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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 5  |  Issue : 1  |  Page : 85-91

Varying trends in geographical distribution and patterns of dermatophytosis and its antifungal susceptibility: A descriptive cross-sectional study in a tertiary care hospital of South India


1 Department of Dermatology, Raja Rajeswari Medical College and Hospital, Bengaluru, Karnataka, India
2 Department of Microbiology, Raja Rajeswari Medical College and Hospital, Bengaluru, Karnataka, India

Date of Submission23-Mar-2020
Date of Decision03-Jun-2020
Date of Acceptance04-Jun-2020
Date of Web Publication19-Feb-2021

Correspondence Address:
Yadalla Hari Kishan Kumar
70, Padma Nivasa, 3rd Cross, Mg Ext. Hv Halli, Raja Rajeswari Nagar, Bengaluru - 560 098, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/CDR.CDR_64_20

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  Abstract 


Background: Dermatophytosis is seen worldwide, causing severe physical, mental, and psychosocial morbidity to the patient. Owing to indiscriminate, inadequate and irregular use of various drugs, cases of anti-fungal resistance have emerged in recent times, leading to ineffective treatment needing multiple drugs over longer treatment durations. Hence, this study was taken up to evaluate the changing geographical trends in the clinico-mycological profile of dermatophytosis and its antifungal susceptibility patterns. Materials and Methods: Two hundred and eleven patients with clinically diagnosed dermatophytosis were evaluated with history, examination followed by a Potassium Hydroxide wet mount. Skin scrapings were also taken for fungal culture and antifungal susceptibility tests against ten commonly used antifungal agents using the Broth Microdilution method as per CLSI M38-A2 guidelines. Results: Tinea incognito was the most common presentation, and Trichophyton rubrum was the predominant dermatophyte isolated. Recurrent dermatophytosis was seen in 11.84% subjects. Terbinafine was the most effective systemic agent, while Luliconazole was the most effective topical agent. Itraconazole and Luliconazole were the most effective systemic and topical agents, respectively, at their lowest minimum inhibitory concentrations inhibiting T. rubrum isolates in vivo. Fluconazole, followed by Griseofulvin, showed the least efficacy. In vitro microbiological resistance to Griseofulvin was found in 15.3% of cases (P < 0.00001). Conclusion: The rapidly evolving geographical trends in clinico-epidemiological profiles of dermatophytosis and its varying antifungal susceptibility patterns highlight the need for updating the knowledge of this disease in the global scenario as well as counseling the rural populations with behavioral and lifestyle modifications.

Keywords: Antifungal susceptibility testing, dermatophytes, recalcitrant dermatophytosis, tinea incognito


How to cite this article:
Kashyap P, Kishan Kumar YH, Belliappa P R, Prakash R. Varying trends in geographical distribution and patterns of dermatophytosis and its antifungal susceptibility: A descriptive cross-sectional study in a tertiary care hospital of South India. Clin Dermatol Rev 2021;5:85-91

How to cite this URL:
Kashyap P, Kishan Kumar YH, Belliappa P R, Prakash R. Varying trends in geographical distribution and patterns of dermatophytosis and its antifungal susceptibility: A descriptive cross-sectional study in a tertiary care hospital of South India. Clin Dermatol Rev [serial online] 2021 [cited 2021 Jul 25];5:85-91. Available from: https://www.cdriadvlkn.org/text.asp?2021/5/1/85/309774




  Introduction Top


Dermatophytes are keratinophilic filamentous fungi capable of causing chronic infections of hair, nails and skin. They represent around 39 closely related species in three genera, namely Trichophyton, Microsporum, and Epidermophyton.[1] Infection of keratinized tissue caused by these fungi is called dermatophytosis, which is among the most common public health problems in hot and humid tropical countries like India. Although these infections are superficial, these fungi can also behave in an invasive manner, causing deeper and disseminated infection, especially in immunocompromised patients.?[2]

Owing to several factors such as indiscriminate, inadequate and irregular use of various drugs, antifungal drug resistance has emerged as a major public health concern in recent times along with changing trends in the clinico-epidemiological profile, thereby leading to ineffective treatment needing multiple drugs over longer treatment durations.[3] Despite anti-mycotic drug resistance emerging as a serious issue in India, specific data on this subject in the clinical scenario are limited. Very few studies are available that address this issue in detail in a large population studying the susceptibility patterns seen for commonly used anti-fungal drugs.

