Incidence and etiological agents of genital dermatophytosis in males

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1 ORIGINAL ARTICLE Incidence and etiological agents of genital dermatophytosis in males Asja Prohić, Mersiha Krupalija-Fazlić, Tamara Jovović Sadiković Department of Dermatovenerology, University Clinical Center Sarajevo, Sarajevo, Bosnia and Herzegovina ABSTRACT Aim To determine the incidence and etiological agents of dermatophytosis of male genitalia in Sarajevo area, Bosnia and Herzegovina, during a 5-year period ( ). Methods A total of 313 male patients with confirmed dermatophyte infection elsewhere in the body was analyzed. All samples (skin scrapings and hairs) were treated with lactophenol to detect a possible presence of fungal elements and then cultured on Sabouraud glucose agar. Dermatophytes species were identified based on macroscopic and microscopic morphology. Corresponding author: Asja Prohić Department of Dermatovenerology, University Clinical Center Sarajevo Bolnička 25, Sarajevo, Bosnia and Herzegovina Phone: ; Fax: ; asjaprohic@hotmail.com Results Dermatopyte infection of penis and/or scrotum was confirmed by positive cultures in 17 (5.4%) patients, of which four had lesions on the penis alone, five had lesions on scrotum and eight patients had lesions on both penis and scrotum. Majority of patients, 12 (70.0%) belonged to the age group Fifteen patients (88.2%) had associated foci of dermatophyte infection, but the inguinal area was most frequently affected, in 10 (66.6%) patients. Microsporum canis was the most frequent dermatophyte found on culture, in 10 (58.8%) patients. Conclusion Dermatophytosis of male genitalia is a rare entity, occurring more often in young males and the main causative species is Microsporum canis. Key words: tinea, male genitalia, incidence, etiology Original submission: 14 October 2014; Accepted: 24 October Med Glas (Zenica) 2015; 12(1):

2 Prohić et al. Dermatophytosis of the male genitalia INTRODUCTION Dermatophyte (tinea) infections of penis and scrotum are relatively rare compared with those involving the inguinal area (1). The infection usually extends from the inguinal area to the scrotum and uncommonly to the penis, but rarely occurs on the glans or prepuce (2). Different factors such as occlusive clothing, systemic diseases and a reservoir of dermatophytes at any other body site are considered to contribute to the occurrence of infections, which mainly affect young males (1,3,4). The incidence of tinea in males is traditionally considered to be very low (4-6). On the other hand, some studies report it as quite common (7-9). Moreover, there are different results regarding the causative dermatophyte species in this particular body site in males (4,7,9) These controversial opinions regarding the rarity of this entity incited us to undertake an investigation to find out incidence and etiological agents of male genitalia in individuals with dermatophytosis of the skin in population of Sarajevo region, Bosnia and Herzegovina. PATIENTS AND METHODS During a five-year period ( ), clinical presence of dermatophytosis of the penis and/ or scrotum has been studied in 313 male patients who reported the Department of Dermatovenerology, University Clinical Center Sarajevo, Bosnia and Herzegovina, with dermatophytosis elsewhere in the body. The samples were taken from a prominent border of the lesions and examined in the Mycological Laboratory of the Institute of Microbiology, Parasitology and Immunology, Sarajevo University Clinical Center. No patient gave any history of diabetes, tuberculosis or any other immunosuppressive condition in the recent past. Mycological examination consisted of direct microscopy and culture identification of causative agents. All scrapings were examined in 10% potassium hydroxide (KOH) solutions directly under the microscope and cultivated on Sabouraud glucose agar with added chloramphenicol and cycloheximide. The cultures were incubated at 27 o C for