| Abstract|| |
Background: This study was conducted to evaluate the occurrence of cutaneous fungal infections affecting athletes. Methods: A respectively study of superficial fungal infections in athletes was carried out during the period March 2002 to December 2006 on 656 mycologically proven cases of dermatophytosis found in athletes in Tehran. Mycological examination consisted of culturing of pathologic material followed by direct microscopic observation. Mycological cultures were carried out on Sabouraud Chloramphenicol Agar, Sabouraud Chloramphenicol and Cyclohexamide Agar, and Dermatophyte Agar incubated at 25° C for at least 28 days. Diagnosis was based on macroscopic and microscopic characteristics of the colonies. Results: We surveyed 1075 athletes suspected of having cutaneous fungal infections from 201 institutions and found that 656 (61%) were positive for fungal infections. The fungal isolates comprised Trichophyton tonsurans (56%), Epidermophyton floccosum (11.8%), Trichophyton mentagrophytes (8.9%), Trichophyton rubrum(8.3%), Trichophyton verrucosum (3.9%), Trichophyton violaceum (3.3%), Microsporum canis (2.5%), Malassezia fur fur (3.3%), and Pityrosporum oval (2%). The distribution of the lesions on the body was: trunk> groin> hair and scalp> sole and toe webs> finger nails> toe nails. Fungal infections were more commonly seen in wrestlers and aerobics. Conclusion: The results suggest that athletic activity seems to be a predisposing factor, especially for fungal infections.
Keywords: Athletes, dermatophytes, fungal infections, Iran, prevention, sport
|How to cite this article:|
Bassiri-Jahromi S, Khaksar AA. Prevalence of cutaneous fungal infections among sports-active individuals. Ann Trop Med Public Health 2010;3:53-7
|How to cite this URL:|
Bassiri-Jahromi S, Khaksar AA. Prevalence of cutaneous fungal infections among sports-active individuals. Ann Trop Med Public Health [serial online] 2010 [cited 2020 Jan 26];3:53-7. Available from: http://www.atmph.org/text.asp?2010/3/2/53/77182
| Introduction|| |
Sports, in general, favors the apparition of a superficial mycosis. Wrestling, judo, swimming, gymnastics, cycling, and horse-riding are the most concerned. The sportsman mainly exposes himself to fungal contamination when frequenting on a regular basis places where sports are practiced barefoot or places such as changing-rooms, bathrooms or showers. 
Fungal and viral cutaneous infections are common among athletes and can develop quickly into widespread outbreaks.  'Tinea corporis gladiatorum' describes a dermatophytosis transmitted mainly from close skin contact among wrestlers. 
Tinea corporis gladiatorum is caused by dermatophytes, usually of the genus Trichophyton, affecting both humans and animals. The fungus causes a characteristic lesion which is often clear in the center with a rough, scaly circular border. Lesions vary in size from very small circular patches to large patches.  This fungal infection is transmitted through close skin-to-skin contact, and the athletes involved in this outbreak, like those described by Shiraki et al., are involved in international competitions. 
Athletic activity may cause or aggravate skin disorders, which in turn may diminish athletic performance. ,
For example, a review of the literature shows skin infections are more prevalent in top-level athletes than in the general population, particularly during periods of intensive training.  The athlete is exposed to a wide spectrum of skin diseases that may or may not be unique to a particular sport or activity. 
The large cohorts provided by its emergence in judo teams, between 2001 and 2003, allowed the computation of risk factors that had long remained undisclosed. Concern should be raised about inter-sport challenges since cases have been recently identified in wrestlers and karate players. Frequent remote international competitions are the most likely vehicle of tinea corporis gladiatorum around the world. The efficiency of preventive measures will need a worldwide consensus, integrated into rules of the international competition by the regulatory organization and relying on objective information provided to athletes and coaches. 
