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Tinea capitis: Focus on African American women
SUPPORTED
BY AN EDUCATIONAL GRANT FROM
GALDERMA LABORATORIES
Tinea capitis: Focus on African American women Nanette B. Silverberg, MD, Jeffrey M. Weinberg MD, and Vincent A. DeLeo, MD New York, New York Tinea capitis is a common cutaneous fungal infection in US school children, but adults may be carriers of tinea pathogens in the scalp. However, few cases of actual tinea capitis in adults have been reported in the literature. A retrospective analysis of all adult patients with positive scalp fungal cultures from June 1997 to March 2000 were reviewed. Seventy-nine cases of tinea capitis were identified. Nine (11.4%) were adults, 7 of whom were African American women, who were an average of 46 years old (range, 25 to 64 years). Three of these patients had prior exposure to a child with tinea capitis. These results suggest that tinea capitis affects adult African Americans, particularly women. Widespread scalp culture is indicated for papulosquamous disease and alopecia in this segment of the population. (J Am Acad Dermatol 2002; 46:S120-4.)
T
inea capitis is a common fungal infection, usually afflicting children between the ages of 3 and 7 years.1 In the past 10 years, an 84.7% increase in tinea capitis in children of all races and a 209.7% increase in African American children, have been observed.2 Contagion from household members who are either symptomatic or carriers has contributed significantly to this soaring incidence.3 The carrier state is common in adult female caretakers of children with tinea capitis.3 A rising incidence of tinea capitis in adults has been documented in France,4 Italy,5,6 and Taiwan,7,8 but progression to clinically active disease in adult women has not been well documented in the United States.
MATERIAL AND METHODS This study is a retrospective analysis of culturepositive cases of tinea capitis, seen from June 1997 to
From the Skin of Color Center, Department of Dermatology, St. Luke’s-Roosevelt Hospital, New York. This article is part of a supplement supported by Galderma Laboratories. Disclosures: Dr Silverberg is a clinical investigator for Fujisawa, Convatec, Ferndale Laboratories, and Upjohn Pharmacia. Dr Weinberg is a clinical investigator for Agenix, Cubist Pharmaceuticals, Novartis, Fujisawa, Hill Dermaceuticals, Upjohn Pharmacia, Coherent, Allergan, Aldara, Galderma, Ferndale Laboratories, Convatec, Unilever/Dove soap, and PUVA; and is also a member of the Advisory Board for 3M and a speaker for Novartis. Dr DeLeo is a clinical investigator for Galderma and Novartis. Reprint requests: Nanette B. Silverberg, MD, Department of Dermatology, St. Luke’s-Roosevelt Hospital Center, 1090 Amsterdam Avenue, Suite 11D, New York, NY 10025. Copyright © 2002 by the American Academy of Dermatology, Inc. 0190-9622/2002/$35.00 + 0 16/0/120793 doi:10.1067/mjd.2002.120793
S120
March 2000 in the Department of Dermatology at the St. Luke’s-Roosevelt Hospital Center, New York. The patient population consists primarily of Hispanics (36%) and African Americans (59%). Patients seen at the Department of Dermatology who had clinical evidence of scalp hyperkeratosis were cultured for tinea capitis. Twenty-percent potassium hydroxide in dimethyl sulfoxide was placed on a slide containing superficial cutaneous scrapings from these patients. These scrapings were examined for the presence of hyphae. Cultures were obtained with the following technique: a water-moistened cotton swab was vigorously rubbed over 4 quadrants of the scalp. The swabs were then rubbed onto dermatophyte test medium (DTM), the sticks broken one third of the way from the cotton tip, and the cover of the DTM was then closed partially to allow air entry. The cultures were held for 2 weeks, at which time they were analyzed for test medium color change and typical fungal morphology. Negative scalp cultures were held for another 2 weeks for a second reading.