up to 6 weeks and observed weekly for evidence of growth. The identification of dermatophytes was based on their macroscopic and microscopic characteristics of the colonies (10). RESULTS Among 313 male patients who attended the Department of Dermatovenerology, University Clinical Center Sarajevo, Bosnia and Herzegovina, with dermatophytosis elsewhere in the body, KOH preparations of the skin scraping from the lesions showed mycelia of dermatophyte in 17 (5.4%) patients. The causative dermatophyte species was identified by positive cultures in 17 (5.4%) patients. Microsporum (M.) canis was the most frequent dermatophyte isolated, in 10 (58.8%), followed by Epidermophyton (E.) floccosum, in five (29.4) and Trichophyton (T.) mentagrophytes var. interdigitalis in two (11.8%) patients. Majority of the patients with positive culture findings, 12 (70.0%) belonged to the age group years, followed by years age group, three (17.7%) patients. No patients belonged to age group below 10 or above 51 years of age (Table 1). Table 1. Age distribution of patients with genital dermatopytosis Age group (years) No (%) of patients (5.8) (70) (17.7) (5.8) 51 and above 0 Of the 17 patients with positive culture findings, penile dermatophytosis was found in four (23.5%) patients, scrotal lesions in five (29.4%) patients, both penile and scrotal lesions in eight (47.0%) patients. None of the patients had lesions on the glans or prepuce. Wives of the six married patients (35.3%) were examined and found to be free from genital infection. Solitary involvement of the penis or scrotum without the involvement of the crural region or any other regions was found in two (11.8%) patients. Fifteen (88.2%) patients showed tinea infection at other anatomical sites of whom ten (66.7%) patients presented with tinea cruris, four (26.7) with tinea unguium and one (6.7) patient with tinea pedum (Table 2). Table 2. Sites of involvement in patients with genital dermatopytosis Site of the lesion No (%) of patients Penis 4 (23.5) Scrotum 5 (29.4) Penis and scrotum 8 (47.0) Other sites of dermatophytosis 15 (88.2) Solitary genital involvement 2 (11.8) 53

3 Medicinski Glasnik, Volume 12, Number 1, February 2015 DISCUSSION Dermatophytosis of male genitalia has been regarded as a rare entity since its first description in 1860 by Ferdinand Ritter von Hebra ( ), a founder of the Vienna School of Dermatology (11). So far the same opinion has been supported by many other investigators (4-6). A study conducted in Italy has shown low frequency because the authors reported nine cases of male tinea genitalis over a period of fifteen years (4). In another study from India, of 2200 patients with confirmed dermatophytosis, approximately 1% had penile involvement (8). Some authors attributed rarity of the genital involvement to capric acid and some fungistatic serum factor and sebum (12). Contrary to this, some studies from different researchers showed that dermatophytosis of male genitalia is quite common, particularly from tropical countries, where the reported incidence was 21% (7). Similarly, Gupta and Banerjeer reported six cases of dermatophytes of male genitalia in a short period of three months (9). Our observation shows an incidence of 5.4% of all examined patients to be a relatively rare entity. The low incidence in our study, but also in aforementioned studies, may be due to difference in climate and socioeconomic condition. Climate plays an important role and the higher incidence of the infection in the tropics has been noted during the rainy season of a year when humidity was more than 95% (7). The low incidence could be also attributed to the fact that the disease could go unnoticed because the clinical manifestations are slight and healing is often spontaneous (9). In this study most of the patients with penile and/ or scrotal dermatophytosis (70.37%) belonged to the age group 21-40, which is in concordance with the majority of the studies, which found that young males were most