Epidemiology of Dermatophytoses in Crete, Greece: a 5-year Survey

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1 Med. Mycol. J. Vol. Med. 57E, Mycol. E 69 J. Vol. E 75, 57(No ), 2016 ISSN E69 Original Article Epidemiology of Dermatophytoses in Crete, Greece: a 5-year Survey Sofia Maraki and Viktoria Eirini Mavromanolaki Department of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine University of Crete Medical School, Heraklion, Crete, Greece ABSTRACT Dermatophytoses are among the most frequently diagnosed skin infections worldwide. However, the distribution of pathogenic species and the predominating anatomical sites of infection vary with geographical location and change over time. The aim of this study was to determine the epidemiological and aetiological factors of dermatophytoses in Crete, Greece over the last 5-year period( )and their incidence in relation to the gender and the age of the patients. We compared our findings with those previously reported from the same area and from other parts of the world. A total of 2,910 clinical specimens(skin scrapings, nail clippings, and hair specimens)obtained from 2,751 patients with signs of dermatomycoses were examined using direct microscopy and culture. Overall, 294 specimens(10.1%) were proved mycologically positive for dermatophytes. The age of the patients ranged from 2 to 86 years(mean age, 37 years). corporis was the predominant clinical type of infection, followed by tinea unguium, tinea pedis, tinea capitis, tinea faciei, tinea cruris and tinea manuum. Among dermatophytes, eight species were isolated: Microsporum canis(35.8%), Trichophyton rubrum(35.1%), Trichophyton mentagrophytes(23.3%), Epidermophyton floccosum(2.5%), Microsporum gypseum(1.8%), Trichophyton violaceum(0.7%), Trichophyton verrucosum(0.4%), and Trichophyton tonsurans(0.4%). In our area, the most common dermatophyte was M. canis followed by T. rubrum. Increased migration, mass tourism, and climate changes will contribute to further changes in the epidemiology of dermatophytoses in our area. Continuing studies are necessary for determining the new epidemiological trends and to implement the appropriate control measures. Key words:dermatophytosis, epidemiology, Greece, ringworm, tinea Introduction Dermatophytoses are fungal infections of the skin, hair, and nails caused by filamentous keratinophilic fungi belonging to three genera: Trichophyton, Microsporum, and Epidermophyton 1). They are among the most frequently encountered causative agents of superficial mycoses, leading to tinea infections that are classified according to the affected body site 2). The distribution of dermatophytes varies with geographical location and change by time, being influenced by several factors, such as climatic variations, migration, socioeconomic conditions, lifestyle, age, underlying diseases, and immunocompetence of the host 3 5). Consideration of the current epidemiology is important for treatment and effective control of the infection 6). Many studies have investigated the prevalence of dermatophytoses in different regions of the world and in many parts of Greece 7 10). Crete is the biggest island located in the southernmost part of the country. The island is visited by thousands of tourists all year around, and currently many immigrants arrive every day. Consequently, the distribution of some species will be influenced, and the epidemiological profile will be changed in this geographical area. The purpose of this study was to determine the Address for correspondence: Sofia Maraki Department of Clinical Microbiology, Parasitology, Zoonoses and Geographical Medicine, University Hospital of Heraklion, Crete, Greece Received: 5, April 2016, Accepted: 21, May sofiamaraki@in.gr

