ijd3880768

Report
Onychomycosis in Lahore, Pakistan
Mohammad Azam Bokhari, MCPS, MSc, Ijaz Hussain, FCPS, Mohammad Jahangir, MCPS,
MSc, Tahir Saeed Haroon, FRCP, FCPS, Shahbaz Aman, MCPS, and
Khawar Khurshid, MCPS, FCPS

From the Department of Dermatology, Abstract

King Edward Medical College/Mayo
Hospital, Lahore, Pakistan
Correspondence
Mohammad Azam Bokhari, MCPS, MSc
13-A, Punjab Medical College Colony
Faisalabad
Pakistan
Background Onychomycosis, a common nail disorder, is caused by yeasts,
dermatophytes, and nondermatophyte molds. These fungi give rise to diverse clinical
presentations. The present study aimed to isolate the causative pathogens and to
determine the various clinical patterns of onychomycosis in the population in Lahore,
Pakistan.
Patients In 100 clinically suspected cases, the diagnosis was confirmed by mycologic
culture. Different clinical patterns were noted and correlated with causative pathogens.
Results Seventy-two women (mean age, 32.6 ⫾ 14.8 years) and 28 men (mean age,
40.6 ⫾ 15.8 years) were studied. Fingernails were involved in 50%, toenails in 23%, and
both fingernails and toenails in 27% of patients. The various clinical types noted were
distolateral subungual onychomycosis (47%), candidal onychomycosis (36%), total
dystrophic onychomycosis (12%), superficial white onychomycosis (3%), and proximal
subungual onychomycosis (2%). Candida was the most common pathogen (46%),
followed by dermatophytes (43%) (Trichophyton rubrum (31%), T. violaceum (5%),
T. mentagrophytes (4%), T. tonsurans (2%), and Epidermophyton floccosum (1%) and
nondermatophyte molds (11%) (Fusarium (4%), Scopulariopsis brevicaulis (2%),
Aspergillus (2%), Acremonium (1%), Scytalidium dimidiatum (1%), and Alternaria (1%).
Conclusions Onychomycosis is more common in women of 20–40 years of age.
Distolateral subungual onychomycosis and candidal onychomycosis are the most common
clinical presentations, and Candida and T. rubrum are the major pathogens in Pakistan.

Onychomycosis, by definition, encompasses all fungal infec-
tions caused by primary nail pathogens, i.e. dermatophytes,
yeasts, and nondermatophyte molds.1 It accounts for up
to 50% of nail diseases and 30% of all mycotic infections
of the skin.2 The incidence of the disease varies from 3 to
5% and it may reach up to 20% in certain subgroups, e.g.
miners, sportsmen.2 Clinically, onychomycosis is sub-
classified into various forms: distolateral subungual
onychomycosis (DLSO), superficial white onychomycosis
(SWO), proximal subungual onychomycosis (PSO), can-
didal onychomycosis (CO), and total dystrophic onycho-
mycosis (TDO).1,2
The causative pathogens of the disease may show geo-
graphic or temporal distribution.1,2 Like other superficial
dermatomycoses, onychomycosis is also common in
Pakistan. Nevertheless, few data exist on the prevalence of
pathogens and their clinical presentations in our commun-
ity. This study was planned to isolate the causative fungi,
to determine the various clinical patterns of onychomycosis,
and to evaluate the clinicoetiologic correlation.
Patients and methods
This was an observational study carried out at the Depart-
ment of Dermatology, Mayo Hospital, Lahore, Pakistan,
over a period of 1 year from January 1997 to December
1997. The study population comprised 100 patients (age
range, 2–75 years; mean, 34 ⫾ 15.5 years).
Patients on systemic antifungal therapy within the last
4 weeks or topical antifungal therapy within the last 1 week
were not included. A detailed history of the patients, clinical
examination, and relative investigations were recorded on
a predevised proforma. The most severely affected nail was
selected as the target nail for sampling for direct microscopy
and culture. Clinically, the disease was classified as follows:
(i) DLSO: if there was onycholysis, discoloration, subungual 591

© 1999 Blackwell Science Ltd International Journal of Dermatology 1999, 38, 591–595
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592 Report Onychomycosis in Lahore, Pakistan Bokhari et al.

