non-athletes, and to examine swimming pools as a route of infection. The subjects were 282 ... Tinea pedis (TP) is commonly called 'athlete's foot' because it is ...
Public Health (1997) 111, 249–253 © The Society of Public Health, 1997
Tinea pedis outbreak in swimming pools in Japan T Kamihama1, T Kimura1, J-I Hosokawa1, M Ueji2, T Takase3 and K Tagami1 1
Laboratory of Exercise and Environmental Health, Institute of Health and Sport Sciences, University of Tsukuba, Tsukuba, Ibaraki 305, Japan; 2Graduate School of Medicine, University of Tsukuba, Tsukuba, Ibaraki 305, Japan; and 3Laboratory of Dermatology, Institute of Clinical Medicine, University of Tsukuba, Tsukuba, Ibaraki 305, Japan This study was conducted to show a higher prevalence of interdigital tinea pedis in athletes by comparing athletes and non-athletes, and to examine swimming pools as a route of infection. The subjects were 282 athletes, 137 non-athletes, and 140 students enrolled in a swimming class at the University of Tsukuba. This study included the taking of cottonswab samples from the interdigital skin surfaces of both feet and cultures, microscopical examinations of scales collected from subjects with lesions, and questionnaires. There was a significant difference between athletes and nonathletes in the prevalence of the relevant pathogens, and a higher risk of infection was shown in athletes. The study also found that 63.6% of the swimming class students were carriers, and that 85.0% of their dermatophytes were Trichophyton mentagrophytes. In addition, dermatophytes were also isolated from the floors of the swimming pool and the public baths. The results of these controlled studies suggested that there was a significant risk of dermatophytosis in both athletes and non-athletes using the swimming pool. Keywords: athlete; Epidermophyton floccosum; interdigital tinea pedis; swimming pool; Trichophyton mentagrophytes; Trichophyton rubrum
Introduction Tinea pedis (TP) is commonly called ‘athlete’s foot’ because it is known to be very common among athletes,1–3 and the pathogens that cause it have been isolated on the floors of swimming pool dressing rooms and showers.4,5 Moreover, studies have shown that infections generally occur when individuals’ feet are exposed to these pathogens.3,4,6,7 Epidemiological studies on TP in athletes have been performed only cross sectionally in swimmers,4,5,8 marathon runners9 and judokas10 in western countries. In particular, in their studies on occult athlete’s foot, Attye et al 5 and Auger et al 9 pointed out the significantly higher prevalence of infection among athletes. However, studies of the disease in athletes have not been reported in Japan, and almost all studies conducted on the disease’s symptoms have focused on patients examined in skin clinics.11 In serious cases, TP can severely limit an individual’s lifestyle.12 Therefore, it is important to investigate the incidence of infection and the route or the causes of symptoms in individuals engaged in sporting activities. Accordingly, we investigated the prevalence of interdigital TP in non-athletes as well as in athletes involved in seven different sports. Furthermore, we examined the role played by swimming pools in promoting infection and the associated risk factors. Methods Materials Area of study. The study was conducted at a university made up of three clusters of colleges, three specialized schools, and two graduate schools. In 1995, 9517 undergraduates (male; 6166, female; 3351) and 4341 graduate Correspondence: T Kamihama. Accepted 1 February 1997
school students (male; 3217, female; 1124) were registered at this university. Almost all of the first-year undergraduates and half of second-year undergraduates live in student dormitories. The total number of dormitory residents as of April 5, 1995 was 3821 (male; 2289, female; 1359, family use; 173). These dormitories consist of three areas, each with its own public baths. The sport and physical education facilities at the university are managed by the Sport and Physical Education Center. Physical education classes, including undergraduate swimming classes held in the indoor swimming pool, are available, and ordinary students take one class a week throughout the year. Subjects. We examined 559 students by classifying them into three groups: an Athletes’ group, a Non-athletes’ group, and a Swimming class participants’ group. The first group consisted of 282 undergraduates (222 males and 60 females) at the School of Health and Physical Education who belonged to one of seven athletic teams, namely swimming, water polo, track (long distance running), soccer, basketball, kendo and judo. The second group consisted of 137 ordinary undergraduates (65 males and 72 females) from the colleges or schools other than the School of Health and Physical Education. These students had never taken the swimming class. The third group consisted of 140 non-athletic undergraduates (79 males and 61 females) who were not enrolled in the School of Health and Physical Education, and who attended the swimming class. All the subjects gave informed consent to these examinations. Culture medium and reagents. Sabouraud dextrose-chloramphenicol-cycloheximide agar: 65 g/l Sabouraud dextrose agar (Eiken Chemical Co., Tokyo, Japan), 500 mg/l cycloheximide (Wako Pure Chemical Industries, Osaka, Japan) and 50 mg/l chloramphenicol (Wako Pure Chemical Industries, Osaka, Japan) were dissolved in one litre of
