Journal of Dermatology 2015; 42: 245–249
doi: 10.1111/1346-8138.12678
REVIEW ARTICLE
Trichophyton tonsurans infection in Japan: Epidemiology, clinical features, diagnosis and infection control Junichiro HIRUMA,1 Yumi OGAWA,2 Masataro HIRUMA3 1
Department of Dermatology, Tokyo Medical University, 2Department of Dermatology and Allergology, Juntendo University Graduate School of Medicine, and 3Ochanomizu Institute for Medical Mycology and Allergology, Tokyo, Japan
ABSTRACT In this review, we summarize the status of Trichophyton tonsurans infection in Japan in terms of epidemiology, clinical features, diagnosis and infection control. Since approximately 2000, outbreaks of T. tonsurans infections among combat sports club members have been reported frequently, with the infection then spreading to their friends and family members. The most common clinical features of T. tonsurans infection are tinea corporis, which is difficult to differentiate from eczema, and tinea capitis. Tinea capitis is classified as the seborrheic form, kerion celsi form or “black dot” form, although 90% or more of patients are asymptomatic carriers. The diagnosis of symptomatic T. tonsurans infection is established by potassium hydroxide examination and fungal culture. However, because there are many asymptomatic carriers of T. tonsurans infection, tests using the hairbrush culture method are necessary. An increase in asymptomatic carriers of T. tonsurans makes assessment of the current prevalence of the infection challenging and underscores the importance of educational efforts and public awareness campaigns to prevent T. tonsurans epidemics.
Key words:
clinical features, diagnosis, epidemiology, infection control, Trichophyton tonsurans infection.
INTRODUCTION Trichophyton tonsurans originated in South-East Asia and Australia and spread via the Iberian Peninsula to Latin American in colonial times. In the 1950s, this organism was introduced to the USA and Canada and is currently known as a major causative organism of tinea capitis.1,2 In the 1990s, T. tonsurans was introduced into Europe through international competition events for combat sports and now is the major causative organism of tinea corporis and tinea capitis in Western Europe.3,4 In Japan, reports of T. tonsurans infection have significantly increased among combat sports participants, such as wrestlers, judo athletes and sumo wrestlers, since approximately 2000. The infection subsequently spread among the friends and family members of the athletes and is now recognized as one of the fungal emerging infections, posing a serious public health problem.5,6
EPIDEMIOLOGY OF T. TONSURANS INFECTION In 2000, we reported the case of a 6-year-old Japanese girl with tinea capitis caused by T. tonsurans.7 Within a year, other outbreaks of T. tonsurans infection were reported,5,6 and we initiated a preliminary study to investigate the prevalence of the
infection. We initially screened 31 members of a university judo club and found that 11 had tinea corporis (35.5%) and two had tinea capitis (6.5%).8 All judo-club members were then tested by the hairbrush culture method, and 11 (35.5%) were found to be positive for T. tonsurans, indicating an extremely high prevalence rate. Many dermatologists failed to recognize T. tonsurans, which accelerated the spread of this infection. During the period between approximately 2001 and 2003, an epidemic of T. tonsurans infection promoted the anxiety among combat sports club members.5,6 We developed a simple examination method using a standardized questionnaire form and the hairbrush culture method and examined a total of 1000 judo club members belonging to 49 institutions, including junior high schools, high schools, universities and adult organizations across Japan.9 The hairbrush culture results were positive in 11.5% of the members. When the background factors were compared among those positive for T. tonsurans found by the hairbrush culture method, the positive rates were 40.0% in those who reported the presence of tinea corporis for more than a half year, 14.0–20.0% in male athletes living in a dormitory who had friends with tinea corporis, and 3.0% in those without previous or current tinea corporis (asymptomatic carriers) (Table 1). Studies conducted through 2004 described the epidemic of T. tonsurans infection among combat sports participants.
Correspondence: Masataro Hiruma, M.D., Ph.D., Ochanomizu Institute for Medical Mycology and Allergology, Nakamura Building 2F, 2-12-4 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. Email: [email protected] Received 17 September 2014; accepted 18 September 2014.
© 2015 Japanese Dermatological Association
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J. Hiruma et al.
