A study on etiologic agents and clinical manifestations of dermatophytosis in Yazd, Iran

Authors

1 Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

2 00000

Abstract

Background and Purpose: Dermatophytosis is one of the most common infections of skin, hair, and nails, caused by a group of keratinophilic fungi known as dermatophytes. Species identification of these fungi is of great significance from epidemiological and therapeutic points of view. The objective of the present study was to investigate dermatophytosis and its causative agents in patients, referring to the Central Mycology Laboratory of Yazd University of Medical Sciences, Yazd, Iran.
Materials and Methods: In total, 139 clinically suspected cases of dermatophytosis were examined during 12 months from February 2014 to February 2015. Skin scrapings were assessed through direct microscopic examinations and culture studies. Dermatophyte isolates were identified based on colony morphology on potato dextrose agar and dermatophyte test medium, nutritional requirements, urease and hair perforation tests, and microscopic characteristics on slide cultures.
Results: Dermatophytosis was mycologically confirmed in 26 (18.70%) out of 139 cases. Although there was a statistically insignificant difference between male and female subjects, men were dominantly affected. Infection was significantly common in the age group of ≤ 29 years (p <0.043). The most common clinical manifestation of dermatophytosis was tinea corporis (69.2%), followed by tinea cruris (15.4%), tinea manuum (11.5%), and tinea pedis (3.8%). Trichophyton mentagrophytes complex was the main etiologic agent (38.5%), followed by T. rubrum (23%), T. violaceum (15.5%), T. verrucosum (11.5%), Microsporum canis (7.7%), and Epidermophyton floccosum (3.8%).
Conclusion: In comparison with previous research, epidemiology of dermatophytosis has changed in Yazd over the past decades. Therefore, periodical investigations on the epidemiological aspects of this infection are required for efficient control and prevention of this cutaneous dermatophytic disease.

Keywords


Introduction

Dermatophytes by involving the skin, hair, and nails can cause dermatophytosis [1]. Classically, tinea is categorized into eight major types, i.e., tinea corporis, tinea cruris, tinea pedis, tinea manuum, tinea faciei, tinea barbaee, tinea capitis, and tinea ungium [2, 3]. Tinea capitis is a common condition in children [4], whereas tinea cruris is predominant in male adults [5]. Of these major types, tinea ungium is usually regarded as a chronic infection of nails in adults [6].

Dermatophytes are divided into three distinct anthropophilic, zoophilic, and geophilic groups. Human infection may be caused by the members of these three groups. Three genera of dermatophytes including Epidermophyton, Trichophyton, and Microsporum with nearly 40 species have been identified [2]. The prevalence of dermatophytes varies in different geographical regions [1,7-18]. In Iran, epidemiology of dermatophytosis has changed over the past decades [19]. In fact, in several studies in Iran, predominance of zoophilic dermatophytes over anthropophilic fungi has been reported in some regions [20, 21].

In the present study, we aimed to determine the current status of dermatophytosis, based on demographic data, clinical manifestations, and etiologic agents in patients, referring to the Central Mycology Laboratory of Yazd University of Medical Sciences, Yazd, Iran.

Material and Methods

Study population

In total, 139 patients (70 males and 69 females) with a clinical suspicion of dermatophytosis were studied during 12 months from February 2014 to February 2015 in the Central Mycology Laboratory of Yazd University of Medical Sciences, Yazd, Iran. The age range of subjects was 1-72 years. Informed consent forms were obtained from all adults, children's parents, or their guardians.

Mycological examination

Considering the localization and characterization of lesions, skin scrapings were obtained and assessed through direct microscopic examination and culture studies. Direct microscopic examination with 10% potassium hydroxide (KOH) was performed on a section of each specimen to determine the presence of hyphae and arthrospores. The remaining samples were cultured on Sabouraud dextrose agar (Merck, Darmstadt, Germany) with or without cycloheximide.

The slants were incubated at 28°C for one to four weeks. The cultures were checked twice weekly for evidence of colony growth. According to basic mycological techniques, all isolates were identified by determining the macroscopic colony characteristics and microscopic features of slide cultures on potato dextrose agar (Merck, Darmstadt, Germany). Differential diagnostic methods such as pigment production, hair perforation test, nutritional requirements, and urease test were also performed if needed [22].

