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MICROBIAL ECOLOGY IN HEALTH AND DISEASE VOL 1: 131-135 (1988) Tinea Pedis: The Relationship Between Symptoms, Organisms and Host Characteristics SUSAN A. HOWELL*, YVONNE M. CLAYTON, Q. G. PHAN and W. C. NOBLE Microbial Diseases Unit, Institute of Dermatology, UMDS, London. Received 2 October 1987; revised 1 1 January 1988 Studies of foot infection in coal miners and in office and shop workers revealed high prevalence rates of fissuring and maceration associated with filamentous fungi and/or Gram-negative bacilli. The more severely affected had higher prevalence rates for potential pathogens, but this was not reflected in quantitative counts of organisms. Those practicing sports were less likely to have signs or symptoms of foot infection, though wet sports were more often associated with Gram-negative bacilli than were dry sports. KEY WORDS-Foot infection; Athletes foot; Dermatophytes; Gram-negative bacilli. INTRODUCTION Studies of foot infection in coal miners5*’ have shown that infection can be attributed to dermatophytes, to Gram-negative bacilli or, more rarely, to other organisms, but that in many cases a wide variety of potential pathogens can be isolated. With the exception of itching, more common in those with a dermatophyte infection, there seemed no particular sign or symptom which indicated infection with any particular group of organisms. The prevalence of disease observed, about 70 per cent, seemed high and studies were initiated in other groups of workers for comparison; in addition a semi-quantitative approach was made in an attempt to clarify the role of the Gram-negative bacilli. MATERIALS AND METHODS Coal miners (107 men) were from two collieries in the Nottinghamshire area. Office and shop workers (146 men and 150 women) were volunteers from three groups in the London area, and since no real clinical or microbiological differences could be discerned they have been considered together. Samples from the miners and office workers were collected and processed by the same individuals. In all instances the appearance of the toewebs was recorded on a four point scale (0, 1 + 2 + 3 +) for *Author to whom correspondence should be sent. Current Address: Lambeth Hospital, Renfrew London, SEI 1 4TH. 0891460)3/88/02013 1 4 5 $05.00 0 1988 by John Wiley &Sons, Ltd Rd, itching/soreness (regarded as a symptom) and for physical signs of cracking/fissuring, blistering/ maceration and malodour, though perception of malodour was especially observer dependent and not regarded as a reliable physical sign. Records were also made of other sites affected, e.g. nails, soles etc. The age and sex of all individuals was recorded. Ages ranged from 18 to 60 years, populations were arbitrarily divided into approximately equal groups on the basis of age. All were asked whether they or any specified member of their families had eczema or hayfever and whether they played any sports; replies on sport were divided into wet (e.g. swimming, boating) or dry (e.g. tennis, squash, football) on a scale of never/occasionally/ regularly (weekly). Microbiological samples were taken as follows: scrapings of skin, normally from the fourth interdigital toe space, were examined by direct microscopy in 30 per cent KOH and were also inoculated on Sabouraud dextrose agar containing 1 per cent mycological peptone (Oxoid L40), 4 per cent dextrose, 1.5 per cent agar, 50 pg/ml chloramphenicol and 500 pg/ml cycloheximide. Swab samples from the same toe space were taken prior to scraping using cotton swabs moistened in transport medium (Sterilin) and stored in that medium for up to 36 h. One swab was inoculated on Sabouraud dextrose agar containing chloramphenicol for yeast culture, the other was shaken vigorously in 10per cent sterile saline using a vortex mixer and aliquots of this and 132 a 1:lOO dilution drop-inoculated on C.L.E.D. medium (Oxoid CM 301) to provide semi-quantitative counts. Initial studies used C.L.E.D., blood agar base and coryneform agar. However bacterial species and numbers isolated from the latter two were found to be equivalent to C.L.E.D. All media for isolation