RESULTS Seventy-nine patients were identified who were either culture positive, had a positive potassium hydroxide examination, or both. Forty-seven men and 32 women were identified. All the cultures were positive for Trichophyton tonsurans by color change of the medium from yellow to red and growth of colonies with typical morphology (powdery white-tan colonies with notation of red-brown pigment spread to the underlying medium, wherever possible). The average age of the group was 9.9 years. Of these patients, 9 were older than age
Silverberg, Weinberg, and DeLeo S121
J AM ACAD DERMATOL VOLUME 46, NUMBER 2
Table I. Patient demographic and disease information for adult cases of tinea capitis Patient Number Sex
Age
Race
KOH
DTM
Previous diagnosis
Previous therapy
Tinea variant
Contact history
1
F
25
AA
+
+
Folliculitis
Oral antibiotics
Seborrheic
Nephew with tinea capitis Child with tinea capitis Homeless
2
F
33
AA
+
-
Seborrheic dermatitis
Shampoos
Seborrheic
3
F
42
AA
+
+
Alopecia areata
4 5
F F
42 50
AA AA
+ +
+ +
Tinea capitis Seborrheic dermatitis
Alopecia areata/ black dot Kerion/ black dot On prednisone Seborrheic
6
F
64
AA
+
+
Seborrheic dermatitis
7
F
67
AA
+
+
Seborrheic dermatitis
8
M
22
AA
+
+
Seborrheic dermatitis
9
M
37
AA
+
+
Seborrheic dermatitis
Mid-potency steroid solutions Butenafine cream Mid-potency steroid solutions Mid-potency steroid solutions Mid-potency steroid solutions Mid-potency steroid solutions Mid-potency steroid solutions
Seborrheic
Cares for a child
Seborrheic
At least 5 years with illness
Seborrheic Seborrheic
AA, African American; DTM, dermatophyte test medium; KOH, potassium hydroxide.
20 (11.4%). All 9 patients were culture positive at 2 weeks. Pediatric patients The 70 pediatric patients consisted of 45 male and 25 female patients, average age 6.1 years. Fifty-eight of these patients were African American, average age 8.2 years. Fifty-seven patients had varying degrees of alopecia. A single child had only occipital lymphadenopathy in the presence of a positive scalp fungal culture. The 11 Hispanic children had an average age of 5.2 years. One child was a 12-year-old white male with seborrheic tinea capitis. Adult patients The patients older than age 20 were all African American: 7 were women and 2 men (Table I) (Figs 1 and 2). All the patients had some degree of alopecia. Seven had seborrheic-type tinea capitis, 2 had black dot, and 1 had alopecia areata-type and a kerion. These patients were, on average, 42 years old (range 22-67 years). Four patients previously had been given a diagnosis of seborrheic dermatitis, 1 of alopecia areata, 1 of folliculitis, and 1 of tinea capitis. Four had been treated with topical steroid medications, 1 with oral antibiotics, and 3 with shampoos for seborrhea. One patient was taking prednisone for rheumatoid arthritis (patient 4). Two patients (patients 1 and 2) were known to have a culturepositive household contact (a nephew and a daughter, respectively). By patient self-report, comb sharing was not a practice in any patient’s household. Three patients regularly tended or took care of chil-
dren (patients 1, 2, and 4); 2 of these children had tinea capitis. One patient (patient 3) was homeless and lived in a shelter with children. The length of clinical disease ranged from 2 weeks in the 25-yearold to at least 5 years in a 67-year-old.
DISCUSSION Tinea capitis appears to be increasing in African American women. A study done in Taiwan in the early 1990s documented that 3% to 5% of patients with tinea capitis were adults.8 Our study showed that 11.4% of tinea capitis patients were adult African Americans, and 77% of these adults were women, ages 25 to 67. Each of the women had mild alopecia in the presence of seborrhea-like scalp scaling. In a recent French study, 11% of patients with positive cultures were adults, 75% of whom were female.4 All the French patients had some degree of scalp hyperkeratosis: 62.5% had alopecia and 25% had pustular lesions (in the absence of a frank kerion). Tinea capitis in adults is often caused by various Trichophyton species. In the French cohort, the culture isolates were diverse, including a variety of Trichophyton and Microsporum species. It also has been documented that in Taiwan, tinea capitis caused by T tonsurans is now more common in adult females than in children.7,8 (The average age of these adults was 56 to 58 years.) In the study by Chao et al,7 14 of 17 patients had black dot tinea. Close to 20% of the adult patients with scalp problems seen in a South African clinic in Cape Town have tinea capitis resulting from T violaceum, a fungal species with similar phenotype and genotype to T tonsurans.9
S122 Silverberg, Weinberg, and DeLeo
J AM ACAD DERMATOL FEBRUARY 2002
Fig 1. Patient 1, a 25-year-old African American woman with tinea capitis, presumed to have been caught from a nephew.
Fig 2. Patient 9, a 37-year-old African American man with tinea capitis that developed shortly after getting a haircut in a barbershop.
