Veterinary Parasitology 126 (2004) 1535

www.elsevier.com/locate/vetpar

Review

The zoonotic significance and molecular

epidemiology of Giardia and giardiasis
R.C. Andrew Thompson*
WHO Collaborating Centre for the Molecular Epidemiology of Parasitic Infections and
Western Australian Biomedical Research Institute, Veterinary and Biomedical Sciences,
Murdoch University, South Street, Murdoch, WA 6150, Australia

Abstract
The taxonomy and molecular epidemiology of Giardia and Giardia infections are reviewed in the
context of zoonotic and waterborne transmission. Evidence to support the zoonotic transmission of
Giardia is very strong, but how frequent such transmission occurs and under what circumstances,
have yet to be determined. Zoonotic origin for waterborne outbreaks of Giardia infection appears to
be uncommon. Similarly, livestock are unlikely to be an important source of infection in humans. The
greatest risk of zoonotic transmission appears to be from companion animals such as dogs and cats,
although further studies are required in different endemic foci in order to determine the frequency of
such transmission.
# 2004 Elsevier B.V. All rights reserved.
Keywords: Giardia; Taxonomy; Molecular epidemiology; Zoonoses; Transmission; Waterborne

Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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2. What is Giardia? Historical perspectives and evolutionary biology . . . . . . . . . . . .

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3. Current taxonomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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4. Developmental biology and pathogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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* Tel.: +61 08 9360 2466; fax: +61 08 9310 4144.

E-mail address: andrew_t@central.murdoch.edu.au.
0304-4017/$ see front matter # 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.vetpar.2004.09.008

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R.C.A. Thompson / Veterinary Parasitology 126 (2004) 1535

5. Transmissionthe impact of molecular epidemiology

5.1. Host specificity . . . . . . . . . . . . . . . . . . . . . . .
5.2. Cycles of transmission . . . . . . . . . . . . . . . . . .
5.2.1. Humans . . . . . . . . . . . . . . . . . . . . . . .
5.2.2. Cattle . . . . . . . . . . . . . . . . . . . . . . . .
5.2.3. Dogs and cats . . . . . . . . . . . . . . . . . .
5.2.4. Wildlife . . . . . . . . . . . . . . . . . . . . . . .
5.3. Zoonotic and waterborne transmission . . . . . . .

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6. Diagnosis and detection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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7. Treatment and control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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8. Conclusions and looking to the future . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

31

1. Introduction
Although humans have undoubtedly suffered the consequences of Giardia infection for
thousands of years, we had to await the invention of the microscope before it was observed
for the first time, and another 200 years until it was properly described (Lambl, 1859).
Today, Giardia is one of the most widely studied organisms. Not only because of its
ubiquity as a parasite, but also because of its importance in evolutionary biology and
molecular genetics.
Giardia duodenalis has a global distribution causing an estimated 2.8  108 cases per
annum (Lane and Lloyd, 2002), and is the most common intestinal parasite of humans in
developed countries. In Asia, Africa and Latin America, about 200 million people have
symptomatic giardiasis with some 500,000 new cases reported each year (WHO, 1996). It
is also a frequently encountered parasite of domestic animals, especially livestock, dogs
and cats, and numerous species of wild mammals and birds have been documented as hosts
of Giardia.
As a parasite, Giardia has a broad host range, although the adverse consequences of
Giardia infection and its pathogenic potential are best recognised in humans. Its simple life
cycle involving an environmentally resistant cyst, provides ample opportunities for the
parasite to be transmitted directly from one infected individual to another, or indirectly
through contamination of the environment or food. In this respect, water is an important
vehicle for the transmission of Giardia to people. Giardiasis is the most frequently
diagnosed waterborne disease and along with Cryptosporidium, is the major public health
concern of water utilities in both developed and developing nations (Levine et al., 1990;
Thurman et al., 1998; Hoque et al., 2002; Leclerc et al., 2002). However, although we
understand much about the waterborne transmission of Giardia, the public health
significance of infected non-human hosts as sources of water contamination remains an
unresolved issue. Indeed, the role of zoonotic transmission in the epidemiology of human
Giardia infections has yet to be resolved.

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17

2. What is Giardia? Historical perspectives and evolutionary biology

The characteristic and distinctive morphological features of Giardia are well known and
were described initially in the latter part of the 1800s. The non-encysted, motile
trophozoite is bilaterally symmetrical, piriform to ellipsoidal in shape, 1215 mm  6
8 mm, with a convex dorsal surface and large unique adhesive or sucking disc on the
ventral surface. It is binucleate, with four pairs of flagella and a pair of distinctive median
bodies (Fig. 1). Giardia, along with other multi-flagellates are grouped in the Class
Zoomastigophorea and Order Diplomonadida.
The phylogenetic affinities of Giardia have been a matter of controversy for a number of
years. However, there is now broad consensus of Giardias primitive origins as an early
branching eukaryote lineage that diverged before mitochondrial acquisition (Simpson et
al., 2002). Giardia has thus become a key organism in attempts to understand the evolution
of eukaryotic cells. Giardia has a very simple intracellular organization, with no
mitochondria or peroxisomes but does have a primitive vesicular secretory system that has
been proposed as the archetype of the Golgi secretory apparatus in higher organisms (Marti
et al., 2003a,b).

