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Fungal nail disease (Onychomycosis); Challenges and solutions

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DOI: 10.4103/2321-4848.133811

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Review Article

Fungal nail disease (Onychomycosis); Challenges


and solutions
M. Suchitra Shenoy, M. Manjunath Shenoy1
Department of Microbiology, Kasturba Medical College, Manipal University, Manipal, Mangalore, Karnataka, 1Department of Dermatology,
Yenepoya Medical College,Yenepoya University, Mangalore, Karnataka, India

ABSTRACT
Onychomycosis (fungal nail infection) is caused by three groups of fungal pathogens namely dermatophyte molds (DM), non-DM
(NDM) and yeasts. It is primarily a cosmetic problem but may induce impact on quality of life. Clinically it is characterized by five
morphologically distinctive types; distal lateral subungual onychomycosis (DLSO), superficial white onychomycosis (SWO), proximal
subungual onychomycosis (PSO), and endothrix onychomycosis. It is difficult to detect the fungal agent responsible for a particular type
of onychomycosis by clinical features alone. Mycological methods like direct demonstration of fungal agents by potassium hydroxide
mount or nail plate histopathology with Periodic acid Schiff (PAS) staining are sensitive methods for the detection of pathogens. Fungal
culture alone is commonly used as a standard for the detection of etiological agent. Molecular biological techniques are currently used
only in research laboratories or epidemiological purposes. Therapy is generally not satisfactory. Both topical and systemic agents are
used in the therapy. Topical Ciclopirix and Amorolfine are found to be effective but only in early and limited disease. Terbinafine and
Itraconazole seems to be the best drugs for the systemic therapy. Clinical cure rates are generally lower than the mycological cure rates.

Key words: Onychomycosis, dermatophyte, fungal culture, terbinafine

Introduction abnormal nails, which were often considered as colonizers or


contaminants. However, currently it is generally accepted that
Onychomycosis (fungal nail infection) is not a life-threatening they are capable of causing nail disease. Nondermatophytes are
often accountable for a significant number of onychomycosis
disease and it is primarily a cosmetic problem by causing
and may outnumber that caused by dermatophytes in certain
disfigurement. It may as a reservoir of cutaneous and systemic
geographic areas.[1] Some of these NDM are also capable
infection. It is caused by three groups of fungal agents namely
of producing invasive fungal diseases in neutropenic and
dermatophyte molds (DM), non-DM (NDM) and yeasts. Role
immune-suppressed patients, and hence their eradication
of dermatophytes in onychomycosis is well-established.
may be essential.[2] Candida albicans is the most common
Fungi other than dermatophytes are often isolated from yeast associated with onychomycosis, and is seen generally
in the presence of finger nail paronychia. It can directly invade
Access this article online the nails in chronic mucocutaneous candidiasis, a condition
Quick Response Code: associated with immunodeficiency.[3] It is difficult to clinically
Website:
www.amhsjournal.org
diagnose onychomycosis since many other nail diseases can
resemble. It is even more difficult to obtain etiological diagnosis
DOI: since isolation of the causative agent by microbiological
10.4103/2321-4848.133811 techniques is a challenge. It is difficult to treat onychomycosis
because eradication of the fungus (mycological cure) from

Corresponding Author:
Prof. M. Manjunath Shenoy, Department of Dermatology,Yenepoya Medical College,Yenepoya University, Mangalore - 575 018,
Karnataka, India. E-mail: manjunath576117@yahoo.co.in

48 Archives of Medicine and Health Sciences / Jan-Jun 2014 / Vol 2 | Issue 1


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Shenoy and Shenoy: Onychomycosis: Challenges and solutions

the nail is difficult. In spite of the mycological cure, structural in toenail and 50% in fingernail infections may be caused
abnormality of the nail may not get corrected. by dermatophytes.[9,10]

