|
 
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| ORIGINAL ARTICLE |
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| Year : 2017 | Volume
: 8
| Issue : 2 | Page : 74-81 |
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A clinicomycologic study of onychomycosis at a tertiary health-care center in Chennai
Chandan Ashokan, Aditya Kumar Bubna, Anandan Sankarasubramaniam, Mahalakshmi Veeraraghavan, Sudha Rangarajan, Adikrishnan Swaminathan
Department of Dermatology, Sri Ramachandra University, Chennai, Tamil Nadu, India
| Date of Web Publication | 7-Aug-2017 |
Correspondence Address:
Aditya Kumar Bubna
Department of Dermatology, Sri Ramachandra University, Porur, Chennai - 600 116, Tamil Nadu
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/mjmsr.mjmsr_71_16
Background: Onychomycosis poses to be an important public health problem. There has been a worldwide increase in the prevalence of onychomycosis with factors such as diabetes mellitus, poor peripheral circulation, indulgence in sporting activities, and prolonged antibiotic usage playing major contributory roles. Further, management of fungal infections of nails usually requires a prolonged course with a tendency for relapse. Aim: To study the clinical, epidemiologic, and demographic profile of onychomycosis and determine various organisms responsible for the same. Methods: A cross-sectional study was done over a 1-year period, wherein after patient enrollment, a thorough clinical evaluation was performed, followed by microscopically examining the infected nail specimen under 40% potassium hydroxide, which was succeeded by cultivating the organisms on fungal culture media and identifying the pathogen both by closely studying colony morphology in culture and also microscopically utilizing lactophenol cotton blue staining. Results: Females (67.3%) were more commonly affected than males (32.7%). The most common age group affected was 20-40 years(47%). Majority of patients demonstrated both finger and toe nail involvement (43.6%). Distal and lateral subungual onychomycosis (55.4%) was the most common clinical variant of onychomycosis identified in our study. Out of the 101 patients in our study, 86 demonstrated a positive fungal growth on culture. Non-dermatophyte moulds (NDM) (58.1%) were the most common fungal isolate followed by Candida species (36%) and dermatophytes (5.8%). Conclusion: Unlike most studies, NDM constituted the major pathogen among our participants. Keywords: Candida, dermatophytes, non-dermatophyte moulds, onychomycosis
How to cite this article:
Ashokan C, Bubna AK, Sankarasubramaniam A, Veeraraghavan M, Rangarajan S, Swaminathan A. A clinicomycologic study of onychomycosis at a tertiary health-care center in Chennai. Muller J Med Sci Res 2017;8:74-81 |
How to cite this URL:
Ashokan C, Bubna AK, Sankarasubramaniam A, Veeraraghavan M, Rangarajan S, Swaminathan A. A clinicomycologic study of onychomycosis at a tertiary health-care center in Chennai. Muller J Med Sci Res [serial online] 2017 [cited 2023 Mar 25];8:74-81. Available from: https://www.mjmsr.net/text.asp?2017/8/2/74/212419 |
| Introduction | |  |
Onychomycosis is a general term designated for any fungal nail infection.[1] Although not life threatening, onychomycosis constitutes an important public hazard owing to the impact it could produce on the patients' emotional, social, and occupational functioning.[2] There has been a worldwide increase in the incidence of onychomycosis with factors such as diabetes mellitus (DM), poor peripheral circulation, human immunodeficiency virus, immunosuppressive therapy, cancer chemotherapy, and antibiotic usage contributing significantly in its development.[3] Furthermore, design of the nail apparatus per se allows sequestration of fungal elements in between the nail plate and nail bed, and along with slow growth of the nail plate, multiplication of fungal elements is further enhanced. Our study was done to determine the clinical, epidemiologic, and demographic profile of onychomycosis among our participants and to identify various causative fungi responsible for the same.