Adult cases of tinea capitis caused by Microsporum species do exist, but they are uncommon. In a 4-year observational study done in the 1990s on tinea capitis caused by Microsporum species, only 2 of 41 patients were adults.10 Another study from Italy documented only 5 postmenopausal women with Microsporum scalp isolates in a group of 181 patients.6 An observational study in Poland on tinea capitis incidence detected that Microsporum was the causative pathogen in 78% of cases. However, only 6.7% of Microsporum-induced cases occurred in patients older than age 15. Unfortunately, a breakdown of isolates for patients ages 20 and older was not done.11 One possible reason for the paucity of adult tinea capitis cases caused by Microsporum species is the increase of sebum production in adulthood. The triglyceride-rich content of sebum may have fungistatic properties against M ectothrix infections; however, sebum cannot prevent endothrix infections caused by such Trichophyton species as T tonsurans.12,13 In spite of this, Kligman14 demonstrated in 1952 that Microsporum sp could be inoculated onto the adult scalp. The gender differential in adults for active tinea capitis as well as carrier states has been observed since the 1950s.15 The disorder continues to occur predominantly in females in all geographic locations, irrespective of climate or species of dermatophyte.3,4,8-10,16-19 It has been estimated that 66% to 94% of carriers and active cases in adults older than age 20 are women, agreeing with our current data.3,4,8,9,20,21 In the 1980s, Bronson20 evaluated 9 adults, ages 20 to 65, with tinea capitis caused by T tonsurans: 6 of these patients were women. In the 1990s, Aste et al5 reported 17 adult tinea capitis cases from Italy, all women between the ages of 17 and 76.
Only 1 study, a population-based study of tinea isolates in Turin, Italy,22 has demonstrated an incidence favoring males who were postpuberty. However, this study did not involve an analysis of cases in adults ages 20 and older. The lack of an adult subpopulation analysis compromises the overall results of this study. Adult tinea capitis mirrors childhood disease as far as dermatophyte isolates are concerned. Carriers from areas in which T tonsurans is endemic are likely to have T tonsurans, whereas those from areas where Microsporum sp are endemic will likely carry Microsporum.21 Cases of adult tinea capitis related to T rubrum infection have been reported, but this was not noted in our patients. However, the dermatophyte test medium used in our study may have limited morphologic assessment of isolates. T tonsurans is the predominant etiologic agent for tinea capitis in the United States for both children and adults. Evidence in support of cases caused by T tonsurans isolates in our study involves the fact that 3 of our patients reported contact with children, 2 of whom had tinea capitis. The role of the woman as the primary caretaker of children in the household likely has contributed to the rise of the disease in these women. As early as 1983, Bronson et al20 reported a disproportionate number of cases of tinea corporis in women of childbearing age, which the authors attributed to contagion from childhood index cases. The spread of active tinea capitis from child to mother was reported in 1952 by Pipkin,15 and has been documented more recently in the study done in Taiwan, mentioned earlier.7 In Cuetara et al’s23 study of Spanish schoolchildren, one third of the adults related to these children manifested symptomatic tinea capitis. Twenty-five percent of the
J AM ACAD DERMATOL VOLUME 46, NUMBER 2
patients in the French study mentioned earlier reported that they took care of children.4 In a study from South Africa, 19% of parents of children with tinea capitis tested positive for the carrier state. Contagion is bidirectional: untreated adult parents with the disease can infect children, and untreated children with the disease can infect parents. In a study by Cremer et al,4 1 of the adult patients had untreated disease since childhood. This patient had been treated for presumed psoriasis with topical steroids and went on to infect 3 children with tinea capitis and 1 adult with tinea corporis. This geometric progression of infectivity from index case to the surrounding community could represent a public health issue. Contagion is difficult to control in cases of tinea capitis caused by T tonsurans. Fomites can persist on surfaces for an extensive period. Infections have resulted from contact with a preowned car, classroom surfaces, brushes, and other personal items, including a doll’s hair.24 Barbers may serve as local reservoirs of disease.25 Women are most likely to manage and style their child’s hair, giving them a high level of exposure to spores on the scalp. Given the high degree of potential exposure in an endemic area, it often becomes difficult to determine the source case of tinea capitis. One of the patients with tinea capitis was living in a homeless shelter for women and children. We believe the exposure to children in the shelter to be the cause of her illness. A recent survey of homeless men living in a shelter in Boston revealed no cases of tinea capitis, although tinea pedis was the leading diagnosis in this population.26 Possibly, there is less exposure to childhood index cases in homeless men. Given the contagious risk of fomites, a shelter with even a few affected children could represent a reservoir of disease. Further exploration of the incidence of tinea capitis in homeless females living in shelters is required to properly assess the epidemiology in this selected population of patients. Clinically, childhood and adult tinea capitis cases are similarly polymorphic in appearance. A combination of alopecia, seborrhea, “black dot” hairs, and inflammatory changes is expected with T tonsurans infection. This is less true of T rubrum tinea capitis, which is rare in adults and children alike. Recently reported cases of T rubrum tinea capitis presented with scarring alopecia and crusting, but lacked the “black dots” seen with T tonsurans.27,28 Tinea capitis, when caused by T tonsurans, is often unrecognized and mistaken for clinical mimics. This is especially true for adults because of the high incidence of seborrhea in postadolescence. In our adult patients, seborrheic dermatitis, alopecia areata,
