A nationwide survey of Trichophyton tonsurans infection among combat sport club members in Japan using a questionnaire form and the hairbrush method

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1 A nationwide survey of Trichophyton tonsurans infection among combat sport club members in Japan using a questionnaire form and the hairbrush method Yumi Shiraki, MD, a Masataro Hiruma, MD, PhD, a Nobuyoshi Hirose, PhD, b Takashi Sugita, PhD, c and Shigaku Ikeda, MD, PhD a Tokyo and Chiba, Japan Background: The emerging outbreak of Trichophyton tonsurans infection among members of combat sports clubs in Japan during the last 4 years has become a serious public health problem. To overcome this outbreak, a survey for T. tonsurans infection in Japan may be essential. Objectives: We sought to clarify the prevalence of T. tonsurans infection among members of combat sports clubs in Japan. Methods: We conducted a survey of members of participating combat sports clubs using a standardized questionnaire to assess background factors and using the hairbrush method to identify T. tonsurans infection. Statistical significance of the correlation between data from the questionnaire and the hairbrush culture results was determined. Results: We surveyed 1000 people (826 male) from 49 institutions and found 115 (11.5%) were positive for T. tonsurans infection revealed by the hairbrush method. Demographic factors associated with high positive rates ($20%) of the infection were familial T. tonsurans infection (20.0%), history (24.2%), increased dandruff (32.1%), and concomitant tinea corporis (31.6%). Those with positive hairbrush culture results without current or previous tinea were considered asymptomatic carriers. Limitations: The study population was limited to members of judo clubs all over Japan; they were asked to participate in this survey via the All Japan Judo Federation. Conclusion: Infection of T. tonsurans appears to have spread widely among members of combat sports club in Japan. The questionnaire used in this study is a simple and useful tool to estimate epidemiology of this infection. ( J Am Acad Dermatol 2006;54:622-6.) In Japan, the reports of Trichophyton tonsurans infection among combat sport club members have been significantly increasing since 2001, From the Department of Dermatology, Juntendo University School of Medicine, Tokyo a ; Seminar of Judo, School of Health and Sports Science, Jaunted University, Chiba b ; and Department of Microbiology, Meiji Pharmaceutical University, Tokyo. c Funding sources: None. Conflicts of interest: None identified. Accepted for publication November 1, Reprint requests: Yumi Shiraki, MD, Department of Dermatology, Juntendo University School of Medicine, 2-1-1, Hongo, Bunkyoku, Tokyo, , Japan. yshiraki@med.juntendo.ac.jp. Published online February 1, /$32.00 ª 2006 by the American Academy of Dermatology, Inc. doi: /j.jaad suggesting that this infection is becoming a serious public health problem. 1-5 Screening examinations of the disease at combat sport institutions initiated in December 2001 showed that the infection rate ranged from 35% to 40%. 1 During the screening, we detected several asymptomatic carriers who showed a positive fungal culture and lacked clinical symptoms or signs of tinea capitis. To control outbreak of T. tonsurans infection, it would be insufficient to treat symptomatic patients, because asymptomatic carriers could be the reservoirs and spread the organism. From these considerations, the first step in controlling outbreak of T. tonsurans infection is to determine the prevalence of the disease and at the same time identify the asymptomatic carriers. To assess the current situation of T. tonsurans infection in Japan, we conducted a nationwide 622