| Methods | | |
This was a cross-sectional hospital-based study done in the Department of Dermatology of our institute over a 1-year period. 101 patients who were clinically diagnosed with onychomycosis for the first time and who consented for the study constituted our participants. Patients having any other nail or periungual disease apart from onychomycosis were excluded from our study, thereby making our patient selection highly specific. After a brief history, a detailed clinical examination of the nails was done, and the clinical type of onychomycosis was identified. This was succeeded by specimen collection from the affected nails. After cleaning the specimen site with 70% isopropyl alcohol for each of the clinical types of onychomycosis, the nail material was collected as per the stated guidelines,[4] as follows:
Distal and lateral subungual onychomycosis
Following clipping of the abnormal nail, proximally, the nail bed and the undersurface of the nail plate were scraped with a 1 mm curette. The outermost debris was discarded and the test material was collected from the area most proximal to the cuticle which harbours maximum amounts of fungal elements.
Proximal subungual onychomycosis
The normal surface of the nail plate was pared down at the lunula with a number 15 blade. Following this, a sample of the proximal nail plate and white debris present in the deeper portion of the nail plate was collected.
White superficial onychomycosis
White spots present on the nail plate were scraped and discarded. This was followed by collection of white debris directly beneath these white spots.
Total dystrophic onychomycosis
Any abnormal area of the nail plate or nail bed was used here.
Once the specimen was collected, it was placed on an autoclaved black chart paper. A part of the specimen was sent for 40% potassium hydroxide (KOH) microscopic examination, and the remaining for fungal cultures on Sabouraud's dextrose agar (SDA) plain, SDA with chloramphenicol, and SDA with chloramphenicol and cycloheximide. In those patients whose first specimen for 40% KOH examination was negative, the material was once again obtained either from the same nail or from another nail for microscopy, and only after three successive examinations, if still no fungal elements were identifiable, the specimen was labeled negative. For cultures, the specimen was inoculated in each media and incubated at 25*C and 37*C. All cultures in our study were performed on media utilizing test tube slants. The cultures were examined at weekly intervals for colony growth. If no growth was witnessed at the end of 8 weeks, the specimen was discarded. Where growth was observed, based on colony morphology, fungal organisms were identified. In cases where Non-dermatophye moulds (NDM) were identified, the culture was repeated again after 8 weeks on all patients, wherein the first culture sample grew NDM. In these patients, twenty separate nail specimens were obtained from the diseased nail apparatus and separately inoculated onto the culture media. Out of these twenty inocula, if five demonstrated the same NDM in pure culture, the patient was diagnosed as having NDM onychomycosis. Following culture, a lactophenol cotton blue staining was done to further delineate the microscopic characteristics of the causative fungi.
| Results | | |
Our study comprised 101 cases clinically suspected of have onychomycosis. Out of these, 46 (45.5%) had a positive finding by direct microscopy on 40% KOH mount and 86 (85.1%) were culture positive.
In these 101 patients, 68 (67.3%) were females and 33 (32.7%) were males. The most common age group affected was 20–40 years (47%), followed by 41–60 years (42%), 61–80 years (8%), and <20 years (3%). Further active workers such as painters, homemakers, students, and nurses comprised 91 (90.1%) cases whereas the remaining 10 (9.9%) were constituted by retired personnel and people leading a sedentary life style.
Finger nail involvement was demonstrated in 40 (39.6%) patients. Interestingly, all the forty (39.6%) patients were females, thereby making the authors speculate a link with respect to an occupational component for the same. However, the relation between gender and type of nail involvement was not considered statistically significant (P > 0.05) in this study. In 17 (16.8%) patients, only involvement of toe nails was identifiable, out of which 15 (14.9%) were office goers with a history of wearing occlusive footwear and 2 (1.9%) were school teachers. The remaining 44 (43.6%) demonstrated both finger and toe nail involvement, and out of these, 3 (2.9%) had all 20 nails involved. In the three(2.9%) patients who had all the twenty nails involved, a history of working in paddy fields was forthcoming, thereby making us conclude regarding a relationship between onychomycosis and profession with respect to finger and toe nail involvement and also the number of nails involved.
In 35 (34.6%) patients, duration of the disease was <6 months whereas in the remaining 66 (65.3%), the disease duration ranged from 6 months to 24 months.