of fungi were incubated at 26°C for up to 3 weeks. Bacterial cultures were incubated overnight at 37°C and at bench temperature for 2 to 3d before being counted. Bacteria were identified by Gram stain and morphology and conventional clinical laboratory tests. They are here reported as staphylococci and micrococci, coryneforms, Gramnegative bacilli or as ‘other’, which included Bacillus spp. and Gram-negative cocci. Only seven of the 403 subjects examined had Staphylococcus aureus isolated from their toewebs, this bacterium was therefore included with the Gram-positive cocci. Colonyforming units (cfu), were calculated as the number shaken from the swab in the original 10 ml saline; it is thus a comparative count and cannot be directly related to the number of organisms at the original skin site. Fungi are reported as filamentous fungi, a term which here includes occasional Hendersonula and Scytalidium species as well as Trichophyton and Epidermophyton species; yeasts are reported as total yeast species (there was only one isolate of Candida albicans amongst the 94 yeast species identified). RESULTS Overall the rates for any symptom or sign of foot infection were office females 53 per cent, office males 70 per cent and miners 88 per cent. The prevalence of individual symptoms or signs and of organisms in the three populations are presented in Table 1. It is evident that males had more symptoms or signs and potential pathogens than did females and that miners were more often affected than male office workers. All potential pathogens were more common in men and most common in the miners. It is probable that staphylococci and coryneforms were universally present but difficult to isolate (or had failed to grow) on media with large numbers of Gram-negative bacilli. In office workers, only filamentous fungi were more common in those with symptoms/signs than in those without, but in the miners this also applied to the Gram-negative bacilli (Table 2). The relation between symptoms/signs and any potential pathogen is significant by the Chi’ test for the two male populations only; it is notable that a substantial proportion of office workers had symptoms or signs S. A. HOWELL ET AL. Table 1 . Percentage prevalence of symptoms or signs of tinea pedis and presence of organisms in various populations Populationand number studied Office Office females males Miners Symptoms None Cracking/fissuring Blistering/maceration Itching/soreness Malodour Microorganisms Filamentous fungus Yeasts Gram-negative bacteria Staphylococci and micrococci Coryneform 150 146 107 47 49 19 7 10 30 62 38 12 19 12 62 58 31 4 15 28 22 29 98 80 36 29 57 90 64 11 14 100 79 of tinea pedis which failed to yield a potential pathogen. There were no significant quantitative differences in bacteria between those with and without symptoms or signs. Although there were significantly fewer miners in all three age groups who had no pathogens associated with their symptoms or signs, male and female office workers differed significantly only in the over 50 age group, where 85 per cent of those women with any combination of symptoms or signs failed to yield pathogens (Table 3). This was not associated with erythrasma (data not shown). Those with severe symptoms or signs (grade 2 + on both cracking/ fissuring and blistering/maceration) more often yielded filamentous fungi than those with only grade 1 + in the miners and more often yielded Gram negative bacilli in both miners and office males; there was no other apparent effect of severity of symptoms or signs (data not shown). Isolation of Proteus mirabilis and Pseudomonas aeruginosa occurred only in those with symptoms or signs and at the following frequencies: Proteus mirabilis was isolated from one office female (< lo5 cfu, symptoms or signs moderate), seven office males (three > lo5 cfu, one with severe symptoms or signs; four <lo5, one with severe symptoms or signs), five miners (three > lo5 cfu, one severe symptoms or signs; two < lo5 cfu). Pseudomonas aeruginosa was isolated from five office males (four > lo5, two 133 VARIABLES IN FOOT INFECTION Table 2. Prevalence of potential pathogens in those