, Nepal
DrShiva Raj Adhikari, Associate
Professor of Economics,
Department of Economics, Patan
Multiple Campus, Tribhuvan
University, Lalitpur, Nepal
Email: sssadhikari@yahoo.com
Key words: universal health coverage, malaria, Nepal, health-systems

strengthening
Introduction
There are considerable debates on how to assess whether a
country has achieved universal health coverage (UHC).1,2 There
is no straightforward or defined way to achieve UHC; many
paths towards UHC are found in the literature and no particular
path to reach UHC is endorsed.3,4 There is no doubt, however,
that UHC is desirable because it makes the current health
achievements sustainable. It also improves health outcomes
through greater access to health services and provides financial
protection against the cost associated with illness.
UHC is a means to achieving better health status and to
sustaining economic and social development. It is associated
with better health, equity and financial protection.3 Achieving
UHC is a long journey and requires a huge investment to
design health systems that allow universality in health care.
Amovement for UHC is now in progress after being endorsed

by the World Health Assembly through a resolution in 2005.
UHC is being considered as the umbrella health goal in the post2015 development agenda. In December 2012, the movement
prompted the United Nations General Assembly to call on
governments to urgently and significantly scale-up efforts to
accelerate the transition towards universal access to affordable
and quality health-care services. Universal indicates equality
and for everyone to have the opportunity. Coverage may be
the outcomes of the intervention. UHC means that all people
can use health services, while being protected against financial
hardship associated with paying for them.3
Nepal has made remarkable achievements in health outcomes
and poverty reduction over the past two decades. International
development partners are providing technical and financial
support to work on elements and issues related to UHC;
103
Adhikari: Universal health coverage and malaria in Nepal
however, designing the path of UHC is not straightforward

and national average data hide the inequality in progress at
the local level. In this situation, more evidence is needed at
local level to find ways to improve the coverage of existing
interventions and to design a health-care financing system.5
Building evidence in support of UHC is more important than
measuring the relative achievement of UHC. In addition, we
need to know how to increase access, coverage, and utilization
of quality services, and how to address obstacles that hinder
success of interventions.
Specifically, this paper aims to answer two questions from a

UHC perspective. (1) What are the important elements of UHC
at the local level? (2) How we can measure UHC, particularly
related to tropical diseases using the example of malaria? The
analysis aims at assessing the effective coverage of malaria
interventions and the catastrophic and impoverishing impact
from the use of these interventions in Nepal by utilizing the data
from health information systems and national representative
household surveys.
This paper contributes to the aforementioned literature with

discussion of how to measure UHC by utilizing the locally
available data related to tropical diseases. Tropical diseases,
such as malaria in Nepal, are linked to progress towards
the Millennium Development Goals (MDGs). In Nepal,
we have made good progress in terms of national averages;
however, there may be inequalities and disparities among
population groups. Measuring UHC focusing on tropical
diseases highlights the progress made towards elimination of
diseases and exhibits health-system bottlenecks in achieving
the goal of elimination of diseases. The World malaria report
2013 indicated such possible gaps; for example, worldwide,
between 2000 and 2012, estimated malaria mortality rates
decreased by 45% in all age groups and by 51% among
children under 5years of age; however, millions of people
at risk of malaria still do not have the access to interventions
such as an insecticide-treated bednets, indoor residual spraying
(IRS), diagnostic testing and artemisinin-based combination
therapies.6 The concept of UHC represents both improvements
in health outcomes and protection of people from poverty
induced by health-care costs. Progress against malaria provides
evidence of the tangible benefits of population-wide access to
life-saving interventions. Analysis of financing strategies for
tropical-disease care is needed in order to know the impact of
health-care cost on household economies.
METHODS AND MATERIALS
Several studies have suggested that there is a lack of

consideration of the health-system context in interventions
for tropical-disease control since factors of health systems
can constrain the success of programmes such as tuberculosis
control and malaria control.79 A comprehensive and more
integrated assessment of health-system functioning requires
measurement of UHC for disease-specific interventions. It is
important for the country to know the relative status of UHC.
For example, the Nepal health sector implementation plan
20102015 has set an objective to improve the health system
to achieve universal coverage of essential health services.10
The Sixty-fourth World Health Assembly Resolution
WHA64.17 on malaria adopted in May 2011 focuses on
developing strategic and operational plans for achieving and
maintaining universal coverage of malaria interventions. As a
Member State, Nepal has a strategic vision of a malaria-free
Nepal by 2026; however, situation analysis and programme
evaluation were primarily based on epidemiological data.
Analysis of the situation of malaria intervention from a
health-system approach is a major missing element despite
the importance of better understanding the sustainability
of programmes and the current status of UHC for malaria
interventions in Nepal.
104
Conceptual framework
This paper focuses on the elements of UHC as outlined by the
World Health Report 2010: providing all people with access
to needed health services of sufficient quality to be effective
and ensuring that the use of these services does not expose
the user to financial hardship.3 The Report provided a threedimensional conceptual framework for UHC breadth, depth,
and height of coverage to demonstrate population coverage,
service coverage and financial coverage. In this context,
breadth is defined as the proportion of the population covered
across various population subgroups, which highlights equity
in coverage across consumption quintile groups, gender, age,
and place of residence among others. The service coverage
dimension captures the character of services covered and need
of range of services. The financial coverage dimension ensures
that people do not suffer financial hardship linked to paying
for these services at the time they need them. Although the
conceptual framework is clear, operationalizing measurable
indicators for tracking a countrys level of coverage is not
straightforward; for example, what are the indicators for
service coverage or financial coverage?
Several studies have suggested approaches to measure
coverage: for example, the PiotFransen model for sexually
transmitted infections;11 the Tanahashi model for health
services;12 and the model for environment and access to health
care.13After rigorous review of various concepts based on the
available literature in order to measure service coverage, we
concluded that the concept developed by Tanahashi may be a
better fit for measuring the elements of UHC.
There are numbers of reasons behind reaching this conclusion,
for example: (a) the model focused on effectiveness of coverage
as an output indicator; (b) the model allows us to assess potential
capacity of a health system and the utilization of that capacity;
(c) it allows assessment of the capacity of the health system to
deliver the full effect of interventions and quality of services;
(d) some organizations such as UNICEF and The World Bank
have used this concept to show health-system bottlenecks in
marginal budgeting bottleneck analysis or investment cases;
(e) it can be applied to national or decentralized health systems;
(f) it is easy to apply to scaled-up health care.
Coverage can be defined as the proportion of the population
who receive an intervention among those who need it. Coverage
is influenced by supply (provision of services) and demand
by people in need of services. The Tanahashi health-servicedelivery framework has been applied to evaluate the effect
of the availability, accessibility, acceptability, and quality of
health services on utilization and coverage of malaria services
among vulnerable populations.14,15 The dimensions of access
and coverage of services that are derived from the Tanahashi
model are shown in Figure 1.
Coverage is measured as the ratio of services in relation to
the target population. The top three coverage indicators are
related to the demand perspective and the remaining three
coverage indicators are the supply perspective. Availability
of critical health-system inputs, such as drugs, long-lasting
insecticide-treated nets (LLIN) stocks, human resources for
functioning of the health system, and accessibility of malaria
interventions to clients are the important elements while
assessing the service coverage. Initial utilization describes
preconditions for clients such as availablity of at least any
type of bednets or the first contact with services to continue
the utilization of services. Continuous utilization indicates
adequate coverage such as percentage of households having
at least one LLIN. Effective coverage is a critical indicator
that measures health-system performance and quality of care.
It is an impact indicator based on given interventions such as
percentage of children younger than 5 years sleeping under a
LLIN the previous night. The Government of Nepal, with the
support of external development partners has executed malaria
control interventions: IRS, LLIN, rapid malaria diagnosis and
artemisinin-based combination treatment. Malaria is a focal
disease in Nepal. The recent microstratification based on
village development committees (VDCs) suggested that only
52% of the population is at risk. Choices of tracer intervention
and service delivery modes are primarily determined by the
availability of indicators.
To assess financial coverage requires total expenditures from