2 E70 Medical Mycology Journal Volume 57, Number 4, 2016 causative agents of dermatophytoses by age, gender, and affected body site in patients admitted to the University Hospital of Heraklion, in Crete, Greece between 2011 and The results were compared with those previously reported from the same area, Greece, Europe, and other regions of the world. Material and methods During a 5-year period( ), a total of 2,910 specimens obtained from patients with clinically suspected dermatomycosis were examined in the Mycology Laboratory at the University Hospital of Heraklion, Crete, Greece. Gender, age, site of involvement, and contact with animals were recorded for each patient. The pathological material(hair, skin scales, nail fragments)was subjected to direct microscopy and culture. Microscopy of specimens was carried out after the addition of 2-3 drops of 20% KOH solution with 36% dimethylsulfoxide. Cultures were performed on Sabouraud dextrose agar containing chloramphenicol, and on Sabouraud dextrose agar containing chloramphenicol and cycloheximide(biomérieux, S.A., Marcy lʼ Etoile, France). Plates were incubated at for 21 days and were examined twice weekly. Incubation of plates showing no growth in 21 days was prolonged for one additional week before discarding them. Identification of the isolated dermatophytes was carried out on the basis of the macroscopic and microscopic characteristics of the fungi, urea testing, growth on Trichophyton agars, and hair perforation assays 11). Statistical analysis of data was based on chisquare test. A difference between groups was considered significant when P < Results Out of 2, 910 clinical specimens obtained from 2,751 patients with signs of dermatomycoses, 294 (10. 1%)were proved mycologically positive for dermatophytes by direct microscopic examination and/or culture. Of these, 15(5. 1%)were found to be positive by direct microscopy only, 6 (2%)were found to be positive by culture only, while 273 were found to be positive by both techniques direct examination and culture. One hundred and fifty-five(52.7%)of the 294 patients were males and 139(47. 3%)were females. The Table 1. Aetiological agents of dermatophytoses in Crete, Greece( ) Species No. Percentage (%) Microsporum canis Trichophyton rubrum Trichophyton mentagrophytes Epidermophyton floccosum Microsporum gypseum 51.8 Trichophyton violaceum Trichophyton verrucosum Trichophyton tonsurans Total age range was 2-86 years(mean, 37 years). The dermatophytic species isolated and their frequencies are shown in Table 1. M. canis was the most frequently isolated species, followed by T. rubrum, T. mentagrophytes, and E. floccosum. These dermatophytes represented 96.7 % of the strains isolated. corporis(34. 4%)was the most common type of infection, followed by tinea unguium(20.1 %), tinea pedis(17. 2 %), tinea capitis(12. 6%), tinea faciei(8.6 %), tinea cruris(3.9%), and tinea manuum(3.2%)(table 2). The prevalence of the various dermatophytes varied between different sites of infection(table 2). M. canis was the most common cause of ringworms of the body, scalp, and face, while T. rubrum was the most prevalent dermatophyte isolated from tinea unguium, tinea pedis, and tinea cruris. The distribution of dermatophyte infections in male and female patients is shown in Table 2. capitis was more frequently observed in children and teenagers. corporis was observed among patients of all age groups, but had maximum prevalence among children < 15 years. unguium occurred mostly among patients years old(table 3). Table 4 indicates the frequency with which the different species occurred in relation to the age of the patients. M. canis was isolated most frequently from patients aged < 15years, while T. rubrum and T. mentagrophytes were more frequently found in dermatomycoses of patients 31-45years. Dermatophytoses occurred throughout the year with substantially higher incidence of M. canis and T. mentagrophytes infections in fall, and T. rubrum infections in summer and winter(fig. 1).