3. Current taxonomy
More than 50 species of Giardia have been described, the majority between 1920 and
1930 (Kulda and Nohynkova, 1996; Thompson et al., 1990; Thompson, 2002). The small
number recognised today (Table 1) follows a comprehensive re-evaluation and
rationalization proposed by Filice (1952) based on the morphological similarity of the
described species and doubts over the validity of host specificity as a criterion for
taxonomic recognition.
Although species of Giardia inhabit the intestinal tracts of virtually all classes of
vertebrates, G. duodenalis (sometimes referred to as Giardia intestinalis; Giardia
lamblia) is the only species found in humans and the majority of domestic and wild
mammals from which Giardia has been examined (see Thompson, 2002). It was to
this species that Filice (1952) allocated the majority of species previously described.

Fig. 1. Giemsa-stained trophozoite of Giardia duodenalis showing multiple flagella, nuclei and median bodies
(400). [Figure courtesy of Nicolette Binz.].

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R.C.A. Thompson / Veterinary Parasitology 126 (2004) 1535

Table 1
Recognised species in the genus Giardia (from Thompson, 2002)
Species

Hosts

Morphological characteristics

Trophozoite dimensions:
length/width (mm)

G. duodenalis

Pear-shaped trophozoites
with claw-shaped median bodies

1215/68

G. agilis

Wide range of domestic

and wild mammals
including humans
Amphibians

2030/45

G. muris

Rodents

G. ardeae

Birds

G. psittaci

Birds

Long, narrow trophozoites with

club-shaped median bodies
Rounded trophozoites with small
round median bodies
Rounded trophozoites, with
prominent notch in ventral disc
and rudimentary caudal flagellum.
Median bodies round-oval to
claw-shaped
Pear-shaped trophozoites, with no
ventro-lateral flange. Claw-shaped
median bodies

912/57
10/6.5

14/6

He recognised that his proposal was only a temporary solution in view of growing
evidence of phenotypic variability between isolates within the species G. duodenalis.
However, at the time, the methodology was not available to reliably discriminate
between these variants.
Filices taxonomic rationalism was a major step forward, as was the recognition by the
World health Organization (WHO) of the zoonotic potential of Giardia as a result of
epidemiological data and cross-infection experiments (WHO, 1979). The subsequent
development of axenic in vitro culture procedures that enabled laboratory amplification of
isolates of Giardia in axenic culture was also an important advance. It was now possible to
grow individual isolates of the parasite in the laboratory and produce sufficient numbers to
genetically characterise the isolates using procedures such as allozyme electrophoresis. As
a result, research over the last ten years has produced valuable information about the
genetic structure of Giardia populations and has demonstrated considerable levels of
genetic diversity within the G. duodenalis group.
Until recently it has been difficult to interpret the extensive genetic variability within G.
duodenalis in a taxonomic perspective. Although the ability to axenize and amplify isolates
of G. duodenalis in laboratory culture was a tremendous breakthrough in terms of
providing sufficient material for genetic characterisation, not all isolates of the parasite can
be established in axenic in vitro culture. This includes a significant proportion of human
isolates. Isolates from some species such as dogs are largely refractory to in vitro culture as
well. As a consequence it has not been possible, until recently, to genetically characterise
many isolates of G. duodenalis. Much of the available genetic data were therefore based on
a small pool of culture-selected isolates that could not be considered to be representative of
the extensive gene pool existing in nature. The inability to amplify all isolates obtained
from the field in in vitro culture has also been a major limitation to our understanding of the
epidemiology and transmission of Giardia.

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The recent application of PCR-based procedures has circumvented the need for in vitro
culture and amplification, with direct characterization of the parasite possible from faecal
and environmental samples, and has enabled the characterisation of previously inaccessible
genotypes (Van Keulen et al., 1998; Monis et al., 1998; Hopkins et al., 1997, 1999). Using
PCR-based procedures in conjunction with analysis of conserved genetic loci such as
rDNA and a variety of housekeeping genes including that coding for glutamate
dehydrogenase (GDH), elongation factor 1- alpha (ef1-a) and triose phosphate isomerase
(tpi), combined with much larger data sets, it has been possible to elucidate the
fundamental genetic divisions within the G. duodenalis group (Table 2). A number of
laboratories in different countries have contributed to this work and a consensus has
emerged (Hopkins et al., 1997, 1999; Monis et al., 1996, 1998, 1999). This shows that G.
duodenalis is clearly not a uniform species but a species complex comprising a variety of
genetically and phenotypically distinct, yet morphologically similar genotypes which also
exhibit differences in host specificity (Thompson, 1998; Thompson et al., 1999, 2000;
Monis and Thompson, 2003). These genotypic groupings of G. duodenalis are also
geographically widely distributed and genetically conserved.
Giardia isolates recovered from humans fall into one of the two major genotypic
groupings or assemblages (Table 2). Distributed world-wide, these two assemblages
comprise several genotypes and are now widely referred to as Assemblages A and B.
Molecular analyses have shown that the genetic distance separating these two assemblages
exceeds that used to delineate other species of protozoa (Andrews et al., 1989; Mayrhofer
et al., 1995; Monis et al., 1996; Monis and Thompson, 2003). Although all the genetic
evidence suggests that separate species names for each of these assemblages may be
warranted, there is also significant genetic sub-structuring within each assemblage.
Assemblage A consists of isolates that can be grouped into two distinct clusters; AI consists
of a mixture of closely related animal and human isolates which are geographically
widespread, and most attention regarding the zoonotic potential of Giardia has focused on
this AI subgroup. In contrast, the second subgroup, AII consists entirely of human isolates.
Assemblage B comprises two subgroups, III and IV, of which the latter appears to be
human-specific.
Interestingly, some of the genotypic groupings, or assemblages, are genetically quite
uniform and appear to be confined to specific animal hosts. Giardia genotypes exhibiting a
limited host range include those recovered from cats, dogs, rats, voles/muskrats and hoofed
animals (Table 2). Unlike the uncertainty regarding the taxonomic status of genotypic
Table 2
Genotype and host range of isolates within the Giardia duodenalis morphological group
Genotype/Assemblage

