REPORT
CANDIDA ALB/CANS —SAPROPHYTE OR PATHOGEN? RADZI JAAFAR, M.Ii.B.S. (MAL), DIP. tDERM. (LON), DIP. VEN. (LON), AND JOHN H.S. PETTIT, M.D. (LON), F.R.C.P.
Abstract Skin scrapings taken from toe spaces of 200 healthy volunteers and from toe webs and groins of 150 pediatric patients were cultured for Candida albicans using the serum germtube test. The results showed that Candida albicans can be isolated in about 15% of normal toe spaces and 14% of children with normal groins. Although Candida albicans can be found in various grades of athlete's foot and also in some abnormal groins, we believe that it is not necessarily responsible for these conditions and is often present at these sites only as a saprophyte. IntJ Dermatol 1992; 31:783-785
The terms "tinea pedis" and "tinea interdigital" are commonly used by dermatologists and general physicians alike, but "tinea" is best reserved for those conditions caused by a dermatophyte. It is not always possible to find such an organism growing in the interdigital spaces, and, as has been shown in a number of studies, the recovery of dcrmatophytes from clinically abnormal toe spaces is often less than 25%. It is, therefore, preferable to use the term "athlete's foot" to describe those itchy, scaly, interdigital lesions unless a dermatophyte has been isolated by direct microscopy or culture of specimens from the affected toe webs. As Hmmons et al. pointed out, not only can dermatophytes and a number of other skin pathogens be found in interdigital skin, various species of Candida may also grow.' Of these, Candida albicans is the most frequently recognized form, but Candida stellatoidea, Candida tropicalis, and Candida parapsilosis may sometimes be recognized. Neither Candida alhicans nor any other of the Candida species is a member of the normal flora of the skin, but in most intertriginous sites Candida species may be fairly frequent colonizers.' The aim of this study was to determine whether Ca?idida albicans acts as a pathogen in various severities of athlete's foot or is a saprophyte in clinically normal interdigital spaces playing no etiologic role in athlete's foot.""
We also took the opportunity to extend our work to find out the frequency of Candida albicans in the groins of young children. Dixon et al. having reported that although Candida albicans was found in 4 1 % of napkin eruptions, it was found in only 1 of 68 normal infants.^ Materials and Methods Study of Interdigital Spaces: Two hundred volunteers students and staff of the Faculty of Medicine, National University of Malaysia and patients attending the university's Dermatology Clinic - were recruited into tbis study. Tbey were randomly selected, tbe purpose of tbe study explained, and verbal informed consent obtained. The fourth interdigital space of each left foot was examined, and findings were classified as follows: K1, normal, no changes in toe webs; K2, dermatophytosis simplex, scaling and peeling witbout inflammatory signs or symptoms; K3, dermatophytosis complex, white maceration and soggy scaling; and K4, athlete's foot with byperkeratosis and foul-smelling white erosions. This grouping had been used by Leyden and KMgman in a study of the interaction of dermatophytes and resident flora in interdigital athlete's foot." In all our cases, scrapings from the predetermined site were taken and transferred immediately on to Sabouraud's agar. Any yeast that grew after a few days' incubation at room temperature was submitted to tbe serum germ-tube test in which 0.5 mL of serum in a small tube was Innoculated lightly witb the yeast and incubated at 37°C for ap'proximately 2 hours. On microscopy, the presence of even a small number of germ-tubes (more than five) was taken as diagnostic of Candida albicans.'' Study of Groins of Children: Our study was extended to include 150 children under the age of 12 admitted to the pediatric wards of tbe university for various medical conditions but without any dermatologic complaint. The left groin was clinically examined, and findings were indicated as normal or abnormal. Study of Children's Feet: Skin scrapings for culture of Candida albicans were also taken from the fourth left interdigital space of each child after tbe toe web was examined, and clinical findings were noted.
From the Faculty of Medicine, National University of Malaysia, Jalan Raja Muda Abd. Aziz, Kuala Lumpur, Malaysia. '• A pathogen is usually defined as a living microorganism or other agent causing disease. A saprophyte is a living organism that obtains some nutrition from dead or decaying matter (including keratin) but does not produce recognisable disease. Saprophytes do not grow on living tissue.