susceptible to the dermatophyte infection of genital region (7,13). Surprisingly no patients belonged to age group below 10 or above 50 years of age which was also abserved by Pandey et al. (14) and Vora et Mukhopadhyay (7). Further investigations are required particularity in this age group. The presence of tinea infection at other anatomical sites may serve as a reservoir of infection. Especially tinea cruris, tinea pedis and toenail onychomycosis are common sources of infection of male genitalia (7,8,14,15). In our study, the lesions situated on penis and scrotum were preceded by dermatophytosis in inguinal area in 58.8% patients, which indicates that the infection probably started in the crural region and spread later to the genitalia. Glans penis involvement is considered even rarer (16), whereas dermatophytosis of the prepuce has not been reported in the literature. In our case series, none of the patients had lesions on glans and/or prepuce, which supports earlier reports. Solitary involvement of the penis or scrotum without the involvement of any other regions was found in 11.8 % males, which indicates the possibility that penis and scrotum may be infected with dermatophytosis de novo without involvement of any other area (2,6,17). Our study has confirmed zoophilic dermatophyte M. canis as being the most common species isolated from genital area. However, most studies reported T. rubrum as a common pathogen (4,7,9,15,17,18), although E. floccosum and T. mentagrophytes var. interdigitale have also been isolated from the genital region (4,7,17). High isolation rate of M. canis from the genital region (58.8%) correlates with the high frequency of this species in our population in general (19). In the last fifteen years, an increasing incidence of zoophilic dermatophytes, especially M. canis has been observed in many regions in Europe (20). Generally, the prevalence of M. canis in our population is one of the highest in Europe (90.4) (20) and is comparable only with rates reported from Italy (90.5) (21), Grace (84.5%) (22) and Spain (63.5%) (23). The high prevalence of this dermatophyte species can be attributed to the increase in the number of domestic animals particularly cats living outside homes and consequently an increase in the phenomenon of animals stray and semistray (24). Presumably stray cats are the major reservoir and carriers of M. canis. It is widely accepted that dermatophytes are keratinophilic in nature and they invade their host by enzymatic digestion of keratin. This can explain the rarity of tinea infections on male genitalia, since anatomically the glans penis and inner surface of the prepuce are covered with non-keratinized epithelium. Overweight, occlusion, high moisture, inadequate hygiene, diabetes, previous antibiotic treatment and immunosuppression are common predisposing factors. 54

4 Prohić et al. Dermatophytosis of the male genitalia In tinea of the genital region individual treatment approach is needed, considering both local and systemic susceptibility factors. Topical antifungal treatment is usually sufficient in acute infections. In many cases, systemic treatment with either azoles or terbinafin may be needed in cases of widespread dermatophytic infection (25). To conclude, our results suggest that dermatophytosis of male genitalia with an incidence of 5.4% is rare mycotic infection of this particular REFERENCES 1. Nenoff P, Krüger C, Schaller J, Ginter-Hanselmayer G, Schulte-Beerbühl R, Tietz HJ. Mycology - an update Part 2: Dermatomycoses: Clinical picture and diagnostics. J Dtsch Dermatol Ges 2014; 12: Dekio S, Jidoi J. Tinea of the glans penis. Dermatologica 1989; 178: Aridogan IA, Izol V, Ilkit M. Superficial fungal infections of the male genitalia: a review. Crit Rev Microbiol 2011; 37: Romano C, Ghilardi A, Papini M. Nine male cases of tinea genitalis. Mycoses 2005; 48: Arnold HL, Jr, Odom RB, James WD. Andrews Diseases of the Skin-Clinical Dermatology (8th ed.). Philadelphia: WB Saunders Co., Palleschi