Dermatophytes are aerobic fungi that produce protease and keratinase, which digest keratin and allows colonization, invasion, and infection of the stratum corneum of the skin, the hair shaft, and the nail. Infection is generally cutaneous and restricted to the nonliving cornfield layers because the fungi are not able to penetrate the deeper tissue or organ of healthy immune-competent host.
The infection is commonly attributed to ringworm or tinea. Cutaneous fungal infections can be caused by dermatophytes, yeasts, and non-dermatophyte molds, although dermatophytes cause most of the cutaneous fungal infections. Dermatophytes are molds belonging to the three genera of imperfect fungi including Microsporum, Trichophyton, and Epidermophyton.
Different epidemiological reports have documented that dermatophytosis has remained a public health problem in many communities . Epidemiology of dermatophytosis may change based on alterations in some conditions including climate, socioeconomic, lifestyle, immigration, and war.
Herein, we aimed to determine the prevalence of cutaneous mycosis, especially dermatophytosis, in Damascus, Syria, which has a hot and humid climate and is more favorable for the development of different superficial mycoses. In Syria, studies on the prevalence of dermatophytosis are rare; only one study was published on this subject over the past eight years .
Materials and Methods
The study population included 4080 patients clinically suspected of having dermatophytosis.
Specimens were collected in our mycological laboratory between September 2008 and June 2016 from various body sites by scraping the active edge of the affected skin and fingernail, as well as clipping, and epilating of the infected lusterless hair. The samples were subjected to direct microscopic examination using 30% KOH solution.
A total of 179 collected specimens were cultured on Sabouraud Dextrose Agar 4% (Avonchem Ltd, UK). Cultures were incubated at 25°C for up to 28 days and checked for growth twice a week. Negative cultures were confirmed after four weeks of no growth. Fungal isolates were identified based on colony morphology and micromorphology of microconidia and macroconidia, nature of sporu-lation, special structures such as spirals, racquet hyphae, and chlamydospores . The demographic information including age, gender, and season of the disease were collected by a questionnaire.
Statistical analysis was performed using Minitab ver. 17 (2010). The percentage rates and the confidence intervals were applied to describe the prevalence of each studied factor. The Z-test was utilized for measuring the ratios and to assess the significance of the difference between these ratios. A P-value less than 0.05 was considered statistically significant .
Results and Discussion
In the present study, a total of 4080 patients, comprising of 57.50% female patients, were enrolled. Out of the 4080 cases, 1138 (27.89 %) were positive on direct KOH examination, while 2912 (72.11 %) cases were negative.
In rural India, the positive rate is very similar to our finding (27.6 %) , but in other studies the positivite rate ranged from 14.2 % to 52.2 % [5-12]. This variation may be due to the climatic condition. The distribution of clinical types in suspected cases was as follows: toenail onychomycosis 1126, tinea corporis 930, tinea pedis 679, tinea capitis 598, fingernail onychomycosis 473, and tinea manuum 274.
From the 679 suspected cases of tinea pedis, 319 (46.98% CI: 0.42-0.52) cases were positive in direct examination as the most common dermatophytosis. Similar findings were reported by Kak et al. in India  and by Abastabar et al. in Iran . This positive rate was in agreement with findings of a similar study by Kawai et al. in Japan (46.1%) , while this rate was lower than the rate reported by Cai et al. in China (71.19%) . All the positive cases were observed in adults, and this condition was not diagnosed in children. This type of infection is generally of low incidence in children as mentioned in studies conducted in Nigeria and Ethiopia [17, 18]. The positive rate was higher in males (54.23%) than females (45.76%; P=0.03). The study of Didehdar et al. in Iran showed that the frequency of dermatophytosis was higher in males than females . In this study, dermatophytosis were more frequently isolated (99.05%) than candidiasis (0.95%).
The suspected tinea capitis cases consisted of 463 children and 135 adult. In addition, 238 (39.79%, CI: 0.35-0.45) children were found positive by direct exam as reported in India . In the Nigerian community, the incidence of this tinea was 35.2%, which is slightly similar to our result , but it was lower in an Ethiopian study (8.7%) . In our study, male children were more frequently infected with tinea capitis than female children (65.12%, 34.88%, respectively; P=0.00). The higher incidence in males could be due to their higher contact with animals or some activities that are more common among males than females. Microsporic tinea was more frequent (82.35 %) than trichophytic tinea (17.65 %). The same result was published in Italy , which showed that ectothrix pattern of hair invasion is more common (72%). In contrast, the studies carried out in Kenya and Palestine showed higher prevalence rate of Trichophyton spp. than Micropsorum spp. in children [22, 23].