Table 1. Associations between positive status of hairbrush culture results and tinea corporis in Trichophyton tonsurans infection (n = 1000) Reported absence of tinea corporis
Reported presence of tinea corporis
Hairbrush culture results
Negative history of tinea corporis
Positive history of tinea corporis
Negative history of tinea corporis
Positive history of tinea corporis
Positive hairbrush culture Negative hairbrush culture Total
17 (3.0%) 550 (97.0%) 567
39 (15.9%) 207 (84.1%) 246
7 (12.3%) 50 (87.7%) 57
52 (40.0%) 78 (60.0%) 130
Fisher’s exact test P = 0.0000000
Adapted with permission from Shiraki et al.9 and from present authors’ original work.
Based on concern about the prevalence of T. tonsurans infection among players of other sports, such as kendo, football and gymnastics, we used the hairbrush culture method to examine all 497 students in a department of sport science at a residential university.10 However, T. tonsurans infection was detected in combat sports club members alone. This result showed that as of 2004, T. tonsurans infection mainly affected combat sports athletes, and we hoped that the spread of infection could be prevented by education of this group and by treating them.10 While T. tonsurans infection had been recognized as spreading among high school and college students belonging to judo and wrestling clubs, reports began to emerge in 20055,6 describing T. tonsurans infection in elementary school children and junior high school students. This led to a concern that this infection would also spread to younger children. Thus, we conducted an epidemiological study of T. tonsurans infection for participants in the national junior high school judo tournament. Out of 496 participants enrolled in this study, 45 (9.1%) were positive for T. tonsurans by the hairbrush culture method, revealing the real spread of this infection for the first time.11 Since 2005, both combat sports participants and dermatologists have shown increased awareness of T. tonsurans infection, although the infection remains challenging. The number of reports of T. tonsurans infection presented in academic meetings has decreased; however, the infection has become a “hidden problem” due to the increase in asymptomatic carriers. With asymptomatic carriers, it becomes difficult to assess the prevalence of T. tonsurans infection. Asymptomatic carriers of T. tonsurans account for 90% or more of the patients.12
Figure 1. Clinical feature of tinea corporis due to Trichophyton tonsurans seen in a 19-year-old judo player. It appears as a pink flaky lesion that is difficult to differentiate from eczema. (Reproduced from Hiruma21 with permission and also our original works.)
CLINICAL FEATURES OF T. TONSURANS INFECTION Tinea corporis and tinea capitis are the two most common clinical features of T. tonsurans infection. Unlike dermatophytosis due to other dermatophytes, the clinical features of T. tonsurans infection are initially not very apparent and are frequently overlooked. Tinea corporis appears as small, pink, flaky plaques, often measuring only 1–2 cm in diameter and without clearing at the center, and the condition is difficult to differentiate from eczema (Fig. 1). Tinea capitis can be classified into one of three types: (i) the seborrheic form, which is mainly characterized by dandruff and crusts; (ii) the kerion celsi form; and (iii) the “black dot” form (Figs 2,3).
246
Figure 2. Clinical feature of “black dot” ringworm due to Trichophyton tonsurans seen at the hairline in the occipitotemporal region in a 20-year-old judo player. (Reproduced from Hiruma21 with permission and also our original works.) We analyzed a total of 92 patients with T. tonsurans infection who visited a dermatology clinic of a university hospital during a 5-year period from 2000 to 2004. For judo practitioners, we found that the commonly affected body sites are the
© 2015 Japanese Dermatological Association
T. tonsurans infection in Japan
hairline in the occipitotemporal region and sites that rub against the judo uniform during judo practice.13 The inflammatory reactions associated with various types of dermatophytosis differ depending on the causative species, and clinical features of dermatophytosis also vary. In general, infections with anthropophilic species tend to provoke mild inflammatory responses, whereas those associated with zoophilic species tend to provoke severe inflammatory responses. T. tonsurans is highly infectious and difficult to cure, yet the organism provokes only mild inflammatory responses. Using a human cytokine antibody array,14 we analyzed cytokine secretion profiles of human keratinocytes after infection with T. tonsurans compared to Arthroderma benhamiae, which is a zoophilic species. Secretion of cytokines involved in various inflammatory reactions was limited in T. tonsurans infection, but abundant in A. benhamiae infection. These results suggest
Figure 3. Dermoscopic feature of the same area as Fig. 2. “Black dots” due to Trichophyton tonsurans are small. Dermoscopy is a convenient and useful tool for examining the “black dots”. (Reproduced from Hiruma21 with permission and also our original works.)
that the differences in clinical features between T. tonsurans infection and A. benhamiae infection may be related with the differences in the cytokine secretion profiles of keratinocytes, which play an important role in the defense mechanism against dermatophytosis (Fig. 3).