Silverberg, Weinberg, and DeLeo S123
and folliculitis were the 3 diagnoses made before the diagnosis of tinea capitis. Clinical mimicry of seborrheic and atopic dermatitis for tinea capitis has long been an issue of clinical significance in pediatric dermatology, with recent recognition in adults.29 Consequently, we concur with other researchers that clinicians observing adult seborrhea, alopecia areata, and scalp folliculitis should entertain tinea capitis in their differential diagnosis. HIV infection has been implicated in previously reported cases of adult tinea capitis, although adult cases have been reported in African patients in the absence of HIV infection.30 Six of the 8 patients in the French report4 were immunocompromised (2 with lymphoma, 1 HIV positive, 1 with psoriasis on therapy, 1 with thrombocythemia). However, only 1 of our patients was known to be immunocompromised. Thus, we do not believe that HIV infection, AIDS, or other manifestations of immune compromise are responsible for all cases of tinea capitis. Based on our cases and the report of both HIV30 and non-HIV25 infected adults with tinea capitis in Africa, it seems likely that endemic pathogens causing tinea capitis in the general population are more responsible for the rise of adult disease in this population. The incidence of tinea capitis has been reported to account for 12% of all childhood skin disorders in Africa.18 Because 25% of the African population is estimated to have HIV infection, it would not be surprising that many African tinea capitis cases would be seen in HIV-infected individuals. Reports from Nigeria before the HIV epidemic demonstrated few adult tinea capitis cases, with only 2 out of 58 patients being older than age 25. More recently, there has been a rise in the overall adult incidence of tinea capitis on the African continent and in tinea capitis cases in adult immigrants from Africa.17,31 Whether these observations are related to the HIV epidemic is unknown. The incidence of tinea capitis has been reported to be as high as 12.19% in a population.18 It is likely that our adult cases reflect the recent overall rise in tinea capitis of more than 200% in African American children2 and the African American community. The carrier rate is known to be higher in adult female caretakers than in male caretakers and can approach 30% for cases caused by T tonsurans.31-33 Some authors5 have hypothesized that there is a hormonal basis for adult tinea based on endocrinologic evaluation. In their analysis, 12 cases showed altered hormonal patterns. Compounding matters further are hair care practices in African Americans, including less shampooing, which has some spore-removal benefits, and traction hair styling, which can allow easier fungal
S124 Silverberg, Weinberg, and DeLeo
access to the impaired hair shaft. Sharma et al34 have recently shown that hair care plays a minimal role in development of disease in children; rather, exposure to index cases is the factor most likely to be associated with the development of disease. Most probably, the incidence in women worldwide is related to a combination of being the primary caretaker of children with disease, high-level exposure from the background population, and hair care practices.31-33
CONCLUSION Tinea capitis may be rising in African American women, and this rise is likely to escalate. The worldwide prevalence in women is undoubtedly the result of a number of gender-specific factors (eg, their role as primary caretakers of children with disease and hair care practices) as well as high-level exposure from the background population. It will become more important for practitioners to perform scalp cultures on adult African American women with any signs of persistent seborrhea or alopecia. REFERENCES 1. Elewski BE. Tinea capitis: a current perspective. J Am Acad Dermatol 2000; 42:1-20. 2. Lobato MN, Vugia DJ, Frieden IJ. Tinea capitis in California children: a population-based study of a growing epidemic. Pediatrics 1997;99:551-4. 3. Pomeranz AJ, Sabnis SS, McGrath GJ, Esterly NB. Asymptomatic dermatophyte carriers in the households of children with tinea capitis. Arch Pediatr Adolesc Med 1999;153:483-6. 4. Cremer G, Bournerias I, Vandemeleubroucke E, Houin R, Revuz J. Tinea capitis in adults: misdiagnosis or reappearance? Dermatology 1997;194:8-11. 5. Aste N, Pau M, Biggio P. Tinea capitis in adults. Mycoses 1996;39:299-301. 6. Romano C. Tinea capitis in Siena, Italy. An 18-year survey. Mycoses 1999;42:559-62. 7. Chao S-C, Hsu MM-L. Trichophyton tonsurans infection in Tainan area. J Formos Med Assoc 1994;93:697-701. 8. Lee JY-Y, Hsu M-L. Tinea capitis in adults in southern Taiwan. Int J Dermatol 1991;30:572-5. 9. Neil G, Hanslo D, Bucimazza S, Kibel M. Control of the carrier state of scalp dermatophytes. Pediatr Infect Dis 1990;9:57-8. 10. Maraki S, Tselentis Y. Survey on the epidemiology of Microsporum canis infections in Crete, Greece over a 5-year period. Int J Dermatol 2000;39:21-4. 11. Nowicki R. Dermatophytoses in Gdansk area, Poland: a 12-year survey. Mycoses 1996;39:399-402. 12. Rudolph AH. The diagnosis and treatment of tinea capitis due to Trichophyton tonsurans. Int J Dermatol 1985;24:426-31. 13. Seale ER, Richardson JB. Trichophyton tonsurans: a follow-up of treated and untreated cases. Arch Dermatol 1960;81:87-94.