In this study, we attempted to identify and assess the changing geographical trends in clinico-epidemiological profiles of dermatophytosis and its antifungal susceptibility patterns, which would, in turn, contribute to the more effective management of these conditions in the present global scenario as well as tropical countries.


  Materials and Methodology Top


After obtaining Ethics committee approval from the Institutional Ethics committee, RXXXH-IEC/34/2018-19 dated October 28, 2017, a descriptive cross-sectional study was conducted over 18 months from December 2017 to May 2019, in a rural tertiary care hospital of south India. A sample size of 211 subjects attending the out-patient department of Dermatology were included. The study included subjects of all age groups and any gender with clinically diagnosed dermatophytosis involving the skin. Any subjects with the history of use of antifungal agents in the preceding 4 weeks were excluded.

After acquiring informed written consent, each subject was evaluated with a detailed history and physical examination. A semi-structured questionnaire was used to collect relevant information, followed by a collection of skin scrapings for wet mount using 10% potassium hydroxide (KOH) to look for refractile filamentous hyphae [Figure 1]. Irrespective of positive or negative direct microscopy results, fungal culture was done on Sabouraud's Dextrose Agar. The species were identified based on the morphological features of the culture colonies, hyphal structures, and micro-/macro conidia using Lactophenol Cotton Blue Stain [Figure 2] and [Figure 3].
Figure 1: Potassium hydroxide mount showing filamentous hyphae of dermatophytes (×40)

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Figure 2: Lactophenol cotton blue stain showing hyphae and conidia of Trichophyton rubrum (×40)

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Figure 3: Lactophenol cotton blue stain showing hyphae and conidia of Trichophyton mentagrophytes (×40)

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Anti-fungal sensitivity testing (AFST) was done by Broth microdilution method (MD) as per CLSI M38-A2 guidelines to find the minimum inhibitory concentration (MIC) of each drug for the test fungal isolates.[4] Susceptibility of dermatophytes to 10 commonly prescribed anti-fungal drugs were tested, which included systemic drugs such as Terbinafine, Itraconazole, Voriconazole, Griseofulvin, and Fluconazole; and topical drugs such as Ketoconazole, Luliconazole, Sertaconazole, Clotrimazole, and Miconazole.

Anti-fungal agent stock solutions were prepared in Dimethyl Sulfoxide (Sigma Aldrich), except Fluconazole which was prepared in distilled water. The stock solutions were stored in sterile tubes at -70°C. The drug concentrations tested were 0.001–0.5 μg/ml for Itraconazole and Terbinafine, 0.125–64 μg/ml for Griseofulvin and Fluconazole, 0.016–16 μg/ml for Luliconazole and 0.0313–16 μg/ml for Voriconazole, Ketoconazole, Sertaconazole, Clotrimazole, and Miconazole.[5],[6],[7]

To prepare fungal inoculum, isolates were sub-cultured on corn meal agar slants for 1 week at 35°C to produce conidia. Sterile normal saline was added to the agar slant, and the cultures were gently swabbed with a cotton-tipped applicator to dislodge the conidia from the hyphal mat. The suspension was transferred to a sterile tube, and the volume was adjusted to 10 ml with sterile normal saline and centrifuged at 3000 rpm for 5 min. The resulting supernatant adjusted to 0.5 Mc Farland standard was diluted in Roswell Park Memorial Institute (RPMI) 1640 medium (Sigma Aldrich) to the desired concentration.