DIAGNOSIS OF T. TONSURANS INFECTION The clinical features of T. tonsurans infection are minimal, making a clinical diagnosis often difficult to achieve. As with other dermatophytosis, the diagnosis of T. tonsurans infection is established by demonstrating the presence of fungal elements by potassium hydroxide preparation and performing fungal culture to isolate and identify the causative organisms. The diagnosis of T. tonsurans in carriers requires detection using the hairbrush culture method. The hairbrush culture method has long been used, and its efficacy also has been demonstrated in our epidemiological study.9 However, fungal culture has not been widely adopted as daily medical examination at dermatology clinics in Japan, and facilities capable of performing fungal cultures are limited even in hospital central laboratories and private clinical laboratories. For diagnosis of T. tonsurans which can be a “hidden” infection, widespread adoption of fungal culture method is urgently needed. The hairbrush culture method is a reliable method, but the incubation period required for the hairbrush culture is at least 2 weeks. A more rapid detection system would be desirable. We have reported that a diagnosis can be made within 5 h by real-time polymerase chain reaction (PCR) to detect specific T. tonsurans ribosomal (r)DNA in the fluid used for rinsing a tested hairbrush.15 PCR was effective in detecting fungal rDNA in specimens yielding 50 or fewer colonies on hairbrush cultures, below the threshold for detection by light microscopy. We conducted a molecular biological study of variable internal repeat regions of the rDNA gene of T. tonsurans isolates obtained in a nationwide epidemiological survey and demonstrated that the prevalent forms of the organism in Japan had identical genotypes. This finding suggests that a single specific genotype strain has rapidly spread throughout Japan.16,17
Table 2. Treatment protocol of Trichophyton tonsurans infection Tinea corporis (must be adequately treated in the early stage by a dermatologist) 1. Patients with negative hairbrush culture results are treated with topical antifungal ointment for 6 weeks without oral antifungal medication 2. Patients with positive hairbrush culture results are treated with itraconazole or terbinafine as described below Tinea capitis and positive result by hairbrush method 1. Itraconazole 2. Terbinafine
100 400 125 500
mg/day mg/day mg/day mg/day
for for for for
6 1 6 1
weeks week† weeks week†
Adapted with permission from Shiraki et al.19 and from present authors’ original work. If the hairbrush culture yields only one or two colonies, the patients can be treated with antifungal shampoo and monitored closely. The hairbrush culture should be repeated 3 months after treatment to confirm that the treatment was effective. This prescription applies to patients weighing 60–70 kg. Dose needs to be adjusted according to age, weight and severity of symptoms.19 †These pulse therapies are not permitted by the Japanese national insurance program.
© 2015 Japanese Dermatological Association
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J. Hiruma et al.
