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48 Archives of Medicine and Health Sciences / Jan-Jun 2014 / Vol 2 | Issue 1
Review Article
Introduction
Onychomycosis (fungal nail infection) is not a life-threatening
disease and it is primarily a cosmetic problem by causing
disfigurement. It may as a reservoir of cutaneous and systemic
infection. It is caused by three groups of fungal agents namely
dermatophyte molds (DM), non-DM (NDM) and yeasts. Role
of dermatophytes in onychomycosis is well-established.
Fungi other than dermatophytes are often isolated 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
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
Fungal nail disease (Onychomycosis); Challenges
and solutions
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 fi ve
morphologically distinctive types; distal lateral subungual onychomycosis (DLSO), superfi cial white onychomycosis (SWO), proximal
subungual onychomycosis (PSO), and endothrix onychomycosis. It is diffi cult 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 Amorolfi ne are found to be effective but only in early and limited disease. Terbinafi ne 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, terbinafi ne
abnormal nails, which were often considered as colonizers or
contaminants. However, currently it is generally accepted that
they are capable of causing nail disease. Nondermatophytes are
often accountable for a significant number of onychomycosis
and may outnumber that caused by dermatophytes in certain
geographic areas.[1] Some of these NDM are also capable
of producing invasive fungal diseases in neutropenic and
immune-suppressed patients, and hence their eradication
may be essential.[2] Candida albicans is the most common
yeast associated with onychomycosis, and is seen generally
in the presence of finger nail paronychia. It can directly invade
the nails in chronic mucocutaneous candidiasis, a condition
associated with immunodeficiency.[3] It is difficult to clinically
diagnose onychomycosis since many other nail diseases can
resemble. It is even more difficult to obtain etiological diagnosis
since isolation of the causative agent by microbiological
techniques is a challenge. It is difficult to treat onychomycosis
because eradication of the fungus (mycological cure) from
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Archives of Medicine and Health Sciences / Jan-Jun 2014 / Vol 2 | Issue 1 49
Shenoy and Shenoy: Onychomycosis: Challenges and solutions
the nail is difficult. In spite of the mycological cure, structural
abnormality of the nail may not get corrected.
Etiology and Prevalence
There seems to be a great geographic variation in the
incidence of onychomycosis. Several factors such as age,
climate, occupation, travel and hygiene seems to play
a role in the prevalence of the disease. There is great
variation in the agents causing onychomycosis in various
geographic areas. Undoubtedly, dermatophytes are the most
common causative organisms. Trichophyton rubrum is the
most common causative agent among the dermatophytes
followed by Trichophyton mentagrophytes.[4] Prevalence as
high as 51.6% for NDM has been reported, but in general
it is much less.[1] Dermatophytes affect both finger and
toe nails but NDM generally affect toe nails. NDM are
saprophytic and plant pathogens. Aspergillus species were
more frequently isolated than other agents among the
NDM.[5-7] Scopulariopsis brevicaulis has also been reported
as a frequent cause of onychomycosis.[8] Table 1 shows
the causes of dermatophytic and NDM onychomycosis. C.
albicans is the most common cause of onychomycosis caused
by yeasts but other Candida species are also rarely reported.
Studies show various prevalence, but approximately 90%
in toenail and 50% in fingernail infections may be caused
by dermatophytes.[9,10]
Clinical Features
There are no specific clinical patterns for onychomycosis caused
by DM and NDM, and all patterns as seen with dermatophytic
infections are seen with NDM too.[9] It is difficult to distinguish
dermatophytic infections from NDM infections by clinical
features alone. Prior history of trauma, absence of tinea pedes
and lack of response to systemic antifungals may suggest
a possibility of onychomycosis due to nondermatophytes.