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14. Kligman AM. The pathogenesis of tinea capitis due to Microsporum audouinii and Microsporum canis. I. Gross observations following the inoculation of humans. J Invest Dermatol 1952;18:231-45. 15. Pipkin JL. Tinea capitis in adult and adolescent. Arch Dermatol 1952;66:9-40. 16. Van Hecke E, Meysman L.Tinea capitis in an adult (Microsporum canis). Mykosen 1980;23:607-8. 17. Grin EI. Epidemiology and control of ringworm of the scalp. Pan American Health Organization: International Symposium on Mycoses; Washington 1970. p. 149-56. 18. Malhotra YK, Garg MP, Kanwar AJ, Nagrajan S. A study of tinea capitis in Libya (Benghazi). Sabouradia 1979;17:181-3. 19. Ridley CM.Tinea capitis in an elderly woman. Clin Exp Dermatol 1979;4:247-9. 20. Bronson DM, Desai DR, Barsky S, Foley SM. An epidemic of infection with Trichophyton tonsurans revealed in a 20-year survey of fungal infection in Chicago. J Am Acad Dermatol 1983;8:32230. 21. Ive FA.The carrier stage of tinea capitis in Nigeria. Br J Dermatol 1966;78:219-21. 22. Marchisio VF, Preve L, Tullio V. Fungi responsible for skin mycoses in Turin (Italy). Mycoses 1996;39:141-150. 23. Cuetara MS, del Palacio A, Pereiro M, Amor E, Alvarez C, Noriega AR. Prevalence of undetected tinea capitis in a school survey in Spain. Mycoses 1997;40:131-7. 24. Hebert AA, Head ES, MacDonald EM. Tinea capitis caused by Trichophyton tonsurans. Pediatr Dermatol 1985;2:219-23. 25. Soyinka F. Epidemiologic study of dermatophyte infections in Nigeria (clinical survey and laboratory investigations). Mycopathologia 1978;63:99-103. 26. Stratigos AJ, Stern R, Gonzalez E, Johnson RA, O’ Connell JO, Dover JS. Prevalence of skin disease in a cohort of shelter-based homeless men. J Am Acad Dermatol 1999;41:197-202. 27. Bargman H, Kane J, Baxter M-L, Summerbell RC. Tinea capitis due to Trichophyton rubrum in adult women. Mycoses 1995;38: 231-4. 28. Vannini P, Guadagni R, Palleschi GM, Difonzo EM, Panconesi E. Tinea capitis in the adult: two case studies. Mycopathologia 1986;96:53-7. 29. Honig PJ, Smith LR. Tinea capitis masquerading as atopic or seborrheic dermatitis. J Pediatr 1979;94:604-5. 30. Lateur N, Andre J, De Mabubeuge J, Poncin M, Song M. Tinea capitis in two black African adults with HIV infection. Br J Dermatol 1999;140:722-4. 31. Fuller LC, Child FC, Higgens EM. Tinea capitis in south-east London: an outbreak of Trichophyton tonsurans infection. Br J Dermatol 1997;136:132-48. 32. Vargo K, Cohen BA. Prevalence of undetected tinea capitis in household members of children with disease. Pediatrics 1993; 92:155-7. 33. Babel DE, Rogers AL, Beneke ES. Evaluation of the adult carrier state in juvenile tinea capitis caused by Trichophyton tonsurans. J Am Acad Dermatol 1989;21:1209-12. 34. Sharma V, Silverberg NB, Howard R,Tran CT, Laude TA, Frieden IJ. Do hair care practices affect the acquisition of tinea capitis? A case-control study. Arch Pediatr Adolesc Med 2001;155:818-21.