INFECTION CONTROL AGAINST T. TONSURANS Based on the course described above, we established a T. tonsurans infection study group in 2003. We conducted an awareness campaign for combat sports players, coaches, schools and families through publication of pamphlets on the “Guideline for Trichophyton tonsurans infection: Hairbrush examination, treatment and prevention”18 and a video program entitled “Trichophyton tonsurans infection: Diagnosis and treatment” available on the study group’s website (http://tonsurans. jp/index.html). The treatment protocol for T. tonsurans infection recommends that no treatment be given to individuals who have no exanthema and who test negative by the hairbrush culture method. For patients who have tinea corporis and who test negative by the hairbrush culture method, prescription of antifungal ointment is recommended. Those found to be positive for T. tonsurans by the hairbrush method should be treated with p.o. administration of itraconazole or terbinafine and the use of antifungal shampoo (Table 2).18,19 The following precautions are recommended for combat sports participants in order to reduce the risk of T. tonsurans infections: (i) thorough cleaning of training rooms and facilities; (ii) frequent washing of training clothes; (iii) showering immediately after practice; and (iv) prompt treatment of suspicious lesions. The guidelines described above were recommended for patients with positive hairbrush cultures in the epidemiological studies that have been conducted to date. Compliance with these guidelines and treatment protocol resulted in a culturenegative conversion rate of approximately 80%.12,19,20 Judo athletes often have a full practice or competition schedule and may be indifferent to treatment; consequently, in routine clinical practice, thorough explanation of the infection to patients is essential to improve culture-negative conversion rates. To improve compliance, innovative treatment strategies, such as pulse treatment, are also needed. Using these guidelines, screening examinations and infection control were performed in athletes registered in the University Judo Federation of Tokyo every year from 2008 to 2014. The percentage of judo athletes with a positive hairbrush culture test12 decreased over the study period from approximately 10% to 5%; however, the rate has remained 5%. Our activities appear to be successful. In the future, the same screening examinations and infection control will be performed in younger athletes including elementary children, junior high school students and high school students.
CONCLUSION The epidemic of T. tonsurans infection has spread from combat sports enthusiasts to athletes at junior high/elementary schools, as well as to family members and friends of the athletes. If patients with this infection are examined by dermatologists who are not familiar with the organism, these patients may be misdiagnosed and prescribed steroid ointment, which further exacerbates the symptoms. Awareness of T. tonsurans
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infection greatly varies among combat sport players, coaches, family members and other individuals. In order to prevent this infection and limit the spread of T. tonsurans, it is extremely important to provide information and promote awareness to people involved in combat sports and to the medical community. A future task is to further enhance cooperation between doctors and individuals involved in combat sports.5,21
ACKNOWLEDGMENTS: This work was partly supported by Health and Labor Sciences Research Grants (H25-shinko-ippan-006). CONFLICT OF INTEREST:
The authors declare that they
have no conflicts of interest to disclose.
REFERENCES 1 Gupta AK, Summerbell RC. Increased incidence of Trichophyton tonsurans tinea capitis in Ontario, Canada between 1985 and 1996. Med Mycol 1998; 36: 55–60. 2 Abdel-Rahman SM, Eric Schuenemann NF, Stering TK, Preuett B, Magie R, Campbell A. The prevalence of infections with Trichophyton tonsurans in schoolchildren. Pediatrics 2010; 125: 966– 973. 3 Fuller LC, Child FC, Midgley G, Higgins EM. Scalp ringworm in south-east London and an analysis of a cohort of patients from a paediatric dermatology department. Br J Dermatol 2003; 148: 985– 988. 4 Alshawa K, Lacroix C, Benderdouche M, Mingui A, Derouin F. Feuilhade de Chauvin M. Increasing incidence of Trichophyton tonsurans in Paris, France: a 15-year retrospective study. Br J Dermatol 2012; 166: 1149–1150. 5 Hiruma M. The present state and management of Trichophyton tonsurans infection. Derma 2006; 114: 54–59. 