2 JAM ACAD DERMATOL VOLUME 54, NUMBER 4 Shiraki et al 623 questionnaire survey by using the hairbrush method in combat sport club members in Japan. METHODS Participant registry We have published a leaflet showing the clinical characteristics, methods of diagnosis, and treatment regimens of T. tonsurans infection. These leaflets were distributed to judo institutions all over Japan via the All Japan Judo Federation, asking members to participate in the survey. 1 Directing managers or coaches of the institutions who agreed to participate in the survey were asked to complete application forms describing the location of the institution and the number of club members who agreed to participate in the survey. All club members who agreed to participate provided written informed consent. After receiving the application forms, we sent participating clubs the questionnaire forms and round, 126-bristle, shampoo hairbrushes (Makoto Co., Sakai, Osaka, Japan). Participants were asked to fill out the questionnaire forms under the supervision of their managers or coaches. Demographic information requested in the questionnaire included age, sex, height, weight, and residence conditions (eg, house, apartment, dormitory). The participants were also monitored for current or previous possible tinea corporis eruptions. For the hairbrush culture, participants were asked to brush their hair all over the head 10 to 15 times. The brushes were sent back to us in individual sterile plastic bags, and then spikes of each brush were stabbed into Mycosel agar (Eiken Chemical Co., Bunkyo, Tokyo, Japan), creating 126 inoculations corresponding to the 126 bristles per brush. Cultures were examined after 2-week incubation at 258C, and causative fungi were identified by morphology of cultured fungi. The number of colonies was also recorded. Statistical significance of the correlation between the significance of each item in the questionnaire and the positive status of fungus in the hairbrush culture was determined using Fisher exact, Mann-Whitney U, ort test. RESULTS Participants We screened a total of 1247 members at 49 institutions (22 colleges, 22 high schools, 3 junior high schools, and 2 others). The mean number of members of judo clubs was 25.4, and the response rate was perfect. We excluded 247 participants who did not answer all of the questions in the questionnaire form, leaving 1000 participants whose information was sufficient for the analysis. The 1000 evaluable participants consisted of 826 men (82.6%) and 174 women (17.4%). The majority (501; 50.1%) lived in houses with their families, and the remainder lived in dormitories (264; 26.4%) or apartments (235; 23.5%). Of the 1000 evaluable participants, 161 (16.1%) had atopic dermatitis. Most (597; 59.7%) had club members infected with tinea corporis, and 75 (7.5%) had family members with T. tonsurans infection. More than one third (376; 37.6%) had a history, 326 (32.6%) reported previous treatment for tinea corporis, and 187 (18.7%) showed concomitant tinea corporis. A total of 101 showed recurrent dandruff formation (10.1%), and 53 (5.3%) had recently increased dandruff. Hairbrush culture results Of the participants tested, 115 (11.5%) were positive for T. tonsurans by the hairbrush method. The number of colonies formed from the 126 bristles per hairbrush stabbed in the culture medium ranged from 1 to 4 in 41 of 115 (35.7%), from 5 to 50 in 32 (27.8%), and from 51 to 126 in 42 (36.5%). Associations between positive status of hairbrush culture results and demographic factors Table I summarizes the demographic factors that correlate with the positive results in the hairbrush culture. Multiple factors (sex, residence condition, presence of familial T. tonsurans infection, presence of colleagues with T. tonsurans infection, history of tinea corporis, history of treatment for tinea corporis, increased dandruff, current tinea corporis, and atopic dermatitis) were statistically associated with positive results in hairbrush culture. Among the factors associated with high positive rates ($20%) in the hairbrush culture were the following: presence of familial infection (15/75; 20.0%), history (91/376; 24.2%), history of treatment for tinea corporis (83/326; 25.5%), increased dandruff (17/53; 32.1%), and concomitant tinea corporis (59/187; 31.6%). We also assessed the association of current or previous tinea corporis infection with positive or negative culture results by the hairbrush method. For this analysis, the 1000 participants were classified into 4 categories: group 1, those without current or history (3.0%); group 2, those without previous tinea corporis infection with current tinea corporis (15.9%); group 3, those with concomitant tinea corporis without previous tinea corporis (12.3%); and group 4, those with both

