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ORIGINAL ARTICLE
Year : 2016  |  Volume : 17  |  Issue : 2  |  Page : 95-100

Clinico-mycological study of onychomycosis in children from a tertiary care center


1 Department of Dermatology, Sheri Kashmir Institute of Medical Sciences, Srinagar, Jammu and Kashmir, India
2 Department of Pediatrics, Sheri Kashmir Institute of Medical Sciences, Srinagar, Jammu and Kashmir, India
3 Department of Dermatology, Government Medical College, Srinagar, Jammu and Kashmir, India
4 Department of Microbiology, Government Medical College, Srinagar, Jammu and Kashmir, India
5 Department of Pathology, Sheri Kashmir Institute of Medical Sciences, Srinagar, Jammu and Kashmir, India

Date of Web Publication30-Mar-2016

Correspondence Address:
Shazia Jeelani
Department of Dermatology, Sheri Kashmir Institute of Medical Sciences, Bemina, Srinagar, Jammu and Kashmir
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2319-7250.179411

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  Abstract 

Introduction: Onychomycosis is rare in children as compared to adults and hence the presence of any nail changes in children needs careful examination and carrying out proper diagnostic tests to cure this treatable cause of dystrophic nails.
Aim: The study was undertaken to study in detail the clinico-mycological aspects of onychomycosis in children.
Materials and Methods: A
prospective hospital-based cross-sectional study was done on ninety children with a strong clinical suspicion of onychomycosis during a period of 2 years. All the children were subjected to three diagnostic tests, namely direct microscopy, fungal culture, and histopathological examination using periodic acid Schiff staining (HPE-PAS).
Results: Distal and lateral subungual onychomycosis is the most common type (82%), and toe nails (57.78%) are more commonly involved than fingernails. Direct microscopy yielded results in 62%, culture in 64%, and HPE-PAS in 71.1%. Dermatophytes were the most common group of organisms isolated (58%) with Trichophytonmentagrophytes as the most common isolate (31%). However, nondermatophytic molds and Candida species also accounted for 25% and 17% of the culture positive cases in children.
Conclusion: As children <18 years constitute one-third of our population, we suggest the need for careful evaluation of onychomycosis in this subgroup.

Keywords: Children, dermatophytes, onychomycosis


How to cite this article:
Jeelani S, Lanker AM, Jeelani N, Ahmed QM, Fazili T, Bashir H. Clinico-mycological study of onychomycosis in children from a tertiary care center. Indian J Paediatr Dermatol 2016;17:95-100

How to cite this URL:
Jeelani S, Lanker AM, Jeelani N, Ahmed QM, Fazili T, Bashir H. Clinico-mycological study of onychomycosis in children from a tertiary care center. Indian J Paediatr Dermatol [serial online] 2016 [cited 2019 Aug 23];17:95-100. Available from: http://www.ijpd.in/text.asp?2016/17/2/95/179411


  Introduction Top


Onychomycosis is the fungal infection of nails caused by dermatophytes, yeasts, or nondermatophytic molds (NDM). It accounts for half of all the nail disorders and hence most common nail disease in adults. Studies have shown that prevalence of onychomycosis increases with age.[1] Pediatric onychomycosis is rare, with an approximate worldwide prevalence in children below the age of 18 years of <0.5%.[2] However, prevalence in adolescents aged 12–17 years has been reported to be 3.4% in various studies.[3] Differential diagnosis of dystrophic nails in children is varied and hence care should be taken when diagnosing onychomycosis in children, as the sole clinical appearance is not enough to establish a diagnosis and laboratory evidence is always necessary.


  Materials and Methods Top


A prospective, hospital-based, cross-sectional study was conducted on ninety children with a high degree of suspicion of onychomycosis attending the Department of Dermatology of a tertiary care hospital over a period of 2 years. Informed consent was taken from the parents. Clinical details were collected from all the children. Demographic details, pertinent history including chief complaints, duration, fungal infection elsewhere on body, family history of fungal infections, and associated disorders were recorded. Detailed nail examination including the site involved and morphological type was recorded for each case. Clinically, cases were classified into following morphological types: Distal and lateral subungual onychomycosis (DLSO), superficial white onychomycosis, proximal subungual onychomycosis, and total dystrophic onychomycosis.