Statistical analysis

Statistical analysis was performed, using SPSS version 20. Categorical variables were compared with universal standards, using Fishers exact test. The statistical confidence level was set at 95% and P-value less than 0.05 was considered statistically significant.

Results

Among 139 examined patients, 26 (18.7%) cases were found to have dermatophytosis. Infection was confirmed by both microscopic examination and culture studies. The affected patients included 12 females and 14 males within the age range of 1-72 years. Dermatophytosis was significantly more common in the age group of ≤ 29 years. Further information is presented in Table 1.

Tinea corporis (69.2%) was the predominant clinical manifestation, followed by tinea cruris (15.4%), tinea manuum (11.5%), and tinea pedis (3.8%). Despite the higher frequency of tinea corporis and tinea cruris in male subjects and tinea manuum and tinea pedis in females, the difference in infection rate between the genders was statistically insignificant (P=0.828).

Age groups(years) Dermatophytosis Total
Positive Negative
N % N % N %
≤ 29 15 18.1 68 81.9 83 100
30-59 7 14.2 42 85.8 49 100
≥ 60 4 57.1 3 42.9 7 100
Total 26 18.7 113 81.3 139 100
N: Number
Table 1.Distribution of the study population based on the age and the results of mycological examinations
Clinical forms Etiologic agents
T. mentagrophytes T. rubrum T. violaceum T. verrucosum E. floccosum M. canis Total
N % N % N % N % N % N % N %
Tinea corporis 6 33.3 4 22.2 4 22.2 3 16.8 0 0 1 5.6 18 100
Tinea cruris 1 25 1 25 0 0 0 0 1 25 1 25 4 100
Tinea manuum 2 66.6 1 33.4 0 0 0 0 0 0 0 0 3 100
Tinea pedis 1 100 0 0 0 0 0 0 0 0 0 0 1 100
Total 10 38.5 6 23 4 15.4 3 11.5 1 3.8 2 7.7 26 100
T: Trichophyton, E: Epidermophyton, M: Microsporum, N: Number
Table 2.Frequency and distribution of the isolated dermatophyte species according to clinical manifestations
Occupational status Dermatophytosis Total
Positive Negative
N % N % N %
Self-employed 3 12.5 21 87.5 24 100
Student 2 50 2 50 4 100
University student 2 11.8 15 88.2 17 100
Housewife 10 26.3 28 73.7 38 100
Employee 1 8.4 11 91.6 12 100
Worker 0 0 8 100 8 100
Retired 0 0 5 100 5 100
Total 18 16.7 90 83.3 108 100
Table 3.Distribution of the study population, based on the occupational status and the results of mycological examinations

The etiologic agents in 26 positive cases were identified as Trichophyton mentagrophytes (38.5%), T. rubrum (23%), T. violaceum (15.4%), T. verrucosum (11.5%), Microsporum canis (7.7%), and Epidermophyton floccosum (3.8%). The clinical presentations and causative agents of positive cases are summarized in Table 2.

Fisher's exact test was performed to determine the correlation between dermatophytosis and gender, age, genus/species of organisms, and patients' occupational status. Based on the findings, patients ≤ 29 years of age were more affected by dermatophytosis, and a significant correlation was observed between dermatophytosis and age (P=0.043).

As the findings indicated, dermatophytosis was not significantly correlated with patients’ gender or genus/species of the organism (P=0.828 and 0.761, respectively). Despite the higher incidence of dermatophytosis among housewives and self-employed subjects (Table 3), Fisher's exact test did not reveal a significant relationship between occupational status and dermatophyte infection (P=0.394).

Discussion

Dermatophytosis is a common fungal infection in humans and animals. This infection has a global distribution and is regarded as a public health concern. Generally, individuals from all age groups may present with dermatophytosis, although young adults of both genders are more commonly affected. The frequency of this infection varies, depending on the site of infection, the immunological response of the host, and species of the causal agent. Also, many other factors such as migration patterns, frequent travelling, and lifestyle may affect the epidemiology of dermatophytic infection [23].

In our investigation, male subjects were more commonly affected by dermatophytosis, compared to females; in fact, males were affected 1.16 times more than females in our research. Infection was mainly reported in the age group of ≤ 29 years, which was in agreement with the results of previous studies in Iran [4, 12, 24-28]. Similar to a previous investigation in Yazd, the present study introduced tinea corporis (69.2%) as the predominant form of infection. This finding was in line with several studies [25, 28-30] and in contrast with the results of several articles in different parts of Iran [12, 24, 26, 31].