Etiology and Prevalence Clinical Features


There seems to be a great geographic variation in the There are no specific clinical patterns for onychomycosis caused
incidence of onychomycosis. Several factors such as age, by DM and NDM, and all patterns as seen with dermatophytic
climate, occupation, travel and hygiene seems to play infections are seen with NDM too.[9] It is difficult to distinguish
a role in the prevalence of the disease. There is great dermatophytic infections from NDM infections by clinical
variation in the agents causing onychomycosis in various features alone. Prior history of trauma, absence of tinea pedes
geographic areas. Undoubtedly, dermatophytes are the most and lack of response to systemic antifungals may suggest
common causative organisms. Trichophyton rubrum is the a possibility of onychomycosis due to nondermatophytes.
most common causative agent among the dermatophytes Mechanical and chemical factors have a role in nail infection
followed by Trichophyton mentagrophytes.[4] Prevalence as with surface adhesion followed by the invasion in to the
high as 51.6% for NDM has been reported, but in general layers of nail apparatus seems to be the determinants in the
it is much less.[1] Dermatophytes affect both finger and pathogenesis and the eventual type of onychomycosis.[10,11]
toe nails but NDM generally affect toe nails. NDM are
saprophytic and plant pathogens. Aspergillus species were Clinical forms of onychomycosis are distal lateral subungual
more frequently isolated than other agents among the onychomycosis (DLSO) [Figure 1], superficial white
NDM.[5-7] Scopulariopsis brevicaulis has also been reported onychomycosis (SWO), proximal subungual onychomycosis
as a frequent cause of onychomycosis.[8] Table 1 shows (PSO), endothrix onychomycosis and total dystrophic
the causes of dermatophytic and NDM onychomycosis. C. onychomycosis (TDO) [Figure 2].[9-11] Relative lack of effective
albicans is the most common cause of onychomycosis caused cell-mediated immunity in the nail apparatus seems to make
by yeasts but other Candida species are also rarely reported. the nail more vulnerable to fungal infections.[11] There is also
Studies show various prevalence, but approximately 90% increased incidence of onychomycosis with advancing age.[12]
Candidal onychomycosis is more frequent in women.[13]
Table 1: List of dermatophytic and nondermatophytic moulds reported
to be a cause of onychomycosis Distal lateral subungual onychomycosis is the most common
Dermatophytic moulds Nondermatophytic moulds form of onychomycosis. The nail plate gets first affected from
Trichophyton rubrum Aspergillus species
Trichophyton mentagrophytes Scopulariopsis brevicaulis
the under and lateral edges, and then spreads proximally
Trichophyton tonsurans Alternaria species along the nail bed resulting in to deposition of debris under
Trichophyton megnini Fusarium species the nail (subungual hyperkeratosis) and lifting up of the
Trichophyton schoenleinii Cladosporium species
Trichophyton soudanense Curvularia lunata nail plate (onycholysis). PSO is a rarer form and is often
Trichophyton violaceum Acremonium species reported in the presence of HIV disease. Fungus enters
Epidermophyton floccosum Penicillium species
Onychocola candidensis through the proximal part of the nail plate from under the
surface of the proximal nail fold. Nail on the proximal part
Figure 1: Distal and lateral subungual onychomycosis of great toe
with tinea pedes Figure 2: Total dystrophic onychomycosis of great toe nail

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Shenoy and Shenoy: Onychomycosis: Challenges and solutions