Sterile round-bottomed 96-well microdilution plates were set up in accordance with the CLSI M38-A reference method [Figure 4]. The drug stock solutions were diluted in RPMI in twice the final concentration followed by addition of an equal volume of the preadjusted inoculum of dermatophyte isolates. Columns 1 through 10 were filled with 100 μl of the inoculum and 100 μl of the serially diluted antifungal agent. Column 11 was filled with 100 μl of the inoculum and 100 μl of media that served as growth control. Column 12 was filled with 200 μl of RPMI medium to serve as a sterility control. Trichophyton rubrum American Type Culture Collection (ATCC) 1546 and Candida parapsilosis ATCC strains were used for quality control. The MD plates were incubated at 35°C for 4 days or until sufficient growth (i.e., confluent hyphal growth covering the bottom of the well) was observed in the control wells containing media without antifungal drugs.
Figure 4: Microtiter plates set up as per CLSI 38 A2 guidelines

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The MIC was defined as the concentration of drug at which the growth of the organism was inhibited up to 80% compared with the growth in the control well.[8] All isolates were run in duplicate, and the results were read visually. MIC50 and MIC90 are defined as the drug concentration that can inhibit the growth of 50% and 90% isolates, respectively.

Data analysis

Data analysis was performed using SPSS for Windows, Version 11.0. (Chicago, SPSS Inc.). Results on quantitative data were presented as Mean ± standard deviation, and results on qualitative data were presented in terms of frequency and percentages. Descriptive tables and graphs were used for a pictorial representation of descriptive data. For categorical data, the ChiSquare test and one-tailed Z-test was used to find the significance of study parameters. With 95% confidence interval, P < 0.05 was considered statistically significant.


  Results Top


[Table 1] represents the clinico-epidemiological findings of dermatophytosis in our study. Tinea incognito was the most common clinical presentation [Figure 5]. Out of all Trichophyton isolates in general, T. rubrum was the most common species at 51.76%, followed by Trichophyton mentagrophytes 21.18%. [Figure 6] shows the various dermatophyte species isolated by culture in our study.
Table 1: Clinico-epidemiological findings of dermatophytosis in our study

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Figure 5: Tinea incognito

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Figure 6: Percentage of dermatophyte species isolated by culture

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The in vitro sensitivity profile of 10 commercially available antifungal agents against 85 dermatophyte isolates belonging to 10 different species was evaluated using the Broth MD. The MIC range, MIC50, MIC90, and Geometric Mean (GM) of MIC of each drug were calculated for every dermatophyte species. [Table 2] shows the over-all MIC range, MIC50, MIC90, and GM of MIC of the antifungal agents tested [Table 2].
Table 2: Minimum inhibitory concentration range, minimum inhibitory concentration 50, minimum inhibitory concentration 90 and geometric mean of a minimum inhibitory concentration of the antifungal agents tested

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Amongst the isolates of T. rubrum, 20% isolates were inhibited at the lowest MIC for Itraconazole, while only 2% isolates were inhibited by the lowest MIC of Griseofulvin and Terbinafine each. This was found to be statistically significant (P = 0.0073) [Table 3].
Table 3: Comparison between the percentage of Trichophyton rubrum isolates inhibited at the lowest minimum inhibitory concentrations: Itraconazole versus other systemic agents

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As among the topical antifungal drugs tested, the lowest MIC of Luliconazole inhibited 73% of T. rubrum isolates, which was significantly higher than all other topical drugs (P < 0.0001) [Table 4].
Table 4: Comparison between the percentage of Trichophyton rubrum isolates inhibited at the lowest minimum inhibitory concentrations: Luliconazole versus other topical agents

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However, in terms of MIC range and GM, Terbinafine (0.004–0.25 μg/ml, 0.05 μg/ml) showed the highest susceptibility followed closely by Itraconazole (0.016–0.5 μg/ml, 0.07 μg/ml), while Fluconazole followed by Griseofulvin were the least effective systemic drugs.

Based on over-all parameters, Terbinafine showed the best efficacy followed closely by Itraconazole amongst the systemic agents. Luliconazole was the most effective topical agents. One of the new anti-fungal drugs, Voriconazole, showed good efficacy in all isolates but was, in general, less effective than Itraconazole and Terbinafine.

Fluconazole, followed by Griseofulvin showed the lowest efficacy amongst the systemic agents, while Ketoconazole was the least effective amongst the topical agents. Microbiological in vitro resistance to Griseofulvin (MIC ≥4 μg/ml) in our study was found in 15.3% isolates (n = 13), which had a Zcal value of-5.76 (P < 0.00001).


