The epidemiological and mycological profile of superficial mycoses in india from 2015 to 2021: A systematic review
Saibal Das1, Sanjib Bandyopadhyay2, Sanket Sawant3, Sirshendu Chaudhuri4
1 Scientist D (Medical), Indian Council of Medical Research - Centre for Ageing and Mental Health, Kolkata, West Bengal, India; Doctoral Student, Department of Global Public Health, Karolinska Institutet, Stockholm, Sweden
2 Associate Professor, Department of Community Medicine, Burdwan Medical College, Mumbai, Maharashtra, India
3 Independent Pharmacologist, Mumbai, Maharashtra, India
4 Assistant Professor, Indian Institute of Public Health, Hyderabad, Telangana, India
Correspondence Address:
Sirshendu Chaudhuri
Indian Institute of Public Health, Kavuri Hills, Madhapur, Hyderabad - 500 033, Telangana
India
Source of Support: None, Conflict of Interest: None
DOI: 10.4103/ijph.ijph_987_22
Background: The epidemiological and mycological patterns of superficial mycoses across various geographic regions of India across the last few years are changing. Objective: This study was performed to evaluate the epidemiological and mycological profile of superficial mycoses in India between 2015 and 2021. Methods: In this systematic review, the PubMed database was searched for all observational studies published between January 1, 2015, and December 31, 2021, which had evaluated the clinico-mycological profile of superficial mycoses among outpatients from various parts of India. Descriptive statistics was used to represent the results. Results: Forty studies (21 from the north, three from the northeast, five from the east, seven from the south, one from the west, and three from multiple regions of India) were included. Male patients and those of the age group of 21–40 years were most commonly affected. The proportion of dermatophytes as causative organisms was consistently high across all regions and throughout the study period (23.6%–100%). Among dermatophytes, the proportion of Trichophyton mentagrophyte (14.0%–97.2%) and Trichophyton rubrum (0%–69.1%) was consistently high across all regions. The prevalence of T. mentagrophyte showed a rising trend, while that T. rubrum showed a declining trend from 2015 to 2021. Conclusions: The epidemiological and mycological pattern of superficial mycoses showed a fairly similar trend across various regions of India from 2015 to 2021. Dermatophytes were the main causative agents of superficial mycoses; the most common species were T. mentagrophyte and T. rubrum. A rising trend of T. Mentagrophyte infection was found.
Keywords: Dermatophytosis, epidemiological, India, mycological, superficial mycoses, Trichophyton mentagrophyte
Dermatophytosis Research Group Souvik Sardar, MD, Consultant Dermatologist, Eleganz Skin and Hair Clinic, Kolkata, India, Abin Augustine, MD, Independent Pharmacologist, Kochi, India, Manasi Limaye, MD, Independent Pharmacologist, Mumbai, Maharashtra, India
Superficial mycoses include superficial fungal infections of the skin, hair, and nail (onychomycosis). It is caused by dermatophytes, yeasts (e.g., Candida, Malassezia), and nondermatophyte molds. Amongst these, dermatophytes are responsible for the highest proportion of cases.[1] Dermatophytes are classified under three asexual genera, namely Trichophyton, Epidermophyton, and Microsporum.[1]
The prevalence of superficial mycoses has recently increased by many folds in India resulting in an epidemic-like situation.[2],[3] Various factors have been implicated, such as hot and humid climatic conditions, overcrowding, poor hygiene, occlusive tight garments and footwear, low compliance to treatment, and irrational use of topical corticosteroids.[4] Furthermore, there is a changing trend in the disease presentation, severity, treatment response, and relapse rate.[1] This has a significant impact on the quality of life of the patients[5] and poses a huge psychosocial and financial burden.[6]
The epidemiological trend of superficial mycoses varies both with time and geographical regions and has been attributed to the climate, social practices, population migration, and traveling.[1] Such variation has a significant clinical implication in the treatment of the disease.[7] Although several reports on superficial mycoses are available from various parts of India, it is required to systematically summarize the literature to appreciate the changing epidemiological and mycological pattern of the disease across various geographic regions of India across the last few years. This can serve as a guide to choosing appropriate antifungal agents based on the changing trend of the disease.[8],[9] Hence, we have systematically evaluated the epidemiological and mycological profile of superficial mycoses in India between 2015 and 2021.
Eligibility criteria
In this systematic review, we included all observational studies published between January 1, 2015, and December 31, 2021, in the English language which evaluated the clinico-mycological profile of superficial mycoses among outpatients from various parts of India. We excluded studies that evaluated inpatients, immunocompromised patients, and patients on immunosuppressants; and studies on fungal keratitis, deep mycoses, Malassezia, and Fusarium. We excluded case reports, case series, reviews, commentaries, viewpoints, or opinions, as well as abstracts, conference proceedings, and studies for which the full text was unavailable.