GM, Guadagni R, Difonzo E, Panconesi E. Tinea of the penis: a rare occurrence. Internat J Dermatol 1986; 25: Vora NS, Mukhopadhyay AK. Incidence of dermatophytosis of penis and scrotum. Indian J Dermatol Venerol Leprol 1994; 60: Kumar B, Talwar P, Kaur S. Penile tinea. Mycopathologia 1981; 75: Gupta R, Banerjee U. Tinea of the penis. Ind J Dermatol Venereol Leprol 1992; 58: Moriello KA. Diagnostic techniques for dermatophytosis. Clin Tech Small Anim Pract 2001; 16: La Touche CJ. Scrotal dermatophytosis : an insufficiently documented aspect of tinea cruris. Brit J Dermatol 1967; 79: Pavitran K. Dermatophytosis of the scrotum, penis and lip. Ind J Dermatol Venereol Leprol 1987; 53: Phadke SN, Gupta DK, Agarwal S. Dermatophytosis in Jabalpur. Ind J Pathol Bacteriol 1973; 16:42. body site. The infection affects more often young males, occurring more often on the penis and scrotum at the same time. Zoophyte species M. canis is the most frequently isolated dermatophyte. FUNDING No specific funding was received for this study. TRANSPARENCY DECLARATION Competing interests: None to declare 14. Pandey SS, Chandra S, Guha PK, Kaur P, Singh G. Dermatophyte infection of the penis. Association with particular undergarments. Internat J Dermatol 1981; 20: Pielop J, Rosen T. Penile dermatophytosis. J Am A Dermatol 2001; 44: D Antuono A, Bardazzi F, Andalou F. Unusual manifestation of dermatophytosis. Int J Dermatol 2001; 40: Das JK, Sengupta S, Gongopadhyay A. Dermatophyte infection of the male genitalia. Indian J Dermatol 2009; 54: Mukhopadhyay AK. Trichophyton rubrum infection of the prepuce. Indian J Dermatol Venereol Leprol 2005; 71: Prohić A. Prevalence of zoophilic dermatophytes in Sarajevo area. Med Arh 2003; 57: Skerlev M, Miklić P. The changing face of Microsporum spp. infections. Clin Dermatol 2010; 28: Romano C. Tinea capitis in Siena, Italy. An 18-year survey. Mycoses 1999; 42: Frangoulis E, Athanasopoulou B, Katsambas A. Etiology of tinea capitis in Athens, Greece - a 6-year ( ) retrospective study. Mycoses 2004; 47: del Boz J, Crespo V, Rivas-Ruiz F, de Troya M. A 30-year survey of paediatric tinea capitis in southern Spain. J Eur Acad Dermatol Venereol 2011; 25: Proverbio D, Perego R, Spada E, Bagnagatti de Giorgi G, Della Pepa A, Ferro E. Survey of dermatophytes in stray cats with and without skin lesions in Northern Italy. Vet Med Int 2014; 2014: Pires CA, Cruz NF, Lobato AM, Sousa PO, Carneiro FR, Mendes AM. Clinical, epidemiological, and therapeutic profile of dermatophytosis. An Bras Dermatol 2014; 89:

5 Medicinski Glasnik, Volume 12, Number 1, February 2015 Incidenca i etiološki agensi genitalne dermatofitije kod muškaraca Asja Prohić, Mersiha Krupalija-Fazlić, Tamara Jovović Sadiković Klinika za kožne i spolne bolesti, Klinički centar Univerziteta u Sarajevu, Sarajevo, Bosna i Hercegovina SAŽETAK Cilj Utvrditi incidencu i etiološke agense genitalne dermatofitoze kod muškaraca na području Sarajeva, u petogodišnjem periodu (od do godine). Metode Analizirano je ukupno 313 muškaraca s potvrđenom dermatofitnom infekcijom druge lokalizacije. Svi uzorci (ljuske s kože i dlake) preparirani su u laktofenolu radi otkrivanja eventualno prisutnih gljivičnih elemenata i zatim kultivirani na Sabouraud glukoza agaru. Rezultati Dermatofitna infekcija penisa i/ili skrotuma potvrđena je pozitivnom kulturom kod 17 (5,4%) pacijenata, od kojih je četiri imalo promjene samo na penisu, pet na skrotumu, dok je njih osam imalo promjene na penisu i skrotumu. Većina pacijenata, 12 (70%), pripadala je dobnoj skupini od 21 do 40 godina. Petnaest (88,2%) pacijenata imalo je dermatofitnu infekciju druge lokalizacije, od kojih je najčešće bilo zahvaćeno ingvinalno područje, 10 (66,6%). Microsporum canis bio je najčešće izolirani specijes u kulturi, 10 (58,8%). Zaključak Dermatofitoza muških genitalija je rijetka pojava, češće prisutna kod mlađih muškaraca, a glavni uzročnik je Microsporum canis. Ključne riječi: tinea, genitalije muškarca, incidenca, etiologija 56