250
Tinea pedis outbreak in swimming pools T Kamihama et al
redistilled water, and sterilized with an autoclave (121 C, 15 min). Cotton swab. Ordinary cotton swabs with a diameter of 5 mm and with a wooden handle of 5 cm were used. They were transferred individually into glass spits with stainlesssteel caps, and sterilized in an autoclave (121 C, 15 min). Staining solution. 20% KOH solution containing 20% Parker ink (Parker blue-black Super Quink ink, Parker Pen USA Ltd., Janesville, USA) was used to conduct microscopic examinations. Survey of prevalence and factor analysis of TP infection in athletes and non-athletes (Examination 1) The aim of this examination was to ascertain the prevalence of interdigital TP and extract risk factors in university athletes, based on comparisons of athletes and non-athletes. From September to November, 1995, specimens were collected from the feet of athletes before/after their sport activities and from the feet of non-athletes during physical education class. The authors collected specimens from both feet, and a 63-item questionnaire on lifestyle or behavior involving subjective data was completed by each student. The dermatophytes collection method described by Nishimoto13 (cotton swab sampling method; CSSM), consisted of firmly rubbing the interdigital skin surfaces of both feet of each subject using a sterile cotton swab moistened with sterile water. The specimens taken from the subjects were transferred immediately from the tip of the swab on to sterile petri dishes, and melted Sabouraud dextrosechloramphenicol-cycloheximide agar kept at 50 C was poured on them. The agar plate was incubated at room temperature (25 C) for 2–3 weeks. The positive cultures were further subcultured on a Sabouraud dextrose agar and identified according to the usual macroscopic observation and slide culture method.14,15 In cases with lesions in the interdigital skin, we collected scales for KOH microscopic examination, and identified them according to the usual Parker ink-KOH method.16,17 Survey of TP infection through swimming pool use (Examination 2) We conducted an examination to clearly determine the role that swimming pools play in bringing about TP infection, based on an investigation of the prevalence of the disease among non-athletic swimming class participants during
their activities in the swimming pool. This examination was carried out during swimming class in an indoor swimming pool in the middle of November 1995. Examination 2 involved the collection of samples and a questionnaire, just as in Examination 1. Isolation of dermatophytes on the floors of swimming pools and public baths (Examination 3) The purpose of this examination was to consider the route of TP infection at the University of Tsukuba based on the isolation of dermatophytes on the floors of the swimming pool and public baths in the dormitories. Sampling was carried out on 30 points on the floor of the swimming pool area, namely pool sides, male and female shower/dressing rooms and whirlpool bath, and on 36 points on the floors and floor mats in male/female dressing rooms of the three public baths. This was done in the middle of November, 1995. The floor surface (20 20 cm) was rubbed firmly with a sterile piece of cotton (5 5 cm). The rubbed cotton was spread on petri dishes containing Sabouraud dextrosechloramphenicol-cycloheximide agar. The plate was incubated at room temperature (25 C). The positive cultures were subcultured on Sabouraud glucose agar and identified according to the usual method,14,15 just as in Examination 1. The subjects were classified into a dermatophyte positive group and a negative group. The positive group consisted of subjects identified as dermatophyte positive by CSSM or by KOH microscopic examination. Furthermore, the positive subject group was divided into subjects with lesions (symptomatic subjects) and those without lesions (asymptomatic subjects) in the interdigital skin. The statistical validity of the results was assessed using the chi-square test and Fisher’s exact probability test. Differences of P < 0.05 were considered significant. Moreover, we considered the degree of influence of the exposition factor with sports activity by odds ratio (OR).