Host range

Zoonotic/A
Zoonotic/B
Dog/C, D
Livestock/E
Cat/F
Rat/G
Muskrats/Vole

Humans, livestock, cats, dogs, beavers, guinea pig, slow loris

Humans, slow loris, chinchillas, dogs, beavers, rats, siamang
Dog
Cattle, sheep, pigs
Cat
Domestic Rats
Wild rodents

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R.C.A. Thompson / Veterinary Parasitology 126 (2004) 1535

assemblages A and B, there is probably sufficient data supporting the restricted host
range of these genotypes to warrant species designation. Consequently, consideration
could be given to reinstating previously invalidated species such as G. canis and G. bovis
(Thompson, 2002). However, the situation is likely to be much more complicated than that
summarised in Table 2, as illustrated by the discovery of novel genotypes, such as those
occurring in Australian marsupials (Adams and Thompson, 2002).

4. Developmental biology and pathogenesis

Giardia is not invasive and lives and multiplies by asexual multiplication on the
lumenal surface of the small intestine of its vertebrate host. The pathogenesis of Giardia
is not clearly understood and symptoms which include acute or chronic diarrhoea,
dehydration, abdominal pain and weight loss are highly variable (Thompson et al.,
1993), and may not be evident in a significant proportion of infected individuals
(Rodriguez-Hernandez et al., 1996). However, recent research is starting to provide
information on the diversity of processes that are triggered by an infection with Giardia,
which all contribute to a complex pathophysiological process (Buret et al., 2002a). One
of the fundamental changes is altered epithelial permeability that appears to result from a
direct cytopathic effect induced by products of the parasite (Buret et al., 2002b).
Peripheral membrane proteins, and in particular the tight junction-associated protein
zonula occludin-1 (ZO-1), which play an important role in the regulation of epithelial
permeability are disrupted. The resultant increased epithelial permeability leads to an
inflammatory response and both digestive and absorptive changes, that correlate with
brush border injury and disaccharidase deficiencies (Scott et al., 2002). Giardia also
induces apoptosis that correlates with the loss of epithelial barrier function via the
disruption of tight junctional ZO-1 and the subsequent increase in permeability (Chin et
al., 2002). Interestingly, apoptosis and the severity of disease is determined by straindependent virulence factors of the parasite, as well as by the developmental, nutritional
and immunological status of the host (Chin et al., 2002; Scott et al., 2002). It should also
be noted that increased intestinal permeability may result in the uptake of lumenal
antigens. This may exacerbate the occurrence of allergic disorders, a complication often
reported in humans infected with Giardia (Scott et al., 2002) and a factor that may
confuse the aetiology of nutritional disorders.
It is not surprising that such a multifactorial pathophysiological process that is both
parasite and host dependent is so variable in its expression in terms of symptomatology,
clinical consequences and severity. In this respect, the contribution of host factors has
not been given much attention. It seems likely that the pathophysiological changes
described above may occur in the majority of hosts infected with Giardia but that
the consequences of such changes may vary depending upon nutritional factors and
immune status, as well as concurrent enteric infections with other parasites.
For example, the chronicity of Giardia infections in disadvantaged children whose
nutrition may be suboptimal and who suffer infections with other gastrointestinal
parasites such as Hymenolepis or hookworm, is recognised as an important contributor
to poor growth (Thompson, 2000; Sackey et al., 2003). Similarly, in young animals

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21

and birds that are nutritionally compromised or exposed to stress through overcrowding
or low temperatures, Giardia may be an additional factor that culminates in the
expression of severe disease. For example, this is likely to be the cause of mortalities in
nestling ibis (McRoberts et al., 1996). The risk factors for clinical giardiasis may be
closer to being resolved, and they clearly involve host and environmental factors, as well
as the strain of the parasite. The precise nature of these factors requires further
characterisation, as do the complex interactions in the host that result in the expression of
giardiasis.

5. Transmissionthe impact of molecular epidemiology

Based on what is known about the prevalence of Giardia in different animal species,
including humans, and our current understanding of the major genetic groupings in G.
duodenalis, there are four major cycles of transmission that maintain the parasite in
mammalian hosts (Fig. 2). However, we need to consider how these cycles may interact,
and try to determine the frequency of transmission of zoonotic genotypes.
5.1. Host specificity
The phenotypic trait that has provided most controversy and disagreement in the context
of species recognition in Giardia has been that of host specificity. Indeed, until Filices
revision (Filice, 1952), the majority of species had been described principally on the basis
of host occurrence (see above). However, the question of host specificity has not only had
an important influence on Giardia taxonomy but also on the ongoing debate as to whether
giardiasis is a zoonosis. Although, the results of experimental cross-infection experiments
questioned the notion of host adapted species as a tenable criterion for species recognition,
it is now clear that some species may be host specific and others are capable of infecting a
broad range of host species.
Experimental cross transmission studies have often been questionable because of
uncertainty about the Giardia-free status of experimental animals and the common use
of high doses of cysts that are unlikely to represent a natural infection. (Thompson et al.,
1990; Monis and Thompson, 2003). This has been further emphasised by recent results
which have raised the possibility that infected hosts may not produce cysts in sufficient
quantities to be detected by microscopy (McGlade et al., 2003; Traub et al., 2004). Cross
transmission studies have also used uncharacterised isolates, limiting their usefulness in
determining the host specificity of the different genotypes. For example, an avian isolate
of G. duodenalis exhibiting aggressive pathogenesis has been shown experimentally to
establish infections in domestic kittens and lambs (McDonnell et al., 2003). However,
the isolate has yet to be characterised genetically with respect to the known genetic
groupings (Table 2) thus limiting the significance of the study. An interpretation of the
results of cross transmission studies is also difficult when some report successful cross
infection between species while others are unsuccessful. Such results may reflect the
genetic diversity of the isolates being used, differences in the viability of the cysts,
variation in the immune status of experimental hosts, or insensitive detection techniques.