The most common clinical type of onychomycosis identified was distal and lateral subungual onychomycosis (DLSO) (56, 55.4%) [Figure 1]a, followed by total dystrophic onychomycosis (TDO) (20, 19.8%) [Figure 1]b, DLSO + TDO combination (17, 16.8%), DLSO + proximal subungual onychomycosis (PSO) combination (5, 4.9%), PSO (2, 1.9%) [Figure 1]c, and white superficial onychomycosis (1, 1%) [Figure 1]d. The association between clinical types of onychomycosis and involvement of either finger nails or toe nails was statistically significant (P < 0.05) [Table 1]. | Figure 1: (a) Distal and lateral subungual onychomycosis. (b) Total dystrophic onychomycosis. This case had total black discoloration of all the toe nails. Fungal cultures in this individual demonstrated growth of Aspergillus niger. (c) Proximal subungual onychomycosis. (d) White superficial onychomycosis
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 | Table 1: Clinical types of onychomycosis seen in our study and their sites of involvement
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Out of the specimens taken for KOH evaluation, a positive finding [Figure 2] was detected in 46 (45.5%) patients and the remaining 55 (54.5%) patients did not reveal any findings on KOH mount examination. From the 46 (45.5%) positive specimens on 40% KOH examination, dermatophytes were detected in 4 (3.9%) specimens, yeasts in 17 (16.8%) specimens, and NDM in 25 (24.8%) specimens on culture. From the 55 (54.5%) specimens that were negative on 40% KOH microscopy 25(24.8%) patients were culture positive for NDM, and in these 25(24.8%) specimens staining with lactophenol cotton blue staining further confirmed the causative organism. Among the NDM, Aspergillus niger [Figure 3]a and [Figure 3]b was most common with 29 (33.7%) cases, followed by Aspergillus flavus [Figure 4]a and [Figure 4]b in 4 (4.7%). Fusarium sp. in 3(3.5%) cases [Figure 5] and A. pollulans in 1(1.2%) [Figure 6] and [Table 2]. | Figure 2: Fungal hyphae as observed under 40% potassium hydroxide (×10). Culture revealed Aspergillus flavus in this specimen
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 | Figure 3: (a) Black colonies of Aspergillus niger on Sabouraud's dextrose agar with chloramphenicol and without cycloheximide. (b) Microscopic characteristics of A. niger on lactophenol cotton blue stain (×20)
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 | Figure 4: (a) Yellow-green-colored colonies of Aspergillus flavus on Sabouraud's dextrose agar with chloramphenicol and without cycloheximide. (b) Microscopic characteristics of Aspergillus flavus using lactophenol cotton blue stain (×20)
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 | Figure 5: Fusarium species seen under microscopy using lactophenol cotton blue stain (×20)
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 | Figure 6: Aureobasidium pullulans seen under microscopy using lactophenol cotton blue stain (×20)
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 | Table 2: Various isolates in our study with 40% potassium hydroxide positivity and negativity
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Among the yeasts, Candida tropicalis [Figure 7]a and [Figure 7]b constituted the majority with 13 (14%) cases followed by Candida albicans in 6 (7%) and Geotrichum sp. [Figure 8] in 5 (5.8%) cases [Table 2]. | Figure 7: (a) Growth of Candida tropicalis on Sabouraud's dextrose agar. (b) Microscopic characteristics of Candida species (×20)
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 | Figure 8: Geotrichum species seen under microscopy using lactophenol cotton blue stain (×20)
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Trichophyton mentagrophytes was the most common dermatophyte infection observed in two patients followed by one case each of Tichophyton rubrum, Trichophyton verrucosum and Epidermophyton flocossum [Figure 9] and [Table 2]. | Figure 9: Epidermophyton floccosum seen under microscopy using lactophenol cotton blue stain (×20)
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In 15 (14.9%) patients, there was no growth identifiable on culture.
A significant statistical correlation (P < 0.01) was detected between the type of fungal organism grown and the clinical type of onychomycosis [Table 3].