3 Med. Mycol. J. Vol. 57(No. 4), 2016 E71 Table 2. Distribution of the various dermatophyte species in relation to gender and the site of infection Dermatophyte corporis unguium pedis capitis faciei cruris manuum Microsporum canis 17/33 0/2 0/1 19/14 8/50/1 Trichophyton rubrum 14/522/17 15/11 2/3 4/2 2/1 Trichophyton mentagrophytes 12/10 7/6 8/9 1/1 3/2 1/2 2/1 Epidermophyton floccosum 1/0 0/1 2/2 1/0 Microsporum gypseum 0/3 0/1 1/0 Trichophyton violaceum 1/0 0/1 Trichophyton verrucosum 1/0 Trichophyton tonsurans 1/0 Total 45/51 30/26 25/23 20/15 13/11 6/5 6/3 M, male ; F, female. Table 3. Age distribution of patients with dermatophytosis according to the type of tinea Age group(years) < 15y y 31-45y y > 60 y corporis unguium pedis capitis faciei cruris manuum All values are in percentages number of isolates Winter Spring Summer Fall M. canis T. rubrum T. mentagrophytes Fig. 1. Seasonal distribution of the three prevalent dematophyte isolates. Table 4. Age distribution of patients with dermatophytoses according to the dermatophyte species Discussion Dermatophyte Age group(years) < 15y y 31-45y y > 60 y Microsporum canis Trichophyton rubrum Trichophyton mentagrophytes Epidermophyton floccosum Microsporum gypseum Trichophyton violaceum Trichophyton verrucosum Trichophyton tonsurans All values are in percentages Dematophytoses are among the most frequently encountered superficial mycoses worldwide. It has been estimated that they account for 5% of all skin disorders in Greece 9). Dermatophytic infections vary in terms of causative agents and their prevalence according to geographical location and over time in the same area, mainly due to climatic and socioeconomic conditions. In Europe, the incidence and distribution of dermatophytes have changed significantly over the last few decades 12). The present survey revealed a significant decrease in the incidence of dermatophytoses in Crete from 24.2%( )to 10.1%( ) 7). Previous studies from the same area showed that the decrease was gradual 7, 8). Studies from other parts of Greece have demonstrated a similar decline that reflects improved social conditions and sanitary standards 10, 13). M. canis was the most prevalent dermatophyte species isolated from 35.8% of dermatophytic infec-

4 E72 Medical Mycology Journal Volume 57, Number 4, 2016 tions, followed by T. rubrum(35.1%). Previous epidemiological studies from Crete have shown that T. rubrum was the most common species from 1992 to , 8, 14). The present study revealed that the incidence of M. canis significantly increased, compared with previous assessments (P < ). A recent epidemiological survey from southwestern Greece has shown that M. canis is the most common species present since ). Mostly cats and dogs serve as the reservoir of the dermatophyte. Investigators in central Italy found that cats living in rural areas are more frequently infected by M. canis. All 100 stray cats examined were found infected by the dermatophyte, while 8% of cats living in private households were asymptomatic carriers of M. canis 15). Similarly, Khosravi et al. found that 84.6% of the stray cats harbouring M. canis were asymptomatic 16). The low incidence of M. canis in the Grenoble area of France is explained by the absence of wandering cats in the city 17). On the contrary, in Crete, stray cats and dogs are increasing, despite sporadically implemented measures. M. canis was the only dermatophyte isolated from 40% of cats and dogs in northern Italy 18). A similar epidemiologic situation was also reported from southern Italy 19). The infectious arthrospores from the fur of the cats survive in the environment and retain its virulence for a year. Humans can become infected by direct contact with sick animals, healthy carriers, or by contact with contaminated dust, brushes, or clothing 5). corporis was the main clinical type encountered, and it accounted for 34.4% of all infections. This finding is in agreement with our previous data from Crete and from southwestern Greece 8, 10). Similarly, in central and northern Italy, central Poland, and Slovenia, tinea corporis is the most commonly diagnosed clinical type 20 23). M. canis was the most frequent aetiological agent(52.1%), followed by T. mentagrophytes (22.9%)and T. rubrum(19.8%). According to several epidemiologic studies worldwide, the aetiology of tinea corporis is very heterogeneous. In several countries in central, southern, and eastern Europe, M. canis prevail, while in countries in western and northern Europe, in the USA, and in Latin America(Mexico), T. rubrum is the main aetiological agent. In UK and in the USA the anthropophilic species