6 6
Results Investigation of TP among university athletes (Examination 1) Table 1 shows the results of Examination 1. These results clearly indicate that the prevalence of dermatophytes was higher in athletes than in non-athletes (OR 2.5; P < 0.001). A comparison of the prevalence in athletes involved in each sport versus non-athletes showed that the prevalence was significantly different for each of five sports, namely long
Table 1 Comparisons of dermatophytes culture between athletes versus non-athletes, and among sport events Number of dermatophytes positive
Non-athletes Athletes long distance running swimming water polo soccer basketball kendo judo
(n 137) (n 282) (n 36) (n 31) (n 17) (n 79) (n 61) (n 36) (n 22)
Symptomatic
Asymptomatic
Total
9 39 5 6 5 11 5 4 3
23 83 15 11 4 24 19 8 2
32 122 20 17 9 35 24 12 5
OR odds ratio; P P value; N.S. no significance.
Negative
OR
P
105 160 16 14 8 44 37 24 17
1.00 2.50 4.10 3.98 3.69 2.61 2.13 1.64 0.97
< 0.001 < 0.001 < 0.001
—
0.009 0.001 0.021 N.S. N.S.
Tinea pedis outbreak in swimming pools T Kamihama et al
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Table 2 Total of cases and the rates of occurrence according to the species of dermatophytes by cotton swab sampling method in athletes and non-athletes
Non-athletes Athletes long distance running swimming water polo soccer basketball kendo judo
T. rubrum
T. mentagrophytes
E. floccosum
Mixed flora
Microscopically positive (culture failed)
Total
10 61 15 6 5 15 9 7 4
16 41 2 9 3 9 15 3 0
3 8 1 0 0 6 0 1 0
1a 6 2b 1c 0 3d 0 0 0
2 6 0 1 1 2 0 1 1
32 122 20 17 9 35 24 12 5
T. mentagrophytes E. floccusum (1). T. rubrum T. mentagrophtyes (1), T. rubrum E. floccosum (1). T. rubrum T. mentagrophytes (1). d T. rubrum E. floccosum (2), T. mentagrophytes E. floccosum (1). a
b c
distance running, swimming, water polo, soccer and basketball. In judo and kendo athletes, however, there was no significant difference in prevalence. Table 2 shows the dermatophytes isolated in Examination 1. The two most predominant species among athletes were Trichophyton rubrum (61; 50.0%) and Trichophyton mentagrophytes (41; 33.6%). However, the most predominant species among non-athletes was T. mentagrophytes (16; 50.0%), followed by T. rubrum (10; 31.3%). These results showed the difference in the distribution of dermatophyte species between athletes and non-athletes. In the athletes involved in five of the above-mentioned sports, namely judo (80.0%), long distance running (85.0%), kendo (58.3%), water polo (55.6%), and soccer (48.6%), the predominant species was T. rubrum, while in basketball (62.5%) and swimming (58.9%), T. mentagrophytes was the predominant species. Mixed flora was found in six athlete cases (4.9%) and one non-athlete case (3.1%). Six athlete cases (4.9%) and two non-athlete cases (6.2%) were microscopically positive, but cultures failed.
Table 3 presents the risk factors extracted from positive subjects. Three major risk factors were identified by comparisons between the values of positive subjects and those of negative subjects in the athletes’ group. Habitual use of the swimming pool (OR 1.90; P 0.025), and anamnesis of interdigital lesions (OR 1.72; P 0.041) were associated with the development of TP, however habitual use of sandals (in winter) (OR 0.44; P 0.013) was a negative factor. Meanwhile, two major risk factors, living quarters (dormitory) (OR 2.46; P 0.048), and anamnesis of interdigital lesions (OR 3.28; P 0.005) were identified as being associated with the development of TP in nonathletes. Furthermore, habitual use of the swimming pool (OR 3.52; P 0.140) was considered in the case of nonathletes; however, this factor did not prove to be statistically significant. We also examined the rate of asymptomatic subjects in positive subjects. 68.0% of dermatophyte positive athletes were asymptomatic, and the rate was lower in male athletes than in female athletes (male, 65.0%; female, 81.8%). On
Table 3 Risk factors of athletes and non-athletes extracted from positive subjects Athletes (n 282) Variables
Categories
Non-athletes (n 137)
Positive
Negative
OR
P
Positive
Negative
OR
P
100 22
122 38
1.42 1.00
N.S.
16 16
48 57
1.19 1.00
N.S.
dormitory apartment
50 69
51 107
1.52 1.00
N.S.