Thorough cleansing of the nail area was done with spirit swab before collecting the nail scrapping along with the attached subungual debris by the use of scalpel blade without causing much discomfort to the patient. Sample was divided into two equal portions: One portion for direct microscopy and the remainder for culture.

The sample for direct microscopy was mounted in a solution of 20% potassium hydroxide (KOH) +40% dimethysulphoxide. The softened material was covered by coverslip and examined under low as well as high power of microscope for the presence of fungal elements.

Fungal cultures were obtained by inoculating the sample on Sabouraud's dextrose agar (without cycloheximide) and dermatophyte test medium (with cycloheximide and phenol red as indicator) at room temperature incubation for a period of about 2–4 weeks. Growth if any was identified by cultural characteristics and wet mount microscopy with lactophenol cotton blue stain.

Histopathological examination of nails was also done using periodic acid-Schiff stain (HPE-PAS). Nail clippings along with the attached subungual debris were collected with the use of standard nail clippers in a manner described by Hull et al. without any prior softening.[4] The presence of intensely stained reddish dots or thread-like structures in between the cells of the nail plate was considered to be a positive result.

Criteria for diagnosing onychomycosis: “Clinical morphological findings of onychomycosis and at least one positive test result.”


  Results Top


During a period of 2 years, ninety children who reported to the hospital with a high degree of clinical suspicion of onychomycosis were included in this study. Age of the patients ranged from 6 months to 18 years with a mean of 12.84 ± 4.09 years [Table 1]. Pediatric onychomycosis occurred more commonly in children ≥12 years of age (58 out of ninety, 64.44%). Male to female ratio was 0.7:1 with the predominance of female patients (53 vs. 37). Onychomycosis was more common in children from rural areas (56 children, 62.2%) than urban areas (34 children, 37.8%). In the pediatric age group, the usual duration of disease was 1 year or less (in 52 children, 57.78%). Only 9 children had a duration of disease >5 years. [Figure 1] depicts line diagram representation of the duration of the disease in years.
Table 1: Distribution in relation to age of children with onychomycosis

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Figure 1: Line diagram showing the duration of onychomycosis in children in years

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All the children came to the hospital with the chief complaint of discoloration of nails. Pain and paronychia were seen in 2% and 13% of children, respectively. History of trauma was elicited in 24 children (27%). Family history of fungal infection was seen in 32 cases (35.6%).

Five children had the significant associated medical history present. There was one patient with autoimmune polyglandular syndrome on replacement, one patient with bronchial asthma on oral steroids, one patient of nephrotic syndrome on systemic steroids, one infant of chronic mucocutaneous candidiasis, and one patient with palmoplantar psoriasis.

Coexisting fungal infection anywhere else in the body was found in 38 cases [Table 2]. Tinea pedis alone accounted for 29 cases with concomitant fungal infection.
Table 2: Coexisting fungal infection in children with onychomycosis

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Among ninety children, 45 had toenail involvement, 38 had fingernail involvement, and 7 had both toe and fingernail involvement. Overall, toenail involvement was seen in more than half of children (52 children, 57.78%).

The DLSO was the most common morphological type of onychomycosis in 82.2%. [Figure 2] shows the percentage of various morphological subtypes. [Figure 3] shows the various morphological types of onychomycosis seen.
Figure 2: Different morphological types of onychomycosis seen in children

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Figure 3: (a) Distal and lateral subungual onychomycosis in a 5-year-old child. Black discoloration with subungual hyperkeratosis on the right distal thumbnail. (b) Total dystrophic onychomycosis in a 6-month-old child having chronic mucocutaneous candidiasis

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Direct microscopy yielded results in 56 cases (62%), culture in 58 cases (64%), and HPE-PAS stain in 64 cases (71.1%). On culture, NDM grew as contaminants in ten cases which were negative on direct microscopy and did not yield growth on subinoculation [Table 3].
Table 3: Different diagnostic tests used for evaluating onychomycosis in children

