|Year : 2015 | Volume
| Issue : 2 | Page : 153-158
|Clinico-mycological study of dermatophyte toenail onychomycosis in New Delhi, India
Pravesh Yadav1, Archana Singal1, Deepika Pandhi1, Shukla Das2
1 Department of Dermatology and STD, University College of Medical Sciences and Guru Teg Bahadur Hospital, University of Delhi, Delhi, India
2 Department of Microbiology, University College of Medical Sciences and Guru Teg Bahadur Hospital, University of Delhi, Delhi, India
|Date of Web Publication||3-Mar-2015|
B-14, Law Apartments, Karkardooma, Delhi - 110 092
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Introduction: There is a constant need to define the epidemiological and mycological characteristics of onychomycosis (OM) for optimal management strategies. Objectives: To define the epidemiological and mycological characteristics of patients with dermatophyte toenail OM in a tertiary care hospital. Materials and Methods: Hundred consecutive patients of KOH and culture-positive dermatophyte toenail OM were subjected to detailed history, clinical examination and investigations. Results: Maximum number of patients (40%) belonged to 31-45 years age group and there was a male preponderance (M:F = 6.7:1). The mean duration of disease was 54 months. Thirty-three patients had fingernail involvement in addition to the toenail OM and 37% had co-existent cutaneous dermatophyte infection. Discoloration was the most common symptom (98%). Ninety-four (94%) patients had distal lateral subungual onychomycosis (DSLO) while two had superficial onychomycosis (SO) and only one had proximal superficial onychomycosis (PSO). Trichophyton interdigitale was the most common etiological agent (61%) followed by Trichophyton rubrum and Trichophyton verrucosum. Conclusions: Toenail OM is more common in males. DSLO was the most common clinical variant and T. interdigitale the most common etiological fungus responsible for toenail OM in our region. The importance of early diagnosis and treatment is highlighted as long-standing toenail OM predisposes to fingernail onychomycosis and recurrent tinea pedis.
Keywords: Delhi, dermatophyte, epidemiology, India, onychomycosis, toenail
|How to cite this article:|
Yadav P, Singal A, Pandhi D, Das S. Clinico-mycological study of dermatophyte toenail onychomycosis in New Delhi, India. Indian J Dermatol 2015;60:153-8
|How to cite this URL:|
Yadav P, Singal A, Pandhi D, Das S. Clinico-mycological study of dermatophyte toenail onychomycosis in New Delhi, India. Indian J Dermatol [serial online] 2015 [cited 2019 Jun 25];60:153-8. Available from: http://www.e-ijd.org/text.asp?2015/60/2/153/152511
What was known?
- The incidence of onychomycosis is on a rise with a considerable variation according to geographical location and time.
- Dermatophytes are the most frequently implicated agents, Trichophyton rubrum being the most common from Delhi.
- Correct etiological diagnosis of onychomycosis important in deciding the best antifungal agent warranted in a particular case.
| Introduction|| |
Onychomycosis (OM) denotes infection of nails caused by dermatophyte fungi, non-dermatophyte fungi or yeast and represents about 30% of cutaneous mycotic infections. It is the most common nail disease and accounts for approximately 50% of all onychopathies.  Various factors including age, trauma, sports activity, diabetes, HIV, poor peripheral circulation, occupation and climate influence the prevalence, etiology, progression and treatment outcome of OM. It can be caused by dermatophytes, yeasts (Candida albicans) and non-dermatophyte molds (NDM) (Acremonium, Aspergillus, Fusarium, Onychocola canadensis, Scopulariopsis brevicaulis, Scytalidium dimidiatum). Dermatophytes are the most frequently implicated agents and out of these Trichophyton rubrum and Trichophyton interdigitale (formerly Trichophyton mentagrophytes var interdigitale) are responsible for nearly 90% of toenail and at least 50% fingernail OM.  However, there is a considerable variation according to geographical location and time.
Several clinical types of OM have been recognized and recently a new classification has been proposed by Hay et al. comprising of primary and secondary OM. Primary includes clinical variants like distal lateral subungual onychomycosis (DLSO), superficial onychomycosis (SO), endonyx onychomycosis (EO), proximal subungual onychomycosis (PSO), mixed pattern onychomycosis (MPO) and total dystrophic (TDO).  Diagnosis is primarily based upon KOH examination, culture and histopathological examination of nail clippings or nail biopsies. Relapse of OM depends on several factors, including genetic predisposition,  reduced nail growth rate in elderly  and underlying disease e.g., psoriasis,  peripheral vascular diseases, diabetes,  immunosuppression, HIV infection,  and cigarette smoking.  Choice of treatment is based upon factors like patient's age, infecting fungus, number and degree of nails involved, co-morbid conditions and possible drug interactions. The correct etiological diagnosis is important in deciding the best antifungal agent warranted in a particular case.
| Materials and Methods|| |
This study comprised of 100 KOH and culture-proven patients of dermatophyte toenail OM. An institutional ethical committee approval was taken. Patients with nail disease attributable to other dermatoses were excluded.