different sources on malaria interventions. Health-system goals
are not only improving health due to malaria interventions
but also protecting people from the financial consequences of
malaria. There may be financial consequences of out-of pocketpayments (OOP) for malaria care on households. The paper
uses financial coverage indicators of catastrophic payments
and impoverishment that reflect the concept of hardship to
utilize malaria interventions. Malaria diagnosis and treatment
are provided free of cost at public health facilities; however the
Nepal Living Standard Survey (NLSS) 20102011 suggested
that people had paid some amount of money for malaria care.
The private sector uses a variety of rapid diagnostic tests
including antibody-based tests and treatment with artemisinin
monotherapy as well as other forms of malaria combination
treatment.
Indicators of UHC and sources of data

The indicators in Table 1 were used to measure UHC for
malaria interventions. Tracer interventions that represent the
service coverage are selected only if data are available for each
of its six coverage indicators: availability of commodities and
human resources; geographical accessibility; initial utilization;
continued utilization; and effective coverage level. A tracer
intervention is representative of other similar indicators within
the service delivery mode. This analysis used indicators of
financial coverage as suggested by the literature to measure
the capacity of current financial coverage to provide protection
from financial risk due to malaria illness.
RESULTS
Population coverage
Effective Coverage - Quality/impact

People who receive effective care
Continuous coverage - Continuous coverage

People who use the services
Target Population who don't

have continuous coverage
Initial utilization - Proportion of service capacity used

People who will to use services
Accessibility Coverage - Physical access of services

People who can use services
Availability Coverage - Human resources of correct skills mix

People for whom service is available
Availability Coverage - Essential commodities and equipment

People for whom service is available
Target Population
Figure 1: Tanahashi model dimensions of service access and

coverage.
Consultations of malaria care are conditional on need or illness.

This analysis disaggregated the types of illness by gender,
development region, rural/urban residence, age group and
consumption quintile. Malaria care may be different from other
health care; however, malaria and other health services are
provided under the same roof by health providers. Therefore,
analysis of population coverage in relation to other types of
illness may be interesting because it gives some idea about the
burden of malaria relative to other illnesses.
Data from the NLSS 20102011 indicating the percentage
distribution of acute illness by type show that the burden of
malaria illness is around 1%.16 Data from the NLSS 2010
2011 also indicate the percentage of health consultations for
acute illnesses by status and practitioner type across various
population subgroups. They show that almost 30% of people
with acute illness did not consult any health-care providers,
indicating that in aggregate, the services do not cover almost
30% of the population for some reason. Table 2 shows the
calculated inequalities within population subgroups. The
highest inequality was found between different age groups.
This is followed by inequality in coverage in development
regions; however, no difference is found between ruralurban
categories.
105

Table 1: Indicators and data sources
Indicators of population
coverage
Data sources and

analysis
Indicators
of service
coverage
Effective
coverage of
diagnosis
and treatment
intervention
NLSS 2010
2011;16 MOHP
(2010); MOHP
(2012); MOHP
(2011)23
Data sources
and analysis
Population coverage
measures service and
financial coverage across
population subgroups
NLSS data
(nationally
representative),
201020111
Gender, residence,
consumption quintile and
age groups
Category of illness:
malaria and others
Effective
coverage of LLIN
intervention at the
targeted malaria
risk areas and
malaria risk areas
MOHP (2011);23
MOHP (2012);18
Mehata et al
(2012);4 MOHP
(2010);17 WHO
(2011)5
Service coverage by
population subgroups
Consulted any type

of health providers
and not consulted
of services after
illness; percentage
of not consulted is
the proxy indicator
of not covered
Effective
coverage of IRS
at the targeted
risk areas
NLSS 2010
2011;16 MOHP
(2010);17 WHO
(2011)20
Composite
effective
coverage index
From 1,2 and 3