  Discussion Top


With a rising trend of anti-fungal drug resistance, the current scenario of increased incidence, recurrence, relapse, and recalcitrance of superficial dermatophytosis in South India has turned into an alarming issue in the last few years. The widespread use of over-the-counter medications such as topical steroids presenting with steroid-modified tinea can pose a diagnostic and therapeutic dilemma for the Dermatologist. In this study, 211 cases of clinically diagnosed dermatophytosis involving the skin were evaluated by light microscopy under 10% KOH, followed by culture and AFST using the Broth MD.

Similar to the observations made in prior studies, in our study, we observed a male predominance in the subjects with male-to-female ratio of 2.14:1 along with majority of the subjects belonging to 21–40 years of age.[3],[9],[10],[11]

Based on the type of clinical presentation, tinea incognito was the most common in our study, followed by tinea corporis and tinea cruris. However, Bhatia and Sharma and Mahajan et al. reported that tinea corporis and tinea corporis et cruris, respectively, were the predominant presentations in their studies.[3],[11] On the other hand, Grover and Roy reported that the most common presentation of dermatophytosis in their study was tinea pedis, followed by tinea cruris.[12] The huge predominance of tinea incognito in our study could be because the study was conducted in a rural tertiary care hospital, and the majority of our patients belong to lower socioeconomic groups with higher rates of illiteracy, less awareness about personal hygiene and rampant use of over-the-counter medications including topical steroids. Recurrent episodes were seen in 11.84% cases, of which the most common presentation was tinea incognito.

Similar to the observations made by Gopi et al. and Sardana K et al., KOH mount positivity in our study was seen in 71.56% of specimens.[8],[9] About 43.60% of specimens were positive in both direct microscopy as well as fungal culture. These findings are in agreement with those by Kumar et al. who got 40.80% specimens showing both KOH and culture positivity.[10]

Out of a total of 211 specimens collected, 116 cultures were positive, comprising 85 dermatophyte isolates (40.28%) and 31 nondermatophytes. The low culture positivity in our study could also be attributed to the fact that the majority of subjects had previously used some form of over-the-counter topical preparation containing corticosteroids. However, other south Indian studies by Poluri et al. and Penmetcha et al. reported higher culture positivity rates of 56.36% and 75.2%, respectively.[13],[14]

Trichophyton was the most common genus isolated, followed by Microsporum and Epidermophyton. Out of the species of Trichophyton, T. rubrum was the predominant species, followed by T. mentagrophytes. This finding is in agreement with the observations made by Poojary et al., Gopi et al. and Kumar et al.[9],[10],[15] In the recent past, some authors have reported that T. mentagrophytes was the predominant dermatophyte isolated in their studies.[3],[8],[16] A molecular study of dermatophytosis using polymerase chain reaction enzyme-linked immunosorbent assay by Nenoff et al. done on 201 specimens collected across the country reported that 92.62% of the culture isolates yielded T. mentagrophytes. In contrast, only 7.38% yielded T. rubrum.[17] On an unusual note, another study from North-East India observed a predominance of Trichophyton tonsurans followed by T. rubrum.[12] However, our findings are in agreement with three other studies from South India, which have shown a rising prevalence of T. rubrum in recent times in these geographical regions.[13],[14],[18]

Over the past few decades, the number of antifungal agents used in clinical practice for the treatment of dermatophytosis has increased.[19] However, not all species have the same susceptibility pattern, and there is also rising evidence of antifungal resistance in dermatophytes.[20]

Among the systemic agents in our study, Terbinafine was the most effective drug followed closely by Itraconazole, while amongst the topical antifungal agents Luliconazole was the most effective. Our findings agree with the observations made by Hanafy and Indira.[21],[22] Although Mukherjee et al. had reported a T. rubrum isolate that showed resistance to Terbinafine,[23] all dermatophyte isolates tested in our study showed excellent susceptibility to Terbinafine, Luliconazole, Itraconazole, Miconazole, Sertaconazole, Voriconazole, Clotrimazole, and Ketoconazole in the same order. In accordance with the results published in prior studies, we found that Fluconazole was the least effective drug in AFST, followed by Griseofulvin.[5],[7],[8],[21],[22],[24],[25]