Search strategy
We performed our search on the PubMed database. The search terms used in various combinations were: “superficial mycoses,” “dermatophytes,” “dermatophytosis,” “dermatomycosis,” “dermatomycoses,” “onychomycosis,” “superficial skin infections,” “fungal,” “antifungal,” “sensitivity,” “susceptibility,” “pattern,” “profile,” “epidemiological,” “clinico-mycological,” and “India.” This search strategy was used to obtain titles and abstracts of the relevant studies, and they were independently screened by two authors, who subsequently retrieved abstracts, and if necessary, the full text of the articles to determine the eligibility. Disagreement resolution was performed with a third author.
Outcomes
We evaluated the epidemiological characteristics of superficial mycoses across various regions of India from January 1, 2015 to December 31, 2021. For the diagnosis of superficial mycoses, clinical or in the laboratory methods (culture, potassium hydroxide preparation, or both) were considered. These include patient demographics (age, gender, occupation, common comorbidities, prior use of topical corticosteroids, and history of superficial mycoses in family members), distribution of lesions, and the causative fungal species.
Data extraction and management
The risk of bias in each observational study was analyzed by the Newcastle–Ottawa scale.[10] Data extraction was carried out independently by two authors using a pre-formatted data extraction spreadsheet. Information on the demographic characteristics of the patients and fungal species was collected. Descriptive statistics was used to present the findings. Prevalence in different groups was presented in a range. Microsoft Excel (Redmond, WA) was used for all analyses.
Ethics
No ethical approval was required as this is a systematic review article with no original research data. All data used in this research are available in the public domain.
After screening a total of 1082 studies, we finally included 40 studies in our analyses [Figure 1]. These studies included a total of 6251 patients and 1101 samples. All studies were conducted in an outpatient setting of tertiary care hospitals and were observational in nature. The risk of bias in the included studies is enumerated in [Table S1].
Epidemiological profile
Of the 40 studies, 21 (52.5%) were conducted in the north,[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31] three (7.5%) in the north-east,[32],[33],[34] five (12.5%) in the east,[35],[36],[37],[38],[39] seven (17.5%) in the south,[40],[41],[42],[43],[44],[45],[46] one (2.5%) in the west,[47] and three (7.5%) were multicentric involving more than one region.[48],[49],[50] Of the included studies, 33 studies (82.5%) reported males to be predominantly infected. Twenty-one studies (52.5%) reported the age-wise distribution of superficial mycoses. Patients aged 21–40 years (19/21 studies, 90.5%) were most affected (35.1%−79.4%). The pediatric (<10 years) (1.6%−8.4%) and elderly (>60 years) populations (0.7%−19.8%) were the least affected. Eight out of 40 studies (20.0%) reported only patients with onychomycosis. Of the 26 studies that reported sites of the lesion, the trunk was most commonly involved in isolation (11 studies [42.3%]), followed by mixed infections (11 studies [38.5%]). Out of the 12 studies (30.6%) that had mentioned the occupation of the patients, homemakers (9/12 studies [75.0%; range, 20.8%−36.8%]) followed by farmers and laborers (5/12 studies [41.7%; range: 4.0%−46.6%]) were reported to be most affected. Few studies also reported sports persons and students among commonly affected with the condition.
Comorbidities were reported in 15/40 studies (37.5%), of which diabetes mellitus (13/40 studies [32.5%]) and immunosuppressed conditions (7/40 studies [17.5%]) were the most common. Prior use of topical corticosteroids (0%−100%) and family history of superficial mycoses (1.0%−72.0%) were reported in 16/40 studies (40%) each [Table 1].
Mycological profile
The diagnosis of superficial mycoses was made either clinically or in the laboratory (culture, potassium hydroxide preparation, or both). The proportion of dermatophytes (23.6%–100%) as causative organisms was high across all regions of India [Figure 2] and throughout the study period [Figure 3]a. The proportion of Candida as the causative organism ranged between 0 and 53%, whereas, for nondermatophytes, the range varied between 0 and 61.6%. Candida infection was reported in 5/8 studies (62.5%) collectively in the eastern and north-eastern regions when compared to that from the northern region alone [7/21 studies (33.3%)]. Among dermatophytes, the proportion of Trichophyton mentagrophyte (14%–97.2%) and Trichophyton rubrum (0%–69.1%) was high across all regions [Figure 2]. We noticed a slowly declining trend for Candida and nondermatophyte molds, while the trend for dermatophytes showed a steady upward movement although only a marginal increase overall from 2015 to 2021. The proportion of T. mentagrophyte showed a rising trend, whereas that of T. rubrum showed a declining trend among dermatophytes from 2015 to 2021. The proportions of other Trichophyton species were low in all regions [Figure 3]b.