above
Indicators
of Financial
coverage
Out-of-pocket
payment for
malaria care
and distribution
by consumption
quintile
Catastrophic
payment and
impoverishment
impact
Data sources
and analysis
NLSS 2010
201116
Methods used
as suggested
in ODonnell
(2008);26
Adhikari et al.
(2009);27 and van
Doorslaer et al.
(2006)21
Methods used
Concentration
index (who suffer as suggested
from catastrophic in ODonnell
(2008) and van
payment)
Doorslaer et al.
(2006)6
Total malaria
expenditure
Estimated using
data from NLSS
2010201116 and
various other
sources
MOHP = Ministry of Health and Population
Self-reported adequacy of health services can be used as an

indicator for population coverage in UHC. In the NLSS 2010
2011, respondents were asked about adequacy of health-care
services (which included malaria care). The results, shown in
Table 3, highlight that 90% of the richest quintile experienced
just adequate health services; however, only 68% of
the poorest quintile people perceived services to be just
adequate.16 There is an almost 10 percentage point difference
between rural and urban in adequacy of health services. These
results suggest that minimum population coverage in terms of
just and more than adequate services was 67%.
Service coverage
The service coverage dimension of UHC for malaria
interventions includes availability of services, utilization of
services and quality of services that are captured by the facilitybased as well as household survey data. Malaria interventions
can be broadly categorized into two groups curative and
preventive although the roles of promotion and rehabilitation
services are significant in providing health outcomes. An
assessment of service coverage is based on diagnosis and
treatment and prevention of malaria.
106
Diagnosis and treatment

A microscopy facility is available in available at the district
hospital, primary health care centre (PHCC) and some of the
health posts (HPs) in endemic districts, while rapid diagnostic
tests are available in HPs and sub-health post (SHPs) where
a microscopy facility is not available. Antimalarial drugs
are provided free of charge from all the public sector health
facilities. Antimalarial drugs are provided free of charge
through the female community health volunteer (FCHV)
network in high-risk areas according to national treatment
guidelines.18 In malaria endemic areas, where there is no
microscopy facility, rapid diagnostic tests are made available
for the diagnosis. For diagnosis and treatment interventions,
the aim is to ensure prompt and effective treatment of malaria.
Figure 2 shows coverage of diagnosis and treatment of malaria.
Availability and accessibility of malaria interventions are the
preconditions for willingness to use and utilization of these
interventions. Effective coverage of a malaria intervention
indicates the quality of the intervention; for example, treatment
of severe malaria with antimalarials as per national guidelines is
66% although 92% of people show willingness to use diagnosis
and treatment services. The indicators shown in the figures

Table 2. Health consultations for acute illnesses across population subgroups16
Percentage of service consultation
Consulted any
types of health
providers
Not consulted
Total
Male
70.5
29.5
100
Female
68.5
31.5
100
Eastern
67.6
32.4
100
Central
66.3
33.7
100
Age groups
Consumption
quintile
Rural/
Urban
Development
regions
Gender
Population sub-groups
Nepal
Western
75.3
24.7
100
Mid-western
71.0
29.0
100
Far western
72.7
27.3
100
Urban
69.6
30.4
100
Rural
69.4
30.6
100
Poorest
71.1
28.9
100
Second
69.4
30.6
100
Third
68.3
31.7
100
Fourth
69.6
30.4
100
Richest
69.2
30.8
100
0-5 years
79.7
20.3
100
6-14 years
69.7
30.3
100
15-44 years
68.0
32.0
100
46-59 years
63.7
36.3
100
60+ years
61.1
38.9
100
Total
69.4
30.6
100
Table 3: Self-reported adequacy of health services16

Population
sub-groups
Consumption Urban/ Development
quintile
Rural
regions
Inequality
Eastern
Central
Western
Mid-west
Far west
Less than
adequate
16.4
12.9
17.5
30.7
32.0
Urban
Ratio of highest and

lowest value
1.07
1.36
1.00
1.10
1.92
82.2
83.8
80
68.9
66.2
More than
adequate
0.6
2.4
2.1
0.4
1.1
10.2
87.7
1.0
1.2
100
Rural
20.7
77.2
1.7
0.5
100
Poorest
Second
Third
Fourth
Richest
30.2
24.1
22.4
15.2
7.4
68.2
73.8
75.5
82.3
90.3
0.9
1.6
1.4
2.1
1.6
0.7
0.5
0.7
0.4
0.7
100
100
100
100
100
Just adequate
Not applicable
Total
0.8
0.8
0.5
0.0
0.6
100
100
100
100
100
107
Coverage indicators
% of severe malaria treated with antimalarials as per

national guidelines
66
% of confirmed cases of uncomplicated malaria

treated with antimalarials as per national guidelines
70
population) live in high-risk VDCs; 2660692 (9.79%) live in

moderate-risk VDCs; and 9378735 (34.52%) live in low-risk
VDCs. A total population of 14139920 (52.05%) live in norisk VDCs.22
% of patient treatment provided out of laboratory

confirmed cases of Malaria
92
% Households having access PHCCs and hospitals

within one hour distance
54
% of filled posts at PHCCs and district hospitals by

doctors and staff nurses
82
% of in district facilities have no stock outs of tracer

drugs/commodities for more than a month
77
0
10 20 30 40 50 60 70 80 90 100
Per cent
Figure 2: Coverage of diagnosis and treatment of malaria
provide at least two views: (a) the situation of availability or