In 13 (12.9%) patients, DM was present as a comorbidity. Out of them, five (4.9%) patients were diagnosed with Candida sp. as the causative agent for onychomycosis, having involvement of only finger nails and ranging in involvement from five to ten nails in total. Onychomycosis secondary to NDM in these diabetic patients was witnessed in seven (6.9%) patients with A. niger as the causative organism in five (4.9%) patients and A. flavus in two (2%) patients, all of whom had both finger and toe nails involved ranging from 8 to 15 nails. Only one (1%) patient here demonstrated dermatophyte (E. floccosum) onychomycosis that depicted the involvement of two finger nails. Out of these 13 (12.9%) patients, DLSO was the most common type identified in 9 (8.9%) patients, TDO in 2 (2%) patients, and PSO in the remaining 2 (2%) patients.
Fungal infections, in other parts of the body, were identified in seven (6.9%) patients. Tinea cruris was seen in 2 (2%) patients, tinea faciei in 2 (2%) patients, 1 (1%) with tinea corporis (trunk), and the remaining 2 (2%) patients had pityriasis versicolor of the chest.
| Discussion | | |
As onychomycosis is a chronic disorder with frequent relapses, it becomes imperative on the part of the clinician to identify the causative organism. Further, studying its various characteristics also gives an insight to the treating dermatologist with regard to management strategies.
In contrast to most other studies[5],[6],[7],[8],[9],[10],[11],[12],[13],[14] that depicted a male preponderance for onychomycosis, our study demonstrated a female preponderance. Female susceptibility has also been demonstrated in reports by Jesudanam et al.,[15] Bokhari et al.,[16] Banerjee et al.,[17] and Khosravi et al.[18]
Maximum patients in our study belonged to the 20-40 years age group. Higher prevalence in this age group has also been substantiated by other studies.[6],[7],[8],[9],[10],[11],[12],[13],[14],[16],[19] The occurrence of onychomycosis in this age group could be related to trauma following occupational and sporting activities, use of occlusive footwear, and cosmetic awareness. Moreover, in the elderly, even with the presence of this disease, many may not report to a clinician because of its asymptomatic presentation.
Maximum number (43.6%) of our participants had both finger and toe nails involved. This was in contrast to most other studies, wherein dual finger and toe nail involvement was the least.[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[16],[19] In almost all studies, finger nail involvement predominated, except for studies by Gupta et al.[6] and Ilkit,[20] wherein toe nails were majorly involved. The reason for predominance of both finger and toe nail involvement in our study could be linked with the maritime climate associated with high humidity experienced in Chennai in contrast to the continental dry climate found in Iran,[5] New Delhi,[8],[9],[11],[14] Shimla,[6] Pakistan,[16] and Turkey[20] where similar studies were previously performed.
Like all other previous studies,[5],[6],[7],[10],[11],[12],[13],[14],[16] DLSO was the most common clinical type of onychomycosis detected by us. Next in line was TDO, in agreement with findings observed by Grover[7] and Sarma et al.[11] However, Aghamirian and Ghiasian[5] Veer et al.,[13] Lone et al.,[10] and Vinod et al.[12] demonstrated PSO to be the second most common type of onychomycosis in their study, whereas Gupta et al.[6] and Bokhari et al.[16] depicted a higher occurrence of candidal onychomycosis in their study after DLSO.