21 8
48 45
2.46 1.00
0.048
dormitory (public) apartment (private)
38 68
32 98
1.71 1.00
N.S.
19 13
47 56
1.74 1.00
N.S.
yes no
35 87
28 132
1.90 1.00
0.025
3 29
3 102
3.52 1.00
N.S.
yes no
15 107
38 120
0.44 1.00
0.013
2 30
6 98
1.09 1.00
N.S.
yes no
90 30
101 58
1.72 1.00
0.041
23 9
46 59
3.28 1.00
0.005
Sex male female House Bath Habitual use of the swimming pool Habitual use of sandals (winter) Anamnesis of interdigital lesions
OR odds ratio; P P value; N.S. no significance.
252
Tinea pedis outbreak in swimming pools T Kamihama et al
Table 4 Comparison of infection rate between swimmers versus non-swimmers Number of dermatophytes positive
swimming class participants non-swimming class participants
Symptomatic
Asymptomatic
Total
12 9
89 23
101 32
(n 140) (n 137)
Negative
OR
39 105
8.50 1.00
P
< 0.001 —
OR odds ratio; P P value.
the other hand, 71.9% of positive non-athletes were asymptomatic, and again the rate was lower in male nonathletes than in female non-athletes (male, 56.3%; female, 87.5%). Investigation of TP among swimming class students (Examination 2) Table 4 shows the results of Examination 2. Among swimming class participants, 101 out of 140 subjects (72.1%) were positive, although 88.1% were asymptomatic. The prevalence of dermatophytes was higher among swimming class participants than among non-swimming class participants (OR 8.5; P < 0.001). The dermatophytes isolated by CSSM in swimming class were T. mentagrophytes (85 cases; 85.0%) and T. rubrum (12 cases; 12.0%). Mixed flora was identified in only three cases (3.0%). In the positive swimming class participants, the prevalence among males was almost the same as among females (male, 72.2%; female, 72.1%). The rate of asymptomatic males among the positive swimming class participants was lower than that of asymptomatic females (male, 82.5%; female, 95.5%). Of the risk factors listed in Table 3, only one, anamnesis of interdigital lesions (OR 2.77; P 0.009), was found among swimming class participants. Isolation of dermatophytes from the floor of pool/public bath (Examination 3) We isolated one case of T. mentagrophytes from the floor of the whirlpool bath in the swimming pool and one case of T. mentagrophytes from the floor of the dressing room of a women’s public bath in one of the dormitories. Discussion Although it is generally believed that TP is more common in athletes than in non-athletes, recently very few comparative or definitive studies showing the higher prevalence among athletes have been carried out.5,9,10 This comparative study found that the difference of prevalence in athletes relative to non-athletes was significant, although both groups lived in the same environment. The predominant species found were T. rubrum in athletes and T. mentagrophytes in non-athletes. In several reports, T. rubrum was isolated in a high percentage of cases involving symptomatic subjects,18 and T. mentagrophytes was isolated in a high percentage of cases involving asymptomatic subjects.5 As a result, these reports concluded that T. rubrum has a higher pathogenicity than T. mentagrophytes. Our results therefore suggested that the risk of TP infection among those engaged in sports was higher.