utilization of interventions; and (b) determinants of system
bottlenecks of the intervention. For example, out of laboratory
confirmed cases of malaria only 92% of clients received
treatment indicating the gap in service coverage; at the same
time, it indicates that 92% clients are willing to use services but
not why the percentage of treatment with antimalarials (both
severe and complication) as per national guidelines is lower
by at least 20%. Figure 2 shows the problems in the supply
side. The Annual Report of the Department of Health Services
20102011 also indicated problems or constraints in the supply
side such as irregular and inadequate supplies of antimalarial
drugs, lack of orientation on the malaria programme for all
health workers, irrational use of rapid diagnostic tests and
malaria microscopy against national protocols, and lack of
coordination between the microscopic networks and collection
centres.18 Without improving supply-side indicators such as
availability of essential commodities and drugs and human
resources, and accessibility of malaria care, increasing the
effective coverage (or impact indicator) such as percentage
of severe malaria treatment may not be possible. Figure 2
indicates the situation of coverage of diagnosis and treatment
of malaria. Different processes should be followed in the
different services delivery mode, such as facility-based or
community-based, while providing diagnosis and treatment
services. Figure 2, however, does not provide a comprehensive
picture with regard to diagnosis and treatment of malaria,
such as the huge gap between clinically suspected malaria and
laboratory confirmed cases;20 but such a problem is indicated
by the 82% available human resource with correct skill mix at
the facility. Data availability and choice of appropriate tracer
intervention are critical issues while analysing the depth of
service coverage.
Preventive intervention
A recent microstratification report on malaria risk in Nepal
demonstrated that 54 VDCs came under the high-risk category,
201 VDCs came under the moderate-risk category, 999 came
under the low-risk category and 2718 (68.36%) came under the
no-risk category. A total population of 985636 (3.62% of the
108
The Ministry of Health and Population (MOHP) with the

support of external development partners has implemented a
malaria control programme including IRS and LLIN. LLINs
are distributed according to the existing LLIN distribution
guidelines, one LLIN per two persons in a house.18 LLINs are
distributed through a campaign with the strategy of one third
target VDCs per year in each district so as to cover the entire
high-risk VDCs by the end of the third year. Two rounds of
routine IRS are carried out annually in each high-risk VDC
unless LLIN population coverage in that VDC exceeds 80%.
The first round is undertaken during MayJune and the second
round in AugustSeptember.
Different sources report different coverage of LLINs. Reported
data used different denominators such as targeted population
or total population. Survey-based data are more reliable than
reported data; however, survey-based data are not frequently
available. Some of the VDCs achieved more than 90%
coverage; however, a field survey report suggested 80%
coverage with at least one LLIN in the targeted intervention
areas.20 In other words, more than 80% people are agreeable to
use an LLIN; however, as shown in Figure 3, only 76% people
utilized the LLIN.17 Effective coverage, i.e. the proportion of
children younger than 5 years who children slept under an
LLIN the previous night is only 61%. The effective coverage
indicator indicates that the behaviour change communication
strategy is not very effective.
LLIN coverage in targeted areas is found satisfactory;
however, in the endemic districts, the coverage is very low.
The recent national household survey shows that effective
coverage in the endemic districts is only 10%.19 The demandside barriers in use of LLINs in endemic districts are shown in
Figure 4. On the other hand, the results from the demand side
suggest that there are some problems with LLINs reaching
the household level or problems in LLIN distribution. From
the point of view of UHC, coverage indicators do not show
satisfactory results.
LLIN and IRS are complementary interventions; however, the
aim is to increase the coverage of LLINs and to reduce IRS.
As mentioned previously, two rounds of IRS campaigns are
conducted in a year in villages at risk. The efficacy of IRS is
about 12 weeks; therefore, to make IRS more effective, the
second round IRS is crucial. The literature suggest that IRS
coverage is very poor and effective coverage is found to be
zero because the second round of spraying was not conducted
for some reasons in 2009.20 This does not mean that the second
round IRS campaign is in the guideline but not in the practice;
it means that sometimes two rounds of the IRS campaign do not
happen on time or do not cover all households of that the first
round is also covered in the second round. The major problems,
as indicated by the results shown in Figure 5, are in the supply
side such as lack of equipment or commodities. Willingness to
use IRS is also less than willingness to use LLINs.
% of under five children in the targeted intervention

areas slept under LLIN in the previous night
61
76
% of at least one LLIN in the targeted intervention

areas
% of households used the services
80
Coverage indicators
Coverage indicators
% of people living in the targeted intervention areas

slept under the LLIN in the previous night
100
% active Female Community Health Volunteer

(FCHVs) at the community
100
% of filled posts at the facility
% of receiving LLIN through annual campaign as per

national guidelines
100
% of availability of drugs/essential
commodities/equipment
20
40
60
80
100
40
% of households willing to use service
% households living near distribution point or

reached by annual campaigns
34
% of households received effective care
61
% households having access health facility
84
91
88
0
120
Figure 3: LLIN coverage in the targeted areas
% of children under five in endemic districts who

slept under a LLIN the previous night
Coverage indicators
Figure 6: Composite coverage index
On occasion, demand-driven activities exert sufficient pressure

to improve supply-side efficiency. This analysis used the
composite coverage index (CCI) as suggested Boerma et
al.23 This composite index aggregates malaria intervention
coverage indicators. With providing equal weight to all tracer
interventions, CCI is presented in Figure 6.
10
% of households in endemic districts with at least

one LLIN
15
% of households in endemic districts with at least

one any type of bed net
56
% households living near distribution point or

reached by annual campaigns
100
Financial coverage
% active Female Community Health Volunteer

(FCHVs) at the community
100
Disease account
% of receiving LLIN through annual campaign as per

national guidelines
100
20
40
60
80
100
120
Per cent
Figure 4: LLIN coverage in endemic districts
Coverage indicators
10 20 30 40 50 60 70 80 90 100
Per cent
Per cent
% of households with effective coverage of IRS
% of households IRS second round sprayed at the

same risk VDCs as per national guidelines
% of households IRS first round sprayed at the risk

VDCs as per national guidelines
17
% households having access Health Post/Sub-health