According to a study by Hashemi et al., tinea corporis was the most frequent form of dermatophytosis in Arak, Iran [27]. In congruence with previous research in Iran, T. mentagrophytes, T. rubrum, and T. violaceum were the main causes of tinea corporis in the present study [9, 20, 27, 32-34]. Interestingly, this finding was in contrast with previous reports from Yazd, which introduced T. verrucosum as the most common agent, followed by E. floccosum and T. violaseum. [34]; this indicates a shift in causative agents of dermatophytosis in Yazd, Iran.

According to the present study, tinea cruris (15.4%) was the second most common clinical presentation. Even though this finding was in accordance with some previous reports from Iran [25, 35], it was in contrast with previous studies in Yazd [34], Kerman [24], Isfahan [20], Hamadan [30], Tehran [31, 36], Rasht [11], and Gorgan [37], in which tinea cruris was the most common type of dermatophytosis.

E. floccosum, T. mentagrophytes, T. rubrum, and M. canis were the etiologic agents of tinea cruris in the present study. In our investigation, tinea cruris was more frequent in males, as reported by previous researches in Yazd and other parts of Iran [5, 13, 34]. However, unlike a study by Mosavi et al. [24] in Kerman, which reported tinea manuum as the main form of dermatophytosis, in the present study, tinea manuum was ranked third in terms of frequency. Although this finding was supported by some previous studies [34-36], it was in contrast with other reports from Iran [20, 25, 26, 34].

Higher frequency of tinea manuum in females was reported in the present study, as well as previous research. Also, T. mentagrophytes, followed by T. rubrum, was the most common cause of disease in our research, similar to several previous studies [9, 24, 29, 36]. Contrary to previous studies in Yazd [34], Isfahan [20], Kerman [24], Shiraz [26], Rasht [11], and Zahedan [35], the present research showed tinea pedis (3.5%) to be the less frequent type of dermatophytosis; however, our finding was in agreement with a study by Shamsian et al. in Mashhad [25]. In the present study, only one case of tinea pedis was observed in a female patient, caused by T. mentagrophytes; this finding confirms the results of previous research in Iran [9, 36].

In this study, the common age group affected by dermatophytosis was ≤ 29 years (57.5%). Our findings were similar to several studies [4, 12, 19, 24-28], while in contrast with previous reports from Iran [20, 35, 36, 38, 39]. Moreover, similar to several studies [12, 25, 26, 34, 38], the present research like some other studies indicated that the frequency of dermatophytosis in males (53.9%) is higher than females (46.1%). However, studies in Kerman, Rasht, and Kermanshah [11, 24, 29] reported the high rate of dermatophytosis in females rather than males.

The incidence rate of dermatophytosis varies in different regions of Iran. Hot and humid environments provide favorable conditions for better growth of dermatophytes. This leads to the higher frequency of this fungal infection in cities with hot and humid climatic conditions such as Ahvaz and Bandar Abbas in comparison with other regions in Iran.

Dermatophytosis is one of the common cutaneous fungal infections in Yazd, Iran. Public health care and self hygiene play important roles in the control and prevention of this contagious disease. Notable changes in clinical forms and causative agents of dermatophytosis have been observed in different parts of the world including the United States and Europe.

An increase in anthropophilic cases of dermatophytic infections has been reported in Europe, while M. canis is still the major cause of tinea corporis in Mediterranean countries. However, in the Middle East, tinea corporis is widely caused by T. mentagrophytes [40]. The discrepancy between the findings may be an outcome of diversity in the cultural background, socioeconomic, geographical, and climatic conditions, close contact with domestic and wild animals, and use of public health and recreational facilities.

The present study is the second report of cutaneous dermatophytosis in Yazd since 2001. The discrepancy between our analysis and previous research may be a result of the above mentioned factors and migration of people with different traditions and cultures from rural to urban regions of Yazd.

Conclusion

In comparison with previous research, epidemiology of dermatophytosis has changed in Yazd over the past decades. Therefore, periodical investigations on the epidemiological aspects of this infection are required for the efficient control and prevention of this cutaneous disease.