with or without any symptom or sign Office females Percentage prevalence of: Symptoms 80 Office males None 70 Symptoms 102 Miners None 44 Symptoms 94 None 13 40 30 61 86t 14 46 15 77 12 59 6 91 9 84 16 8 23 31 46t 54 31 0 77 8 62 0 85 15 69 31 ~~ Filamentous fungi Yeasts Gram-negative bacilli Any pathogen No pathogen Gram-negative bacilli > lo5 < 105 Staphylococci and > lo' micrococci < lo5 Coryneform > lo5 < 105 Total bacterial count > lo5 < 105 > 106 < 106 22.5 12.5 16 41 59 5 9 90 10 68 10 91 9 76 24 6 10 13 27 73 4 10 82 18 65 15 84 16 78 22 severe symptoms or signs; one <lo s) and four miners (four > 10' one severe symptoms or signs). There was an apparent relation between increased microbial numbers and the presence of symptoms or signs only for the Gram-negative bacilli in miners, but this was not statistically significant (Table 2). Amongst miners 22 of 9 4 (23 per cent) of those with symptoms or signs had more than lo6 Gramnegative bacilli compared with 2 of 13 (1 5 per cent) of those without symptoms or signs. There was no relationship between the presence of potential pathogens and eczema/hayfever in the volunteers or their families; nor was there any relationship between symptoms and eczema or hayfever (data not shown). It is also clear that in every case symptoms or signs are more common in those who do not practice sports whilst the potential pathogens are almost equally prevalent in those who do and do not engage in sport (Table 4). Although sports activities are more common in the younger age groups the trend is not significant. Subdivision of sporting activities into wet and dry failed to reveal any further differences relating to symptoms or signs (data not shown). Insufficient people practiced sports regularly to make analysis meaningful. In all three populations Gram-negative bacilli were more common in those who practiced wet, or wet and dry 33 24.5 30 62* 38 13 16 83 14 68 10 91 9 78 22 14 18 27 43 * 57 11 16 80 20 67 18 84 16 70 30 sports compared to those who only practiced dry sports (office females, wet sports 35 per cent of 63; dry only 27 per cent of 26; office males, wet sports 20 per cent of 64; dry only 12 per cent of 25; miners wet sports 73 per cent of 15; dry only 43 per cent of 37) but this reached statistical significance only for miners (x2 = 3.9 p <0.05). DISCUSSION Previous reports have described foot infection in 90 per cent' and 70 per cent5 of the mining populations studied. Here 88 per cent of miners, and 70 per cent of male and 53 per cent of female office workers were affected. Whilst these results appear high, the populations were obtained on a volunteer basis and a proportion of the respondants were probably seeking help. However, artificially high proportions of foot infection should not invalidate comparisons between the populations. In general this study agrees with other reports for industrial populations that in about one third to one half of persons, foot infection is associated with filamentous f ~ n g i . ~ *However, ~ * ' ~ in contrast to workers in Eastern Europe'.' we recovered few C. albicans. The findings for the office workers were interesting as there were substantial proportions of affected 134 S. A. HOWELL ET AL. Table 3. Prevalence of organisms in relation to age and symptom signs Age (years) Office females N = Percentage prevalence of: Filamentous fungi Yeasts Gram-negative rods No potential pathogen Office males N = Percentage prevalence of: Filamentous fungi Yeasts Gram-negative rods No potential pathogen Miners N = Percentage prevalence of: Filamentous fungi Yeasts Gram-negative rods No potential pathogen < 29 > 50 3M9 Any Symptoms None Any Symptoms None Any Symptoms None 26 25 29 21 20 20 19 23 34 10 17 5lt 0 46* 0 12 12 80 9 9 80 20 10 20 50 16 15 44 20 5 5 10 85tO 34 12 25 25 56* 20 7 13 60 5 25 30 55 44 21 29 29fO 29 29 57 43 25 3 34 29 36 34t 55 8 14 36 32 52 20* 0 33 33 67 45 25 65 9t 12 25 37 37 29 43 57 212 23 7 0 Table 4. Relation between sporting activities and symptoms expressed as percentage prevalence of symptoms or organisms Office females Office males Miners Any sport None Any sport None Any sport None Percentage