becomes yellow-white discolored and that gets spread paper or cardboard folder and transported to the mycology
distally across the nail bed. SWO is also a rare variety laboratory.
where there is a direct invasion of the nail plate with white
discoloration and flakiness without nail bed being affected. Specimen Analysis
Endonyx onychomycosis begins as DLSO, but nail plate gets
discolored with minimal or no subungual hyperkeratosis or Direct microscopy and laboratory culture for fungus is done
onycholysis. All these varieties eventually may lead to TDO to confirm and identify the etiological agent. Culture is
over a long period of time. mandatory even if the preliminary microscopic examination
is negative as even a small amount of fungus is sufficient to
Dermatophytes like T. rubrum, T. mentagrophytes, isolate it in culture.
Trichophyton tonsurans, Epidermophyton floccosum are
known to be causative agents of DLSO. Nondermatophytes Direct Microscopy
that may be associated with DLSO are S. brevicaulis,
Aspergillus species, Acremonium species and Fusarium Different methods of microscopic techniques with or
oxyspor um. [10] White super ficial onychomycosis without stains are used as screening tests for confirming
onychomycosis may be caused by T. mentagrophytes, the presence or absence of fungi in the nail specimens even
Acremonium species, Aspergillus species and Fusarium.[10,14] if the false negativity of this method amounts to 5-15%.[10]
Most commonly potassium hydroxide mount is used as the
It is difficult to distinguish onychomycosis caused by the microscopic method in the diagnostic laboratories. Adding
various types of fungi. Associated infection of the foot (tinea a drop of parker blue-black ink or lactophenol cotton blue
pedes) is a feature favoring dermatophyte infections, but helps to visualize the fungal elements clearly. Use of chlorazol
there are exceptions.[15] Nondermatophyte onychomycosis is black E helps to differentiate between the fungi and elastic
often associated with inflammation of nail folds (paronychia), fibers or cotton fibers. Calcoflour white stain helps to
white discolotration of nail plates (leukonychia), or dark confirm the presence of the fungi without any doubt. The only
discoloration (melanonychia).[16,17] disadvantage of this stain is the requirement of fluorescent
microscope.
Yeast like C. albicans is a part of the normal flora of the skin,
mucosa and gut. Nail infection by them may result due to four Histopathological examination of nail clippings
underlying mechanism namely chronic paronychia, secondary using periodic acid-Schiff stain helps to differentiate
candidiasis, distal nail infection, or as a manifestation of onychomycosis from other nail disorders such as psoriasis,
chronic mucocutaneous candidiasis.[18] The most common or lichen planus. The test has very high sensitivity, and
form of Candida onychomycosis manifests secondary to may also help to observe the depth of tissue invasion, type
paronychia, which is seen usually in patients with wet of mold (whether dermatophyte or nondermatophyte) to
occupations. Damage to the cuticle is an important factor some extent.[20,21]
in pathogenesis, due to which yeasts and bacteria enter
the subcuticular space at the proximal part of the nail.[18] Culture
Secondary candidal onychomycosis occurs in other diseases
of the nail apparatus, most notably psoriasis. Chronic With the growing problem of antifungal resistance to common
mucocutaneous is a rare variety seen in association with drugs culture of the specimens of onychomycosis helps to
an immunocompromised state. There is direct invasion of identify the causative organism and also has the advantage
the nail plate and swelling of the proximal and lateral nail of subjecting the isolate to antifungal susceptibility testing.
folds leading to a pseudo-clubbing (“chicken drumstick”).[10]
Table 2: Nail sampling for the laboratory diagnosis of onychomycosis
Laboratory Diagnosis Type of Specimen collected
onychomycosis
Collecting the nail specimen and transport Distal subungual Nail bed scrapings after nail clipping where concentration of
Heavily soiled nails especially toe nails have to be cleaned onychomycosis viable fungi is highest
Proximal subungual After cutting the nail material from the infected proximal nail bed
with soap and water; rub with alcohol to remove bacteria onychomycosis is removed using a sharp 1 mm or 2 mm serrated curette
before collecting the nail sample.[19] The collection techniques White superficial A no. 15 scalpel blade or sharp curette can be used to scrape the
onychomycosis white area and collect the infected debris
recommended for different sites of infection of the nail Candida onychomycosis Material from the proximal and lateral nail edges is used
apparatus for optimal recovery of the fungus are summarized Endonyx/total dystrophic Nail clippings
in Table 2.[10,20] The sample is collected on a sterile black filter onychomycosis

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Shenoy and Shenoy: Onychomycosis: Challenges and solutions