hyperkeratosis, and nail thickening affecting the distal and/ Table 1 Demographic data
or lateral nail; (ii) PSO: if discoloration and onycholysis
affected the proximal part of the nail; (iii) SWO: when Males Females Total
white opaque spots were seen on the nail surface with
Sex 28 72 100
textural changes; (iv) CO: if there was paronychia and Age (years)
lateral onycholysis, distal and lateral onycholysis without Range 6–72 2–75 2–75
paronychia, or total nail dystrophy due to Candida; (v) Mean 40.6 ⫾ 15.8 32.6 ⫾ 14.8 34 ⫾ 15.5
TDO: if there was involvement of the entire nail bed and Family history of disease 2 3 5
Occupation
nail plate.
Housewives – 48 48
The selected nail was cleaned with 70% alcohol and nail Office workers 8 7 15
dust samples were taken with the help of a specially Students 4 9 13
designed nail drill. When both fingernails and toenails were Miscellaneous 15 9 24
involved simultaneously, specimens were collected from
both sites after selecting target nails. All the samples were
examined by direct microscopy with the help of 20%
Table 2 Clinical types and sites of involvement (n ⫽ 100)
potassium hydroxide (KOH) together with calcofluor white
stain (1 part KOH and 1 part calcofluor white stain) under
Clinical type Fingernails Toenails Fingernails and
the fluorescence microscope. (n ⫽ 50) (n ⫽ 23) toenails (n ⫽ 27)
For culture, the specimens were inoculated on
Sabouraud’s dextrose agar medium together with 0.05% DLSO 14 18 15
chloramphenicol, with or without 0.5% cycloheximide. CO 28 4 4
SWO 3 0 0
The culture Petri dishes were incubated at 25–30 °C for
PSO 2 0 0
1–4 weeks. The pathogenic organisms were identified by TDO 3 1 8
gross colony morphology and microscopy examination
with lactophenol cotton blue preparation. DLSO, distolateral subungual onychomycosis; CO, candidal
The samples, which were positive on direct microscopy onychomycosis; SWO, superficial white onychomycosis;
but failed to grow, were recultured at least three times. In PSO, proximal subungual onychomycosis; TDO, total
the case of concomitant fungal infection of the feet, hands, dystrophic onychomycosis.
or any other site, samples were also taken from these sites
and processed in the same manner. For the identification
of pathogens, the diagnostic criteria of English3 were (47%), followed by CO (36%), including four cases of
followed: for dermatophytes: if a dermatophyte is isolated chronic mucocutaneous candidiasis, TDO (12%), SWO
in culture, it is to be taken as the pathogen; for nondermato- (3%), and PSO (2%). DLSO was significantly more com-
phyte molds and yeasts: (i) the presence of a fungus on mon than the other clinical types (P ⬍ 0.001), except for
direct microscopy; (ii) isolation of the same fungus from CO (P ⬍ 0.3). Similarly, CO was statistically more frequent
culture on three different occasions at an interval of at than SWO, PSO, and TDO (P ⬍ 0.05), while TDO was
least 7 days between each; (iii) at least five out of 20 more common than SWO and PSO (P ⬍ 0.03).
inocula should yield fungus. Fifty patients had fingernail involvement alone, while 23
All the collected data were processed in a database patients showed toenail involvement only. Twenty-seven
computer program for tabulation and compilation of the patients had both fingernail and toenail involvement. The
results. The results were statistically analyzed using two- number of nails involved ranged from 1 to 20. Six patients
sided, chi-squared test. A P value of ⬍ 0.05% was consid- showed involvement of all 20 nails. The most common
ered to be significant. clinical feature was discoloration seen in 100% of patients
(brown–black in 40%, yellow–brown in 32%, greyish-
black in 20%, and white or greyish-white in 8%). Other
Results
signs included onycholysis (37%), paronychia (34%),
The demographic data of the 100 evaluated patients are subungual hyperkeratosis (23%), broken nails (18%), pit-
given in Table 1. Females outnumbered males (2.6 : 1, ting (15%), ridging (9%), leukonychia (8%), Beau’s lines
P ⬍ 0.001). Of the 72 female patients, the number of (7%), and onychogryphosis (3%).
housewives or housemaids was statistically significant The various causative fungi are shown in Table 3. Out
(P ⬍ 0.001). of 100 culture-positive cases, the most common pathogen
Table 2 shows the various clinical types. DLSO was the isolated was Candida spp. (in 46% of patients), followed
most common clinical type encountered in 47 patients by dermatophytes (43%) (Trichophyton rubrum, 31%;

International Journal of Dermatology 1999, 38, 591–595 © 1999 Blackwell Science Ltd
 13654632, 1999, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1365-4362.1999.00768.x by University Of Southern Queensland, Wiley Online Library on [11/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Bokhari et al. Onychomycosis in Lahore, Pakistan Report 593

Table 3 Isolated pathogens (n ⫽ 100)