From a total of 930 suspected tinea corporis, only 236 (25.38%, CI: 0.22-0.29) cases were positive in direct examination. There was no significant difference between males and females in this regard (P=0.09). Most positive cases were observed in adults (87.71%), compared to children (12.29%). Dermatophytes were the most frequently (80%) isolated fungi (Table 1). The obtained rate in this study were higher compared to that reported from Nigeria (5.8%) .This type of tinea was the most prevalent in Iranian studies [24, 25].
The positive rate of toenail onychomycosis in our study was 20.33% (CI: 0.18-0.23) by direct exam, while in Serbia this rate was 85.98% . However, this rate was 14.2% in Italy  and 23.7% in Japan . In the current study, females were more positive than males (58.51% and 41.48%, respectively; P=0.00). All the positive cases were observed in adults, and this condition was not diagnosed in children in an Ethiopian study . Analysis of feet and hand onychomycosis in this study showed an increased relationship between dermatophytes and Candida species. In our study, Candida species have high incidence in fingernail onychomycosis, while dermatophytes had a relatively low incidence; in toenail onychomycosis, the opposite was true. Our results are similar to those of studies performed in China and India [19, 20].
|Fungal Infection||Cultures||Positive||Trichophyton rubrum||Candida spp||Aspergillus spp||Micropsorum canis||Trichophyton interdigitale|
|Total||177||69 (38.98)||34(49.27%)||30 (43.47%)||2(2.89%)||2(2.89%)||1(1.44%)|
From the 274 suspected cases of tinea manuum, 44 (16.06%, CI: 0.12-0.22) samples were positive by direct exam. There are few studies available on the epidemiology of tinea manuum at present. In our study, dermatophyte infection was more common than Candida infection (93.08% and 6.92%, respectively).
The difference between males (53.92%) and females (45.14%) was not significant (P=0.07). All the positive cases were observed in adults, and no such cases were diagnosed in children. In the 473 suspected cases of fingernail onychomycosis, 72 (15.22%, CI: 0.12-0.19) cases were positive by direct exam. Distribution frequency of derm-atophytes was 44.45%, while this rate for Candida spp. was 55.55%. Candida infection was more frequent in females (77.5%) than males (22.5%), while dermatophytes infection was equally prevalent in males and females. All the positive cases were observed in adults, and females were more positive (65.27%) than males (34.72%; P=0.00), and no cases of this condition were diagnosed in children.
Only 69 from the 177 cultured samples were positive. Of the 69 positive cultures (Table 1), dermatophyte was the most prevalent isolate (53.62 %) followed by yeasts (43.47%) and non-dermatophyte molds (2.85%). Similar results were obtained in China .
Trichophyton rubrum was the common isolated organism (49.27%), followed by Candida spp. (43.47%), Micropsorum canis (from tinea corporis; 2.89%), Aspergillus spp. (2.89%), and Trichophyton interdigitale (1.44%) (Table 1). Trichophyton rubrum is the most prevalent fungal pathogen. Increased incidence of this species was observed in toenail onychomycosis (91.17%).
From the causative fungal species isolated from fingernail onychomycosis, Candida spp. were the most frequent fungal species (83.33%). As we have noted, the genus Trichophyton was the most common genera of dermatophytes isolated in our study. The prevalence of this causative agent was similar to reports from several regions of the world [12, 13, 18, 20, 26-29].
The frequency of fungal infections vary according to season. The highest frequency of tinea pedis (41.19%) was in summer. Our results are similar to those reported by Sei in Japan . Nonetheless, the highest frequency of cases of tinea capitis were reported in winter and spring (31.95% and 24.10%, respectively). The same result was reported in a similar study conducted in Iran .
Tinea corporis increased in winter and autumn (25.18% and 27.30%, respectively), while the incidence rate of toenail onychomycosis was the highest in summer (25.78%; Table 2). In conclusion, when comparing this study to previous ones on the same subject , the epidemiology of superficial mycosis in Damascus did not significantly change from 2008.
- Ismail MT, Al Kafri A. Study of the types of dermatophytes infections in damascus and its countryside, and the importance of fungal culture in diagnosis. J Arab Board Med Special. 2008; 9(3):51-9.
- Badillet G. Les dermatophytes. Atlas Clinique et biologique. Editions Varia: Paris; 1982.
- Minitab 17 Statistical Software. Minitab, Inc: State College, PA; 2010.
- Lakshmanan A, Ganeshkumar P, Mohan SR, Hemamalini M, Madhavan R. Epidemiological and clinical pattern of dermatomycoses in rural India. Indian J Med Microbiol. 2015; 33(Suppl):134-6.
- Desai SC, Bhat ML. Dermatomycoses in Bombay A study on incidence, clinical features incriminating species of dermatophytes and their epidemically. Indian J Med Res. 1961; 49(4):662-7.
- Ellabib MS, Khalifa Z, Kavanagh K. Dermatophytes and other fungi associated with skin mycoses in Tripoli, Libya. Mycoses. 2002; 45(3-4):101-4.