The dermatological problems are related to the athlete's skin type, age, sex, sporting activities, environment and hereditary factors. , Areas such as public showers, health club bathing facilities, swimming pools, changing rooms and toilets will contain layers of skin shed from an infected person. The shed skin contains fungal spores, and individuals with fissured or hyperhydrotic skin conditions are at risk for infection. ,
This article describes the evolution of the outbreak, with the aim of raising awareness across Iran.
The purpose of this study was to evaluate the importance of cutaneous mycoses in sporting people, in terms of sport nature. In addition, the study attempted to specify the lesions' fungal etiology, to establish whether fungus species are the difference as were previously.
| Material and Methods|| |
A total of 1075 patient samples including nail clippings, sub ungual debris, hair and skin scrapings were collected at our medical mycology laboratory from March 2002 through March 2006. Specimens were obtained from clinically suspected fungal infections of various body and groin, head and scalp, face, hand, toe and fingernails.
All collected specimens were analyzed by direct microscopy and culture. Microscopic examination of these specimens was carried out in potassium hydroxide solution (20%) with dimethyl sulfoxide (4%). These specimens were cultured on sabouraud glucose agar with chloramphenicol and sabouraud glucose agar with chloramphenicole and cycloheximide and dermatophyte agar. Cultures were incubated at 25° C for up to 28 days and checked twice weekly for growth. Negative cultures were confirmed after four weeks of no growth. Identification of dermatophyte isolates was on the basis of microscopic morphology, urea testing growth on Trichophyton agars, and hair perforation assays. 
Non-dermatophyte molds were identified by microscopic morphology.  The data collection form included questions about age, sex, number of siblings, residence, and hair-loss history for other siblings and income level.
| Results|| |
In total, 1075 athletes were referred to our laboratory and 656 episodes of fungal infections were observed: 638 infected athletes were male and 80 were female, and the mean age was 19.6 years (range 6 to 42). The outbreak affected 72.9% of the wrestlers (478/656), most of them practicing in the south and east-south clubs of Tehran. Traumatic lesions were frequently seen in wrestlers; lesion types and localizations varied by sport type. Most of the athletes with fungi were males (97.2%). Whereas very few members of the other groups girls were involved (2.8%). The prevalence of fungi was higher in individuals between 10 and 30 years of age. The results can be summarized as follows [Table 1]: -
- Three different sports are associated with more than 90% of lesions: wrestling, aerobics, and mutao.
- Trichophyton tonsurans was the most frequently isolated agent (56%). - In 28 (4.3%) cases tinea corporis was present among the family members of infected athletes.
- Dermatophytes isolated in 94.7%.
- Tinea versicolor was observed in 3.3%.
- Isolation of fungal species shows nine usual pathogenic species [Table 2]: Trichophyton tonsurans (359), Epidermophyton floccosum (76), Trichophyton mentagrophytes (57), Trichophyton rubrum (53), Trichophyton verrucosum (25), Trichophyton violaceum (21), Microsporum canis (16), Malassezia furfur (21), and Pityrosporum oval (13).
- The trunk was the most infected site in this study [Table 3].
- The highest number of cases of tinea pedis and tinea cruris occurred in the summer months, while tinea capitis, tinea corporis and tinea unguium occurred in the spring and winter months.
|Table 1: Frequency of skin infections among athletes attending the Medical Mycology Department Pasteur Institute of Iran|
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| Discussion|| |
Tinea corporis is extremely common in wrestling and other sports involving extensive skin-to-skin contact and can result in outbreaks. This specific way of spreading through the practice of combat sports had previously been recognized concerning the herpes virus. A clinical identity had been proposed by Selling and Kibrick in 1964 under the name of ''Herpes gladiatorum'. 
High-contact sports regularly allow transmission of infectious agents, including fungi such as dermatophytes. The occurrence of dermatophytosis outbreaks among wrestlers has been extensively described since the '90s.  Tinea corporis gladiatorum has been spreading in wrestling teams worldwide for four decades, without being stopped. 