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R.C.A. Thompson / Veterinary Parasitology 126 (2004) 1535

Fig. 2. Major transmission cycles of Giardia duodenalis.

From a review of the results of cross-infection experiments (Thompson et al., 1990;

Monis and Thompson, 2003), probably the most valuable results from epidemiological
and zoonotic perspectives are that: it has been possible to infect dogs with G. duodenalis
from Assemblage A, group I; and that beavers are susceptible to infection with isolates
of human origin (see Monis and Thompson, 2003).

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5.2. Cycles of transmission

5.2.1. Humans
Human to human transmission of Giardia can occur indirectly through the accidental
ingestion of cysts in contaminated water or food, or directly in environments where
hygiene levels may be compromised, such as day care centres or disadvantaged community
settings. In environments where the frequency of transmission is high and/or conditions are
conducive to direct person-to-person transfer, such as localised endemic communities or
institutional settings such as day care centres, it would be expected that competitive
interactions might result in the predominance of particular genotypes. However, this does
not appear to be the case. A study that examined Giardia from humans and dogs in the same
community found that all of the human isolates were either Assemblage A or B and that all
of the dog isolates, with a single exception, were Assemblage C or D (dog-specific
assemblages) (Hopkins et al., 1997). The exception was a dog that had a mixed infection of
Assemblage B and C, which suggests that perhaps the dog was infected from a human
source. Similarly, a recent molecular epidemiological investigation on the aetiology of
giardiasis in gorillas in a remote area in Uganda found that they were infected with
Assemblage A, and that human rangers were the likely source of the infections as a result of
indiscriminate defaecation (Graczyk et al., 2002).
A recent UK study that examined 35 human clinical samples found that 64% were
Assemblage B, 27% were Assemblage A genetic group II and the remainder were a
mixture of Assemblage B and Assemblage A genetic group II (Amar et al., 2002).
Similarly, an institutional survey in Australia found that infections with Assemblage B
were more prevalent (70%) than Assemblage A (30%) (Read et al., 2001). The Assemblage
B genotype was also found to be responsible for an outbreak in a nursery in the UK where
21 of 24 (88%) cases were infected with this genotype (Amar et al., 2002). In tea growing
communities in Assam, India, the proportion of Assemblage B and A infections in 18
infected people was 61% and 39%, respectively (Traub et al., 2004). Apart from these
studies, no large-scale surveys of Giardia infections in humans have isolated and
genetically characterised the isolates of Giardia detected and so it is not possible to
determine the distribution and prevalence of human-infective genotypes. Such surveys will
provide valuable data since there is evidence that Assemblages A and B genotypes differ in
virulence. A longitudinal study in day-care centres in Perth, Western Australia, found that
children infected with isolates of Giardia belonging to Assemblage A were 26 times more
likely to have diarrhoea than children infected with Assemblage B isolates (Read et al.,
2001). Thus children infected with isolates of Giardia from Assemblage B will not be
excluded from such day-care centres since exclusion is dependent on the occurrence of
diarrhoea. This would explain why infections with Assemblage B are more common in
such environments. Children with such infections are likely not to be treated which also
raises questions about the long term consequences of such chronic infections if they persist
and there is no self cure. This is thought to be significant in situations where infected
children are disadvantaged in terms of nutrition and exposure to concurrent enteric
infections with other parasites such as Hymenolepis and Ancylostoma. This is the situation
in isolated Aboriginal communities in northern Australia, where Giardia infections are
recognised as contributing to nutritional disorders and poor growth. In such communities,