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Hence, 48 culture positive causative fungi were isolated with dermatophytes as the major group in 28/48 (58%) and NDM in 12/48 (25%) and Candida in 8/48 cases (17%) each [Figure 4]. [Figure 5] and [Figure 6] show the gross and microscopic appearance of some of the common isolates obtained on culture. Among the dermatophytes, Trichophytonmentagrophytes was most common isolate in 15 cases followed by Trichophytonrubrum in 9 cases [Table 4].
Figure 4: Percentage of different causative organisms isolated on culture in children with onychomycosis

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Figure 5: (a) Gross colony morphology of Trichophyton mentagrophytes showing a flat white to yellow colony color, with a granular surface and central folding. (b) Gross colony morphology of Trichophyton rubrum. The overall surface is white, sometimes becoming rose on aging. The reverse is typically wine-red

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Figure 6: (a) Lactophenol cotton blue mount of Trichophyton rubrum microconidia on hyphae “birds on a wire” where the pyriform (teardrop shaped) microconidia are attached to the hyphae at the narrow end (tail) (×400). (b) Lactophenol cotton blue mount of Aspergillus fumigatus showing spherical conidiophores (×400)

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Table 4: Causative fungi in children with onychomycosis

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Among the NDM, Scytalidium was most common isolate in 5 cases followed by Scopularis,Aspergillus, and Trichosporon in 2 each and Fusarium in one case.


  Discussion Top


For pediatric onychomycosis, age standard of 18 years has been set.[5],[6],[7],[8],[9],[10] In this study, all the children <18 years, with strong clinical suspicion of onychomycosis were included.

Onychomycosis in children is rare. In a study in 1997, Gupta et al. found a prevalence of 0.44% in children.[10] This study also summarized studies around the world and found a prevalence of 0.35%. Low prevalence in children is due to faster nail growth, smaller surface area available for exposure to causative fungi, lack of cumulative trauma, and reduced environmental exposure to public places that harbor high densities of infective hyphae and spores.[5],[6],[7],[10] Though in this study, prevalence of onychomycosis was not investigated upon.

Adolescents between age group of 12–18 comprised the single largest class of onychomycosis (58 cases, 64.44%) as has been reported by Lange et al. and Kim et al.[8],[11] A case series study from Peru reports, in fact, a prevalence of onychomycosis in adolescents aged 12–17 years of 3.4%.[12] In fact, only three children under the age of 3 years had onychomycosis in our study population. Piraccini et al. in their review article have also suggested that the prevalence of onychomycosis increases with child age, with higher frequency above the age of 12 years, cases in infants however occur.[2],[13]

Onychomycosis was more in girls than boys in our study. This is however incoherent with studies of Lateur et al.,[5] however, some authors have reported that sex did not seem to be a risk factor for onychomycosis, in contrast to some previous reports. In this study, onychomycosis was more prevalent in children from rural areas, this agrees with the studies by Rodríguez-Pazos et al.[9] because of less health care facilities and more of environmental exposure in rural areas.

In adults, onychomycosis has asymptomatic and indolent course and persisted for 5–10 years before diagnosis as observed by Ramesh et al.[14] However, duration of the disease at the time of presentation was 1 year or less in most of the children (52 cases, 57.78%). The reasons why onychomycosis is less persistent is due to increased awareness of parents, early treatment, screening in schools, and faster clearance of infection due to faster growth rate of nails.

Our study showed that 26.7% of children had a significant family history of fungal infection. Any family history of tinea pedis or onychomycosis is thought to be a potential source of onychomycosis infection [6],[8],[9],[10],[13],[15] and this study identified such a relationship.

Thus, it may be necessary to evaluate family members for fungal infection to decrease the chance of reinfection. Rebell and Zaias showed that onychomycosis due to anthropophilic dermatophytes such as T. rubrum are familial due to a genetic predisposition to the infection inherited in an autosomal dominant manner.[16]

Coexisting fungal infection in other parts of the body was seen in 38 cases with tinea pedis (29 cases) accounting for most of them. In most of the studies, tinea pedis has been shown to be the most common concurrent disease with onychomycosis, especially toenail onychomycosis.[8],[9],[10]

Toenail infections comprised a higher proportion of the overall onychomycosis.