A clinical diagnosis of OM was made on the basis of findings that included whitish or brownish yellow opacities in the nail, subungual hyperkeratosis, dystrophy and/or onycholysis. All patients underwent detailed history pertaining to age, sex, duration and progression of the disease, occupation, history of preceding trauma; co-morbid conditions e.g., diabetes, immune suppression, etc., A thorough clinical examination including systemic examination and cutaneous examination for evidence of co-existent fungal infection in the fingernails and other body part was performed. Nails were examined for number of involved nails, pattern and extent of involvement and findings were recorded in a predesigned proforma.
Clinical diagnosis was confirmed by positive KOH wet mount and isolation of fungus on culture. A specimen was obtained from the most severely affected nail. Site was cleaned with 70% alcohol and full thickness clippings from the discolored, dystrophic, brittle nail (as proximal as possible) were obtained. The specimen collected was examined under direct microscopy and cultured immediately or was placed in a sterile dry container in case of delay. The direct examination was carried out in KOH at 30-40% with glycerine and followed by tube KOH. The remaining specimen was divided and inoculated into specific agar surfaces. Culture media included Sabouraud's dextrose agar with chloramphenicol (0.05 g/l), gentamicin (20 mg/l) and cycloheximide (0.5 g/l) and Dermatophyte Identification Media (DIM). All inoculated tubes were incubated at 25C for optimal growth. In case of growth, an etiological agent was confirmed by the characteristic morphology of the colony and by studying the microscopic appearance of the fungus on Lacto Phenol Cotton Blue (LPCB) mount.
| Results|| |
The age of the study population ranged from 21 to 75 years (mean age 42.4 ± 13.5 years), with maximum patients (40%) belonging to the 31-45 years age group. There was a striking male (87%) preponderance (M:F = 6.7:1). The duration of disease ranged from 3 to 240 months (mean duration 54.1 ± 46.9 months) with 29% having disease duration of more than 5 years. The demographic characteristics of patients are depicted in [Table 1].
Concomitant medications included oral steroids for chronic obstructive pulmonary disease and anti-tubercular therapy for pulmonary tuberculosis in two patients each. Coronary artery disease with or without hypertension was reported by six patients and five of them had diabetes, of which one had poor glycemic control.
Thirty-three (33%) patients had fingernail OM in addition to the toenail involvement and 37 had evidence of co-existent tinea pedis of which two had extensive tinea corporis also. Discoloration was the most common symptom (98%) followed by brittle nails (89%). The average number of infected toenails was 5.4 ± 2.2; 28 (28%) had involvement of at least eight toenails. Single nail involvement was seen in only 3% patients. Thirty-three (33) patients (32 patients with DLSO and 1 with DLSO + SO) complained of pain due to paronychia. Paronychial inflammation was caused by T. interdigitale, T. rubrum and T. verrucosum in 17, 14 and 2 patients, respectively. DSLO was the most common morphological variant seen in 97 followed by SO and PSO in 3 and 2 patients, respectively. Three patients had a combination of DLSO and SO [Figure 1]. T. interdigitale was the most common fungus isolated on culture in 61 patients followed by T. rubrum (34%) and T. verrucosum (5%) [Figure 2]. PSO was caused by T. interdigitale. Though SO was caused by T. rubrum and T. verrucosum, T. interdigitale and T. rubrum were isolated in mixed pattern DLSO and SO in one patient each [Table 2].
|Table 2: Correlation between clinical type of onychomycosis and the causative fungi |
Click here to view
There was no significant correlation between the causative dermatophyte isolated and clinical type of OM, age and sex of the patient, fingernail involvement and presence of tinea infection at other body sites.
| Discussion|| |
The incidence of OM is on the rise because of several predisposing factors such as ageing population leading to increase in chronic health problems such as diabetes and poor peripheral circulation; an increase in the number of immunocompromised persons because of HIV infection and immunosuppressive therapies, antibiotics, avid sports participation leading to increasing use of health clubs, communal swimming pools and occlusive footwear for exercise. It is thus important to understand the epidemiology of OM in a particular population.