Mechanical and chemical factors have a role in nail infection
with surface adhesion followed by the invasion in to the
layers of nail apparatus seems to be the determinants in the
pathogenesis and the eventual type of onychomycosis.[10,11]
Clinical forms of onychomycosis are distal lateral subungual
onychomycosis (DLSO) [Figure 1], superficial white
onychomycosis (SWO), proximal subungual onychomycosis
(PSO), endothrix onychomycosis and total dystrophic
onychomycosis (TDO) [Figure 2].[9-11] Relative lack of effective
cell-mediated immunity in the nail apparatus seems to make
the nail more vulnerable to fungal infections.[11] There is also
increased incidence of onychomycosis with advancing age.[12]
Candidal onychomycosis is more frequent in women.[13]
Distal lateral subungual onychomycosis is the most common
form of onychomycosis. The nail plate gets first affected from
the under and lateral edges, and then spreads proximally
along the nail bed resulting in to deposition of debris under
the nail (subungual hyperkeratosis) and lifting up of the
nail plate (onycholysis). PSO is a rarer form and is often
reported in the presence of HIV disease. Fungus enters
through the proximal part of the nail plate from under the
surface of the proximal nail fold. Nail on the proximal part
Table 1: List of dermatophytic and nondermatophytic moulds reported
to be a cause of onychomycosis
Dermatophytic moulds Nondermatophytic moulds
Trichophyton rubrum Aspergillus species
Trichophyton mentagrophytes Scopulariopsis brevicaulis
Trichophyton tonsurans Alternaria species
Trichophyton megnini Fusarium species
Trichophyton schoenleinii Cladosporium species
Trichophyton soudanense Curvularia lunata
Trichophyton violaceum Acremonium species
Epidermophyton fl occosum Penicillium species
Onychocola candidensis
Figure 2: Total dystrophic onychomycosis of great toe nail
Figure 1: Distal and lateral subungual onychomycosis of great toe
with tinea pedes
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50 Archives of Medicine and Health Sciences / Jan-Jun 2014 / Vol 2 | Issue 1
Shenoy and Shenoy: Onychomycosis: Challenges and solutions
becomes yellow-white discolored and that gets spread
distally across the nail bed. SWO is also a rare variety
where there is a direct invasion of the nail plate with white
discoloration and flakiness without nail bed being affected.
Endonyx onychomycosis begins as DLSO, but nail plate gets
discolored with minimal or no subungual hyperkeratosis or
onycholysis. All these varieties eventually may lead to TDO
over a long period of time.
Dermatophytes like T. rubrum, T. mentagrophytes,
Trichophyton tonsurans, Epidermophyton floccosum are
known to be causative agents of DLSO. Nondermatophytes
that may be associated with DLSO are S. brevicaulis,
Aspergillus species, Acremonium species and Fusarium
oxysporum.[10] White superficial onychomycosis
onychomycosis may be caused by T. mentagrophytes,
Acremonium species, Aspergillus species and Fusarium.[10,14]
It is difficult to distinguish onychomycosis caused by the
various types of fungi. Associated infection of the foot (tinea
pedes) is a feature favoring dermatophyte infections, but
there are exceptions.[15] Nondermatophyte onychomycosis is
often associated with inflammation of nail folds (paronychia),
white discolotration of nail plates (leukonychia), or dark
discoloration (melanonychia).[16,17]
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
underlying mechanism namely chronic paronychia, secondary
candidiasis, distal nail infection, or as a manifestation of
chronic mucocutaneous candidiasis.[18] The most common
form of Candida onychomycosis manifests secondary to
paronychia, which is seen usually in patients with wet
occupations. Damage to the cuticle is an important factor
in pathogenesis, due to which yeasts and bacteria enter
the subcuticular space at the proximal part of the nail.[18]
Secondary candidal onychomycosis occurs in other diseases
of the nail apparatus, most notably psoriasis. Chronic
mucocutaneous is a rare variety seen in association with
an immunocompromised state. There is direct invasion of
the nail plate and swelling of the proximal and lateral nail
folds leading to a pseudo-clubbing (“chicken drumstick”).[10]
Laboratory Diagnosis
Collecting the nail specimen and transport
Heavily soiled nails especially toe nails have to be cleaned
with soap and water; rub with alcohol to remove bacteria
before collecting the nail sample.[19] The collection techniques
recommended for different sites of infection of the nail
apparatus for optimal recovery of the fungus are summarized
in Table 2.[10,20] The sample is collected on a sterile black filter
paper or cardboard folder and transported to the mycology
laboratory.