In this review, we have evaluated the epidemiological and mycological profiles of superficial mycoses in India in the last 6.5 years. Our review found that most studies are reported from the northern regions of India whereas the western region reported the least. There are considerable variations in the reporting of epidemiological and clinical outcomes. Despite such variations, we could identify that male patients and those aged 21–40 years were the most affected. The proportion of dermatophytes was consistently high across all regions of India and throughout the study. Among dermatophytes, the proportion of T. mentagrophyte was consistently high and showed a rising trend.
Evidence from other counties, such as Nepal,[51] Egypt,[52] and Ethiopia[53] also indicated that the middle-aged group (40–60 years) is most susceptible to superficial mycoses predominantly owing to their traveling and occupation.[54] These studies reported individuals dwelling in rural areas who had prolonged contact with water (homemakers and laborers) and soil (farmers and laborers) were affected the most. Even in our study, we found that homemakers, farmers, and laborers were most affected. An earlier study found occupational hygiene to be intrinsically related to fungal infections.[55] We found a high truncal distribution of lesions in our study. This could be attributed to the tropical climate (hot and humid environment) in the country coupled with poor personal hygiene.[56],[57] In our study, diabetes mellitus was found to be the most common comorbidity associated with superficial mycoses and this corroborates with findings of earlier studies.[58] We found a positive history of dermatophytosis in family members among the major risk factors. This is in line with the study by Tuknayat et al. who reported the contribution of such positive family history to the rising epidemic of dermatophytosis in India, often resulting in recalcitrant cases.[59] Our study also points to the problem of the use of topical corticosteroids on dermatophytosis lesions in India. This has been reported by several authors in the past and has been demonstrated that irrational use of topical corticosteroids not only leads to altered morphology of dermatophytosis (tinea incognito) but also results in difficult-to-treat cases.[60]
Similar to our observations, earlier studies have shown the preponderance of dermatophytes as the main causative agents in superficial mycoses.[61] India has witnessed an abrupt rise of T. mentagrophytes as the predominant species in less than a decade.[61],[62] This change was found to be fairly consistent across different regions of the country. This trend could be a direct effect of the growing resistance to antifungal agents resulting from the inadvertent use of topical irrational fixed drug combinations (corticosteroid, antifungal, and antibacterial) in the community.[1] Hence, in the backdrop of a rising prevalence of T. mentagrophytes infections, the treatment should aim at targeting this species effectively.[63]
There are some limitations to our study. First, all included studies were performed in tertiary care centers and hence, the actual epidemiological trend in the community settings has not been captured. Second, the identification of fungal species varied based on the diagnostic methods used (clinical or laboratory methods). This has a clinical implication because diagnostic facilities vary across healthcare settings; thereby the accuracy of diagnosis of superficial mycoses can vary.[64] Third, the distribution of studies across different geographic regions was not uniform. Fourth, in some of the studies, patients had more than one type of superficial mycosis; this may lead to bias in the outcome assessment. Fifth, we used only descriptive statistics because of the heterogeneous reporting of the data (study population, diagnostic methods, and outcome classification). Hence, due to methodological reasons, no quantitative weighted pooled analysis could be performed. Finally, we could not conclusively report the risk factors for the condition owing to the variability among the studies in reporting the epidemiological and clinical profile.
Notwithstanding these limitations, we included a fairly large number of studies from a reliable database (PubMed) with a fairly large total sample size and depicted the epidemiological and mycological profile of superficial mycoses, especially the region- and time-specific trends of the distribution of the causative fungal species from 2015 to 2021. The study has multiple implications for dermatologists and physicians who treat this condition. First, they must be thorough with their clinical diagnosis in absence of a laboratory-based diagnostic facility. Second, the treating physicians must be aware of the recent trends of fungal species prevalent in their respective regions to choose appropriate antifungal agents judiciously. Finally, they must focus rigorously on the identification of risk factors for a better treatment outcome.
Thus, to conclude, superficial mycoses are an extremely common health condition in India. The epidemiological and mycological pattern of superficial mycoses showed a fairly consistent trend across various regions of India from 2015 to 2021. Dermatophytes were the main causative agents of superficial mycoses; the most common species were T. mentagrophyte and T. rubrum. A rising trend of T. mentagrophyte infection was found from 2015 to 2021. This warrants appropriate therapeutic measures to tackle this concerning finding. However, as the precise estimate of the burden of this condition is unknown in India, we strongly recommend multicentric, population-based studies focusing on estimating the burden and identifying the contributing risk factors.
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Nil.
Conflicts of interest
There are no conflicts of interest.
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