Fifty-two of the children (57.8%) had toenail onychomycosis, this agrees with the findings of most of the other workers.[5],[9],[10]

In our study, DLSO was the most common morphological type found in 82% of children finding consistent with reported results.[5],[8],[9],[10],[17]

Direct microscopy using KOH yielded results in 62%, culture in 64%, and HPE-PAS stain in 71.1%. Higher sensitivity has been reported for histopathology by various workers.[18],[19],[20]

In this study, dermatophytes were isolated in 28 out of 48 culture positive confirmed cases of onychomycosis (58.33%). These observations show that dermatophytes are the major etiological agents causing onychomycosis, and this fact has been established by previous studies by other workers.[6],[7],[8],[9],[10]

The most common isolate obtained in our study was T. mentagrophytes in 15 cases (31%). Yadav et al. have also reported T. mentagrophytes as the most common isolate in their studies.[21] However, most other workers such as Gupta et al. and Kim et al.[10],[11] have described T. rubrum as a most prevalent pathogen in pediatric onychomycosis. The high rate of isolation of T. mentagrophytes can be explained on the basis that in our study large number of the cases were associated with interdigital variety of tinea pedis caused mainly by T. mentagrophytes var. interdigitale. T. rubrum (9 cases, 19%) was the second most common isolate in our study.

There were 8 cases of Candida species (17%) in the confirmed cases of onychomycosis. Predisposing factors to Candida onychomycosis are all types of immunodeficiencies including incomplete development of the immune system in premature newborns, chronic mucocutaneous candidiasis, and iatrogenic immunodeficiencies.[22] Furthermore, in this study, 3 out of 4 samples from the immunocompromised patients grew Candida on the fungal cultures.

It is known that T. rubrum, T. mentagrophytes, and Candida species are the main causative pathogens of onychomycosis in children [5],[6],[7],[8],[9],[23] and our study reflects these past findings.

The nondermatophytes could be isolated in 22 cases; however, only 12 cases and 25% were causative. The prevalence of nondermatophyte onychomycosis reported from other parts of the World and India is variable.[24] Moreno and Arenas found that nondermatophyte onychomycosis account for 2–12% of all nail fungal infections and can be caused by a wide range of fungi, mainly Scopulariopsis brevicaulis and Aspergillus species.[25]


  Conclusion Top


To conclude, pediatric onychomycosis has to be suspected in the diagnosis of dystrophic nails in children and careful mycological examination in the form of direct microscopy, culture, and histopathology of nail clippings should be undertaken to identify onychomycosis in this particular age group which have different characteristics from that of the adult population.

Financial Support and Sponsorship

Nil.

Conflicts of Interest

There are no conflicts of interest.

 
  References Top

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Flores JM, Castillo VB, Franco FC, Huata AB. Superficial fungal infections: Clinical and epidemiological study in adolescents from marginal districts of Lima and Callao, Peru. J Infect Dev Ctries 2009;3:313-7.  Back to cited text no. 3
    
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Lateur N, Mortaki A, André J. Two hundred ninety-six cases of onychomycosis in children and teenagers: A 10-year laboratory survey. Pediatr Dermatol 2003;20:385-8.  Back to cited text no. 5
    
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Kim DM, Suh MK, Ha GY. Onychomycosis in children: An experience of 59 cases. Ann Dermatol 2013;25:327-34.  Back to cited text no. 11
    
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Rebell G, Zaias N. Tinea pedis: The child and the family. Pediatr Dermatol 1999;16:157.  Back to cited text no. 16
    
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Wilsmann-Theis D, Sareika F, Bieber T, Schmid-Wendtner MH, Wenzel J. New reasons for histopathological nail-clipping examination in the diagnosis of onychomycosis. J Eur Acad Dermatol Venereol 2011;25:235-7.  Back to cited text no. 20
    
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Moreno G, Arenas R. Other fungi causing onychomycosis. Clin Dermatol 2010;28:160-3.  Back to cited text no. 25
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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