6 Mochizuki T, Tanabe H, Wakasa A, Kawasaki M, Anzawa K, Ishizaki H. Survey of Trichophyton tonsurans infection in Japan –Molecular epidemiology and factors affecting adequate hairbrush sampling. Jpn J Med Mycol 2006; 47: 57–61. 7 Soda N, Hiruma M, Ogawa H. Pediateric Tinea captis due to Trichophyton tonsurans. Pract Dermatol 2002; 24: 841–844. 8 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 2007; 45: 7–12. 9 Shiraki Y, Hiruma M, Hirose N, Sugita T, Ikeda S. A nationwide survey of Trichophyton tonsurans infection among combat sport club members in Japan using a questionnaire form and the hairbrush method. J Am Acad Dermatol 2006; 54: 622–626. 10 Hirose M, Shiraki Y, Hiruma M, Ogawa H. An investigation of Trichophyton tonsurans infection in university students participating in sports clubs. Jpn J Med Mycol 2005; 46: 119–123. 11 Suganami M, Hirose N, Shiraki Y, Hiruma M, Ikeda S. Trichophyton tonsurans infection among judo practitioners who attended the national junior high school judo tournament in Japan (2005): incidence and therapeuitic response. Jpn J Med Mycol 2006; 47: 319– 324. 12 Hirose N, Tamura M, Suganami M, Shiraki OY, Hiruma M. The results of Trichophyton tonsurans screening examinations and Infection management in University Judo Federation of Tokyo Athletes over a 4-year Period. Med Mycol J 2012; 53: 267–271. 13 Shiraki Y, Hiruma M, Hirose N, Ikeda S. Commonly affected body sites in 92 Japanese combat sports participants with Trichophyton tonsurans infection. Mycoses 2008; 52: 339–342. 14 Shiraki Y, Ishibashi Y, Hiruma M, Nishikawa A, Ikeda S. Cytokine secretion profiles of human keratinocytes during Trichophyton
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tonsurans and Arthroderma benhamiae infections. J Med Microbiol 2006; 55: 1175–1185. 15 Sugita T, Shiraki Y, Hiruma M. Real-time PCR TaqMan assay for detecting Trichophyton tonsurans, a causative agent of tinea capitis, from hairbrushes. Med Mycol 2006; 44: 579–581. 16 Sugita T, Shiraki Y, Hiruma M. Genotype analysis of the variable internal repeat region in the rRNA gene of Trichophyton tonsurans isolated from Japanese Judo practitioners. Microbiol Immunol 2006; 50: 57–60. lez GM et al. Divergence among 17 Abdel-Rahman SM, Sugita T, Gonza an international population of Trichophyton tonsurans isolates. Mycopathologia 2010; 169: 1–13.
© 2015 Japanese Dermatological Association
18 Hiruma M, Ogawa Y, Hirose N. Guideline for Trichophyton tonsurans Infection: Hairbrush Examination, Treatment and Prevention, 4th edn. Shomeido Press, Tokyo 2012. 19 Shiraki Y, Hiruma M, Sugita T, Ikeda S. Assessment of the treatment protocol described in the guidelines for Trichophyton tonsurans infection. Jpn J Med Mycol 2008; 49: 27–31. 20 Hirose N, Suganami M, Shiraki Y, Hiruma M, Ogawa H. Management and follow-up survey of Trichophyton tonsurans infection in a university judo club. Mycoses 2008; 51: 243–247. 21 Hiruma M. Trichophyton tonsurans infection from the point of view of diagnosis. Derma 2011; 179: 41–46.
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doi: 10.1111/1346-8138.12678
REVIEW ARTICLE
Trichophyton tonsurans infection in Japan: Epidemiology, clinical features, diagnosis and infection control Junichiro HIRUMA,1 Yumi OGAWA,2 Masataro HIRUMA3 1
Department of Dermatology, Tokyo Medical University, 2Department of Dermatology and Allergology, Juntendo University Graduate School of Medicine, and 3Ochanomizu Institute for Medical Mycology and Allergology, Tokyo, Japan
ABSTRACT In this review, we summarize the status of Trichophyton tonsurans infection in Japan in terms of epidemiology, clinical features, diagnosis and infection control. Since approximately 2000, outbreaks of T. tonsurans infections among combat sports club members have been reported frequently, with the infection then spreading to their friends and family members. The most common clinical features of T. tonsurans infection are tinea corporis, which is difficult to differentiate from eczema, and tinea capitis. Tinea capitis is classified as the seborrheic form, kerion celsi form or “black dot” form, although 90% or more of patients are asymptomatic carriers. The diagnosis of symptomatic T. tonsurans infection is established by potassium hydroxide examination and fungal culture. However, because there are many asymptomatic carriers of T. tonsurans infection, tests using the hairbrush culture method are necessary. An increase in asymptomatic carriers of T. tonsurans makes assessment of the current prevalence of the infection challenging and underscores the importance of educational efforts and public awareness campaigns to prevent T. tonsurans epidemics.
Key words:
clinical features, diagnosis, epidemiology, infection control, Trichophyton tonsurans infection.