Post within one hour distance
83
% of filled posts at PHCCs and district hospitals by

doctors and staff nurses
82
% of in district facilities have no stock outs of tracer

drugs/commodities for more than a month
77
0
10 20 30 40 50 60 70 80 90
Per cent
Figure 5: IRS coverage in village development committees
National health accounts provide evidence to monitor trends

in health spending for all sectors public and private
different health-care activities, providers, diseases, population
groups and regions in a country. They help in developing
national strategies for effective health financing and in raising
additional funds for health. Information can be used to make
financial projections of a countrys health-system requirements
and compare their own experiences with the past or with
those of other countries. Nepal does not yet produce national
disease accounts, although the approach has been popular in
other countries, such as in Australia, for some years. In Nepal,
malaria preventive, diagnostic and curative services are free of
charge in all health facilities; however, national representative
survey data suggest that people have paid some amount of
money to different types of providers such as public or private
providers.
The data on public expenditure24 and number of malaria cases
and OOP for malaria from the survey data and estimation
methods as suggested by the 2011 OECD report25 were used
to estimate the total expenditure on malaria. The data suggest
that OOP including for the private sector was 5% of total
expenditure on malaria. The remaining 95% is jointly covered
by the Government of Nepal and external development partners.
Nepal does not have an insurance system and public facilities
provide the services at free of cost or a heavily subsidized price.
Survey data suggest that average OOP (drug and consultation
109
cost) for malaria care was Nepalese Rupees (NRs) 1624 for
2010201126 (approximately US$ 22); however, hospitalization
costs were not included. The drug cost of OOP for malaria was
almost 90%. Average transportation cost, which indicates the
geographical access to services, was NRs 88 (US$ 1.2).
Distribution of OOP
Household consumption that includes food and nonfood
consumption is used as a living standard measure as suggested
by ODonnell and colleagues.27 From the NLSS 20102011
data on consumption and cost of malaria care it is seen that the
poorest and eighth groups shared almost an equal percentage
in the distribution of total cost for malaria care while the sixth
or richest groups shared the highest percentage. This finding
suggests that the richest group paid relatively less of their
affordable capacity for malaria care; however, the third to sixth
groups paid more.
The concentration index (CI), which summarizes the
information on the relationship between total cost of malaria
care paid by the household and the rank of their living standards,
is found to be 0.1043. The negative sign indicates malariacare payment is higher among the poor. Nevertheless; the CI
is not significant at the 5% level. As malaria is concentrated
in the certain areas of the country, this means missing values
for a national representative survey. It is challenging to get
significant results with limited data sets.
OOP payments can be categorized as catastrophic when they
exceed a given threshold, say 10% of household consumption.
OOP payments are also impoverishing when they are sufficient
to dip a low-income household into poverty. This paper
adopted the methods suggested by Adhikari and colleagues
to measure catastrophic payments and the impoverishment
impact of OOP for malaria care.28 The widely accepted method
for measuring the incidence and intensity of the catastrophic
payments is to use a threshold range from 5% to 40% of
household total consumption and nonfood consumption.29 The
impoverishment impact of a health-care payment is measured
in terms of its poverty incidence and intensity. The difference
between the pre-payment and post-payment income poverty,
gives an estimate of the poverty impact of health care payment
on incidence and intensity. The NLSS 20102011 reported an
average per person consumption NRs 34 829 for all Nepalese
citizens. The average consumption for the first poorest decile
group was NRs 11093; while for the richest decile it was
NRs 102772. We measured systematically catastrophic and
impoverishment impact using national representative data,
but with limited data on malaria care. None of households
faced a catastrophic impact due to payment for malaria care
in the given range of thresholds in the literature. Similarly,
no one was pushed due to malaria care payment to below the
poverty line. As mentioned previously, the reported cost in the
survey did not capture the hospital cost of malaria care. Due to
limitation of measurement of catastrophic payment, it fails to
capture those individuals who do not seek malaria care.
110
DISCUSSION AND CONCLUSION

A three-dimensional framework for UHC as suggested by
WHO (2010) was used to analyse the status of UHC for
malaria interventions in Nepal. There not yet global consensus
on service coverage measurement, especially on issues such as
an essential versus comprehensive service package for UHC
and criteria for selecting particular indicators.1,2 An essential
or narrow service package within the limited fiscal space can
ensure UHC; however, adopting a comprehensive service
package creates more challenges to achieving UHC. This paper
focuses on malaria interventions where services packages are
relatively clear and the interventions are globally acceptable.
Analysis of disease-specific UHC has a number of advantages.
For example, firstly, considering different types of health
care together to assess a service package could be highly
misleading due to the aggregation of many different types of
health intervention with widely different efficacy, effectiveness
and duration of treatment and prevention. Secondly, a
number of tropical diseases have their own peculiarities that
require specific interventions for their control or elimination,
making these virtually independent medical commodities and
definition of effective coverage differs. Thirdly, malaria in
Nepal is in pre-elimination phase, and a number of national
and international experts and stakeholders are engaged to
develop updated strategies; however, they are focusing on a
disease perspective rather than a health-system perspective.
Patterns of disease, care and treatment are changing. These
changes demand new delivery systems. Narrowly defined or
disease perspective strategies may not be sufficient to achieve
the desired outcomes.
This analysis used the Tanahashi approach of six coverage
indicators to measures service coverage. The approach allows
us to update the capacity of the health system to achieve
effective coverage by assessing both the potential capacity and
the utilization of that capacity. The service coverage dimension
captures issues related to availability of services and use of
these services. Population coverage focuses on population
subgroups such as gender and quintile group. Financial
coverage shows the financial hardship to use these services.
These three dimensions ensure priority of population groups,
comprehensive benefit packages, and subsidized cost of care.3
UHC can be defined for the disease-specific situation, for
example UHC can mean greater than 80% coverage of LLINs
for those at risk of malaria, and prompt and effective treatment
of malaria with an effective antimalarial within 24 hours of
onset of fever, in most cases an artemisinin-based combination
therapy. Comparing the current coverage situation of malaria
interventions with the given baseline coverage for UHC
suggests that Nepal, through focusing some of the indicators,
is far below this baseline indicator of UHC. Patterns of malaria
illness and epidemiology can suggest movement towards preelimination; however, several bottlenecks are found from the
results in the Nepalese health system, which strongly suggest a
need to focus on health-system strengthening to shift the health
production function of malaria interventions.
Financial coverage indicators show the financial burden or