Address for correspondence: Dr. Radzi B. Jaafar, Department of Medicine, Faculty of Medicine, National University of Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Malaysia. 783
tiucrnatit)nal Journal of t^crtnatology Vol. .11, No. It, November 1992
Table 2. Groin Studies—Children
RESULTS
Foot Web Studies (Adults) On analysis of the data obtained in the initial study of 200 healthy volunteers, 120 were men and 80 women. The majority of the sample population studied cotnprised Malays (107 cases), 52 Chinese, 16 Indians, and 15 others. Of these, 166 had a normal interdigital space and were classified as K1. A small number of volunteers were found to have "uncomplained" athlete's foot (24 cases of group K2), nine cases of group K3, and a single case was classified as group K4. In the population studied, Candida albicans could be isolated in 24 cases with normal interdigital spaces (Kl) making the isolation rate 14.5%. Of the 24 cases of group K2, only seven (29%) grew the organisrn, while of the nine cases of group K.3 infection, three (33%) were positive. In addition, dermatophytes were grown from four people, three of whom were clinically normal, and one had dermatophytosis simplex. These observations are summarized in Table 1.
Groin Findings
Number of Cases
C. albicans Isolated
Dermatophyte Isolated
Normal
141
21 (14%) 4 (44%)
(0.7%) 0
'•• E.
floccosum.
Toe Web Studies (Children) We also studied the left fourth interdigital space in the children described above. All except one were clinically normal. The single exception had K2 athlete's foot. Results are shown in Table 3. Candida albicans was recovered from 25 (17%) of the 149 clinically normal feet, while all cultures were negative from the single patient with K2 athlete's foot.
DISCUSSION
The fact that scaly, red, pruritic, and even macerated lesions often foutid in the interdigital spaces have been given various names (tinea pedis, tinea interdigital, etc.) shows tbat both derrnatologists and tnycologists have believed that keratophylic fungi play an important role in the etiology of this condition. Other workers at various times have reported the presence of Candida albicans in some of these lesions. As long ago as 1949, Marples and Menna, surveying the occurrence of intertriginous fungal infection in a group of university students, made no mention of the recovery of Candida albicans.'' Later studies of tinea pedis in groups of school children made no reference to isolation of Candida albicans.^-* Leyden and Kligman tnade a study of patients with normal toe spaces,"* and although they isolated a Candida species in approxirnately 20%, Candida albicans was not detected. Simi-
Groin Studies (Children) In the extended study involvitig 150 in-patient children, 75 were boys and 75 girls, with a racial composition of 70 Malays, 40 Chinese, and 40 Indians. Of tbese, 141 were found to have clinically normal groins; the rest, nine cases in all, had mild scaling and hyperor hypopigmentary changes. Candida albicans was grown from 24 cases whose groins were clinically normal; the isolation rate was approximately 14%. Of the nine patients having abnormal groins, four (44%) grew Candida albicans (see Table 2). A dermatophyte was grown from a single patient with a clinically normal groin while none was isolated from any of the cases whose groins were noted as abnormal.
Table 3. Toe Web Studies —Children
Table 1. Toe Web Studies—Adults Athlete's Foot Group Kl (normal) Group K2 (Dermatophytosis simplex) Group K3 (Dermatophytosis complex) Group K4 (Malodorous, erosive, keratotic athlete's foot)
Number of Cases \66
24 f 1
C. albicans Isolated 24
(14.5%) 7 (29%)
" a
9
Abnormal
Athlete's Foot
Dermatophyte Isolated
Group Kl (normal) Group K2 (Dermatophytosis simplex) Group K3 (Dermatophytosis complex) Group K4 (Malodorous, erosive, keratotic athlete's foot)
3''(1.8%) It
(4.2%)
0
(33%)
(0%)
0 (0%)
0 (0%)
» T. mentagrophytes, 1 cases; T. rubrum, 1 case. ' T. mentagrophytes.