The prevalence of OM is known to increase with age  but of late various studies from India and worldwide have shown a lower mean age of 41.35 years,  29.40 years  and 34.96 years. , Consistent with this, the mean age of the study population was 42.4 years in our study and 40% of the patients belonged to the age group of 31-45 years. Similar observation of predominance of patients in the younger age groups has been reported in different studies from west  as well as India. ,,, The higher incidence of toenail OM in younger population could be attributed to the higher exposure of occupation and sports related trauma and use of occlusive footwear. In addition, younger population is usually cosmetically conscious and therefore seeks early and frequent dermatologic consultation. The remarkable male preponderance in toenail OM has been previously reported by Vijaya et al. and has been attributed to the more pronounced outdoor activity in men resulting in higher incidence of trauma and use of occlusive footwear. The mean duration of disease was 54.1 months (approximately 4.5 years) which is significantly lower than that of 8-12.3 years, reported in different studies. ,, The lower mean disease duration in our study could be because of predominance of cosmetically conscious younger population seeking early dermatologic consults for treatment.
Seventeen patients had history of recurrent trauma; all except one being males. Most of them were farmers and laborers making them prone to frequent trauma. This finding is in agreement with studies by Svejgaard et al. (16.9%),  Gupta et al. (13.8%),  and Jesudanam et al. (11.3%).  Diabetes was present in 5% cases in the present study. Diabetes is a known risk factor for OM predominantly due to its effect on microcirculation. Similar association has been found in studies from France (5%)  and Denmark (6.7%)  and New Delhi, India (3.9%)  On the other hand, a higher prevalence (20% and 11.8%) of diabetes in OM has been reported from Southern Indian states. , Association of OM with peripheral vascular disease has also been documented previously. ,, OM secondary to steroid-induced immune suppression was found in three patients though HIV screening has not been routinely recommended in patients of OM. An association with immunosuppression (1%) has also been reported by Guibal et al. Significant family history of OM in 26% and 7% has been reported by Gupta et al. and Kaur et al., respectively. , In our study, only one patient had family history of OM and this could be explained by the high number of male migrant laborers in the study who are staying away from home. Moreover, they may be unaware of the presence of this relatively asymptomatic and benign disease in other family members.
Most of the clinico-mycological studies have included the patients with OM involving both toenails and fingernails and have taken into account OM caused by dermatophytes as well as yeast and NDM. Thirty-three (33%) patients in our study had coexisting OM of fingernails. T. interdigitale was the most common isolate seen in 20/33 patients followed by T. rubrum (11/33) and T. verrucosum (2/33). In most of these patients, fingernail involvement followed toenail infection that could have been a source of infection. Few patients had fingernail involvement preceding the toenails where the reverse could be true. Thirty-seven patients (37%) in our study had evidence of cutaneous fungal infection elsewhere in the body. T . interdigitale was the most common isolate seen in 24/37 patients followed by T. rubrum (11/37) and T. verrucosum (2/37). This aspect has not been studied in the previous studies. This was more common in patients who had extensive and long-standing disease. One patient with extensive tinea corporis had poorly controlled diabetes. In most of patients, toenail infection preceded tinea pedis.
Discoloration was the most common symptom (98%), followed by brittle nails (89%). Pain was reported by 33 patients (33%) and these patients had evidence of paronychial inflammation. Kaur et al. have reported the occurrence of discoloration in 100% of patients and pain in 17% of patients, while Gupta et al. reported the occurrence of discoloration in 92% of patients. Clinical examination forms an important part of the management in OM. It has been suggested that appropriate antifungal therapy should be started without waiting for test results when dermatologists consider OM as the most probable diagnosis in the presence of plantar desquamation because under such circumstances clinical diagnosis is at least as accurate as laboratory tests. 
Studies referring to the clinico-mycological profile of patients with dermatophyte toenail OM are lacking. In our study, DSLO pattern was seen in 94 patients, SWO in 2 and PSO in 1 patient. DLSO was the most common pattern caused by all the three fungi. One case each of SWO was caused by T. rubrum and T. verrucosum. PSO was caused by T. interdigitale. Three patients had a combination of DLSO and SWO; of these two cases were due to T. interdigitale while T. rubrum was isolated from the third patient. In a study from New Delhi, T. rubrum was the most common etiological fungus for DLSO and the only etiological agent for PSO. In this study, T. interdigitale was isolated from two cases of SWO. 