shocks due to payment for malaria care on households. The
literature has frequently suggested that the costs of malaria
care are above 10% of household income;30,31 total household
costs of malaria per year have been reported to be as much as
18% of annual income in Kenya and 13% in Nigeria.32 The
financial shocks or catastrophic payment discourages use of
services not only for other household members but also other
members of society. The results suggest that OOP for malaria
in Nepal does not create financial hardship or discourage use
of services. None of patients faced catastrophic payment and
an impoverishment impact due to malaria care. This paper
does not capture the hospital-based care of malaria. Clients
have to pay more for hospital*based care although services are
provided free of cost at the public hospital, for example, OOP
for hospital-based treatment of kala-azar care was catastrophic
for the household since it extracted 17% of annual household
income and pushed more than 20% of non-poor people below
the poverty line.28
Both the strengths and shortcomings of the key indicators of
UHC for malaria interventions are discussed. There are some
limitations in the paper while measuring service coverage
and financial coverage. The paper tried to use the indicators
from same year, 20102011; however, very limited data were
available to measure the service coverage indicators that did
not permit measurement of depth of service coverage based
on service delivery mode, such as facility-based service
delivery, community-based service delivery and populationbased service delivery. However, the paper is able to
contribute to the existing literature on how to measure UHC
for malaria interventions using available indicators in lowincome countries such as Nepal, and to provide the current
status of UHC for malaria interventions and to reveal system
bottlenecks on which policy-makers and stakeholders should
focus to improve the malaria control strategy of Nepal.
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DOI: 10.4103/2224-3151.115828
The National Academy of Vectors

and Vector Borne Diseases in India:
two decades of progress
Neena Valecha1 and M.R. Ranjit2
Director, National Institute of

Malaria Research, New Delhi, India
and Vice President of the National
Academy of Vector Borne Diseases
2
Deputy Director, Regional
Medical Research Centre,
Bhubaneswa, India and Secretary
General of the National Academy
of Vector Borne Diseases
1
Abstract
The National Academy of Vector Borne Diseases (NAVBD) was founded at
Bhubaneswar in 1994, by Dr AP Dash, along with 15 like-minded scientists from
all over India. NAVBD is a non-profit academic organization in India, dedicated
to advancing and promoting knowledge on vectors and vector-borne diseases,
and encouraging scientists and members of the academy to conduct research on
vectors and vector-borne diseases. NAVBD convenes national and international
seminars, symposia and workshops to exchange knowledge on recent advances
in the field of vectors and vector-borne diseases and raise public awareness.
Plans are under way to expand the Academys activities to the rest of the SouthEast Asia Region.
Key words: India, National Academy of Vector Borne Diseases, vector-borne
diseases, vectors
Background
Vectors are organisms that transmit pathogens and parasites
from one infected person (or animal) to another, causing serious
diseases in human populations. These diseases are commonly
found in tropical and subtropical regions. Vector-borne diseases
(VBDs) account for 17% of the estimated global burden of all
infectious diseases.[1] Mosquito-borne diseases threaten the
lives and livelihoods of millions of people worldwide.[2]
Vector-borne diseases have not only adversely affected
the health of the people in the region but also impeded
overall socioeconomic development.[35] At the same time,
developmental activities without adequate environmental
concerns have increased the scope and scale of transmission
of these diseases. VBDs such as malaria, dengue fever,
chikungunya, Japanese encephalitis, kala-azar and lymphatic
filariasis have emerged as serious public health problems in
India. Many of these, particularly dengue and chikungunya
fever, Japanese encephalitis and malaria, occur in epidemic
forms, causing considerable morbidity and mortality. Dengue
is spreading rapidly to newer areas, with outbreaks occurring
more frequently and explosively. Over the past five decades, the
incidence of dengue has increased 30-fold globally, resulting
in 20000 deaths annually.[6] Chikungunya has re-emerged in

Dr Neena Valecha, National Institute
of Malaria Research, Sector 8
Dwarka, New Delhi 110077, India.
E-mail: director@mrcindia.org,
neenavalecha@gmail.com
India after a gap of more than three decades, affecting many

states of India, such as Andhra Pradesh, Andaman and Nicobar
Islands, Delhi, Gujarat, Karnataka, Kerala, Madhya Pradesh,
Maharashtra, Tamil Nadu and Odisha .[7] Currently, around
3.4billion people live at risk of malaria globally; during 2012
at least 207 million people were affected and, of these, 627000
died as a result of malaria,[8] while India reported more than
one million cases of malaria in 2012 and more than 40% of the
global burden of lymphatic filariasis.[9]
The National Academy of Vector Borne Diseases
Considering the importance of these diseases, the National
Academy of Vector Borne Diseases (NAVBD) was founded
at Bhubaneswar in 1994, by Dr AP Dash, along with 15 likeminded scientists from all over India; this site was chosen in
view of its strategic location in the country in relation to vectorborne diseases, as it is highly endemic for malaria, lymphatic
filarisis, dengue and chikungunya.
NAVBD is a non-profit academic organization in India,
dedicated to:
advance and promote knowledge on vectors and VBDs;
113
Valecha et al.: The National Academy of Vectors and Vector Borne Diseases in India
encourage scientists and members of the academy doing

research on vectors and vector-borne diseases, and assist
them whenever possible;
hold national and international seminars/symposia/
workshops to exchange knowledge on recent advances in
the field of vectors and vector-borne diseases, and create
awareness of vectors and vector-borne diseases among the
general public.
The academy is governed by an elected executive committee,
which consists of a president, vice- presidents, secretarygeneral and other members. Dr VP Sharma and Professor
AP Dash were the founder president and secretary-general,
respectively. The academy was registered under the Society of
Registration Act, Government of India (1880). The membership
of the Academy has now increased to more than 300.
Symposia
The First International Symposium on Vectors and Vector
Borne Diseases was held in November 1994 at the Regional
Medical Research Centre, Bhubaneswar. Dr C Silvera, then
Union Minister of Health and Family Welfare, Government
of India, inaugurated the symposium. At least 150 scientists
of repute from India and abroad participated and engaged in
discussion on all aspects of the prevalent vector-borne diseases.
The recommendations of the symposium were forwarded to the
Government of India and Indian Council of Medical Research
(ICMR).
Since then, the academy has made steady progress and further
symposia were organized in different cities in India, including
Goa, Gwalior, Jabalpur, Madurai, Patiala and Udaipur. These
symposia provided excellent opportunities to reflect on the
recent advances made in research on vector-borne diseases.
They also helped in scaling-up of elimination/prevention of
vector-borne diseases to alleviate suffering and bring about
social growth and development. The World Health Organization
(WHO) Regional Office for South-East Asia has supported the
NAVBD symposia since 2008.
The academy has so far organized 12 international symposia,
the last one being in Udaipur, Rajasthan, which was
inaugurated by Dr VM Katoch, Secretary for Health Research
and Director-General of ICMR, while Dr Leonard I Ortega,
Regional Adviser, WHO South-East Asia Regional Office,
New Delhi, attended as the guest of honour. The symposium
was organized with support from ICMR and the WHO regional
office, with further support from industries as a part of public
private partnership.
Awards and recognition
To encourage scientists working on vector-borne diseases,
the academy has instituted various awards for outstanding
contributions on: environmental management of vectorborne diseases; molecular biological aspects of vector-borne
diseases; and clinical aspects of vector-borne diseases.
114
In addition, at each symposium, the academy makes the