Number of Cases
C. albicans Isolated
149
1
0
" T. mentagrophytes, 1 case; T. rubrum, 2 784
25
3*
(17%)
(2%) 0 (0%)
0
(0%) 0
Dermatophyte Isolated
0
(0%)
0 (0%)
0 (0%)
0 (0%)
Candida alliicans JaaFar and I'crtit
lar findings applied when other grades of athlete's foot were studied. To complicate matters, they also pointed out that more than 40% of cases with more severe athlete's foot were mycologically negative. We have found that many of our cases of athlete's foot and tinea cruris were associated with the growth of Candida alhicans. Marples and her group also investigated the cutaneous distribution of Candida alhicans in the Cook Islands of the Pacific, because they could find very little information about the distribution of this organism in tropical areas.'^ They quoted Harvey Blank and his colleagues, who suspected that in humid tropical areas there was an increase in the incidence of Candida alhicans and suspected the yeast tnight be an important agent in cutaneous disease in a tropical environment. In her studies Marples found that Candida albicans grew on normal skin with surprising frequency being found in over 20% of toe webs of children under 10 years of age. A similar percentage was positive in adults, which led her to suggest that the genus Candida might piay a more important role in the etiology of cutaneous infection than is generally realized. Marples' figures were very similar to those we obtained in this study. Candida albicans is now recognized as an opportunistic organism growing where local conditions are favorable; among these situations, moisture and pre-existing skin conditions are important. Dixon et al. found that Candida albicans could be grown in some 40% of cases of napkin rash but in only one of the 68 normal infants they studied.^ Our results differed in that while recovery of Candida albicans from abnormal groins was much the same as in Dixon's study, positive growth was obtained in about 14% of normal groins. We cannot explain this difference except to postulate that the source of these organisms may have been the anal region; we did not attempt to culture the yeasts from this site. This paper demonstrates similar findings to work done elsewhere. Candida albicans was cultured from approximately 20% of our cases, and we suspect that.
SVFR. OF-
although it can be grown in Malaysia from diseased toe spaces and groins, it is probably not playing an active process in the pathogenesis of the skin condition and is present in these sites as a saprophyte. If this suggestion is true, it would indicate that the finding of Candida albicans in clinically normal skin would not be an indication for therapy, but, when found in sites that are diseased, anti-yeast therapy might be helpful. Acknowledgments: The Mycology Laboratory, Department of Medical Microbiology supplied the Sabouraud's agar. Mr. Zulkafli Ahmad typed the manuscript.
REt'EtlENCES
Emmons CW, Binford CH, Utz JP. Candidiasis. In: Medical mycology. 2nd Ed. Philadelphia: Lea and Febiger, 1970:167. 2.
Roberts SOB, Mackenzie DWR. Mycology. In: Rook A, Wilkinson DS, Ebling FJC, et al. eds. Textbook of dermatology. 4th Ed. London: Blackwell Scientific Publications, 1986:88.').
3.
Dixon PN, Warin RP, English MP. Rose of Candida alhicans infection in napkin rashes. Br Med J 1969- ii23-27.
4.
Lcyden jJ, Kligman AM. Interdigital athlete's foot - the interaction of dermatophytes and resident bacteria. Arch Dermatol 1978; 114:1466-1472. Clayton YM. Personal communication, 1988. Marples MJ. Menna ME. A survey of the incidence of intordigital fungous infection in a group of students from the University of Otago. Med | Aust 1949; 36156-161.
5. 6.
7. 8. ,9.
Marples MJ, Chapman EN. Tinea pedis in a group of schoolchildren. BrJ Dermatol 1959; 7L:413-421. English MP, Gibson MD. Studies in the epidemiology of tinea pedis. Br Med J 1959; i:1442-1448. Marples MJ, Sommerville DA. The oral and cutaneous distribution of Candida alhicans and other yeasts in Rarotonga, Cook Islands. Trans R Soc Trop Med Hyg 1968; 62:256-262.
||3E
ALCOHOL B PEB CENT. Six months, old . s p . Five years old. BO drops. One year old. . lodrops. Ten years old. 30 drops. Two years old. . i5(!rups. Adults. 1 to a teaspoonfuls. As an emetic, repeat every fifieeo minutes until lt acts.