Pathogen Fingernails (n ⫽ 50) Toenails (n ⫽ 23) Fingernails and toenails (n ⫽ 27) Total (n ⫽ 100)

Yeasts
Candida spp. 32
Dermatophytes
T. rubrum
T. mentagrophytes
T. violaceum
T. tonsurans
Epidermophyton floccosum
Nondermatophyte molds
Fusarium spp.
Aspergillus spp.
Scopulariopsis brevicaulis
Scytalidium dimidiatum
Acremonium spp.
Alternaria spp.
5 9
7 9
2 1
5 0
2 0
0 1
2 1
0 1
0 2
0 1
0 1
0 1
46
15 31
1 4
0 5
0 2
0 1
1 4
1 2
0 2
0 1
0 1
0 1

T. violaceum, 5%; T. mentagrophytes, 4%; T. tonsurans, Table 4 Clinicoetiologic correlation (n ⫽ 100)

2%; and Epidermophyton floccosum, 1%). Nondermato-
phyte molds were isolated in 11% of cases (Fusarium spp., Pathogen DLSO PSO SWO TDO CO Total
4%; Aspergillus spp., 2%; Scopulariopsis brevicaulis, 2%;
Yeasts
Acremonium spp., 1%; Scytalidium dimidiatum, 1%; and Candida spp. 8 0 1 3 34 46
Alternaria spp., 1%). Yeast infection and dermatophyte Dermatophytes
infection were not statistically significantly different. Both T. rubrum 18 2 0 11 0 31
yeasts and dermatophytes were significantly more prevalent T. mentagrophytes 2 0 1 1 0 4
T. violaceum 5 0 0 0 0 5
than nondermatophyte molds (P ⬍ 0.05 for both).
T. tonsurans 2 0 0 0 0 2
The correlation between various clinical types and Epidermophyton 1 0 0 0 0 1
isolated pathogens is depicted in Table 4. floccosum
Nondermatophyte molds
Fusarium spp. 2 0 1 1 0 4
Discussion Aspergillus spp. 1 0 0 1 0 2
Scopulariopsis 1 0 0 1 0 2
Onychomycosis is a fungal infection of the nails, mainly brevicaulis
caused by dermatophytes, but nondermatophyte molds and Scytalidium dimidiatum 1 0 0 0 0 1
yeasts do play a major role in its etiology.1,2 The disease Acremonium spp. 1 0 0 0 0 1
can occur at any age, but is more common between 40 Alternaria spp. 1 0 0 0 0 1
Total 47 2 3 12 36 100
and 60 years of age and is unusual prior to puberty.1
The majority of our patients (94%) were adults between
DLSO, distolateral subungual onychomycosis; CO, candidal
the ages of 20 and 40 years. This is in accordance with the
onychomycosis; SWO, superficial white onychomycosis;
reports by Banerjee et al.4 and Khosravi et al.,5 but
PSO, proximal subungual onychomycosis; TDO, total
differs from other reports.6–9 There were only six children, dystrophic onychomycosis.
highlighting the fact that this disease is less common in
this age group. The low prevalence in children may be
attributed to a difference in nail plate structure, a lack of
cumulative trauma, and increased growth rate of the nails in females promotes fungal infections, usually Candida
with subsequent elimination of the fungus. In this study, infection. In a study by Williams,9 Candida infections were
females were more commonly affected than males (72 vs. three times more common in females than in males.
28, P ⬍ 0.05). This observation is also in agreement with The majority of cases (63%) were seen in housewives
other reports.4,5 The increased female prevalence could be and office workers. This is also consistent with previous
due to the fact that, in Pakistan, females are more involved reports.9 Maceration from wet work, dishwashing, and
in wet work, e.g. kitchen work and the laundering of contact with carbohydrates probably contribute to onycho-
clothes. The increased exposure to a wet environment mycosis in housewives, whereas office workers are more

© 1999 Blackwell Science Ltd International Journal of Dermatology 1999, 38, 591–595