The association of DM with onychomycosis in our study was 12.9%, almost more than double the association as witnessed in similar studies performed by Yadav et al. (5%),[14] Guibal et al. (5%),[21] Svejgaard and Nilsson (6.7%),[22] and Sarma et al. (3.9%);[11] however, our findings for this association were much less when compared with the results of Vinod et al. (20%)[12] and slightly higher than the values concluded by Jesudanam et al. (11.8%).[15]
In our study, the occurrence of NDM onychomycosis ranked the highest (58.1%). A similar finding with NDM constituting the predominant pathogen has also been reported by Vinod et al.[12] (47.6%). However, in the study conducted by Vinod et al.,[12] no mention has been made regarding the methodology for specimen collection, therefore whether NDM in their study constituted the primary pathogen or just a secondary commensal still remains a question of dispute. In nearly all prior studies, however, dermatophytes were the most common organisms identified followed by Candida and this has been lucidly depicted in [Table 4]. With reference to yeasts as the causative organism for onychomycosis, some authors could speculate it to be a contaminant rather than a pathogen. However, given the pathogenic potential of C. albicans, Candida parapsilosis, C. tropicalis, Candida glabrata, and Candida krusei, it would be apt to consider these isolates as pathogenic,[23] and with the clinical picture of nails symbolic of onychomycosis, institution of prompt therapy for the same is justified. Other organisms such as Geotrichum sp. and Candida kefyr, though not so commonly encountered in previous reports, may require further studies to prove their value as a causative pathogen for onychomycosis. At present, therefore, not much can be stated in this regard. | Table 4: A comparative table depicting various fungal organisms identified on culture with their percentages as detected in previous studies including ours
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Although NDMs are usually secondary commensals, stringent criteria defining NDM as primary pathogens have been stated by English[24] that include:
- KOH-positive filaments on microscopy
- Negative result for dermatophytes. If at all dermatophytes are isolated, they are implicated as the causative pathogen and not NDM
- Isolating NDM in pure culture in at least five of twenty inocula.
In our study, we witnessed that only 25 patients were diagnosed to have NDM onychomycosis as per the stringent criteria stated by English.[24] However, in another 25 patients, NDMs were identified on culture as per the third diagnostic criteria of English as stated above, along with the absence of growth of dermatophytes on culture, thereby also fulfilling the second criteria of English. However, in these patients, fungal hyphae were not demonstrable on 40% KOH microscopy. Based on the stringent criteria suggested by English, it would seem prudent to label these specimens as false positive or whether we could label the negative values obtained under KOH microscopy as false negative is a query which the authors would like to place because cultures certainly are more superior to KOH microscopy when it comes to diagnosing fungal organisms. We therefore would like to address these cases as false negative rather than false positive with the plausible explanation mentioned below.
It has been seen that, owing to the thick and coarse texture of nail debris, presence of hyphae may usually be sparse with the occurrence of false-negative results in approximately 15% of isolations.[3],[25] In our study, however, the occurrence of false-negative values on KOH microscopy was 50%, a value significantly higher when compared to that stated by Elewski.[3],[25],[26] Nevertheless, the authors of the current study do not undermine the role of KOH microscopy as an important screening tool to rule out fungal infection of the nails. However, in instances wherein the clinical findings are highly pathognomonic of onychomycosis and following appropriate nail cleansing with 70% isopropyl alcohol and culturing the same NDM on at least 5 separate inocula of the 20 inoculations on the respective culture media along with visualization of characteristic morphology of NDM on lactophenol cotton blue microscopy, the authors feel it would still be prudent to label NDM as the potential primary pathogen in these cases despite the negative value on KOH microscopy.
| Conclusion | | |
To conclude, in our study, a female preponderance was witnessed with the 20–40 years' age group being maximally affected by onychomycosis. We further reiterate the fact that DLSO is the most common type of onychomycosis encountered. However, unlike most other studies, NDM constituted the major pathogen among our participants. Whether the high levels of humidity observed in Chennai had an instrumental role for the same needs further elucidation.
As far as the defining criteria are concerned, there are certain points that need to be pondered. Whether the absence of a positive finding on KOH microscopy completely rules out NDM as the primary pathogen for NDM onychomycosis needs to be doubly considered given the chances of false-negative values also being encountered, and if at least five inocula of the twenty depict growth of the same NDM followed by visualizing the characteristic fungal morphology on lactophenol cotton blue microscopy and a negative dermatophyte growth in culture, and with clinical findings at par with onychomycosis, the diagnosis of NDM onychomycosis can be concluded with prompt institution of appropriate therapy for patients. Hence, whether a slight modification in the criteria with regard to KOH microscopy given by English[24] needs implementation is something that can be considered.
As there exists a scarcity of literature for the same, more studies in this setting are warranted to further elucidate the conclusion derived by us.
Acknowledgment
The authors would like to thank Dr. Anupma Jyoti Kindo, Professor, Department of Microbiology, Sri Ramachandra University, Porur, Chennai, for her support to the study.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9]
[Table 1], [Table 2], [Table 3], [Table 4]
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