T. tonsurans is the second most common pathogen of tinea corporis after T. rubrum 3). corporis was more common in children than in adults, as reported by others 24). unguium and tinea pedis ranked second and third in prevalence and have been dominated by T. rubrum, which reached 69.4% and 54.2% of the isolated strains, respectively. Our findings are in accordance with previous studies from the island of Crete, studies from other parts of Greece, as well as similar reports from other developed countries worldwide 3, 4, 7, 8, 14, 17, 25, 26). The feet are particularly prone to dermatophytoses because they are the anatomic structures in the most contact with the environment, where infective structures of dermatophytes may remain viable for years. According to Achilles project, the largest survey on foot disease conducted in 20 European countries, tinea pedis and tinea unguium are the most frequently observed fungal infections 27). Feet and toenails are an important reservoir from which fungal infections could spread to other body sites 28). Onychomycosis is the most common infective nail disorder accounting for about 50% of all consultations for nail disorders 29). Males were more frequently affected than females, and tinea unguium was more prevalent in the elderly. According to Gupta and colleagues, the gender difference may be due to differences in hormone levels that result in a different capacity to inhibit dermatophyte growth 30, 31). Several studies have shown that there is a correlation between age and onychomycosis. Onychomycosis increases steadily with age. This may be attributed to slow-growing nails, reduced peripheral circulation, diabetes mellitus, nail trauma, increased exposure to disease-causing fungi, and immunosuppression 32). capitis continues to be an important health problem in Crete, affecting mainly preschool and school children. In the current study tinea capitis constituted 12.5% of all tineas and mainly occurred in the age group < 15years. M. canis predominated as an aetiological agent(94.3 %), followed by T. mentagrophytes. The incidence of tinea capitis varies by gender, depending on the infecting organism. When the causative agent is M. canis, the infection rate in boys is usually higher 33). capitis is mostly caused by M. canis worldwide and also in Europe and most especially in the Mediterranean area 3 5, 34, 35).Itis noteworthy that there is a shift towards the anthropophilic tineas in Europe, mainly due to high immigration 3 5). In Athens, Greece, the inci-

5 Med. Mycol. J. Vol. 57(No. 4), 2016 E73 dence of tinea capitis due to T. violaceum increased considerably over the last decades due to the immigration wave, mainly from Albania 36). T. violaceum cases of tinea capitis are increasingly reported in Sweden, Barcelona and Madrid in Spain, Italy, and Switzerland; T. tonsurans in UK, France, Netherlands, Spain, and Ireland; and Microsporum audouinii in Germany, UK, France, and Belgium 3 5). Ringworm of the face accounted for 8.6% of all dermatophytoses. Almost half of the cases were diagnosed in children under 15years of age, with a peak between 2 and 12 years. faciei is observed more frequently in children as a result of contact with domestic and stray animals, such as cats and dogs 37, 38). Similar to other studies, males were more frequently affected than females 37). In the present study, the zoophilic species M. canis followed by T. mentagrophytes accounted for the majority(75%)of the isolates, and in 61% of these cases, close contact with animals(mainly cats)was reported, as described by others 37 39). The aetiological agent of tinea faciei varies according to geographic region 3 5). In Northern Greece and Italy, M. canis is the predominant agent; in Spain and in Switzerland (Zurich area), T. mentagrophytes; in Iran, T. verrucosum; in the USA, T. tonsurans, T. rubrum, and M. canis; and in Sweden, T. violaceum 9, 38 43). cruris accounted for 3.9% of all dermatophytoses. Similar to other studies, T. rubrum was the predominant aetiological agent followed by T mentagrophytes 7 9, 14, 21, 43). Adults were much more commonly affected than were children. Risk