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infections with isolates of Giardia from Assemblage B are more common than those
with Assemblage A (Meloni et al., 1995; Thompson and Meloni, 1993; Hopkins et al.,
1999).
5.2.2. Cattle
Attention has focussed on the widespread and exceptionally high levels of infection of
Giardia in young livestock, particularly calves (Thompson, 2000; Olson et al., 2004).
Giardia has been found in both beef and dairy cattle throughout the world, and longitudinal
studies have consistently demonstrated prevalence rates of 100% (OHandley, 2002;
OHandley et al., 1999; Ralston et al., 2003; Xiao and Herd, 1994). The infection pattern of
Giardia is similar between beef and dairy cattle (OHandley et al., 1999; Ralston et al.,
2003) with cysts appearing in the faeces at approximately 4 weeks of age. Calves have the
highest excretion intensities of 105106 cysts per gram of faeces between 4 and 12 weeks of
age (OHandley et al., 1999; Ralston et al., 2003). A periparturient rise in cyst excretion has
also been demonstrated (Ralston et al., 2003). Transmission occurs among infected calves
as well as chronically infected adults, but the frequency of transmission is particularly high
amongst dairy calves (Xiao and Herd, 1994; OHandley et al., 1999, 2000).
Giardia infections in cattle are clinically important and may be of economic
significance by impairing performance (OHandley et al., 2001; Olson et al., 2004).
Giardia has been implicated as an aetiological agent alone and in combination with other
enteric pathogens in calf diarrhoea (Xiao and Herd, 1994; Olson et al., 1995; OHandley et
al., 1999; Huetink et al., 2001). These studies demonstrated that concurrent infections with
Giardia and Cryptosporidium were common in calves and the primary cause of diarrhoea
in calves less than 30 days of age, whereas Giardia alone was associated with diarrhoea in
older calves. The impact of chronic giardiasis in calves on performance may be reflected in
a reduced rate of weight gain, impaired feed efficiency and decreased carcass weight as
demonstrated in experimentally infected lambs (Olson et al., 1995). However, this has yet
to be demonstrated, and in a preliminary study giardiasis was not found to affect average
daily gain, feed intake or feed efficiency in feedlot calves, but there may have been an
insufficient number of animals to demonstrate a production effect (Ralston et al., 2003).
Recent studies have demonstrated that calves in dairy and beef herds may harbour one
of two genotypes of G. duodenalis. Although the livestock genotype (Assemblage E) of
Giardia appears to occur most frequently in cattle, studies in Canada and Australia have
shown that a small proportion of cattle in a herd, <20%, may harbour genotypes in
Assemblage A, the most common genotypes affecting humans (OHandley et al., 2000;
Appelbee et al., 2002). However, a recent more extensive, longitudinal study of dairy herds
in Australia over several months found that 100% of calves become infected during the first
12 weeks of life but all the animals sampled were infected with the livestock genotype.
5.2.3. Dogs and cats
Recent studies in Australia found that G. duodenalis was the most common enteric
parasite of domestic dogs and cats (Bugg et al., 1999; McGlade et al., 2003). It is also
widely prevalent in dogs and cats in the USA and has been shown to be common in pets in
other countries (Thompson and Robertson, 2003). However, it has been suggested that
prevalence rates of Giardia in companion animals are often underestimated because of the

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25

low sensitivity of conventional detection methods, the fact that the parasite may be present
at subclinical levels and the intermittent nature of cyst excretion (McGlade et al., 2003).
Although Giardia is common in dogs and cats, it is rarely associated with clinical
disease in these animals. However, if clinical giardiasis is reported, it is usually associated
with kennel or cattery situations, where the effects of over crowding may cause stress and
exacerbate the effects of an infection (Robertson et al., 2000). Treatment of Giardiainfected dogs and cats is usually recommended whether or not they are clinically ill,
because of the perceived potential for zoonotic transmission. The recent development of
vaccines for the treatment and prevention of Giardia infections in dogs and cats and their
apparent ability to reduce the duration of shedding of cysts may provide an alternative to
drugs for reducing carrier rates in pets and subsequent environmental contamination
(Olson et al., 2000).
Molecular epidemiological studies have shown that dogs may be infected with their
own, host-adapted genotype of Giardia, as well as with zoonotic genotypes (see below).
5.2.4. Wildlife
Although wildlife are susceptible to infection with zoonotic genotypes of G. duodenalis,
the limited evidence collected under natural, pristine conditions suggests that wildlife
harbour their own genotypes/species of Giardia.
For example, genotypic characterisation of Giardia from native marsupials in Australia
has shown that they are infected with a novel, genetically distinct genotype of Giardia
(Adams and Thompson, 2002). Thus the finding of high prevalence rates of G. duodenalis
in a wide range of native animals in Tasmania may not necessarily constitute a risk to
public health as recently proposed (Kettlewell et al., 1998). Distinct genotypes have also
been recovered from microtine rodents and the majority of birds where genotypic
characterisation of the isolates has been undertaken (McRoberts et al., 1996; Thompson,
2002; Monis and Thompson, 2003). However, a recent study in Australia comparing the
disease status of populations of house mice on subantarctic Macquarie Island and
Boullanger Island which has an arid Mediterranean climate, found that the mice harboured
several different genotypes of Giardia (Moro et al., 2003). Zoonotic genotypes were found
in mice on both islands, but on Macquarie Island, mice were also infected with novel
genotypes of G. duodenalis. The source of infection in these mice has still to be
determined.
Animals such as beaver, nutria and deer are also commonly infected with Giardia in
North America with prevalence rates often over 50% (Dixon et al., 2002; Dunlap and
Thies, 2002; Heitman et al., 2002; Rickard et al., 1999) but there is surprisingly little
information on what genotype of Giardia they carry. Recent studies have, however,
confirmed that beavers and white-tailed deer in the wild can harbour infections with
zoonotic genotypes of G. duodenalis (Appelbee et al., 2002; Trout et al., 2003).
5.3. Zoonotic and waterborne transmission
Molecular data have shown that livestock, pets and wildlife may harbour zoonotic
genotypes of G. duodenalis, as well as genotypes that appear to be host specific
(Thompson, 2002). However, although the WHO has considered Giardia to have zoonotic