While MIC50 and MIC90 are used to map the susceptibility patterns of a circulating strain in a particular setting, neither of these parameters can categorize the isolates as resistant or sensitive as they only indicate the sensitivity of 50% or 90% of the tested isolates. For an isolate to be labeled as resistant to Terbinafine, Itraconazole, or Griseofulvin, an MIC of 4 mg/L or more is required, whereas for Fluconazole MIC > 32 mg/L is considered resistant.[16]

For many years, Griseofulvin had been the first line of treatment in dermatophytosis. However, in consistence with previous studies, all dermatophytes exhibited low susceptibilities to Griseofulvin in the present study as well. Griseofulvin resistance with a cut-off MIC ≥ 4 μg/ml was reported by Mahajan et al. in 50% of dermatophyte isolates tested.[3] Keeping that in view, microbiological in-vitro resistance to Griseofulvin was also found in our study in 15.3% (n = 13) isolates, of which 61.5% (n = 8) were T. rubrum isolates (P < 0.00001).

Although antifungal resistance is usually correlated with increased MIC, these values do not always correlate with clinical response to antifungal drugs. Breakpoints, also termed as Interpretive Criteria are used to denote susceptibility and resistance to antifungal agents, as the outcome of AFST. They are categorized as susceptible, intermediate, and resistant. However, till now, clinical breakpoints have not been defined by the CLSI for dermatophytes due to lack of data on the clinical correlation, pharmacokinetic/pharmacodynamic studies, or epidemiological cut-off MIC values. Hence, experts opine that it is logical to not use the term 'resistant' in the absence of these definitive criteria for dermatophytes.[26]

On a detailed analysis of the antifungal susceptibility patterns of T. rubrum, which was the most common isolate in our study, we found that amongst the systemic agents, Itraconazole inhibited a statistically significantly higher number of isolates at its lowest MIC compared to Terbinafine and Griseofulvin (P = 0.0073). This signifies the excellent efficacy of Itraconazole even at its lowest concentration compared to other drugs. Luliconazole was significantly more effective on T. rubrum isolates compared to all other topical agents (P < 0.0001).

However, in terms of GM s and MIC ranges in T. rubrum isolates, Terbinafine showed the lowest range and GM followed very closely by Itraconazole in systemic agents, while amongst the topical antifungal agents Luliconazole was the most effective. On the other hand, Fluconazole followed by Griseofulvin were the least effective drugs in T. rubrum isolates. These observations are in agreement with the findings reported by Indira and Hanafy, who also noted that Terbinafine was the most effective drug in their studies.[21],[22] Another commonly isolated species, T. mentagrophytes also showed the highest susceptibilities to Itraconazole and Terbinafine, while being least susceptible to Fluconazole.


  Conclusion Top


This is the largest study from rural Southern India evaluating the changing geographical trends of various dermatophytoses and its antifungal susceptibility to most commonly prescribed drugs. The susceptibility pattern of dermatophytes varies from species to species, which is why it is important to determine the fungal isolate, especially in cases of recalcitrant dermatophytosis. However, an increase in MIC is not the only factor responsible for recurrence or recalcitrance. Although recurrences may be due to re-infection from affected family members or the environment, it is more likely that the duration of antifungal therapy given may be inadequate.[23] In most instances, the patients tend to stop topical treatment as soon as they get partial relief. The host immunity also plays a major role in recalcitrance. Extending the therapy for at least 2–3 weeks after symptomatic relief should be advised along with appropriate treatment of any infected close contacts and patient counseling regarding behavioral and lifestyle modifications.

Limitations of the study

  • This study does not correlate the antifungal susceptibility patterns with clinical outcomes
  • Further large scale studies from other geographical regions would warrant a clearer picture of both the clinicomycological as well as antifungal susceptibility patterns in the global population
  • The susceptibility patterns of Eberconazole, Oxiconazole, and Fenticonazole could not be tested in this study due to constraints in acquiring raw materials for AFST
  • The results of Broth Microdilution in our study were read visually, which can lead to subjective errors. Future studies should use more accurate methods such as spectrophotometer or colorimetry to read the results of AFST.


Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient (s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initial s will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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  [Full text]  


    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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