INTRODUCTION Trichophyton tonsurans originated in South-East Asia and Australia and spread via the Iberian Peninsula to Latin American in colonial times. In the 1950s, this organism was introduced to the USA and Canada and is currently known as a major causative organism of tinea capitis.1,2 In the 1990s, T. tonsurans was introduced into Europe through international competition events for combat sports and now is the major causative organism of tinea corporis and tinea capitis in Western Europe.3,4 In Japan, reports of T. tonsurans infection have significantly increased among combat sports participants, such as wrestlers, judo athletes and sumo wrestlers, since approximately 2000. The infection subsequently spread among the friends and family members of the athletes and is now recognized as one of the fungal emerging infections, posing a serious public health problem.5,6
EPIDEMIOLOGY OF T. TONSURANS INFECTION In 2000, we reported the case of a 6-year-old Japanese girl with tinea capitis caused by T. tonsurans.7 Within a year, other outbreaks of T. tonsurans infection were reported,5,6 and we initiated a preliminary study to investigate the prevalence of the
infection. We initially screened 31 members of a university judo club and found that 11 had tinea corporis (35.5%) and two had tinea capitis (6.5%).8 All judo-club members were then tested by the hairbrush culture method, and 11 (35.5%) were found to be positive for T. tonsurans, indicating an extremely high prevalence rate. Many dermatologists failed to recognize T. tonsurans, which accelerated the spread of this infection. During the period between approximately 2001 and 2003, an epidemic of T. tonsurans infection promoted the anxiety among combat sports club members.5,6 We developed a simple examination method using a standardized questionnaire form and the hairbrush culture method and examined a total of 1000 judo club members belonging to 49 institutions, including junior high schools, high schools, universities and adult organizations across Japan.9 The hairbrush culture results were positive in 11.5% of the members. When the background factors were compared among those positive for T. tonsurans found by the hairbrush culture method, the positive rates were 40.0% in those who reported the presence of tinea corporis for more than a half year, 14.0–20.0% in male athletes living in a dormitory who had friends with tinea corporis, and 3.0% in those without previous or current tinea corporis (asymptomatic carriers) (Table 1). Studies conducted through 2004 described the epidemic of T. tonsurans infection among combat sports participants.
Correspondence: Masataro Hiruma, M.D., Ph.D., Ochanomizu Institute for Medical Mycology and Allergology, Nakamura Building 2F, 2-12-4 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. Email: [email protected] Received 17 September 2014; accepted 18 September 2014.
© 2015 Japanese Dermatological Association
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J. Hiruma et al.
Table 1. Associations between positive status of hairbrush culture results and tinea corporis in Trichophyton tonsurans infection (n = 1000) Reported absence of tinea corporis
Reported presence of tinea corporis
Hairbrush culture results
Negative history of tinea corporis
Positive history of tinea corporis
Negative history of tinea corporis
Positive history of tinea corporis
Positive hairbrush culture Negative hairbrush culture Total
17 (3.0%) 550 (97.0%) 567
39 (15.9%) 207 (84.1%) 246
7 (12.3%) 50 (87.7%) 57
52 (40.0%) 78 (60.0%) 130
Fisher’s exact test P = 0.0000000
Adapted with permission from Shiraki et al.9 and from present authors’ original work.
Based on concern about the prevalence of T. tonsurans infection among players of other sports, such as kendo, football and gymnastics, we used the hairbrush culture method to examine all 497 students in a department of sport science at a residential university.10 However, T. tonsurans infection was detected in combat sports club members alone. This result showed that as of 2004, T. tonsurans infection mainly affected combat sports athletes, and we hoped that the spread of infection could be prevented by education of this group and by treating them.10 While T. tonsurans infection had been recognized as spreading among high school and college students belonging to judo and wrestling clubs, reports began to emerge in 20055,6 describing T. tonsurans infection in elementary school children and junior high school students. This led to a concern that this infection would also spread to younger children. Thus, we conducted an epidemiological study of T. tonsurans infection for participants in the national junior high school judo tournament. Out of 496 participants enrolled in this study, 45 (9.1%) were positive for T. tonsurans by the hairbrush culture method, revealing the real spread of this infection for the first time.11 Since 2005, both combat sports participants and dermatologists have shown increased awareness of T. tonsurans infection, although the infection remains challenging. The number of reports of T. tonsurans infection presented in academic meetings has decreased; however, the infection has become a “hidden problem” due to the increase in asymptomatic carriers. With asymptomatic carriers, it becomes difficult to assess the prevalence of T. tonsurans infection. Asymptomatic carriers of T. tonsurans account for 90% or more of the patients.12
Figure 1. Clinical feature of tinea corporis due to Trichophyton tonsurans seen in a 19-year-old judo player. It appears as a pink flaky lesion that is difficult to differentiate from eczema. (Reproduced from Hiruma21 with permission and also our original works.)