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potential for over twenty years (WHO, 1979), either through direct faecal-oral or
waterborne routes of transmission, direct evidence has been lacking (Thompson, 1998).
The consumption of drinking water other than metropolitan mains, or other filtered
supplies represents a significant risk for giardiasis (Hoque et al., 2002; Jakubowski and
Graun, 2002). The majority of waterborne giardiasis outbreaks in humans have occurred in
unfiltered surface or groundwater systems impacted by surface run off or sewage
discharges (Jakubowski and Graun, 2002). Irrigation waters used for food crops that are
traditionally consumed raw may also represent a high risk as a source of Giardia (ThurstonEnriquez et al., 2002). Environmental contamination of such water systems and supplies
may result from human, agricultural and wildlife sources (Heitman et al., 2002). These
latter authors undertook a two-year investigation to determine the significance of each
source with regard to the presence of Giardia in the environment and found sewage effluent
to have the highest prevalence of Giardia, although the concentration of cysts was minimal
compared with that detected in cattle faeces. Cow-calf sources contained the highest
concentration of Giardia. Although the overall prevalence of Giardia was lower in wildlife
than in the other two sources tested, the prevalence in aquatic mammals such as beaver and
muskrat was quite high, as for similar studies (see above). An interpretation of these results
in the context of the source(s) of human infections with Giardia should be made in
conjunction with data on the genotypes of Giardia in these animals.
As mentioned above, the greatest zoonotic risk is from genotypes of Giardia in
Assemblage A, particularly those in the AI subgroup, and to a lesser extent genotypes in
Assemblage B. In contrast, the animal-specific genotypes appear to be host-adapted,
restricted to livestock, dogs and rodents (Table 2). There is no epidemiological evidence
to suggest that they occur frequently in the human population and thus their zoonotic risk
appears minimal. This would certainly appear to be the case in cattle. Although there is
clearly a definite potential for microbial contamination of ground and surface waters
from livestock operations (Donham, 2000), studies suggest that the public health risk
from cattle may be minimal, at least in North America and Australia where genotyping
has been undertaken and has shown that the livestock genotype appears to predominate
in cattle (OHandley et al., 2000; Hoar et al., 2001). Cattle are susceptible to infection
with zoonotic genotypes of Giardia and it has been shown that calves infected with
Giardia commonly shed from 105 to 106 cysts per gram of faeces (Xiao, 1994;
OHandley et al., 1999). Thus, even a few calves infected with genotypes in Assemblage
A could pose a significant public health risk directly to handlers or indirectly as an
important reservoir for human waterborne outbreaks of giardiasis. This is of potential
public health significance and may put producers, and other members of the community,
at risk. However, longitudinal studies in Australia suggest that zoonotic genotypes may
only be present transiently in cattle under conditions where the frequency of
transmission with the livestock genotype (Assemblage E) is high and competition is thus
likely to occur. In contrast, a recent molecular epidemiological study in Uganda where
humans appear to have introduced Giardia into a remote national park are also thought to
have been the source of Giardia in a small number of cohabiting dairy cattle (Graczyk et
al., 2002).
The occurrence of Giardia in wildlife, particularly of isolates that are morphologically
identical to G. duodenalis, has been the single most important factor incriminating Giardia

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27

as a zoonotic agent. It is therefore surprising that there is so little evidence to support the
role of wildlife as a source of disease in humans, since this has dominated debate on the
zoonotic transmission of Giardia, and in particular when water is the vehicle for such
transmission. Indeed, it was the association between infected animals such as beavers and
waterborne outbreaks in people that led the WHO (1979) to classify Giardia as a zoonotic
parasite. It is therefore surprising that so little information is available on the genotypes of
Giardia affecting wildlife, as well as in people infected with Giardia as a result of a
waterborne outbreak.
Although wildlife, particularly aquatic mammals, are commonly infected with Giardia
there is little evidence to implicate such infections as the original contaminating source in
water borne outbreaks. It would appear that such animals are more likely to have become
infected from water contaminated with faecal material of human, or less likely, domestic
animal origin. They will thus serve to amplify the numbers of the originally contaminating
isolate (Bemrick and Erlandsen, 1988; Monzingo and Hibler, 1987; Thompson, 1998;
Thompson et al., 1990).
Some studies (e.g. Isaac-Renton et al., 1993) have genetically characterised isolates
associated with waterborne outbreaks, but the typing schemes used did not allow
correlation with the currently recognised assemblages. The one study that did genotype
Giardia of beaver origin, confirmed previous suggestions that the source of Giardia
infection in beavers was likely to be of human origin (Dixon et al., 2002; Monzingo and
Hibler, 1987; Rickard et al., 1999). In this study, 12 of 113 (10.6%) beaver faecal samples
from 6 of 14 different riverbank sites in southern Alberta, Canada, were positive for
Giardia, and all those genotyped using 16S-rRNA gene belonged to the zoonotic genotype,
Assemblage A (Appelbee et al., 2002).
At the present time, it is not known whether zoonotic transmission impacts significantly
on the aetiology of waterborne outbreaks of giardiasis. To date, Giardia of human origin
appears to be the main source of water contamination and as such may impact negatively
on ecosystem health leading to infections in aquatic wildlife. Recent studies have
demonstrated that filter-feeding molluscs are useful indicators of the presence of
waterborne pathogens. Genotypic characterisation was recently utilised in a study that
isolated Giardia cysts from clams in an estuary in North America (Graczyk et al., 1999).
All isolates were identified as belonging to genotype Assemblage A, highlighting
contamination with faeces of mammalian origin, most probably human, that contained G.
duodenalis cysts of public health importance. Such filter-feeding molluscan shellfish can
concentrate waterborne pathogens and thus in combination with appropriate genotyping
procedures can serve as biological indicators of contamination with Giardia cysts and can
thus be used for sanitary assessment of water quality.
The possibility of other animals acting as sources of waterborne contamination with
Giardia of zoonotic significance seems to be minimal. Dogs and cats are susceptible to
infection with zoonotic genotypes of Giardia but the chances of a contamination event
from a dog or cat leading to a waterborne outbreak in humans would seem unlikely.
However, in the case of the Sydney, Australia 1998 water crisis, dead dogs found near a
water supply (McClellan, 1998), were incriminated as a possible source of contamination
with Giardia, but no evidence of infection in the dogs, nor whether any isolates recovered
were genotyped, was provided.