High-contact sports are a well-known cause of transmission of fungi causing skin infections.  Fungi are considered a benign risk in comparison with herpes, though more widely spread: during the 1998-1999 season in the United States, Kohl et al. found that 84% of wrestling teams had at least one case of tinea corporis gladiatorum.The causative agent is always T. tonsurans. Traumatic lesions were frequently seen in soccer players and wrestlers; fungal infections were more commonly seen in swimmers and in soccer players. Lesion types and localizations varied by sport type. 
In this study the most common sport for fungal infections was wrestling [Table 1], and the main infected site was the trunk [Table 3]. The skin-to-skin close contact that occurs during the practice of combat sports creates unusual vectoring conditions that allow the direct transmission of any dermatophyte of the three groups. ,,,
In this study tinea corporis gladiatorum was found to be more prevalent between the ages of 10 to 30 years (92.1%) [Table 4].
|Table 4: Isolation of fungal infections with respect to athletes infected with fungal infections according to athletes age|
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This survey evidenced a significant age-dependent association between sporting activities and the prevalence of superficial fungal infection. The outbreak affected 92.1% of the athletes, who were aged between 10-30 years [Table 4].
Several outbreaks of tinea corporis or ringworm have recently been reported in high school and college wrestling. ,,,,,,, For example, an epidemic of tinea corporis caused by T. tonsurans was reported among 19 wrestlers in Sweden,  and the suspected source of this epidemic was a visiting wrestling team from the US.
A risk factor had been computed concerning the delay between the end of practice and the first shower.  This factor did not appear significant in the French larger survey. 
Trichophyton tonsurans was the main causative agent in this study. Trichophyton tonsurans is a particular pathogenic agent of tinea gladiatorum.  The most common fungi are the anthropophilic dermatophytes: T. tonsurans, E. floccosum, T. mentagrophytes, and T. rubrum. These species can be easily found on the floor or on the uniforms and practice clothing and on the tiling of swimming pools. 
In our study most common fungal infections were seen in the wrestlers [Table 1]. Until the year 2004, reports of outbreaks of tinea corporis gladiatorum were seemingly restricted to wrestling teams. ,, Although the infection has been widespread among wrestlers for some time now, risk factors and prevention strategies are not yet well-defined. Fomites were identified in previous studies of tinea capitis due to T. tonsurans in the elderly. 
T. tonsurans is highly contagious: 40% of Parisian cases of tinea in 1910 were due to T. tonsurans and temporary exclusion from school has long been a compulsory part of treatment.  Despite this long history, treatment guidelines for tinea corporis have failed to produce the desired goals in the particular population of contact sports practitioners. Specific problems appear when dealing with such an outbreak in such a team. First of all, cases must be withdrawn from practice, but discontinuation of practice disrupts individual and team goals and is therefore difficult to accept.
Athletes can be tempted to hide their lesions until competitions are over. The benching period should not be compelling for Adams et al., in those athletes whose lesion can be bandaged.  Reducing the period of contagiousness should allow a shorter benching period. 
Second, these patients are minors, and prevention of infection requiring a daily screening of the entire skin surface raises ethical problems if this screening is to be carried out by a roommate or an adult coach.
Early recognition and treatment of these skin diseases permit the athlete to continue participation without disability or reduced performance.
To suppress the vector, each sick athlete should be benched throughout his contagious period. To prevent such outbreaks, the team physician must be familiar with common cutaneous infections including tinea corporis, tinea capitis and tinea pedis. 
Appropriate treatment and management of these infections allows the athlete to safely return to play and safeguards teammates and opponents against the spread of these diseases.
Boys have a greater risk than girls.  In our study 97.25% of patients were male [Table 1]. In the Japanese survey of Hiruma et al., 72.9% of patients were males (657/ 707), but the authors provided no denominator.  In the study of Shiraki et al., males represented 82.6% of the investigated population and were also more at risk for a positive hairbrush.  Gender may be a confusing factor and lead to false results about sharing hair combs and brushes ; in the French survey, most of the boys closely shaved their beards and hair, therefore had no need for combs or brushes, whereas girls had more common habits about their hair and the way of caring for it, and used shavers or razors for other purposes. 