The most common isolated fungus was T. interdigitale (61%), followed by T. rubrum (34%) and T. verrucosum (5%). This was in contrast to the commonly reported prevalence of dermatophytic fungi in OM reported in various Indian studies [Table 3] and worldwide [Table 4]. Average number of infected nails in the study patients was 5.59. It was similar (5.4) to that reported by Jary et al. Twenty-five of the 76 patients studied (32.9%) had involvement of ≥ 8 nails. Thirty-two percent patients had involvement of ≤ 4 nails.  Number of nails involved was ≤ 5 nails in 57.6% of patients in a study by Gupta et al.
|Table 3: Prevalence of various dermatophytic species causing onychomycosis in different parts of India |
Click here to view
|Table 4: Prevalence of various dermatophytic species causing onychomycosis in different parts of world |
Click here to view
Previous studies from Delhi published in 2008 have reported T. rubrum to be the most common etiological fungus for OM. , However, we found T. interdigitale to be the most commonly isolated species in our study. This indicated that there is a continuous change in the epidemiological and mycological characteristics of OM in the same population as well as the geographical region. Therefore, it is imperative to be aware of these changing patterns and causative fungi for making adequate strategies for prevention and treatment of this infection.
| References|| |
Verma S, Hefferman MP. Superficial fungal infection. In: Wolff K, Goldsmith LA, Katz SI, Gilchrest BA, Pallar AS, Leffell DJ. editors. Fitzpatrick's Dermatology in General Medicine. 7 th
ed. New Delhi: McGraw Hill; 2008. p. 1817.
Elewski BE. Onychomycosis: Pathogenesis, diagnosis and management. Clin Microbiol Rev 1998;11:415-29.
Hay RJ, Baran R. Onychomycosis: A proposed revision of the clinical classification. J Am Acad Dermatol 2011;65:1219-27.
Zaias N, Tosti A, Rebell G, Morelli R, Bardazzi F, Bieley H, et al
. Autosomal dominant pattern of distal subungual onychomycosis caused by Trichophyton rubrum. J Am Acad Dermatol 1996;34:302-4.
Orentreich N, Markofsky J, Vogelman JH. The effect of aging on the rate of linear nail growth. J Invest Dermatol 1979;73:126-30.
Larsen GK, Haedersdal M, Svejgaard EL. The prevalence of onychomycosis in patients with psoriasis and other skin diseases. Acta Derm Venereol 2003;83:206-9.
Gupta AK, Konnikov N, MacDonald P, Rich P, Rodger NW, Edmonds MW, et al
. Prevalence and epidemiology of toenail onychomycosis in diabetic subjects: A multicentre survey. Br J Dermatol 1998;139:665-71.
Gupta AK, Taborda P, Taborda V, Gilmour J, Rachlis A, Salit I, et al
. Epidemiology and prevalence of onychomycosis in HIV-positive individuals. Int J Dermatol 2000;39:746-53.
Gupta AK, Gupta MA, Summerbell RC, Cooper EA, Konnikov N, Albreski D, et al
. The epidemiology of onychomycosis: Possible role of smoking and peripheral arterial disease. J Eur Acad Dermatol Venereol 2000;14:466-9.
Svejgaard EL, Nilsson J. Onychomycosis in Denmark: Prevalence of fungal nail infection in general practice. Mycoses 2004;47:131-5.
Gupta M, Sharma NL, Kanga AK, Mahajan VK, Tegta GR. Onychomycosis: Clinico-mycologic study of 130 patients from Himachal Pradesh, India. Indian J Dermatol Venereol Leprol 2007;73:389-92.
Garg A, Venkatesh V, Singh M, Pathak KP, Kaushal GP, Agrawal SK. Onychomycosis in central India: A clinicoetiologic correlation. Int J Dermatol 2004;43:498-502.
Kaur R, Kashyap B, Bhalla P. A five-year survey of onychomycosis in New Delhi, India: Epidemiological and laboratory aspects. Indian J Dermatol 2007;52:39-42.
Bokhari MA, Hussain I, Jahangir M, Haroon TS, Aman S, Khurshid K. Onychomycosis in Lahore, Pakistan. Int J Dermatol 1999;38:591-5.
Agarwalla A, Agrawal S, Khanal B. Onychomycosis in eastern Nepal. Nepal Med Coll J 2006;8:215-9.
Jesudanam TM, Rao GR, Lakshmi DJ, Kumari GR. Onychomycosis: A significant medical problem. Indian J Dermatol Venereol Leprol 2002;68:326-9.
Sujatha V, Grover S, Dash K, Singh G. A clinico-Mycological evaluation of onychomycosis. Indian J Dermatol Venereol Leprol 2000;66:238-40.
Veer P, Patwardhan NS, Damle AS. Study of onychomycosis: Prevailing fungi and pattern of infection. Indian J Med Microbiol 2007;25:53-6.