3 624 Shiraki et al JAM ACAD DERMATOL APRIL 2006 Table I. Associations between positive status of hairbrush culture results and demographic factors (n = 1000) Background factor No. of participants Positive Negative Positive rate Fisher Mann-Whitney test Sex Male 826 (82.6) 113 (98) 713 (81) 13.7% P =.0 Female 174 (17.4) 2 (2) 172 (19) 1.1% Age, y Mean 6 SD P =.5 P = DF = 1.0 DF = Height, cm Mean 6 SD P =.2 P = DF = 1.0 DF = Weight, kg Mean 6 SD P =.4 P = DF = 1.0 DF = Residence Dormitory 264 (26.4) 43 (37) 221 (25) 16.2% P =.0 Own home 501 (50.1) 55 (48) 446 (50) 11.0% Apartment 235 (23.5) 17 (15) 218 (25) 7.2% Familial T. tonsurans infection Yes 75 (7.5) 15 (13) 60 (7) 20.0% P =.0 No 925 (92.5) 100 (87) 825 (93) 10.8% Infected members Yes 597 (59.7) 82 (71) 515 (58) 13.7% P =.0 No 403 (40.3) 33 (29) 370 (42) 8.2% History Yes 376 (37.6) 91 (79) 285 (32) 24.2% P =.0 No 624 (62.4) 24 (21) 600 (68) 3.8% History of treatment Yes 326 (32.6) 83 (72) 243 (28) 25.5% P =.0 No 674 (67.4) 32 (28) 642 (73) 4.7% Increased dandruff Yes 53 (5.3) 17 (15) 36 (4) 32.1% P =.0 No 947 (94.7) 98 (85) 849 (96) 10.3% Concomitant tinea corporis Yes 187 (18.7) 59 (51) 128 (15) 31.6% P =.0 No 813 (81.3) 56 (49) 757 (86) 6.9% Recurrent dandruff formation Yes 101 (10.1) 9 (8) 92 (10) 8.9% P =.5 No 899 (89.9) 106 (92) 793 (90) 11.8% Atopic dermatitis Yes 161 (16.1) 10 (9) 151 (17) 6.2% P =.0 No 839 (83.9) 105 (91) 734 (83) 12.5% T, Trichophyton. t test previous and current tinea corporis (40%). In the assessment of association of these categories with positive status in fungal culture, there were statistically significant differences between each group (Table II). Those with positive hairbrush culture results classified in group 1 were considered asymptomatic carriers. DISCUSSION Since 2001 several reports have suggested the possibility of an outbreak of T. tonsurans infection in Japan among members of combat sports clubs, such as wrestlers and judo athletes. 2-5 Although transmission of this infection in Japan is so far assumed to be limited to combat sport club members, T. tonsurans

4 JAM ACAD DERMATOL VOLUME 54, NUMBER 4 Shiraki et al 625 Table II. Associations between positive status of hairbrush culture results and tinea corporis (n = 1000) Hairbrush culture results No. of participants Reported absence Reported presence (Group 1) (Group 2) (Group 3) (Group 4) Negative history Positive history Negative history Positive history Fisher exact test Positive hairbrush 17 (3.0%) 39 (15.9%) 7 (12.3%) 52 (40.0%) P =.0 culture Negative hairbrush 550 (97.0%) 207 (84.1%) 50 (87.7%) 78 (60.0%) culture Total infection has been transmitted to patients in longstay wards, in rehabilitation hospitals, and with HIV-1 infection in other countries. These findings strongly suggest that Japan faces an increasing risk for outbreak of the infection. 6-8 Results of mass screening examinations described in earlier reports showed the prevalence by T. tonsurans to be higher than expected, 9-14 underscoring the need for vigilance in monitoring this disease. Although a mass screening examination is the most reliable method for surveillance of some diseases, it is not realistically possible to screen the members of limited cohorts such as combat sports clubs. Therefore, it was necessary to develop a simple examination method that could be used in this study. Previous reports also showed that the hairbrush culture method is effective in detecting asymptomatic carriers with T. tonsurans. 13,14 Toothbrushes have also been used to detect carriage of T. tonsurans, as have cotton swabs. 