References

  1. Anaissie EJ, McGinnis MR, Pfaller MA. Clinical mycology. Elsevier Health Sciences: New York; 2009.
  2. Zaini F, Mehbod AS, Emami M. Comperhensive medical mycology. Tehran University Publication: Tehran; 2013.
  3. Costa AR, Criado PR, Valente NY, Sittart JA, Stelmach RS, Vasconcellos C. Trichophyton raubitschekii: a new agent of dermatophytosis in Brazil?. Dermatol Online J. 2003; 9(1):6.
  4. Mahmoudabadi AZ. A survey of 382 suspected patients with tinea capitis, Ahwaz. Sci Med J. 1997; 22:45-52.
  5. Hedayati MA. Common dermatophytes in Khuzestan province. Sci Med J. 1989; 10:59-65.
  6. Moghadami M, Shidfar MR. A study of onychomycosis in Tehran. Med J Islamic Repub Iran. 1989; 3(3):143-9.
  7. Abastabar M, Rezaei-Matehkolaei A, Shidfar MR, Kordbacheh P, Mohammadi R, Shokoohi T. A molecular epidemiological survey of clinically important dermatophytes in Iran based on specific RFLP profiles of beta-tubulin gene. Iran J Public Health. 2013; 42(9):1049-57.
  8. Rezaei-Matehkolaei A, Makimura K, de Hoog S, Shidfar MR, Zaini F, Eshraghian M. Molecular epidemiology of dermatophytosis in Tehran, Iran, a clinical and microbial survey. Med Mycol. 2013; 51(2):203-7.
  9. Mahmoudabadi AZ. A study of dermatophytosis in South West of Iran (Ahwaz). Mycopathologia. 2005; 160(1):21-4.
  10. Aghamirian MR, Ghiasian SA. Dermatophytoses in outpatients attending the dermatology center of Avicenna Hospital in Qazvin, Iran. Mycoses. 2008; 51(2):155-60.
  11. Alizadeh N, Sadr AS, Golchai J, Maboodi A, Falahati AA. Descriptive study of dermatophytosis in Guilan. Iran J Dermatol. 2004; 7(4):255-60.
  12. Mahboubi A, Baghestani SH, Hamedi Y, Heydari M, Vahdani M. Epidemiology of dermatophytosis in Bandar Abbas, Iran (2003-2004). Med J Hormozgan Univ. 2006; 9(4):227-34.
  13. Pakshir K, Hashemi J. Dermatophytosis in Karaj, Iran. Indian J Dermatol. 2006; 51(4):262-4.
  14. Sepahvand A, Abdi J, Shirkhani Y, Fallahi SH, Tarrahi M, Soleimannejad S. Dermatophytosis in western part of Iran, Khorramabad. Asian J Biol Sci. 2009; 2(3):58-65.
  15. Bassiri-Jahromi S, Khaksari AA. Epidemiological survey of dermatophytosis in Tehran, Iran, from 2000 to 2005. Indian J Dermatol Venereol Leprol. 2009; 75(2):142-7.
  16. Rezvani SM, Sefidgar S, Hasanjani Roushan MR. Clinical patterns and etiology of dermatophytosis in 200 cases in Babol, North of Iran. Casp J Intern Med. 2010; 1(1):23-6.
  17. Sadeghi G, Abouei M, Alirezaee M, Tolouei R, Shams-Ghahfarokhi M, Mostafavi E. A 4-year survey of dermatomycoses in Tehran from 2006 to 2009. J Med Mycol. 2011; 21(4):260-5.
  18. Falahati M, Akhlaghi L, Lari AR, Alaghehbandan R. Epidemiology of dermatophytoses in an area south of Tehran, Iran. Mycopathologia. 2003; 156(4):279-87.
  19. Naseri A, Fata A, Najafzadeh MJ, Shokri H. Surveillance of dermatophytosis in northeast of Iran (Mashhad) and review of published studies. Mycopathologia. 2013; 176(3-4):247-53.
  20. Chadeganipour M, Shadzi S, Dehghan P, Movahed M. Prevalence and aetiology of dermatophytoses in Isfahan, Iran. Mycoses. 1997; 40(7‐8):321-4.
  21. Chadeganipour M, Mohammadi R, Shadzi S. A 10‐year study of dermatophytoses in Isfahan, Iran. J Clin Lab Anal. 2015; 181(1-2):89-104.