Vijaya D, Anandkumar BH, Geetha SH. Study of onychomycosis. Indian J Dermatol Venereol Leprol 2004;70:185-6.
Havu V, Heikkila H, Kuokkanen K, Nuutinen M, Rantanen T, Saari S, et al
. A double-blind, randomized study to compare the efficacy and safety of terbinafine with fluconazole in the treatment of onychomycosis. Br J Dermatol 2000;142:97-102.
Evans EG, Sigurgeirsson B. Double blind, randomized study of continuous terbinafine compared with intermittent itraconazole in treatment of toenail onychomycosis. BMJ 1999;318:1031-5.
Sigurgeirsson B, Olafsson JH, Steinsson JB, Paul C, Billstein S, Evans EG. Long term effectiveness of treatment with terbinafine vs itraconazole in onychomycosis: A 5 year blinded prospective follow up study. Arch Dermatol 2002;138:353-7.
Guibal F, Baran R, Duhard E, Feuilhade de Chauvin M. Epidemiology and management of onychomycosis in private dermatological practice in France. Ann Dermatol Venereol 2008;135:561-6.
Sarma S, Capoor MR, Deb M, Ramesh V, Aggarwal P. Epidemiologic and clinicomycologic profile of onychomycosis from north India. Int J Dermatol 2008;47:584-7.
Kaur R, Kashyap B, Makkar R. Evaluation of clinicomycological aspects of onychomycosis. Indian J Dermatol 2008;53:174-8.
Garcia-Doval I, Cabo F, Monteagudo B, Alvarez J, Ginarte M, Rodríguez-Alvarez MX, et al
. Clinical diagnosis of toenail onychomycosis is possible in some patients: Cross-sectional diagnostic study and development of a diagnostic rule. Br J Dermatol 2010;163:743-51.
Adhikari L, Gupta AD, Pal R, Singh T. Clinico-etiologic correlates of onychomycosis in Sikkim. Indian J Pathol Microbiol 2009;52:194-7.
Lone R, Bashir D, Ahmad S, Syed A, Khurshid S. A study on clinico-mycological profile, aetiological agents and diagnosis of onychomycosis at a government medical college hospital in Kashmir. J Clin Diagn Res 2013;7:1983-5.
Bokhari MA, Hussain I, Jahangir M, Haroon TS, Aman S, Khurshid K, Onychomycosis in Lahore, Pakistan. Int J Dermatol 1999;38:591-5.
Ilkit M. Onychomycosis in Adana, Turkey: A 5-year study. Int J Dermatol 2005;44:851-4.
Agarwalla A, Agrawal S, Khanal B. Onychomycosis in eastern Nepal. Nepal Med Coll J 2006;8:215-9.
Souza LK, Fernandes OF, Passos XS, Costa CR, Lemos JA, Silva MR. Epidemiological and mycological data of onychomycosis in Goiania, Brazil. Mycoses 2010;53:68-71.
Hashemi SJ, Gerami M, Zibafar E, Daei M, Moazeni M, Nasrollahi A. Onychomycosis in Tehran: Mycological study of 504 patients. Mycoses 2010;53:251-5.
Chadeganipour M, Nilipour S, Ahmadi G. Study of onychomycosis in Isfahan, Iran. Mycoses 2010;53:153-7.
Neupane S, Pokhrel DB, Pokhrel BM. Onychomycosis: Clinical pattern and prevailing fungi in Kathmandu. Nepal Med Coll J 2011;13:193-6.
Dias N, Santos C, Portela M, Lima N. Toenail onychomycosis in a Portuguese geriatric population. Mycopathologia 2011;172:55-61.
Dhib I, Fathallah A, Yaacoub A, Zemni R, Gaha R, Said MB. Clinical and mycological features of onychomycosis in central Tunisia: A 22 years retrospective study (1986-2007). Mycoses 2013;56:273-80.
Jary H, Naaber P, Kaur S, Eisen M, Silm H. Toenail onychomycosis in Estonia. Mycoses 2004;47:57-61.
What is new?
- Onychomycosis more commonly presents in male with a predominance of patients in the younger age groups.
- DLSO is the most common pattern and discoloration is the most common symptom of onychomycosis in our region.
- T. interdigitale is the most common dermatophyte, followed by T. rubrum and T. verrucosum causing onychomycosis in our region.
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4]
| Article Access Statistics|
| Viewed||2919 |
| Printed||51 |
| Emailed||0 |
| PDF Downloaded||182 |
| Comments ||[Add] |