594 Report Onychomycosis in Lahore, Pakistan
conscious about their health and report early to the
physician.
DLSO (47%) was the most common type encountered
in this study. Similar observations have been reported
previously.9,10 CO (36%) was the second most common
clinical type seen, as reported previously.11–13 TDO was
mainly observed as secondary to DLSO or CO. SWO (3%)
and PSO (2%) were rare events. PSO was not associated
with any immunodeficiency disease in contrast with previ-
ous reports.14,15
Candida (46%) was the most common pathogen isolated
from fingernails in the present study, especially in females.
Our results are in agreement with some previous reports.13
McAleer16 and Achten and Wanet-Rouard17 isolated Can-
dida in 66% of their cases. Candida was also the most
common pathogen found in Australia16 and Saudi Arabia.11
The predominant involvement of the fingernails by this
pathogen is also consistent with other studies.11,16 The
reason for this may be the ritualistic washing of the hands
and feet, which is a common religious practice, and the
hot and humid weather in this part of the world.
Dermatophytes, the commonest cause of onychomycosis
in other reports,6,18 were the second most frequent patho-
gens (43%) in our study. Of the dermatophytes, T. rubrum
(31%) was the most common organism as reported from
other countries, e.g. Finland,6 Spain,7 UK,8,9 and USA.18
The high prevalence rate of T. rubrum can be explained
by its better adaptation to the hard keratin of nails.
T. violaceum (5%) as a causative agent of onychomycosis
has rarely been reported previously.19 The increased incid-
ence of nail infection with this organism in our region may
be due to the high prevalence of tinea capitis caused by
this fungus.20
In this study, the prevalence of nondermatophyte molds
was 11%. These results are compatible with some previous
reports;6,21 however, the prevalence of different nonderma-
tophyte molds varies in different studies.6,21–23 The higher
prevalence rate of these pathogens observed in our study
may possibly be due to the hot and humid climate of
Pakistan. The nondermatophyte molds are usually consid-
ered as nonpathogens and unable to infect human nails.
Our study shows that these agents can primarily infect
nails and produce disease.
DLSO, CO, and TDO were seen both in fingernails and
toenails, while PSO and SWO were seen only in fingernails.
This study demonstrated a greater involvement of fin-
gernails compared to toenails, especially the middle finger
and ring finger. These results are in agreement with previous
reports,4 while in others11,20,21 toenails were commonly
affected. Fingernails were more commonly involved in
females because of their greater involvement with wet work.
Similarly, CO and dermatophyte infection predominantly
affected fingernails, while nondermatophyte mold infection
International Journal of Dermatology 1999, 38, 591–595
13654632, 1999, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1365-4362.1999.00768.x by University Of Southern Queensland, Wiley Online Library on [11/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Bokhari et al.
was more prevalent in toenails as reported by others.13,14,20
These molds are often present in soil and commonly infect
the toenails.
The clinicoetiologic correlation revealed that a single
pathogen could give rise to more than one clinical type.
Candida spp. usually presented as CO, while DLSO was less
often seen; SWO or TDO was an occasional presentation.
DLSO was the usual manifestation of dermatophyte infec-
tion. TDO was also seen in a sizeable number of patients,
whereas PSO and SWO were rarely encountered. The single
case of SWO was caused by T. mentagrophytes. None of
the patients with dermatophyte infection presented with
CO. Nondermatophyte molds usually presented as DLSO.
TDO was less frequent and SWO was occasionally encoun-
tered. CO was not diagnosed in any patient.
The present study concludes that onychomycosis is more
common in adult females who are involved in wet work.
Although Candida and dermatophytes constitute the major
bulk of pathogens, nondermatophyte molds are also com-
mon. Of the dermatophytes, T. rubrum is the most prevalent
organism in this part of the world. With the exception of
CO, any morphologic form of onychomycosis can be
caused by more than one organism, and it is not possible
to identify the causative fungus by merely looking at the
diseased nail. Conversely, a single pathogen can give rise
to more than one clinical pattern of nail involvement.
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Aging

Close to three decades have been added to life expectancy at birth worldwide since the turn
of the century. There are currently about 580 million people in the world aged 60 years and
over, and this figure is expected to rise to over 1000 million within the next 20 years—a
75% increase in that age group compared to a less than 50% increase in the world’s
population as a whole. By 2020 approximately 70% of the elderly population will be living
in developing countries. These changes represent an unprecedented demographic revolution
and require the immediate attention of policy-makers worldwide. Compared with the speed
at which populations in the developing world are ageing at present, the process in
industrialized countries was much slower. It took 115 years in France for the proportion of
older persons to rise from 7% to 14%, whereas in countries such as China, Brazil and
Thailand, the same doubling will occur in the next 20 years. Concurrently, today’s oldest
populations will age further, the very old (aged 75 and over) being the population subgroup
that will increase the most in virtually all industrialized countries.
What is an extraordinary achievement for this century will be one of the great challenges
for the next: ensuring the quality of life of an unprecedentedly large elderly population.
Central to this challenge is health, which is seen in rich and poor societies alike as the most
valuable asset for a good quality of life, particularly in one’s later years.

From Kalache A. Active ageing makes the difference. Bull World Health Org 1999, 77: 299.

© 1999 Blackwell Science Ltd International Journal of Dermatology 1999, 38, 591–595