  22. De Hoog GS, Guarro J, Gené J, Figueras MJ. Atlas of clinical fungi, Centraalbureau voor Schimmelcultures. Utrecht: Neterlands; 2000.
  23. Nweze EI. Dermatophytosis in Western Africa: a review. Pak J Biol Sci. 2010; 13(13):649-56.
  24. Mosavi A, Amin S, Safizadeh H, Hadizadeh S. Epidemiology of dermatophytosis in patients referred to the medical mycology laboratory of Afzalipoor Faculty of Medicine in Kerman in 2007-2011. Dermatol Cosmetics. 2012; 3(2):114-23.
  25. Shamsian SAA, Yazdan Panah MJ, Majdi MMA, Marjaneh MM, Saboori Rad S. Frequency of dermatophytoses. Med J of Mashhad Univ Med Sci. 2008; 51(2):95-102.
  26. Badiee P, Kordbacheh P, Zaini F, Shidfar MR, Eshraghian MR. Study and diagnosis of superficial and cutaneous fungal disease in patients referring to health care center in Shiraz. Iran J Infect Dis Tropical Med. 2004; 8(1):18-21.
  27. Hashemi SJ, Qomi HA, Bayat M, Haghdost IS. Mycoepidemiologic study of superficial and cutaneous fungal zoonotic disease in patients who referred to skin clinic of Arak. Eur J Experimen Biol. 2014; 4(1):5-8.
  28. Ansari S, Hedayati MT, Zomorodian K, Pakshir K, Badali H, Rafiei A. Molecular characterization and in vitro antifungal susceptibility of 316 clinical isolates of dermatophytes in Iran. Mycopathologia. 2015; 181(1-2):89-95.
  29. Mikaeili A, Mahmodi A, Rezaei M, Ebrahimi A. The dermatophytes species frequency in referral patients to medical mycology lab of Kermanshah-2012. Med J Mashhad Univ Med Scie. 2015; 57(9):990-4.
  30. Omidynia E, Farshchian M, Sadjjadi M, Zamanian A, Rashidpouraei R. A study of dermatophytoses in Hamadan, the governmentship of West Iran. Mycopathologia. 1996; 133(1):9-13.
  31. Eftekarjo Y, Balal A, Taghavi M, Rahimi ZS, Nikaein D. Epidemiology and prevalence of superficial fungal infections among dormitory students in Tehran, Iran. JMR. 2015; 2(1):49-54.
  32. Nejad SB, Khodaeiani E, Amirnia M. A study of dermatophytosis infections in dermatology clinic of sina hospital–Tabriz. Ege Tip Dergisi. 2007; 46(1):21-5.
  33. Ali N, Abdolmajid F, AliReza K. The first case of Microsporum persicolor infection in Iran. Jundishapur J Microbiol. 2012; 2012(1):362-4.
  34. Azizi M, Jivad N. Causal agents of the prevalent cutaneous fungal diseases in Yazd province, 1998. Shahrekord Univ Med Sci J. 2001; 3(2):73-8.
  35. Moalaei H. Study of the prevalence of dermatophytosis infections in different body spots and their etiology. J Sabzevar Univ Med Sci. 2000; 7(1):85-92.
  36. Omran AN, Hashemi SJ, Hashemi F. Epidemiology of superficial and cutaneous mycosis in 5500 suspected patients in Tehran. Tehran Univ Med Sci. 2010; 68(1):45-53.
  37. Dehghan M, Hajian S, Alborzi N, Borgheyee A, Noohi AH. Clinico-mycological profiles of dermatophytosis in Gorgan, north of Iran. Iran J Dermatol. 2009; 12(1):13-5.
  38. Edalatkhah H, Golforoshan F, Azimi H, Mohammadi P, Razi A. Prevalence of various species of dermatophytes in patients referring to the dermatology clinic of Tabriz Haft-e-Tir Hospital. J Ardabil Univ Med Scie. 2006; 6(1):47-52.
  39. Bineshian F. A study on superficial and cutaneous mycosis among Afghan immigrants in Semnan refuge camp. Koomesh. 2007; 8(2):27-35.
  40. Hayette MP, Sacheli R. Dermatophytosis, trends in epidemiology and diagnostic approach. Cur Fungal Infect Rep. 2015; 9(3):164-79.