In our study in 14.7% of isolates causative agents were zoophilic dermatophytes, T. mentagrophytes, T. verrucosum and Microsporum canis [Table 2]. A few reports have actually involved T. verrucosum or T. equinum, but the fungal etiology of tinea corporis gladiatorum is currently largely dominated by one single species, which is the anthropophilic dermatophyte T. tonsurans. ,,,,
The current worldwide spread of this disease, through international sports competitions, sustains a need for worldwide prevention measures that should be based upon an exact knowledge, most of all distinguishing it from the usual forms of tinea corporis.
Due to the chronic and recurrent nature of the lesions, individual and collective prophylactic measures are essential. 
These results indicate a need for improved primary prevention of fungal infections among athletes. Control of an outbreak may be very difficult and effective preventive measures should be considered.
This outbreak is probably part of a wider one diffusing among wrestling teams. Stopping it requires the cooperation of several distinct actors, among whom sports federations as well as sports-related physicians and dermatologists should play a major role.  We speculate that the outbreak is caused, at least in part, by ignorance of the disease among wrestler and Judo students, coaches and officials due to the high incidence of carriers and the mild or asymptomatic form of disease seen in infected individuals. Appropriate measures should be taken immediately to prevent a more severe outbreak of this disease.
| Conclusion|| |
Infection of T. tonsurans appears to have spread widely among members of combat sports clubs in Iran. These results indicate a need for improved primary prevention of tinea corporis gladiatorum among athletes. A preventive program involving education and coach participation is needed to target these individuals. Appropriate treatment and management of these infections allows the athlete to safely return to play and safeguards teammates and against the spread of these diseases.  As participation in active sports continues to grow, it is likely that the clinical and economic impact of superficial fungal infections in these individuals will increase. Awareness of these infections might facilitate implementation of early treatment and preventive measures. Early prevention, recognition and treatment of these skin diseases should permit the athlete to continue participation without further disability or reduced performance. Thus, regular dermatological screening of athletes is critical for rapid identification and treatment of dermatosis disrupting sport performance.
| References|| |
|1.||Chabasse D, Barale T. Mycoses et activités sportives. Revue Française des Lab 1997;???:45-50. |
|2.||Pleacher MD, Dexter WW. Cutaneous fungal and viral infections in athletes. Clin Sports Med 2007;26:397-411. |
|3.||Ergin S, Ergin C, Erdoðan BS, Kaleli I, Evliyaoðlu D. An experience from an outbreak of tinea capitis gladiatorum due to Trichophyton tonsurans. Clin Exp Dermatol 2006;31:212-4. |
|4.||Adams BB. Dermatologic disorders of the athlete. Sports Med 2002;32:309-21. |
|5.||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;54:622-6. |
|6.||Conklin RJ. Common cutaneous disorders in athletes. Sports Med 1990; 9:100-9. |
|7.||Eiland G, Ridley D. Dermatological problems in the athlete. J Orthop Sports Phys Ther 1996;23:388-402. |
|8.||Kantor GR, Bergfeld WF. Common and uncommon dermatologic diseases related to sports activities. Exerc Sport Sci Rev 1988;16:215-53. |