factors for ringworm of the groin include wearing tightly-fitting or wet clothing for extended periods, sharing clothing with others, or coexisting diabetes mellitus or obesity 44). manuum was the least common clinical presentation. T. rubrum and T. mentagrophytes were the most commonly isolated species. This is in accordance with our previous studies from Crete, Greece, and other countries worldwide 7 9, 14, 45). Males were more frequently affected than females, possibly due to their increased involvement in outdoor activities. The highest prevalence of M. canis and T. mentagrophytes infections was registered in fall, while T. rubrum infections showed a peak in summer and winter. With regard to seasonality, Iorio et al. found that M. canis infections occurred more frequently in the warm seasons 15), investigators from India observed higher incidence of dermatophytoses in summer 46), while others from Iran detected a rise in their incidence in winter and fall due to the lower temperature and the higher humidity 47). Continuing studies on dermatophytoses will improve our knowledge on the epidemiology of these infections in our area, which is expected to further change in the future as a result of mass tourism, migration, climatic variations, and changes in population demographic characteristics and lifestyle practices. Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and the writing of the paper. References 1)Dahdah MJ, Scher RK: Dermatophytes. Curr Fungal Infect Rep 2: 81-86, )Degreef H: Clinical forms of dermatophytosis (ringworm infection). Mycopathologia 166: , )Seebacher C, Bouchara JP, Mignon B: Updates on the epidemiology of dermatophyte infections. Mycopathologia 166: , )Havlickova B, Czaika VA, Friedrich M: Epidemiological trends in skin mycoses worldwide. Mycoses 51 Suppl 4: 2-15, )Nenoff P, Krüger C, Ginter-Hanselmayer G, Tietz HJ: Mycology an update. Part 1: Dermatomycoses: causative agents, epidemiology and pathogenesis. J Dtsch Dermatol Ges 12: , )Ely JW, Rosenfeld S, Seabury Stone M: Diagnosis and management of tinea infections. Am Fam Physician 90: , )Maraki S, Tselentis Y: Dermatophytoses in Crete, Greece, between 1992 and Mycoses 41: , )Maraki S: Epidemiology of dermatophytoses in Crete, Greece between 2004 and G Ital Dermatol Venereol 147: , )Devliotou-Panagiotidou D, Koussidou-Eremondi T, Badillet G: Dermatophytosis in northern Greece during the decade Mycoses 38: , )Tsoumani M, Jelasopulu E, Bartzavali C, Vamvakopoulou S, Dimitracopoulos G, Anastassiou ED, Christofidou M: Changes in dermatophytoses in southwestern Greece: an 18-year survey. Mycopathologia 172: 63-67, )Larone DH ed: Medically important fungi a guide to identification, 5th ed, ASM Press, Washington

6 E74 DC, )Hayette MP, Sacheli R: Dermatophytosis, trends in epidemiology and diagnostic approach. Curr Fungal Infect Rep 9: , )Frangoulis E, Papadogeorgakis H, Athanasopoulou B, Katsambas A: Superficial mycoses due to Trichophyton violaceum in Athens, Greece: a 15-year retrospective study. Mycoses 48: , )Maraki S, Nioti E, Mantadakis E, Tselentis Y: A 7- year survey of dermatophytoses in Crete, Greece. Mycoses 50: , )Iorio R, Cafarchia C, Capelli G, Fasciocco D, Otranto D, Giangaspero A: Dermatophytoses in cats and humans in central Italy: epidemiological aspects. Mycoses 50: , )Khosravi AR: Fungal flora of the hair coat of stray cats in Iran. Mycoses 39: , )Faure-Cognet O, Fricker-Hidalgo H, Pelloux H, Leccia MT: Superficial fungal infections in a French teaching hospital in Grenoble area: retrospective study on 5470 samples from 2001 to Mycopathologia 181: 59-66, )Marchisio VF, Gallo MG, Tullio V, Nepote S, Piscozzi A, Cassinelli C: Dermatophytes from cases of skin disease in cats and dogs in Turin, Italy. Mycoses 38: , )Cafarchia C, Romito D, Sasanelli M, Lia R, Capelli G, Otranto D: The epidemiology of canine and feline dermatophytoses in southern Italy. Mycoses 47: , )Panasiti V, Devirgiliis V, Borroni RG, Mancini M, Curzio M, Rossi M, Bottoni U, Calvieri S: Epidemiology of dermatophytic infections in Rome, Italy: a retrospective study from 2002 to Med Mycol 45: 57-60, )Asticcioli