BY AN EDUCATIONAL GRANT FROM
GALDERMA LABORATORIES
Tinea capitis: Focus on African American women Nanette B. Silverberg, MD, Jeffrey M. Weinberg MD, and Vincent A. DeLeo, MD New York, New York Tinea capitis is a common cutaneous fungal infection in US school children, but adults may be carriers of tinea pathogens in the scalp. However, few cases of actual tinea capitis in adults have been reported in the literature. A retrospective analysis of all adult patients with positive scalp fungal cultures from June 1997 to March 2000 were reviewed. Seventy-nine cases of tinea capitis were identified. Nine (11.4%) were adults, 7 of whom were African American women, who were an average of 46 years old (range, 25 to 64 years). Three of these patients had prior exposure to a child with tinea capitis. These results suggest that tinea capitis affects adult African Americans, particularly women. Widespread scalp culture is indicated for papulosquamous disease and alopecia in this segment of the population. (J Am Acad Dermatol 2002; 46:S120-4.)
T
inea capitis is a common fungal infection, usually afflicting children between the ages of 3 and 7 years.1 In the past 10 years, an 84.7% increase in tinea capitis in children of all races and a 209.7% increase in African American children, have been observed.2 Contagion from household members who are either symptomatic or carriers has contributed significantly to this soaring incidence.3 The carrier state is common in adult female caretakers of children with tinea capitis.3 A rising incidence of tinea capitis in adults has been documented in France,4 Italy,5,6 and Taiwan,7,8 but progression to clinically active disease in adult women has not been well documented in the United States.
MATERIAL AND METHODS This study is a retrospective analysis of culturepositive cases of tinea capitis, seen from June 1997 to
From the Skin of Color Center, Department of Dermatology, St. Luke’s-Roosevelt Hospital, New York. This article is part of a supplement supported by Galderma Laboratories. Disclosures: Dr Silverberg is a clinical investigator for Fujisawa, Convatec, Ferndale Laboratories, and Upjohn Pharmacia. Dr Weinberg is a clinical investigator for Agenix, Cubist Pharmaceuticals, Novartis, Fujisawa, Hill Dermaceuticals, Upjohn Pharmacia, Coherent, Allergan, Aldara, Galderma, Ferndale Laboratories, Convatec, Unilever/Dove soap, and PUVA; and is also a member of the Advisory Board for 3M and a speaker for Novartis. Dr DeLeo is a clinical investigator for Galderma and Novartis. Reprint requests: Nanette B. Silverberg, MD, Department of Dermatology, St. Luke’s-Roosevelt Hospital Center, 1090 Amsterdam Avenue, Suite 11D, New York, NY 10025. Copyright © 2002 by the American Academy of Dermatology, Inc. 0190-9622/2002/$35.00 + 0 16/0/120793 doi:10.1067/mjd.2002.120793
S120
March 2000 in the Department of Dermatology at the St. Luke’s-Roosevelt Hospital Center, New York. The patient population consists primarily of Hispanics (36%) and African Americans (59%). Patients seen at the Department of Dermatology who had clinical evidence of scalp hyperkeratosis were cultured for tinea capitis. Twenty-percent potassium hydroxide in dimethyl sulfoxide was placed on a slide containing superficial cutaneous scrapings from these patients. These scrapings were examined for the presence of hyphae. Cultures were obtained with the following technique: a water-moistened cotton swab was vigorously rubbed over 4 quadrants of the scalp. The swabs were then rubbed onto dermatophyte test medium (DTM), the sticks broken one third of the way from the cotton tip, and the cover of the DTM was then closed partially to allow air entry. The cultures were held for 2 weeks, at which time they were analyzed for test medium color change and typical fungal morphology. Negative scalp cultures were held for another 2 weeks for a second reading.
RESULTS Seventy-nine patients were identified who were either culture positive, had a positive potassium hydroxide examination, or both. Forty-seven men and 32 women were identified. All the cultures were positive for Trichophyton tonsurans by color change of the medium from yellow to red and growth of colonies with typical morphology (powdery white-tan colonies with notation of red-brown pigment spread to the underlying medium, wherever possible). The average age of the group was 9.9 years. Of these patients, 9 were older than age
Silverberg, Weinberg, and DeLeo S121
J AM ACAD DERMATOL VOLUME 46, NUMBER 2
Table I. Patient demographic and disease information for adult cases of tinea capitis Patient Number Sex
Age
Race
KOH
DTM
Previous diagnosis
Previous therapy
Tinea variant
Contact history
1
F
25
AA
+
+
Folliculitis
Oral antibiotics
Seborrheic
Nephew with tinea capitis Child with tinea capitis Homeless
2
F
33
AA
+
-
Seborrheic dermatitis
Shampoos
Seborrheic
3
F
42
AA
+
+
Alopecia areata
4 5
F F
42 50
AA AA
+ +
+ +
Tinea capitis Seborrheic dermatitis
Alopecia areata/ black dot Kerion/ black dot On prednisone Seborrheic
6
F
64
AA
+
+
Seborrheic dermatitis
7
F
67
AA
+
+
Seborrheic dermatitis
8
M
22
AA
+
+
Seborrheic dermatitis
9
M
37
AA
+
+
Seborrheic dermatitis
Mid-potency steroid solutions Butenafine cream Mid-potency steroid solutions Mid-potency steroid solutions Mid-potency steroid solutions Mid-potency steroid solutions Mid-potency steroid solutions
Seborrheic
Cares for a child
Seborrheic
At least 5 years with illness
Seborrheic Seborrheic
AA, African American; DTM, dermatophyte test medium; KOH, potassium hydroxide.