CLINICAL FEATURES OF T. TONSURANS INFECTION Tinea corporis and tinea capitis are the two most common clinical features of T. tonsurans infection. Unlike dermatophytosis due to other dermatophytes, the clinical features of T. tonsurans infection are initially not very apparent and are frequently overlooked. Tinea corporis appears as small, pink, flaky plaques, often measuring only 1–2 cm in diameter and without clearing at the center, and the condition is difficult to differentiate from eczema (Fig. 1). Tinea capitis can be classified into one of three types: (i) the seborrheic form, which is mainly characterized by dandruff and crusts; (ii) the kerion celsi form; and (iii) the “black dot” form (Figs 2,3).
246
Figure 2. Clinical feature of “black dot” ringworm due to Trichophyton tonsurans seen at the hairline in the occipitotemporal region in a 20-year-old judo player. (Reproduced from Hiruma21 with permission and also our original works.) We analyzed a total of 92 patients with T. tonsurans infection who visited a dermatology clinic of a university hospital during a 5-year period from 2000 to 2004. For judo practitioners, we found that the commonly affected body sites are the
© 2015 Japanese Dermatological Association
T. tonsurans infection in Japan
hairline in the occipitotemporal region and sites that rub against the judo uniform during judo practice.13 The inflammatory reactions associated with various types of dermatophytosis differ depending on the causative species, and clinical features of dermatophytosis also vary. In general, infections with anthropophilic species tend to provoke mild inflammatory responses, whereas those associated with zoophilic species tend to provoke severe inflammatory responses. T. tonsurans is highly infectious and difficult to cure, yet the organism provokes only mild inflammatory responses. Using a human cytokine antibody array,14 we analyzed cytokine secretion profiles of human keratinocytes after infection with T. tonsurans compared to Arthroderma benhamiae, which is a zoophilic species. Secretion of cytokines involved in various inflammatory reactions was limited in T. tonsurans infection, but abundant in A. benhamiae infection. These results suggest
Figure 3. Dermoscopic feature of the same area as Fig. 2. “Black dots” due to Trichophyton tonsurans are small. Dermoscopy is a convenient and useful tool for examining the “black dots”. (Reproduced from Hiruma21 with permission and also our original works.)
that the differences in clinical features between T. tonsurans infection and A. benhamiae infection may be related with the differences in the cytokine secretion profiles of keratinocytes, which play an important role in the defense mechanism against dermatophytosis (Fig. 3).
DIAGNOSIS OF T. TONSURANS INFECTION The clinical features of T. tonsurans infection are minimal, making a clinical diagnosis often difficult to achieve. As with other dermatophytosis, the diagnosis of T. tonsurans infection is established by demonstrating the presence of fungal elements by potassium hydroxide preparation and performing fungal culture to isolate and identify the causative organisms. The diagnosis of T. tonsurans in carriers requires detection using the hairbrush culture method. The hairbrush culture method has long been used, and its efficacy also has been demonstrated in our epidemiological study.9 However, fungal culture has not been widely adopted as daily medical examination at dermatology clinics in Japan, and facilities capable of performing fungal cultures are limited even in hospital central laboratories and private clinical laboratories. For diagnosis of T. tonsurans which can be a “hidden” infection, widespread adoption of fungal culture method is urgently needed. The hairbrush culture method is a reliable method, but the incubation period required for the hairbrush culture is at least 2 weeks. A more rapid detection system would be desirable. We have reported that a diagnosis can be made within 5 h by real-time polymerase chain reaction (PCR) to detect specific T. tonsurans ribosomal (r)DNA in the fluid used for rinsing a tested hairbrush.15 PCR was effective in detecting fungal rDNA in specimens yielding 50 or fewer colonies on hairbrush cultures, below the threshold for detection by light microscopy. We conducted a molecular biological study of variable internal repeat regions of the rDNA gene of T. tonsurans isolates obtained in a nationwide epidemiological survey and demonstrated that the prevalent forms of the organism in Japan had identical genotypes. This finding suggests that a single specific genotype strain has rapidly spread throughout Japan.16,17
Table 2. Treatment protocol of Trichophyton tonsurans infection Tinea corporis (must be adequately treated in the early stage by a dermatologist) 1. Patients with negative hairbrush culture results are treated with topical antifungal ointment for 6 weeks without oral antifungal medication 2. Patients with positive hairbrush culture results are treated with itraconazole or terbinafine as described below Tinea capitis and positive result by hairbrush method 1. Itraconazole 2. Terbinafine
100 400 125 500
mg/day mg/day mg/day mg/day
for for for for
6 1 6 1
weeks week† weeks week†
Adapted with permission from Shiraki et al.19 and from present authors’ original work. If the hairbrush culture yields only one or two colonies, the patients can be treated with antifungal shampoo and monitored closely. The hairbrush culture should be repeated 3 months after treatment to confirm that the treatment was effective. This prescription applies to patients weighing 60–70 kg. Dose needs to be adjusted according to age, weight and severity of symptoms.19 †These pulse therapies are not permitted by the Japanese national insurance program.