|9.||Poisson AD, Jourdan DN,Silva B, Rousseau CD, Este`ve DE. Tinea corporis gladiatorum: Specificity and epidemiology Tinea corporis gladiatorum: spe´cificite´ et e´pide´miologie. J de Mycologie Me´dicale 2007;17:177-82. |
|10.||Bergfeld WF. Dermatologic problems in athletes. Prim Care 1984;11:151-60. |
|11.||Brenner IK, Shek PN, Shephard RJ. Infection in athletes. Sports Med 1994;17 86-107. |
|12.||Caputo R, De Boulle K, Del Rosso J, Nowicki R. Prevalence of superficial fungal infections among sports-active individuals: Results from the Achilles survey, a review of the literature J Eur Acad Dermatol Venereol 2001;15:312-6. |
|13.||Burton GR, Wendolyn R, Burton W, Engelkirk PG. Microbiology for the Health Sciences, 5 th ed. Philadelphia, PA: JB Lippincott; 1996. |
|14.||Campbell Ck, Johnson EM, Philpot CM, Warnock DW. The dermatophytes. In: ???. Identification of pathogenic Fungi. London: PHLS; 1996. p. 26-68. |
|15.||De Hoog, Guarro J, Gene J, Figueras MJ. Atlas of clinical Fungi. 2 nd ed. Utrecht: Centraalbureau Vor Schimmelcultures; 2000. |
|16.||Selling B, Kibrick S. An outbreak of herpes simplex among wrestlers (herpes gladiatorum). N Engl J Med 1964;270:979-82. |
|17.||Adams BB. Tinea corporis gladiatorum. Am Acad Dermatol 2002;47:286-90. |
|18.||Derya A, Ilgen E, Metin E. Characteristics of sports-related dermatoses for different types of sports: A cross-sectional study. J Dermatol 2005;32:620-5. |
|19.||Kohl TD, Giesen DP, Moyer J, Lisney M. Tinea gladiatorum: Pennsylvania's experience. Clin J Sport Med 2002;12:165-71. |
|20.||Eros N, Karolyi Z, Molnar J. Trichophyton equinum infections among young wrestlers in Hungary. Acta Derm Venereol 1999;8:63-6. |
|21.||Frisk A, Heilborn H, Melen B. Epidemic occurrence of trichophytosis among wrestlers. Acta Derm Venereol 1966;46:453-6. |
|22.||Kohl TD, Lisney M. Tinea gladiatorum. Wrestling's emerging foe. Sports Med 2000;6:439-47. |
|23.||Hirose N, Shiraki Y, Hiruma M, Okawa H. An investigation of Trichophyton tonsurans infection in university students participating in sports clubs. Jpn J Med Mycol 2005;46:119-23. |
|24.||Hiruma M, Shiraki Y, Nihei N, Hirose N, Suganami M. Questionnaire investigation of incidence of Trichophyton tonsurans infection in dermatology clinics in the Kanto area. Jpn J Med Mycol 2005;46:93-7. |
|25.||Hubbard TW, de Triquet JM. Brush-culture method for diagnosing tinea capitis. Pediatrics 1992;90:416-8. |
|26.||Kasai T. Epidemiological survey of Trichophyton tonsurans infection in Tohoku district and its clinical problems. Jpn J Med Mycol 2005;46:87-91. |
|27.||Kohl TD, Martin DC, Berger MS. Comparison of topical and oral treatments for tinea gladiatorum. Clin J Sport Med 1999;9:161-6. |
|28.||Hradil E, Hersle K, Nordin P, Faergemann J. An epidemic of tinea corporis caused by Trichophyton tonsurans among wrestlers in Sweden. Acta Derm Venereol 1995;75:305-6. |
|29.||Estève E, Rousseau D, Defo D, Poisson DM. [Outbreak of cutaneous dermatophytosis in the Judo French Programme in Orleans: September 2004-June 2005] Ann Dermatol Venereol 2006;133:525-9. |
|30.||Stiller MJ, Klein WP, Dorman RI, Rosenthal S. Tinea corporis gladiatorum: An epidemic of Trichophyton tonsurans in student wrestlers. J Am Acad Dermatol 1992;27:632-3. |
|31.||Beller M, Gessner BD. An outbreak of tinea corporis gladiatorum on a high school wrestling team. J Am Acad Dermatol 1994;31:197-201. |
|32.||Poisson DM, Rousseau D, Defo D, Este`ve E. Outbreak of tinea corporis gladiatorum, a fungal skin infection due to Trichophyton tonsurans, in a French high-level judo team. Euro Surveill 2005;10:187-90. |
Department of Medical Mycology, Pasteur Institute of Iran, Tehran
Source of Support: None, Conflict of Interest: None
[Table 1], [Table 2], [Table 3], [Table 4]