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Although the clinical significance of Giardia in dogs and cats appears to be minimal,
there has been much speculation about the public health significance of such infections in
pets. In domestic, urban environments of Australia, genotypes from Assemblage A and the
dog genotype, Assemblage D, are both equally common in dogs (Thompson et al., 1999).
It is therefore considered that there are probably two cycles of transmission taking place in
domestic urban environments with the possibility of zoonotic transmission of Assemblage
A genotypes between pets and their owners. This was highlighted in the study by Bugg et
al. (1999) which found that dogs from multi-dog households were more commonly
infected with Giardia than dogs in single-dog households, emphasising the potential ease
with which Giardia can be spread to in-contact animals and therefore presumably humans
(Bugg et al., 1999). In contrast, a recent survey of domestic dogs in Japan found all isolates
to belong to the dog-specific genotype, Assemblage D (Abe et al., 2003).
From the point of view of direct zoonotic transmission, the finding that similar
genotypes are dispersed in different hosts is not by itself conclusive evidence that zoonotic
transmission is taking place. A better assessment for this can only come from studies which
examine the dynamics of Giardia transmission between hosts living in the same
geographical area or localised endemic focus. Molecular epidemiological studies in
localised endemic foci where the frequency of transmission of zoonotic and non-zoonotic
genotypes is high, such as in Aboriginal communities in Australia, have shown that the dog
genotype predominates in infected dogs (Hopkins et al., 1997). In contrast, in remote tea
growing communities in Assam northeast India, where Giardia occurs in both humans and
their dogs, 20% of dogs were found to be infected with Giardia, but they were all infected
with zoonotic genotypes, mostly from Assemblage A. This difference may reflect a closer
association between individual dogs and their owners in the tea growing communities, and
the frequency with which dogs are able to eat human faeces in these communities (Traub et
al., 2002). In Aboriginal communities in Australia, such behaviour by dogs is less common
and the dogs tend to stay together in packs. In environments where the infection pressure is
less, such as domestic households in urban settings, dogs are just as likely to harbour
zoonotic genotypes of Giardia from Assemblage A as they are their own dog genotype
(Assemblage D).
Presumably, in environments where the frequency of transmission of different
genotypes is high, as in Aboriginal communities in Australia, competitive interactions are
likely to ensure that the host adapted genotypes predominate in respective host species, as
with the livestock genotype in dairy cattle (see above). Under such conditions where
Giardia infections are common in humans and dogs, dogs would be equally likely to be
exposed regularly to infection with both dog and zoonotic genotypes of G. duodenalis
(Hopkins et al., 1997; Thompson, 2002). Australian Aboriginal communities represent
highly endemic foci of Giardia transmission with high rates of infection in children and
dogs, often greater than 50% (Meloni et al., 1993; Thompson, 2000). Under these
circumstances, experimental evidence suggests that the dog-adapted genotype will, by
competitive exclusion, out-compete other genotypes preventing their colonisation in the
dog intestine (Thompson et al., 1996). In domestic, urban environments, and in the tea
growing communities in Assam, India, the frequency of dog to dog transmission will be
less frequent and thus infections acquired with Assemblage A genotypes in dogs are likely
to persist.

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29

Although within-host competition between genotypes may preclude the establishment

of infections with zoonotic genotypes in dogs living in environments where the frequency
of transmission is very high, the role of dogs as mechanical vectors of zoonotic Giardia
genotypes in such situations must be considered. Under such conditions, dogs are very
likely to be contaminated on their coats and muzzle with cysts of Giardia which could be
readily transferred to children.
The study in Assam, India by Traub et al. (2004), has provided the first direct evidence
of zoonotic transmission between dogs and humans, by finding the same genotype of
Giardia in people and dogs, not only in the same village, but also in the same household.
Giardia isolates were characterised at three different loci; the SSU-rDNA, elongation
factor 1-alpha (ef1-a) and triose phosphate isomerase (tpi) gene. Evidence for zoonotic
transmission was supported by strong epidemiological data showing a highly significant
association between the prevalence of Giardia in humans and the presence of a Giardia
positive dog in the same household. A major finding of this study was the importance of
using multiple loci when inferring genotypes to Giardia in epidemiological investigations
(Traub et al., 2004).

6. Diagnosis and detection

Diagnosis of Giardia by traditional microscopic methods following the application of
faecal concentration techniques, especially zinc sulphate flotation and centrifugation
(Zajac et al., 2002), remain a reliable indicator of infection. However, the detection of G.
duodenalis by microscopy or faecal ELISA is of limited epidemiological value, especially
in terms of the source of infection. The development of direct immunofluorescence
microscopy has generally improved the sensitivity of detecting and quantitating faecal
Giardia cysts and may allow for more accurate determination of prevalence rates and cyst
excretion intensities compared to conventional microscopy (OHandley, 2002). However,
it is still not possible to discriminate between morphologically identical, or similar,
organisms that are genetically different using immunofluorescene. Such genotypic
identification is not possible using microscopy alone, and as with any epidemiological
investigation, there is a need for sensitive and specific diagnostic procedures for detecting
the aetiological agents of infectious disease. With Giardia, molecular techniques,
particularly PCR-based procedures have greater sensitivity and specificity than
conventional diagnostics that are reliant on microscopy and/or immunodiagnosis
(McGlade et al., 2003). Molecular techniques have been developed that can provide
information on the genotype or species of Giardia present by combining PCR with
restriction fragment length polymorphism (RFLP) analysis, without having to resort to
costly and time-consuming sequencing (Groth and Wetherall, 2000; Amar et al., 2002;
Caccio et al., 2002). In addition to their excellent sensitivity and specificity, such
procedures are quick and amenable to large sample throughput (Morgan, 2000). Their cost
is declining but there is a need for better technology transfer so that such diagnostic
procedures can be applied directly in the laboratories of developing countries.
One of the major advantages of such PCR-based procedures is the ease of interpretation
which usually involves the visualization of a small number of bands on a gel. However, the