following awards, on a competitive basis:
Vestergaard Frandsen Award for Vector Control: this is
a cash award of INR (Indian rupees) 200000 , sponsored by
Vestergaard Frandsen Ltd since 2008, and is given to active
researchers who are nationals of any member country of
the South Asian Association for Regional Cooperation and
have contributed significantly in the fields of understanding
the mechanism of insecticide resistance, vector bionomics
and control.The cost of travel and other expenses of the
recipient, and the medallion, are borne by Vestergaard
Frandsen;
Biotech International Award: this cash award of
INR100000 is sponsored by Biotech International Ltd,
since 2008 and is to be given to a scientist who has working
experience in India and has made outstanding contributions
in the field of biological control of vectors;
Bayer Environmental Science Award: this cash award for
INR 100000 has been sponsored by Bayer India Ltd since
2008, and is given to a scientist who has working experience
in India and has made an outstanding contribution in any
field of vector-borne diseases, preferably in the aspect of
vector/disease management. In exceptional cases, Indian
nationals working abroad, or foreign scientists,may also be
considered for the award, provided theirwork has made a
significant contribution to the understanding and control of
vector-borne disease in India. The cost of travel and other
expenses of the recipient, and the medallion, are borne by
Bayer Environmental Science;
Godrej Sara Lee Award: Godrej Sara Lee Ltd declared
this award for 2009, which was to be presented during the
tenth annual international/national symposium organized
by the academy, for excellence in research on personal
protection from mosquitoes. The award includes a cash
prize of INR 100000.
So far, the recipients of these awards include Dr VS Chauhan,
Director, Dr Chetan Chitnis and Dr Deepak Gaur, scientists
of the International Centre for Genetic Engineering and
Biotechnology, New Delhi respectively; Dr Shovna Sharma,
Tata Institute of Fundamental Research, Mumbai; Dr Sarla K
Subbarao and Dr NeenaValecha, both Directors of the National
Institute of Malaria Research; Dr YD Sharma, Professor and
Head of Biotechnology, All India Institute of Medical Sciences,
New Delhi; Dr BK Das, Professor of Medicine, SCB Medical
College, Cuttack; Dr Neeru Singh, Director, Regional Medical
Research Centre for Tribals, Jabalpur; Dr P Jambulingam,
Director, Vector Control Research Centre, Pondicherry; Dr
DT Mourya, Director, National Institute of Virology, Pune;
and Dr MM Parida, senior scientist, Defence Research and
Development Establishment, Gwalior. Two scientists from Sri
Lanka have also been honoured.
Since 2008, the academy has also encouraged young scientists
by giving six Best Poster Presentation Awards.
Awareness campaign
In the field of raising awareness, Dr Ashwani Kumar, a member
of NAVBDs executive committee, in collaboration with
Professor D Deobagkar, the President of the academy, made a
cartoon educational film for children, called Mosquito control:
I can do it, which is available on YouTube. This animated
film highlights how mosquitoes cause serious diseases. On
the advice of a doctor, both a girl and her mother take upon
themselves to first acquire knowledge about mosquitoes and the
diseases transmitted by them, and then spread the knowledge by
involving their friends in tackling them. Bholu the monkey,
who is friendly with the children, bestows upon them magical
powers to enter the world of mosquitoes, where they are able
to listen to mosquitoes talking to each other and come to know
about their nefarious designs. Children hear mosquitoes and
malaria parasites boasting about their powers in bringing about
sickness and destruction of many human civilizations in the
past, and the havoc they continue to create even today in the
world.
Hearing this, the children feel greatly concerned and angry.
They then take a pledge to destroy mosquitoes with the help
of friends and parents, and the children start taking various
actions to eliminate mosquito breeding. They mosquito-proof
their homes by screening windows and doors, introduce fish in
wells and ponds, mosquito-proof overhead tanks, safely store
containers and sleep under a mosquito net. After conquering
the mosquitoes, children sing a song to conclude the film.
The film lasts 20 minutes and is ideal to show in the classroom.
It is currently available in English, and will soon be dubbed in
Hindi and various regional Indian languages.
Publications
The abstracts of the papers presented at all international
and national symposia have been published. In addition, the
academy has published two proceedings of the International
Symposia on Vectors And Vector-Borne Diseases held in 1995
and 1997. The academy so far has published eight volumes of
News Letters, which have been circulated to all life members,
as well as other important persons working/interested in the
field of vectors and vector-borne diseases.
Calcutta School of Tropical Medicine, delivered the keynote