Specimen Analysis
Direct microscopy and laboratory culture for fungus is done
to confirm and identify the etiological agent. Culture is
mandatory even if the preliminary microscopic examination
is negative as even a small amount of fungus is sufficient to
isolate it in culture.
Direct Microscopy
Different methods of microscopic techniques with or
without stains are used as screening tests for confirming
the presence or absence of fungi in the nail specimens even
if the false negativity of this method amounts to 5-15%.[10]
Most commonly potassium hydroxide mount is used as the
microscopic method in the diagnostic laboratories. Adding
a drop of parker blue-black ink or lactophenol cotton blue
helps to visualize the fungal elements clearly. Use of chlorazol
black E helps to differentiate between the fungi and elastic
fibers or cotton fibers. Calcoflour white stain helps to
confirm the presence of the fungi without any doubt. The only
disadvantage of this stain is the requirement of fluorescent
microscope.
Histopathological examination of nail clippings
using periodic acid-Schiff stain helps to differentiate
onychomycosis from other nail disorders such as psoriasis,
or lichen planus. The test has very high sensitivity, and
may also help to observe the depth of tissue invasion, type
of mold (whether dermatophyte or nondermatophyte) to
some extent.[20,21]
Culture
With the growing problem of antifungal resistance to common
drugs culture of the specimens of onychomycosis helps to
identify the causative organism and also has the advantage
of subjecting the isolate to antifungal susceptibility testing.
Table 2: Nail sampling for the laboratory diagnosis of onychomycosis
Type of
onychomycosis
Specimen collected
Distal subungual
onychomycosis
Nail bed scrapings after nail clipping where concentration of
viable fungi is highest
Proximal subungual
onychomycosis
After cutting the nail material from the infected proximal nail bed
is removed using a sharp 1 mm or 2 mm serrated curette
White superfi cial
onychomycosis
A no. 15 scalpel blade or sharp curette can be used to scrape the
white area and collect the infected debris
Candida onychomycosis Material from the proximal and lateral nail edges is used
Endonyx/total dystrophic
onychomycosis
Nail clippings
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Archives of Medicine and Health Sciences / Jan-Jun 2014 / Vol 2 | Issue 1 51
Shenoy and Shenoy: Onychomycosis: Challenges and solutions
The nails are cultured on different media which suppress the
contaminating bacteria and fungi. Onychomycosis can be due
to dermatophyte or NDM therefore two media are used one
selective for dermatophyte with cycloheximide and another
without which allows NDM to grow. If there is growth on
both it is dermatophyte otherwise it is NDM. To prevent the
growth of the bacteria the Sabouraud dextrose agar with or
without antibiotics like gentamicin or chloramphenicol and
Littman’s oxgall medium is used. NDM grows in 5-6 days
while Candida grows within 24-48 h of culture. Candida
species can be identified and antifungal susceptibility can
be done using conventional and automated methods.
Isolation of dermatophyte always confirms the pathogen
but the problem arises for the laboratory personnel when
a NDM grows. It should be distinguished from contaminant
and true pathogen. It is recommended to follow Gupta et al.
inoculum counting (Walshe and English criteria) method in
diagnosis of onychomycosis caused by nondermatophytic
filamentous fungi.[9] If NDM is isolated, it should be considered
as laboratory contaminants unless KOH or microscopy
demonstrates atypical frond-like hyphae or if the same
organism is repeatedly isolated.[10]
Molecular typing methods like polymerase chain reaction-
restriction fragment length polymorphism can be used
for epidemiological, research and confirmation purposes.
They are time consuming and expensive methods usually
done only by research laboratories. These methods cannot
distinguish between true pathogens and contaminants on the
sample. Immuno-histochemistry and dual flow cytometry
can be used to identify mixed infections and for quantification
of the fungal load.
Treatment
There have been controversies regarding the therapy of
onychomycosis. The available therapeutic options have not
been proven to be universally efficacious, duration of therapy
is long, and the drugs used are not very safe. Onychomycosis
primarily a cosmetic problem, but it may have a negative
psychological impact on afflicted persons. Persistence of the
fungus in nail can serve as a reservoir for systemic infections
and communicate the fungal infections to family members.