20 (11.4%). All 9 patients were culture positive at 2 weeks. Pediatric patients The 70 pediatric patients consisted of 45 male and 25 female patients, average age 6.1 years. Fifty-eight of these patients were African American, average age 8.2 years. Fifty-seven patients had varying degrees of alopecia. A single child had only occipital lymphadenopathy in the presence of a positive scalp fungal culture. The 11 Hispanic children had an average age of 5.2 years. One child was a 12-year-old white male with seborrheic tinea capitis. Adult patients The patients older than age 20 were all African American: 7 were women and 2 men (Table I) (Figs 1 and 2). All the patients had some degree of alopecia. Seven had seborrheic-type tinea capitis, 2 had black dot, and 1 had alopecia areata-type and a kerion. These patients were, on average, 42 years old (range 22-67 years). Four patients previously had been given a diagnosis of seborrheic dermatitis, 1 of alopecia areata, 1 of folliculitis, and 1 of tinea capitis. Four had been treated with topical steroid medications, 1 with oral antibiotics, and 3 with shampoos for seborrhea. One patient was taking prednisone for rheumatoid arthritis (patient 4). Two patients (patients 1 and 2) were known to have a culturepositive household contact (a nephew and a daughter, respectively). By patient self-report, comb sharing was not a practice in any patient’s household. Three patients regularly tended or took care of chil-
dren (patients 1, 2, and 4); 2 of these children had tinea capitis. One patient (patient 3) was homeless and lived in a shelter with children. The length of clinical disease ranged from 2 weeks in the 25-yearold to at least 5 years in a 67-year-old.
DISCUSSION Tinea capitis appears to be increasing in African American women. A study done in Taiwan in the early 1990s documented that 3% to 5% of patients with tinea capitis were adults.8 Our study showed that 11.4% of tinea capitis patients were adult African Americans, and 77% of these adults were women, ages 25 to 67. Each of the women had mild alopecia in the presence of seborrhea-like scalp scaling. In a recent French study, 11% of patients with positive cultures were adults, 75% of whom were female.4 All the French patients had some degree of scalp hyperkeratosis: 62.5% had alopecia and 25% had pustular lesions (in the absence of a frank kerion). Tinea capitis in adults is often caused by various Trichophyton species. In the French cohort, the culture isolates were diverse, including a variety of Trichophyton and Microsporum species. It also has been documented that in Taiwan, tinea capitis caused by T tonsurans is now more common in adult females than in children.7,8 (The average age of these adults was 56 to 58 years.) In the study by Chao et al,7 14 of 17 patients had black dot tinea. Close to 20% of the adult patients with scalp problems seen in a South African clinic in Cape Town have tinea capitis resulting from T violaceum, a fungal species with similar phenotype and genotype to T tonsurans.9
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Fig 1. Patient 1, a 25-year-old African American woman with tinea capitis, presumed to have been caught from a nephew.
Fig 2. Patient 9, a 37-year-old African American man with tinea capitis that developed shortly after getting a haircut in a barbershop.
