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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.
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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.
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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
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3. Grosshans E, Schwaab E, Samsoen M, Grange D,
Koenig H, Kremer M. (1986). Clinical, epidemiological and economic aspects of fungal infections of
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coal miners and dermatological outpatients. British
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