15,16 We, therefore, selected the hairbrush culture method for our survey. The analysis of demographic factors and positive hairbrush culture results revealed high rates of apparent or silent infection in those: living in a dormitory, currently with tinea corporis, with a history, with a history of treatment for tinea corporis, and with increased dandruff. We assume that members of group 1 (with positive hairbrush culture results but without previous or current tinea corporis) were asymptomatic carriers. Because T. tonsurans is an anthropophilic organism, infection tends to provoke only a weak inflammatory response and patients are often unaware that they are infected. Consequently, development of infection control programs can be a challenging task. The rate of positive culture results was higher in those who reported presence for longer periods. For example, the rate of positive hairbrush culture results was as high as 40.0% among those who reported repeated tinea corporis within the last 1 or 2 years. Therefore, dermatologists should ask patients about the period of tinea corporis in routine clinical practice. Furthermore, athletes with a long history should be treated with oral antifungal drugs. Because this simple survey method allows the detection of asymptomatic carriers, this method is applicable for assessing infection status at each combat sports institution. In fact, a club member likely to be positive for T. tonsurans infection could be identified by some query items in the questionnaire. Based on this surveillance, we expect that we could have a rough epidemiologic estimate on T. tonsurans infection throughout Japan. To obtain more precise information and to increase public awareness of the threat of an outbreak of this infection, we recommend additional nationwide surveys using the questionnaire and the hairbrush culture method by multiple institutions or centers for medical mycology. Of course, preventive measures by medical doctors and combat sport clubs are essential in addition to the survey. REFERENCES 1. Hiruma M, Shiraki Y, Hirose N. Dermatophytes of judoists; hairbrush method, treatment, the guideline of prevention [leaflet]. Tokyo, Japan: Narunia; Mochizuki T, Takeda K, Kawasaki M, Tanabe H, Yanagihara M, Isizaki H, et al. Three cases of tinea capitis in a high-school wrestling team caused by Trichophyton tonsurans. Skin Res 2002;1: Kasai T, Makino Y, Mochizuki T. Tinea corporis by Trichophyton tonsurans spread among judo clubs of some high schools. Jpn J Med Mycol 2002;43(Suppl): Tanabe H, Kawasaki M, Mochizuki T, Ishizaki H, Kimbara T. The outbreak by Trichophyton tonsurans in the high-school judo club revealed by screening examinations. Jpn J Med Mycol 2002;43(Suppl): Shiraki Y, Soda N, Hirose N, Hiruma M. Screening examination and management of dermatophytosis by Trichophyton tonsurans in the judo club of a university. Jpn J Med Mycol 2004;45: Wood B, Rademaker M. Nosocomial Trichophyton tonsurans in a long stay ward. N Z Med J 1997;110: Lewis SM, Lewis BG. Nosocomial transmission of Trichophyton tonsurans tinea corporis in a rehabilitation hospital. Infect Control Hosp Epidemiol 1997;18:322-5.

5 626 Shiraki et al JAM ACAD DERMATOL APRIL Hadacek BM, Nassif A, Roux A, Desplaces N, Huerre M, De Bievre C, et al. Trichophyton tonsurans dermatophyte granuloma in an HIV-1 infected patient. Br J Dermatol 1999; 140: Seale ER, Richardson JB. Trichophyton tonsurans: a follow-up of treated and untreated cases. Arch Dermatol 1960;81: Sharma V, Hall JC, Knapp JF, Sarai S, Galloway D, Babel DE. Scalp colonization by Trichophyton tonsurans in an urban pediatric clinic: asymptomatic carrier state. Arch Dermatol 1988;124: Frieden IJ. Tinea captis: asymptomatic carriage of infection. Pediatr Infect Dis J 1999;18: Bergson CL, Fernaandes NC. Tinea capitis: study of asymptomatic carriers and sick adolescents, adults, and elderly who live with children with the disease. Rev Inst Med Trop Sao Paulo 2001;43: Hay RJ, Clayton YM, Silva NDE, Midgley G, Rossor E. Tinea capitis in south-east Londonea new pattern of infection with public health implications. Br J Delmatol 1996;135: Cuetara MS, Palacio AD, Pereiro M, Noriega AR. Prevalence of undetected tinea capitis in a prospective school survey in Madrid: emergence of new causative fungi. Br J Dermatol 1998;138: Hubbard TW, de Triquet JM. Brush-culture method for diagnosing tinea capitis. Pediatrics 1992;90: Friedlander SF, Pickering B, Cunningham BB, Gibbs NF, Eichenfield LF. Use of the cotton swab method in diagnosing tinea capitis. Pediatrics 1999;104:276-9.

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