S, Di Silverio A, Sacco L, Fusi I, Vincenti L, Romero E: Dermatophyte infections in patients attending a tertiary care hospital in northern Italy. New Microbiol 31: , )Jeske J, Lupa S, Seneczko F, Glowacka A, Ochecka-Szymańska A: Epidemiology of dermatomycoses of humans in central Poland. Part V. corporis. Mycoses 42: , )Dolenc-Voljc M: Dermatophyte infections in the Ljubljana region, Slovenia, Mycoses 48: , )Macura AB: Dermatophyte infections. Int J Dermatol 32: , )Ioannidou DJ, Maraki S, Krasagakis SK, Tosca A, Tselentis Y: The epidemiology of onychomycoses in Crete, Greece, between 1992 and J Eur Acad Dermatol Venereol 20: , )Nasr A, Vyzantiadis TA, Patsatsi A, Louka A, Ioakimidou A, Zachrou E, Chavale A, Kalabalikis D, Malissiovas N, Sotiriadis D: Epidemiology of superficial mycoses in Northern Greece: a 4-year study. J Eur Acad Dermatol Venereol 30: , )Burzykowski T, Molenberghs G, Abeck D, Haneke E, Hay R, Katsambas A, Roseeuw D, van de Medical Mycology Journal Volume 57, Number 4, 2016 Kerkhof P, van Aelst R, Marynissen G: High prevalence of foot diseases in Europe: results of the Achilles Project. Mycoses 46: , )Szepietowski JC, Reich A, Garlowska E, Kulig M, Baran E; Onychomycosis Epidemiology Study Group: Factors influencing coexistence of toenail onychomycosis with tinea pedis and other dermatomycoses: a survey of 2761 patients. Arch Dermatol 142: , )Elewski BE: Onychomycosis. Treatment, quality of life, and economic issues. Am J Clin Dermatol 1: 19-26, )Gupta AK, Jain HC, Lynde CW, Watteel GN, Summerbell RC: Prevalence and epidemiology of unsuspected onychomycosis in patients visiting dermatologistsʼ offices in Ontario, Canada a multicenter survey of 2001 patients. Int J Dermatol 36: , )Clemons KV, Schär G, Stover EP, Feldman D, Stevens DA: Dermatophyte-hormone relationships: characterization of progesterone-binding specificity and growth inhibition in the genera Trichophyton and Microsporum. J Clin Microbiol 26: , )Thomas J, Jacobson GA, Narkowicz CK, Peterson GM, Burnet H, Sharpe C: Toenail onychomycosis: an important global disease burden. J Clin Pharm Ther 35: , )Elewski BE: capitis: a current perspective. J Am Acad Dermatol 42: 1-20, )Maraki S, Tselentis Y: Survey on the epidemiology of Microsporum canis infections in Crete, Greece over a 5-year period. Int J Dermatol 39: 21-24, )Ginter-Hanselmayer G, Weger W, Ilkit M, Smolle J: Epidemiology of tinea capitis in Europe: current state and changing patterns. Mycoses 50 Suppl 2: 6-13, )Frangoulis E, Athanasopoulou B, Katsambas A: Etiology of tinea capitis in Athens, Greece a 6- year( )retrospective study. Mycoses 47: , )Atzori L, Aste N, Aste N, Pau M: faciei due to Microsporum canis in children: a survey of 46 cases in the District of Cagliari(Italy). Pediatr Dermatol 29: , )Lin RL, Szepietowski JC, Schwartz RA: faciei, an often deceptive facial eruption. Int J Dermatol 43: , )Nicola A, Laura A, Natalia A, Monica P: A 20-year survey of tinea faciei. Mycoses 53: , )del Boz J, Crespo V, de Troya M: Pediatric tinea faciei in southern Spain: a 30-year survey. Pediatr Dermatol 29: , )Kieliger S, Glatz M, Cozzio A, Bosshard PP: capitis and tinea faciei in the Zurich area an 8- year survey of trends in epidemiology and treatment patterns. J Eur Acad Dermatol Venereol 29: , )Aghamirian MR, Ghiasian SA: Dermatophytoses in outpatients attending the Dermatology Center of

7 Med. Mycol. J. Vol. 57(No. 4), 2016 Avicenna Hospital in Qazvin, Iran. Mycoses 51: , )Drakensjö IT, Chryssanthou E: Epidemiology of dermatophyte infections in Stockholm, Sweden: a retrospective study from Med Mycol 49: , )Gupta AK, Chaudhry M, Elewski B: corporis, tinea cruris, tinea nigra and piedra. Dermatol Clin 21: , )Zhan P, Geng C, Li Z, Jiang Q, Jin Y, Li C, Liu W: The E75 epidemiology of tinea manuum in Nanchang area, South China. Mycopathologia 176: 83-88, )Goyal R, Tinna G, Gupta A, Sharma BP: Epidemio clinico microbiological study of dermatophytosis in north west region of Rajasthan, India. Int J Curr Microbiol App Sci 4: , )Khosravi A, Kordbacheh P, Bokaee S: An epidemiological approach to the zoophilic dermatophytoses in Iran. MJIRI 7: , 1994.