From the collection of "La Pharmacie Frangaise," New Orleans, Louisiana, Mr. Ben Bavly, Curator. 785
CANDIDA ALB/CANS —SAPROPHYTE OR PATHOGEN? RADZI JAAFAR, M.Ii.B.S. (MAL), DIP. tDERM. (LON), DIP. VEN. (LON), AND JOHN H.S. PETTIT, M.D. (LON), F.R.C.P.
Abstract Skin scrapings taken from toe spaces of 200 healthy volunteers and from toe webs and groins of 150 pediatric patients were cultured for Candida albicans using the serum germtube test. The results showed that Candida albicans can be isolated in about 15% of normal toe spaces and 14% of children with normal groins. Although Candida albicans can be found in various grades of athlete's foot and also in some abnormal groins, we believe that it is not necessarily responsible for these conditions and is often present at these sites only as a saprophyte. IntJ Dermatol 1992; 31:783-785
The terms "tinea pedis" and "tinea interdigital" are commonly used by dermatologists and general physicians alike, but "tinea" is best reserved for those conditions caused by a dermatophyte. It is not always possible to find such an organism growing in the interdigital spaces, and, as has been shown in a number of studies, the recovery of dcrmatophytes from clinically abnormal toe spaces is often less than 25%. It is, therefore, preferable to use the term "athlete's foot" to describe those itchy, scaly, interdigital lesions unless a dermatophyte has been isolated by direct microscopy or culture of specimens from the affected toe webs. As Hmmons et al. pointed out, not only can dermatophytes and a number of other skin pathogens be found in interdigital skin, various species of Candida may also grow.' Of these, Candida albicans is the most frequently recognized form, but Candida stellatoidea, Candida tropicalis, and Candida parapsilosis may sometimes be recognized. Neither Candida alhicans nor any other of the Candida species is a member of the normal flora of the skin, but in most intertriginous sites Candida species may be fairly frequent colonizers.' The aim of this study was to determine whether Ca?idida albicans acts as a pathogen in various severities of athlete's foot or is a saprophyte in clinically normal interdigital spaces playing no etiologic role in athlete's foot.""
We also took the opportunity to extend our work to find out the frequency of Candida albicans in the groins of young children. Dixon et al. having reported that although Candida albicans was found in 4 1 % of napkin eruptions, it was found in only 1 of 68 normal infants.^ Materials and Methods Study of Interdigital Spaces: Two hundred volunteers students and staff of the Faculty of Medicine, National University of Malaysia and patients attending the university's Dermatology Clinic - were recruited into tbis study. Tbey were randomly selected, tbe purpose of tbe study explained, and verbal informed consent obtained. The fourth interdigital space of each left foot was examined, and findings were classified as follows: K1, normal, no changes in toe webs; K2, dermatophytosis simplex, scaling and peeling witbout inflammatory signs or symptoms; K3, dermatophytosis complex, white maceration and soggy scaling; and K4, athlete's foot with byperkeratosis and foul-smelling white erosions. This grouping had been used by Leyden and KMgman in a study of the interaction of dermatophytes and resident flora in interdigital athlete's foot." In all our cases, scrapings from the predetermined site were taken and transferred immediately on to Sabouraud's agar. Any yeast that grew after a few days' incubation at room temperature was submitted to tbe serum germ-tube test in which 0.5 mL of serum in a small tube was Innoculated lightly witb the yeast and incubated at 37°C for ap'proximately 2 hours. On microscopy, the presence of even a small number of germ-tubes (more than five) was taken as diagnostic of Candida albicans.'' Study of Groins of Children: Our study was extended to include 150 children under the age of 12 admitted to the pediatric wards of tbe university for various medical conditions but without any dermatologic complaint. The left groin was clinically examined, and findings were indicated as normal or abnormal. Study of Children's Feet: Skin scrapings for culture of Candida albicans were also taken from the fourth left interdigital space of each child after tbe toe web was examined, and clinical findings were noted.
From the Faculty of Medicine, National University of Malaysia, Jalan Raja Muda Abd. Aziz, Kuala Lumpur, Malaysia. '• A pathogen is usually defined as a living microorganism or other agent causing disease. A saprophyte is a living organism that obtains some nutrition from dead or decaying matter (including keratin) but does not produce recognisable disease. Saprophytes do not grow on living tissue.