© 2015 Japanese Dermatological Association
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INFECTION CONTROL AGAINST T. TONSURANS Based on the course described above, we established a T. tonsurans infection study group in 2003. We conducted an awareness campaign for combat sports players, coaches, schools and families through publication of pamphlets on the “Guideline for Trichophyton tonsurans infection: Hairbrush examination, treatment and prevention”18 and a video program entitled “Trichophyton tonsurans infection: Diagnosis and treatment” available on the study group’s website (http://tonsurans. jp/index.html). The treatment protocol for T. tonsurans infection recommends that no treatment be given to individuals who have no exanthema and who test negative by the hairbrush culture method. For patients who have tinea corporis and who test negative by the hairbrush culture method, prescription of antifungal ointment is recommended. Those found to be positive for T. tonsurans by the hairbrush method should be treated with p.o. administration of itraconazole or terbinafine and the use of antifungal shampoo (Table 2).18,19 The following precautions are recommended for combat sports participants in order to reduce the risk of T. tonsurans infections: (i) thorough cleaning of training rooms and facilities; (ii) frequent washing of training clothes; (iii) showering immediately after practice; and (iv) prompt treatment of suspicious lesions. The guidelines described above were recommended for patients with positive hairbrush cultures in the epidemiological studies that have been conducted to date. Compliance with these guidelines and treatment protocol resulted in a culturenegative conversion rate of approximately 80%.12,19,20 Judo athletes often have a full practice or competition schedule and may be indifferent to treatment; consequently, in routine clinical practice, thorough explanation of the infection to patients is essential to improve culture-negative conversion rates. To improve compliance, innovative treatment strategies, such as pulse treatment, are also needed. Using these guidelines, screening examinations and infection control were performed in athletes registered in the University Judo Federation of Tokyo every year from 2008 to 2014. The percentage of judo athletes with a positive hairbrush culture test12 decreased over the study period from approximately 10% to 5%; however, the rate has remained 5%. Our activities appear to be successful. In the future, the same screening examinations and infection control will be performed in younger athletes including elementary children, junior high school students and high school students.
CONCLUSION The epidemic of T. tonsurans infection has spread from combat sports enthusiasts to athletes at junior high/elementary schools, as well as to family members and friends of the athletes. If patients with this infection are examined by dermatologists who are not familiar with the organism, these patients may be misdiagnosed and prescribed steroid ointment, which further exacerbates the symptoms. Awareness of T. tonsurans
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infection greatly varies among combat sport players, coaches, family members and other individuals. In order to prevent this infection and limit the spread of T. tonsurans, it is extremely important to provide information and promote awareness to people involved in combat sports and to the medical community. A future task is to further enhance cooperation between doctors and individuals involved in combat sports.5,21
ACKNOWLEDGMENTS: This work was partly supported by Health and Labor Sciences Research Grants (H25-shinko-ippan-006). CONFLICT OF INTEREST:
The authors declare that they
have no conflicts of interest to disclose.
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