prevalence of: 89 61 89 57 52 55 Symptoms Potential pathogens 48 57 36 65 56 70 53 65* 79 87* 84 34 * --significant atp<0.01. ' persons for whom no obvious microbial cause could be identified amongst females, this being less evident in men. S. aureus was rarely isolated and there was no overwhelming growth of a single staphylococcus or coryneform, some of which are highly proteolytic and capable of causing skin damage and malodour.6 Perhaps damage to toewebs occurs in an unspecified non-microbial fashion which in some cases may become superinfected with potential pathogens from the environment leading to an increase in symptom severity. Many of the Gramnegative bacilli isolated from feet could be regarded as of environmental origin.' These bacteria have been associated with severity of symptorn~/signs,~ but while the same trend is shown in this study the small numbers resulted in the trend not reaching statistical significance. Whilst Hay et u p reported atopy in outpatients to be significantly more common in those with Trichophyton rubrum infection, he found n o such VARIABLES IN FOOT INFECTION trend in miners. Our results are in keeping with this finding. It seems probable that as Hay and colleagues point out that where ‘there is a high risk of endemic dermatophytosis susceptibility factors such as atopy are of less importance’. The relationship between sports activity and foot infection was of interest as symptoms or signs were more common in non-sport groups while the organisms were equally distributed between those who practiced and did not practice sports. A possible interpretation is that those who are interested in fitness are more conscious of the condition of their body and feet. Only Wrede” has also examined the role of sports in foot infection and found no clinical difference in the appearance of the feet of policemen who practiced sport compared to those who did not. We have not attempted to comment on the complex interactions between fungi and Gram-negative bacteria as little experimental data exists. These studies again emphasise the heterogeneity of conditions so frequently subsumed under the term ‘athletes foot’ and indicate the injustice of this epithet. ACKNOWLEDGEMENTS We are indebted to the EEC and British Coal for supporting this study. The Medical Officers and all others in British Coal, B.B.C., British Rail and the John Lewis Partnership are thanked for their help and participation. REFERENCES 1. Banaskiewicz H. (1984). Analysis of the morbidity of skin mycoses in railway men. Mykosen 27, 305-308. 135 2. Gentles JC, Holmes JG. (1957). Foot ringworm in coal-miners. British Journal of Industrial Medicine 14,22-29. 3. Grosshans E, Schwaab E, Samsoen M, Grange D, Koenig H, Kremer M. (1986). Clinical, epidemiological and economic aspects of fungal infections of the feet amongst industrial workers. Annales de Dermatologie et Venereologie 113,521-533. 4. Hay RJ, Campbell CK, Wingfield R, Clayton YM. (1983). A comparative study of dermatophytosis in coal miners and dermatological outpatients. British Journal of Industrial Medicine 40,353-355. 5. Hope YM, ClaytonYM, Hay RJ, Noble WC, ElderSmith JG. (1985). Foot infection in coal miners: a reassessment. British Journal of Dermatology 112, 405-413. 6. Jackman PJH. (1982). Body odor-the role of skin bacteria. Seminars in Dermatology 1,143-148. 7. Lison E, Clayton Y, Hay RJ, Hope Y, Midgley G, Moore M, Noble WC. (1986). The microbiology of foot infection. Mykosen 29, 147-152. 8. Nevludova D. (1981). Etiology and epidemiology of mycoses of the feet in miners of the Ostravacaruin coal basin CSSR. Vestnik Dermatologii Venerologii 5,57-58. 9. Noble WC, Hope YM, Midgley G, Moore MK, Patel S, Virani Z , Lison E. (1986). Toewebs as a source of Gram negative bacilli. Journal of Hospital Infection 8,248-256. 10. Talwar P, Kumar B, Ayyagiri A, Kaur S. (1985). Prevalence of bacteria and fungi in athlete’s foot of varying seventy and response to topical antibacterial and antifungal therapies. Journal of Medical and Veterinary Mycology 23,303-3 12. 1 1 . Wrede E. (1965). Uber die Verbreitung von Fussmykosen speziell bei kazerneiter Polizei. Mykosen 8,66-76.