Address for correspondence: Dr. Radzi B. Jaafar, Department of Medicine, Faculty of Medicine, National University of Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Malaysia. 783
tiucrnatit)nal Journal of t^crtnatology Vol. .11, No. It, November 1992
Table 2. Groin Studies—Children
RESULTS
Foot Web Studies (Adults) On analysis of the data obtained in the initial study of 200 healthy volunteers, 120 were men and 80 women. The majority of the sample population studied cotnprised Malays (107 cases), 52 Chinese, 16 Indians, and 15 others. Of these, 166 had a normal interdigital space and were classified as K1. A small number of volunteers were found to have "uncomplained" athlete's foot (24 cases of group K2), nine cases of group K3, and a single case was classified as group K4. In the population studied, Candida albicans could be isolated in 24 cases with normal interdigital spaces (Kl) making the isolation rate 14.5%. Of the 24 cases of group K2, only seven (29%) grew the organisrn, while of the nine cases of group K.3 infection, three (33%) were positive. In addition, dermatophytes were grown from four people, three of whom were clinically normal, and one had dermatophytosis simplex. These observations are summarized in Table 1.
Groin Findings
Number of Cases
C. albicans Isolated
Dermatophyte Isolated
Normal
141
21 (14%) 4 (44%)
(0.7%) 0
'•• E.
floccosum.
Toe Web Studies (Children) We also studied the left fourth interdigital space in the children described above. All except one were clinically normal. The single exception had K2 athlete's foot. Results are shown in Table 3. Candida albicans was recovered from 25 (17%) of the 149 clinically normal feet, while all cultures were negative from the single patient with K2 athlete's foot.
DISCUSSION
The fact that scaly, red, pruritic, and even macerated lesions often foutid in the interdigital spaces have been given various names (tinea pedis, tinea interdigital, etc.) shows tbat both derrnatologists and tnycologists have believed that keratophylic fungi play an important role in the etiology of this condition. Other workers at various times have reported the presence of Candida albicans in some of these lesions. As long ago as 1949, Marples and Menna, surveying the occurrence of intertriginous fungal infection in a group of university students, made no mention of the recovery of Candida albicans.'' Later studies of tinea pedis in groups of school children made no reference to isolation of Candida albicans.^-* Leyden and Kligman tnade a study of patients with normal toe spaces,"* and although they isolated a Candida species in approxirnately 20%, Candida albicans was not detected. Simi-
Groin Studies (Children) In the extended study involvitig 150 in-patient children, 75 were boys and 75 girls, with a racial composition of 70 Malays, 40 Chinese, and 40 Indians. Of tbese, 141 were found to have clinically normal groins; the rest, nine cases in all, had mild scaling and hyperor hypopigmentary changes. Candida albicans was grown from 24 cases whose groins were clinically normal; the isolation rate was approximately 14%. Of the nine patients having abnormal groins, four (44%) grew Candida albicans (see Table 2). A dermatophyte was grown from a single patient with a clinically normal groin while none was isolated from any of the cases whose groins were noted as abnormal.
Table 3. Toe Web Studies —Children
Table 1. Toe Web Studies—Adults Athlete's Foot Group Kl (normal) Group K2 (Dermatophytosis simplex) Group K3 (Dermatophytosis complex) Group K4 (Malodorous, erosive, keratotic athlete's foot)
Number of Cases \66
24 f 1
C. albicans Isolated 24
(14.5%) 7 (29%)
" a
9
Abnormal
Athlete's Foot
Dermatophyte Isolated
Group Kl (normal) Group K2 (Dermatophytosis simplex) Group K3 (Dermatophytosis complex) Group K4 (Malodorous, erosive, keratotic athlete's foot)
3''(1.8%) It
(4.2%)
0
(33%)
(0%)
0 (0%)
0 (0%)
» T. mentagrophytes, 1 cases; T. rubrum, 1 case. ' T. mentagrophytes.