The nails are cultured on different media which suppress the the treating physician to choose the regime, but also to
contaminating bacteria and fungi. Onychomycosis can be due predict the prognosis. In spite of eradication of the fungus
to dermatophyte or NDM therefore two media are used one (mycological cure), anatomical abnormality of the nails
selective for dermatophyte with cycloheximide and another may not be corrected (clinical cure). This may be especially
without which allows NDM to grow. If there is growth on true for nondermatophyte infections, because the nail
both it is dermatophyte otherwise it is NDM. To prevent the may be abnormal prior to the fungal invasion.[23] Both
growth of the bacteria the Sabouraud dextrose agar with or topical and systemic therapies are used in onychomycosis.
without antibiotics like gentamicin or chloramphenicol and Combination of drugs with oral and topical therapy is
Littman’s oxgall medium is used. NDM grows in 5-6 days also advocated and seems to be superior to the systemic
while Candida grows within 24-48 h of culture. Candida therapy alone.
species can be identified and antifungal susceptibility can
be done using conventional and automated methods. Currently available antifungal drugs for oral use include
itraconazole, terbinafine, fluconazole, griseofulvin and
Isolation of dermatophyte always confirms the pathogen ketoconazole. [24] All these drugs were found effective
but the problem arises for the laboratory personnel when for the treatment of dermatophyte onychomycosis.
a NDM grows. It should be distinguished from contaminant Itraconazole or terbinafine may be useful in NDM infection
and true pathogen. It is recommended to follow Gupta et al. too. Itraconazole and terbinafine have demonstrated
inoculum counting (Walshe and English criteria) method in efficacy and safety against some cases of S. brevicaulis
diagnosis of onychomycosis caused by nondermatophytic toe onychomycosis. [24] Griseofulvin and ketoconazole
filamentous fungi.[9] If NDM is isolated, it should be considered is not recommended by many for onychomycosis given
as laboratory contaminants unless KOH or microscopy its very long duration of therapy and potentially serious
demonstrates atypical frond-like hyphae or if the same adverse effects respectively. Fluconazole is less effective
organism is repeatedly isolated.[10] than terbinafine and itraconazole in the treatment of
onychomycosis, but it is a choice when patients do not
Molecular typing methods like polymerase chain reaction- tolerate other oral antifungal agents.[25] Minimal dosing
restriction fragment length polymorphism can be used of fluconazole should be 150 mg/week for at least 6
for epidemiological, research and confirmation purposes. months. Itraconazole and terbinafine appear to be the best
They are time consuming and expensive methods usually systemic drugs for the therapy of onychomycosis due to
done only by research laboratories. These methods cannot their reservoir effects in the nails; however therapy is of
distinguish between true pathogens and contaminants on the long duration ranging from 6 weeks to 3 months or longer.
sample. Immuno-histochemistry and dual flow cytometry Candidial onychomycosis responds to treatment with
can be used to identify mixed infections and for quantification itraconazole and fluconazole. Addition of amorolfine to oral
of the fungal load. itraconazole pulse therapy is beneficial in the treatment
of Candida fingernail onychomycosis.[26]
Treatment
Topical treatment with terbinafine (with nail avulsion)
There have been controversies regarding the therapy of or ciclopirox can be successful in the treatment of
onychomycosis. The available therapeutic options have not onychomycosis caused by dermatophytosis and certain
been proven to be universally efficacious, duration of therapy nondermatophytes. [23] Ciclopirox may have a broad
is long, and the drugs used are not very safe. Onychomycosis antimicrobial profile including dermatophytes, yeasts and
primarily a cosmetic problem, but it may have a negative nondermatophytes, and activity of ciclopirox and terbinafine
psychological impact on afflicted persons. Persistence of the suggests many instances of synergy.[27] Amorolfine is a
fungus in nail can serve as a reservoir for systemic infections structurally unique, topical antifungal agent, which possesses
and communicate the fungal infections to family members. both fungistatic and fungicidal activity against dermatophyte,
Uniform guidelines for the therapy are also lacking. All these dimorphic, some dematiaceous and filamentous fungi, and
issues shall be discussed with the patients before the onset some yeast. Application of amorolfine 5% nail lacquer once
of the therapy. Convenient, cost effective antifungals with or twice weekly for up to 6 months produced mycological
high and long-lasting cure rates are necessary, and many and clinical cure in approximately 40-55% of patients with
new therapies for onychomycosis are under investigation.[22] mild onychomycosis.[28]

It is preferable to establish the infection with laboratory Recently the drugs such as itraconazole and terbinafine are
methods before the therapy has begun. This will not ease used in pulsed manner.[29,30] It is popularly given for 1 week in

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31. Elewski B, Pollak R, Ashton S, Rich P, Schlessinger J, How to cite this article: Shenoy MS, Shenoy MM. Fungal nail disease
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parallel-group, multicentre, investigator-blinded study of
Source of Support: Nil, Conflict of Interest: None declared.
four treatment regimens of posaconazole in adults with

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