Uniform guidelines for the therapy are also lacking. All these
issues shall be discussed with the patients before the onset
of the therapy. Convenient, cost effective antifungals with
high and long-lasting cure rates are necessary, and many
new therapies for onychomycosis are under investigation.[22]
It is preferable to establish the infection with laboratory
methods before the therapy has begun. This will not ease
the treating physician to choose the regime, but also to
predict the prognosis. In spite of eradication of the fungus
(mycological cure), anatomical abnormality of the nails
may not be corrected (clinical cure). This may be especially
true for nondermatophyte infections, because the nail
may be abnormal prior to the fungal invasion.[23] Both
topical and systemic therapies are used in onychomycosis.
Combination of drugs with oral and topical therapy is
also advocated and seems to be superior to the systemic
therapy alone.
Currently available antifungal drugs for oral use include
itraconazole, terbinafine, fluconazole, griseofulvin and
ketoconazole.[24] All these drugs were found effective
for the treatment of dermatophyte onychomycosis.
Itraconazole or terbinafine may be useful in NDM infection
too. Itraconazole and terbinafine have demonstrated
efficacy and safety against some cases of S. brevicaulis
toe onychomycosis.[24] Griseofulvin and ketoconazole
is not recommended by many for onychomycosis given
its very long duration of therapy and potentially serious
adverse effects respectively. Fluconazole is less effective
than terbinafine and itraconazole in the treatment of
onychomycosis, but it is a choice when patients do not
tolerate other oral antifungal agents.[25] Minimal dosing
of fluconazole should be 150 mg/week for at least 6
months. Itraconazole and terbinafine appear to be the best
systemic drugs for the therapy of onychomycosis due to
their reservoir effects in the nails; however therapy is of
long duration ranging from 6 weeks to 3 months or longer.
Candidial onychomycosis responds to treatment with
itraconazole and fluconazole. Addition of amorolfine to oral
itraconazole pulse therapy is beneficial in the treatment
of Candida fingernail onychomycosis.[26]
Topical treatment with terbinafine (with nail avulsion)
or ciclopirox can be successful in the treatment of
onychomycosis caused by dermatophytosis and certain
nondermatophytes.[23] Ciclopirox may have a broad
antimicrobial profile including dermatophytes, yeasts and
nondermatophytes, and activity of ciclopirox and terbinafine
suggests many instances of synergy.[27] Amorolfine is a
structurally unique, topical antifungal agent, which possesses
both fungistatic and fungicidal activity against dermatophyte,
dimorphic, some dematiaceous and filamentous fungi, and
some yeast. Application of amorolfine 5% nail lacquer once
or twice weekly for up to 6 months produced mycological
and clinical cure in approximately 40-55% of patients with
mild onychomycosis.[28]
Recently the drugs such as itraconazole and terbinafine are
used in pulsed manner.[29,30] It is popularly given for 1 week in
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52 Archives of Medicine and Health Sciences / Jan-Jun 2014 / Vol 2 | Issue 1
Shenoy and Shenoy: Onychomycosis: Challenges and solutions
a month and such two to three pulses seem to be as effective
as continuous treatment. This has enabled compliance,
reduced cost and possibly lesser adverse effects. Newer
drugs like posaconazole is being evaluated in the therapy.[31]
Very recent addition to the therapeutic armamentarium is
the 1064 nm neodymium-doped yttrium aluminum garnet
laser, whose results are encouraging but the therapeutic
regime needs optimization.[32]
Conclusion
Onychomycosis is a cosmetic problem with negative
psychological impact especially for the people in certain
professions like front desk office, food industries, actors
etc. Clinical and etiological diagnosis is challenging.
Therapeutic outcome is not very satisfactory.[33] Newer
regimes, drugs and even laser and light based therapies
are being explored. For the future, it is an important area
of research for the dermatologists and mycologists.
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How to cite this article: Shenoy MS, Shenoy MM. Fungal nail disease
(Onychomycosis); Challenges and solutions. Arch Med Health Sci 2014;2:48-53.
Source of Support: Nil, Confl ict of Interest: None declared.
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