address. At least 150 scientists, research scholars, doctors, and
postgraduate students attended and presented papers.
On 6 February 2010, a day-long national seminar on Climate
change and vector borne diseases was organized by NAVBD,
in collaboration with The Asiatic Society, at the Asiatic
Society, Kolkata. Professor Dhrubojyoti Chattopadhyay,
Pro-Vice Chancellor, University of Calcutta and Biological
Science Secretary, The Asiatic Society, Kolkata, inaugurated
the seminar. Professor Biswanath Banerjee, President of the
Asiatic Society, delivered the keynote address. At least 110
scientists, research scholars, doctors and postgraduate students
attended and presented papers.
On 19 and 20 November 2010, a national conference on
Environment degradation and its impact on mankind
was organized by NAVBD at Punjabi University, Patiala,
in collaboration with the Punjabi University Environment
Society, Patiala. Dr Jaspal Singh, Vice Chancellor of the
Patiala University inaugurated the conference. Around 120
postgraduate students, researchers and academicians attended
and discussed topics such as health issues related to genetically
modified food and non-food crops; bio-ecology of malaria
vectors in India; ecology and biodiversity of the Himalayan
region; and an integrated model of vermin biotechnology and
Spirulina biotechnology as an effective tool for environmental
conservation.
Future plans
It is planned to expand the academy to a broader sphere in the
South-East Asia Region in the near future. Bearing in mind the
World Health Day 2014 theme of vector-borne diseases, it is
proposed to organize a global meeting on vector-borne diseases
in 2015, which will address recent advances in vector-borne
diseases research and control, and consider future courses of
action.
References
1.
2.
Other activities
Besides international and national conferences, the academy
organizes seminars and conferences in different academic
institutions, for students and young faculty members of
universities and postgraduate colleges. As a part of this
activity, on 13 February 2009, a day-long national seminar on
Challenges of mosquito borne diseases in Indian perspectives
was organized by NAVBD at Asutosh College (University of
Calcutta), Kolkata, in collaboration with the Foundation of
Academic Excellence and Access (FAEA). Professor Subir
Kumar Dutta, Medical Secretary, The Asiatic Society, Kolkata
was the chief guest. Professor AK Hati, former Director of
3.
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et al. Review: Improving our knowledge of male mosquito biology in
relation to genetic control programmes. Acta Trop. 2013 Nov 16. pii:
S0001-706X(13)00328-8.
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Geneva, 2014. http://www.who.int/campaigns/world-health-day/2014/
vector-borne-diseases/en/ - accessed 6 March 2014.
LaBeaud AD, Aksoy S. Neglected funding for vector-borne diseases: a
near miss this time, a possible disaster the next time. PLoS Negl Trop
Dis. 2010 Oct 26;4(10):e847.
Varmus H, Klausner R, Zerhouni E, Acharva T, Daar AS, Singer PA.
Public health. Grand challenges in global health. Science. 2003 Oct
17;302(5644):398-9.
Hill CA, Kafatos FC, StansfieldSk, Collins FH. Arthropod-borne
diseases: vector control in the genomics era. Nat Rev Microbiol. 2005
Mar;3(3):262-8.
Dash AP, Bhatia R, Kalra NL. Dengue in South-East Asia: an appraisal
of case management and vector control. Dengue Bulletin. 2012; 36:1
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Surveillance and outbreak alert: Chikugunya. New Delhi, 2014. www.
searo.who.int/entity/emerging_diseases - accessed 6 March 2014.
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Magnitude of disease: malaria & filariasis. www.nvbdcp.gov.in/ accessed 6 March 2014.
How to cite this article: Neena Valecha N & Ranjit M.R. The
National Academy of Vectors and Vector Borne Diseases in
India: two decades of progress. WHO South-East Asia J Public
Health 2014; 3(1): 113116.
Public health classic
DOI: 10.4103/2224-3151.115828
This section looks at some ground-breaking contributions to public health and

reproduces them in their original form. In this Special Issue on Vector-borne
Diseases we reproduce the article by Sir Ronald Ross published in 1897: On
some peculiar pigmented cells found in two mosquitos fed on malarial blood
(Br Med J 1897;2:1786). The original paper is reproduced by permission of the
British Medical Journal.
117
Ross: On some peculiar pigmented cells found in two mosquitos fed on malarial blood
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119
120
Aide-mmoires Dengue, Kala-azar,

Lymphatic filariasis, Malaria
World Health Organization Regional Office for South-East Asia, New Delhi
ISBN: 9789381559017
Available from: http://www.searo.who.int/entity/world_health_day/2014/en/
This series of aide-mmoires on aims to provide a quick

overview and checklist for policy-makers and programme
managers on specific vector-borne diseases.
Website:
www.searo.who.int/publications/journals/seajph
Bibliography on Vector-borne Diseases

from the South-East Asia Region, 20092013
ISBN: 9789290224525
Available from: http://www.searo.who.int/entity/world_health_day/2014/en/
Vector-borne diseases account for 17% of the estimated global
burden of all infectious diseases. While malaria is still the
deadliest vector-borne disease, dengue has become the fastest
growing with a 30-fold increase in disease incidence over the
past 50 years. The prevalence of malaria, lymphatic filariasis
and kala-azar is decreasing, but we are being challenged by
emerging trends of dengue and chikungunya. Although at
a global, regional and national level we are making good
progress in controlling most of the vector-borne diseases, there
are pockets within countries that continue to be challenging.
More research and better data are needed to understand the
trends in endemic areas. Operational research and generating
evidence on effectiveness of interventions is needed for better
policy guidance. New tools and interventions need to be
field tested and compared to overcome the challenges and to
progress towards disease elimination. To help Member States
in better understanding the available research evidence and data
on vector-borne diseases in order to take informed decisions,
the WHO South-East Asia Regional Office has compiled this
published literature on vector-borne diseases in the Region
from the past five years.
Website:
121
Dengue Bulletin, Volume 37, 2013

IssN: 02508362
Available from: http://www.searo.who.int/entity/world_health_day/2014/DengueBulletin-2013pdf
The WHO Regional Office for South-East Asia, in collaboration

with the Western Pacific Region, has been jointly publishing
the annual Dengue Bulletin. The objective of the Bulletin is
to disseminate updated information on the current status of
DF/DHF infection, changing epidemiological patterns, new
attempted control strategies, clinical management, information
about circulating DENV strains and all other related aspects.
The Bulletin also accepts review articles, short notes,
book reviews and letters to the editor on DF/DHF-related
subjects. Proceedings of national/international meetings for
information of research workers and programme managers
are also published. All manuscripts received for publication
are subjected to in-house review by professional experts and
are peer-reviewed by international experts in the respective
disciplines.
122
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