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R.C.A. Thompson / Veterinary Parasitology 126 (2004) 1535

very high sensitivity of most PCR-based procedures can also present problems of
interpretation. For example, a recent survey of parasites of domestic cats using microscopy
found that 5% were infected with Giardia whereas PCR revealed that 80% were positive, a
level supported by the detection of faecal antigen (McGlade et al., 2003). Similarly, a
survey of dogs in India found a 3% prevalence using microscopy, compared to 20% with
PCR (Traub et al., 2004). Such results could not be accounted for by the intermittent nature
of cyst shedding by Giardia (McGlade et al., 2003) and raise questions concerning both the
clinical and epidemiological significance of such presumably low-level infections with
Giardia that result in minimal excretion of infective stages.
A greater awareness of parasite contamination of the environment and its impact on
health has precipitated the development of better detection methods for waterborne
pathogens such as Giardia (Slifko et al., 2000). Filtration, flocculation, flow cytometry,
immunomagnetisable separation and immunofluorescence with monoclonal antibodies
together constitute the currently acceptable methodology for detecting Giardia in drinking
water (Slifko et al., 2000). These approaches are also used for testing raw and treated
waters, although PCR-based procedures are increasingly being used to complement
immunofluorescence and add a measure of quality control. In addition, molecular
techniques can provide genotypic characterisation of the parasites isolated from water, thus
providing valuable data for determining the source of contamination.

7. Treatment and control

Nitroimidazoles and benzimidazoles are effective antigiardial drugs for treating
infections in humans. The superior palatability and efficacy of benzimidazoles such as
albendazole, offer a useful alternative to the nitroimidazoles, particularly where mass
chemotherapy is required, compliance is an issue, or where treatment failures have
occurred following nitroimidazole treatment. In dogs and cats, benzimidazoles such as
fenbendazole/febantel are proving very valuable alternatives to nitroimidazoles (Barr et al.,
1998; Zajac et al., 1998).
In livestock, benzimidazoles, such as fenbendazole and albendazole, have been shown
to be effective in the elimination of Giardia from both housed and range calves (Xiao et al.,
1996; OHandley et al., 2001; Garossino et al., 2001). Treating calves with fenbendazole
was also able to improve the mucosal microvillus structure and function within seven days
of initiating treatment (OHandley et al., 2001).
Although chemotherapy may be highly effective in eliminating infection, re-infection
frequently occurs if the sources of environmental contamination are not eliminated and the
frequency of transmission is high. This applies to both human and animal infections,
particularly in localised endemic foci such as communities and institutions where hygiene
is inadequate or easily compromised, dairy farms, kennels and catteries (Reynoldson et al.,
1998; Thompson, 1998; OHandley et al., 2001).
Infections with Giardia stimulate humoral immunity that results in self-limiting
infection in many animal species (Olson et al., 2000). Unfortunately, it may take several
months for the host to produce protective antibodies that can eliminate the parasite. Calves
have been shown not to mount an effective humoral immune response against Giardia even

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31

after 100 days of infection (OHandley et al., 2003). Lactating cows produce colostrum and
milk with anti-giardial activity and the consumption of antibodies in colostrum may afford
protection to young calves against infection, since Giardia is usually observed in calves
greater than 34 weeks of age. Dogs and cats have been protected following vaccination
with a commercially available trophozoite extract vaccine (Olson et al., 2000). Such a
prophylactic approach may have potential application in beef and dairy cattle but has not
yet been evaluated experimentally in livestock.

8. Conclusions and looking to the future

The genetic characterisation of Giardia from different hosts and geographical areas has
now provided a wealth of data to support a revised taxonomy of Giardia affecting
mammalian hosts. As a result of such studies, the zoonotic potential of Giardia is no longer
in doubt, but there is limited data on the frequency of zoonotic transmission. What data
there is available suggests that animals are unlikely in most cases to be the original
contaminating source of Giardia in waterborne outbreaks, although aquatic wildlife are
capable of amplifying zoonotic genotypes of Giardia that may contaminate water.
However, there is still very little information available on the genotypes of Giardia
naturally occurring in wildlife, both aquatic and terrestrial. In contrast, a number of studies
have genotyped Giardia in domestic animals, particularly livestock and companion
animals, and have found that they may be infected with zoonotic or species-specific
genotypes. The frequency of infection with zoonotic genotypes appears to be much less in
livestock than in companion animals, particularly domestic dogs. However, the role of dogs
in the zoonotic transmission of Giardia is clearly dependent upon the nature of the
interaction between dogs and their owners and further studies are required in different
endemic foci. Understanding the transmission dynamics of Giardia in endemic areas where
the frequency of transmission is high will require the application of more discriminatory
genotyping tools than those currently available. The search for such tools is an essential
pre-requisite in the development of genetic markers for important phenotypic traits of
Giardia, particularly drug sensitivity and virulence, both of which have been shown to vary
between isolates of the parasite.
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