A significantly higher risk was recognized in those engaged in long distance running, swimming, water polo, soccer, and basketball, based on the prevalence of the disease in each group of athletes relative to non-athletes. Moreover, the predominant species differed depending on the sport, indicating that the pathogens are sport-specific. As a result, we believe that the higher prevalence among athletes is related to their lifestyles (behavior, habits or living environment) and specific training circumstances, since the prevalence and predominant species differ from one sport to another. It is therefore, important to analyze specific factors in athletes engaged in different sports, and find common factors among athletes in each sport to prevent TP infection in men/women engaged in sports. Because kendo/judo are barefoot activities, just like swimming, and because participants often walk barefoot outside the playing area, it was expected that they would have a higher prevalence of infection than athletes in other sports. However, in this study, no significant difference in prevalence relative to non-athletes was recognized. Moreover, prevalence was even lower than in athletes participating in other sports. Subjects who wore sandals in the winter had a lower prevalence of infection than those who did not wear sandals. Fifty percent of kendo/judo athletes wore sandals throughout the year, a rate that is considerably higher than that of athletes involved in other sports. Nickerson et al19 reported that the use of sandals was an effective means of diminishing the incidence of TP. Moreover, it has also been pointed out that one effective way to treat the disease is to dry the feet carefully.3,20 Therefore, we concluded that the disease was less prevalent among these athletes because they were in the habit of drying their feet regularly. Lifestyle and behavior are factors affecting the incidence of TP infection. In this study, living quarters (dormitory) was extracted from positive subjects as a risk factor in non-athletes, but was not considered a risk actor in athletes. The prevalence of TP in males was slightly higher than in females, but the sex was not extracted from positive subjects as a risk factor. The rate of asymptomatic positive males was lower than that of asymptomatic positive females in both athletes and non-athletes. Based on various hospital reports, Kasai11 reported that TP was more common among females than among males. However, the rates of incidence differed according to area. Therefore, he concluded that differences in incidence was due to the lifestyles of men and women, that is, that it was related to their living quarters. Previous surveys conducted on athletes have shown that TP is more prevalent among male athletes than among female athletes.5,9 However, these surveys did not sufficiently clarify the reasons for this. Although the sex distribution of TP infection is a controversial subject, we believe our results are meaningful at least with regard to prevalence among healthy students.
Tinea pedis outbreak in swimming pools T Kamihama et al
Therefore, we concluded that males showed higher risk, particularly with respect to symptom occurrence related to sex-specific lifestyles/hygiene. Furthermore, our results suggested that TP infection occurred as a result of the activities of non-athletes in their living environment. Nevertheless, the environment was regarded as a contributory factor, since sports activities had a greater impact on the risk of infection in athletes. Several reports have suggested that swimming pools are high risk facilities with respect to infection with the disease.4–6,8,21 In this study, athletes involved in swimming/ water polo showed a high infection rate, and a significantly higher risk of infection than non-athletes, and T. mentagrophytes was isolated from 58.8% of the swimmers. Furthermore, we isolated T. mentagrophytes from the floor of the whirlpool bath in the swimming pool. As a result, habitual use of the swimming pool was extracted from positive subjects as a risk factor in athletes. T. mentagrophytes from swimmers was isolated at a high rate by English et al6 (84.4%), and Gentles et al8 (62.1%). Attye et al5 isolated pathogens from the floor of a women’s locker room. All of their results suggested that a significantly higher risk of TP infection was associated with the use of swimming pools. Our study led to the same conclusion. We examined the prevalence of infection in swimmers during their activity in the swimming pool, to clarify the role that swimming pools play in transmitting TP infection. The prevalence of infection in swimming class participants relative to non-swimming class participants showed a significant difference, and dermatophytes were isolated from 72.2% of the students (symptomatic 8.6%, asymptomatic 63.6%). Moreover, the percentage of asymptomatic subjects were far higher (non-swimming class, 16.8%), and 88.8% of the pathogens isolated were T. mentagrophytes. Attye et al5 and Auger et al9 focused on hosts with no symptoms, and concluded that a significantly higher prevalence of the infection was associated with sports activities. Furthermore, they reported that an asymptomatic stage appeared soon after infection. Nishimoto et al22 isolated dermatophytes in unilateral TP patients from feet without lesions. In such cases, they considered that the feet without tinea lesions were in a subclinical infection stage. Our study, however, did not find that all asymptomatic swimming class participants were in a subclinical infection stage, even though their unusually high prevalence and asymptomatic rates suggested that they had been exposed to the pathogen in the swimming pool. Therefore, we concluded that swimming pools were the prime route of T. mentagrophytes infection. We would like to conclude by noting that, public baths have declined in importance in modern Japan. Therefore, swimming pools are now the most important infection route for TP. In this country, more than twenty million men and women use swimming pools every year. For this reason, it is necessary to inform swimming pool managers of the possibility of TP infection, and to take appropriate measures, especially in the case of those engaged in high risk activities. For example, pool managers could post notices such as ‘You have probably been exposed to tinea pedis. To avoid infection, you must wash your feet well as soon as you get home.’. Moreover, managers should clean all floors frequently, since it is known that cleaning floors is an effective way of preventing TP infection.18 Finally, pools should provide equipment that will allow users to wash their feet before leaving the facility.
Acknowledgements We would like to thank Dr. Y. Fukuwatari of the Department of Public Health, School of Medicine, Juntendo University, for his advice and encouragement.
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