Number of Cases
C. albicans Isolated
149
1
0
" T. mentagrophytes, 1 case; T. rubrum, 2 784
25
3*
(17%)
(2%) 0 (0%)
0
(0%) 0
Dermatophyte Isolated
0
(0%)
0 (0%)
0 (0%)
0 (0%)
Candida alliicans JaaFar and I'crtit
lar findings applied when other grades of athlete's foot were studied. To complicate matters, they also pointed out that more than 40% of cases with more severe athlete's foot were mycologically negative. We have found that many of our cases of athlete's foot and tinea cruris were associated with the growth of Candida alhicans. Marples and her group also investigated the cutaneous distribution of Candida alhicans in the Cook Islands of the Pacific, because they could find very little information about the distribution of this organism in tropical areas.'^ They quoted Harvey Blank and his colleagues, who suspected that in humid tropical areas there was an increase in the incidence of Candida alhicans and suspected the yeast tnight be an important agent in cutaneous disease in a tropical environment. In her studies Marples found that Candida albicans grew on normal skin with surprising frequency being found in over 20% of toe webs of children under 10 years of age. A similar percentage was positive in adults, which led her to suggest that the genus Candida might piay a more important role in the etiology of cutaneous infection than is generally realized. Marples' figures were very similar to those we obtained in this study. Candida albicans is now recognized as an opportunistic organism growing where local conditions are favorable; among these situations, moisture and pre-existing skin conditions are important. Dixon et al. found that Candida albicans could be grown in some 40% of cases of napkin rash but in only one of the 68 normal infants they studied.^ Our results differed in that while recovery of Candida albicans from abnormal groins was much the same as in Dixon's study, positive growth was obtained in about 14% of normal groins. We cannot explain this difference except to postulate that the source of these organisms may have been the anal region; we did not attempt to culture the yeasts from this site. This paper demonstrates similar findings to work done elsewhere. Candida albicans was cultured from approximately 20% of our cases, and we suspect that.
SVFR. OF-
although it can be grown in Malaysia from diseased toe spaces and groins, it is probably not playing an active process in the pathogenesis of the skin condition and is present in these sites as a saprophyte. If this suggestion is true, it would indicate that the finding of Candida albicans in clinically normal skin would not be an indication for therapy, but, when found in sites that are diseased, anti-yeast therapy might be helpful. Acknowledgments: The Mycology Laboratory, Department of Medical Microbiology supplied the Sabouraud's agar. Mr. Zulkafli Ahmad typed the manuscript.
REt'EtlENCES
Emmons CW, Binford CH, Utz JP. Candidiasis. In: Medical mycology. 2nd Ed. Philadelphia: Lea and Febiger, 1970:167. 2.
Roberts SOB, Mackenzie DWR. Mycology. In: Rook A, Wilkinson DS, Ebling FJC, et al. eds. Textbook of dermatology. 4th Ed. London: Blackwell Scientific Publications, 1986:88.').
3.
Dixon PN, Warin RP, English MP. Rose of Candida alhicans infection in napkin rashes. Br Med J 1969- ii23-27.
4.
Lcyden jJ, Kligman AM. Interdigital athlete's foot - the interaction of dermatophytes and resident bacteria. Arch Dermatol 1978; 114:1466-1472. Clayton YM. Personal communication, 1988. Marples MJ. Menna ME. A survey of the incidence of intordigital fungous infection in a group of students from the University of Otago. Med | Aust 1949; 36156-161.
5. 6.
7. 8. ,9.
Marples MJ, Chapman EN. Tinea pedis in a group of schoolchildren. BrJ Dermatol 1959; 7L:413-421. English MP, Gibson MD. Studies in the epidemiology of tinea pedis. Br Med J 1959; i:1442-1448. Marples MJ, Sommerville DA. The oral and cutaneous distribution of Candida alhicans and other yeasts in Rarotonga, Cook Islands. Trans R Soc Trop Med Hyg 1968; 62:256-262.
||3E
ALCOHOL B PEB CENT. Six months, old . s p . Five years old. BO drops. One year old. . lodrops. Ten years old. 30 drops. Two years old. . i5(!rups. Adults. 1 to a teaspoonfuls. As an emetic, repeat every fifieeo minutes until lt acts.
From the collection of "La Pharmacie Frangaise," New Orleans, Louisiana, Mr. Ben Bavly, Curator. 785