- 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.
- Papini M, Piraccini BM, Difonzo E, Brunoro A. Epidemiology of onychomycosis in Italy: prevalence data and risk factor identification. Mycoses. 2015; 58(11):659-64.
- 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.
- Bindu V, Pavithran K. Clinico-mycological study of dermatophytosis in Calicut. Indian J Dermatol Venereol Leprol. 2002; 68(5):259-61.
- Yehia MA, El-Ammawi TS, Al-Mazidi KM, Abu El-Ela MA, Al-Ajmi HS. The spectrum of fungal infections with a special reference to dermatophytoses in the capital area of Kuwait during 2000-2005: a retrospective analysis. Mycopathologia. 2010; 169(4):241-6.
- Kannan P, Janaki C, Selvi GS. Prevalence of dermatophytes and other fungal agents isolated from clinical samples. Indian J Med Microbiol. 2006; 24(3):212-5.
- Surendran K, Bhat RM, Boloor R, Nandakishore B, Sukumar D. A clinical and mycological study of dermatophytic infections. Indian J Dermatol. 2014; 59(3):262-7.
- 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.
- Kawai M, Suzuki T, Hiruma M, Ikeda S. A retrospective cohort study of tinea pedis and tinea unguium in inpatients in a psychiatric hospital. Med Mycol J. 2014; 55(2):E35-41.
- Cai W, Lu C, Li X, Zhang J, Zhan P, Xi L. Epidemiology of superficial fungal infections in Guangdong, southern China: a retrospective study from 2004 to 2014. Mycopathologia. 2016; 181(5-6):387-95.
- Kalu EI, Wagbatsoma V, Ogbaini-Emovon E, Nwadike VU, Ojide CK. Age and sex prevalence of infectious dermatoses among primary school children in a rural South-Eastern Nigerian community. Pan Afr Med J. 2015; 20:182.
- Leiva-Salinas M, Marin-Cabanas I, Betlloch I, Tesfasmariam A, Reyes F, Belinchon I. Tinea capitis in schoolchildren in a rural area in southern Ethiopia. Int J Dermatol. 2015; 54(7):800-5.
- Didehdar M, Shokohi T, Khansarinejad B, Ali Asghar Sefidgar S, Abastabar M, Haghani I. Characterization of clinically important dermatophytes in North of Iran using PCR-RFLP on ITS region. J Mycol Med. 2016; 26(4):345-50.
- Barbhuiya JN, Das SK, Ghosh A, Dey SK, Lahiri A. Clinico-mycological study of superficial fungal infection in children in an Urban clinic in Kolkata. Indian J Dermatol. 2002; 47(4):221-3.
- Calabrò G, Patalano A, Fiammenghi E, Chianese C. Tinea capitis in Campania, Italy: a 9-year retrospective study. G Ital Dermatol Venereol. 2015; 150(4):363-7.
- Moto JN, Maingi JM, Nyamache AK. Prevalence of Tinea capitis in school going children from Mathare, informal settlement in Nairobi, Kenya. BMC Res Notes. 2015; 8:274.
- Ali-Shtayeh MS, Yaish S, Jamous RM, Arda H, Husein EI. Updating the epidemiology of dermatophyte infections in Palestine with special reference to concomitant dermatophytosis. J Mycol Med. 2015; 25(2):116-22.
- Rezaei-Matehkolaei A, Rafiei A, Makimura K, Gräser Y, Gharghani M, Sadeghi-Nejad B. Epidemiological aspects of dermatophytosis in Khuzestan, southwestern Iran, an Update. Mycopathologia. 2016; 181(7-8):547-53.
- 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. 2016; 181(1-2):89-95.
- Dubljanin E, Džamić A, Vujčić I, Grujičić SŠ, Arsenijević VA, Mitrović S. Epidemiology of onychomycosis in Serbia: a laboratory-based survey and risk factor identification. Mycoses. 2017; 60(1):25-32.
- Leibovici V, Ramot Y, Siam R, Siam I, Hadayer N, Strauss-Liviatan N. Prevalence of tinea pedis in psoriasis, compared to atopic dermatitis and normal controls-a prospective study. Mycoses. 2014; 57(12):754-8.
- Kiraz N, Metintas S, Oz Y, Koc F, Koku Aksu EA, Kalyoncu C. The prevalence of tinea pedis and tinea manuum in adults in rural areas in Turkey. Int J Environ Health Res. 2010; 20(5):379-86.
- Lim JT, Chua HC, Goh CL. Dermatophyte and non-dermatophyte onychomycosis in Singapore. Australas J Dermatol. 1992; 33(3):159-63.
- Sei Y. 2011 Epidemiological survey of dermatomycoses in Japan. Med Mycol J. 2015; 56(4):J129-35.