Adult cases of tinea capitis caused by Microsporum species do exist, but they are uncommon. In a 4-year observational study done in the 1990s on tinea capitis caused by Microsporum species, only 2 of 41 patients were adults.10 Another study from Italy documented only 5 postmenopausal women with Microsporum scalp isolates in a group of 181 patients.6 An observational study in Poland on tinea capitis incidence detected that Microsporum was the causative pathogen in 78% of cases. However, only 6.7% of Microsporum-induced cases occurred in patients older than age 15. Unfortunately, a breakdown of isolates for patients ages 20 and older was not done.11 One possible reason for the paucity of adult tinea capitis cases caused by Microsporum species is the increase of sebum production in adulthood. The triglyceride-rich content of sebum may have fungistatic properties against M ectothrix infections; however, sebum cannot prevent endothrix infections caused by such Trichophyton species as T tonsurans.12,13 In spite of this, Kligman14 demonstrated in 1952 that Microsporum sp could be inoculated onto the adult scalp. The gender differential in adults for active tinea capitis as well as carrier states has been observed since the 1950s.15 The disorder continues to occur predominantly in females in all geographic locations, irrespective of climate or species of dermatophyte.3,4,8-10,16-19 It has been estimated that 66% to 94% of carriers and active cases in adults older than age 20 are women, agreeing with our current data.3,4,8,9,20,21 In the 1980s, Bronson20 evaluated 9 adults, ages 20 to 65, with tinea capitis caused by T tonsurans: 6 of these patients were women. In the 1990s, Aste et al5 reported 17 adult tinea capitis cases from Italy, all women between the ages of 17 and 76.
Only 1 study, a population-based study of tinea isolates in Turin, Italy,22 has demonstrated an incidence favoring males who were postpuberty. However, this study did not involve an analysis of cases in adults ages 20 and older. The lack of an adult subpopulation analysis compromises the overall results of this study. Adult tinea capitis mirrors childhood disease as far as dermatophyte isolates are concerned. Carriers from areas in which T tonsurans is endemic are likely to have T tonsurans, whereas those from areas where Microsporum sp are endemic will likely carry Microsporum.21 Cases of adult tinea capitis related to T rubrum infection have been reported, but this was not noted in our patients. However, the dermatophyte test medium used in our study may have limited morphologic assessment of isolates. T tonsurans is the predominant etiologic agent for tinea capitis in the United States for both children and adults. Evidence in support of cases caused by T tonsurans isolates in our study involves the fact that 3 of our patients reported contact with children, 2 of whom had tinea capitis. The role of the woman as the primary caretaker of children in the household likely has contributed to the rise of the disease in these women. As early as 1983, Bronson et al20 reported a disproportionate number of cases of tinea corporis in women of childbearing age, which the authors attributed to contagion from childhood index cases. The spread of active tinea capitis from child to mother was reported in 1952 by Pipkin,15 and has been documented more recently in the study done in Taiwan, mentioned earlier.7 In Cuetara et al’s23 study of Spanish schoolchildren, one third of the adults related to these children manifested symptomatic tinea capitis. Twenty-five percent of the
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patients in the French study mentioned earlier reported that they took care of children.4 In a study from South Africa, 19% of parents of children with tinea capitis tested positive for the carrier state. Contagion is bidirectional: untreated adult parents with the disease can infect children, and untreated children with the disease can infect parents. In a study by Cremer et al,4 1 of the adult patients had untreated disease since childhood. This patient had been treated for presumed psoriasis with topical steroids and went on to infect 3 children with tinea capitis and 1 adult with tinea corporis. This geometric progression of infectivity from index case to the surrounding community could represent a public health issue. Contagion is difficult to control in cases of tinea capitis caused by T tonsurans. Fomites can persist on surfaces for an extensive period. Infections have resulted from contact with a preowned car, classroom surfaces, brushes, and other personal items, including a doll’s hair.24 Barbers may serve as local reservoirs of disease.25 Women are most likely to manage and style their child’s hair, giving them a high level of exposure to spores on the scalp. Given the high degree of potential exposure in an endemic area, it often becomes difficult to determine the source case of tinea capitis. One of the patients with tinea capitis was living in a homeless shelter for women and children. We believe the exposure to children in the shelter to be the cause of her illness. A recent survey of homeless men living in a shelter in Boston revealed no cases of tinea capitis, although tinea pedis was the leading diagnosis in this population.26 Possibly, there is less exposure to childhood index cases in homeless men. Given the contagious risk of fomites, a shelter with even a few affected children could represent a reservoir of disease. Further exploration of the incidence of tinea capitis in homeless females living in shelters is required to properly assess the epidemiology in this selected population of patients. Clinically, childhood and adult tinea capitis cases are similarly polymorphic in appearance. A combination of alopecia, seborrhea, “black dot” hairs, and inflammatory changes is expected with T tonsurans infection. This is less true of T rubrum tinea capitis, which is rare in adults and children alike. Recently reported cases of T rubrum tinea capitis presented with scarring alopecia and crusting, but lacked the “black dots” seen with T tonsurans.27,28 Tinea capitis, when caused by T tonsurans, is often unrecognized and mistaken for clinical mimics. This is especially true for adults because of the high incidence of seborrhea in postadolescence. In our adult patients, seborrheic dermatitis, alopecia areata,
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and folliculitis were the 3 diagnoses made before the diagnosis of tinea capitis. Clinical mimicry of seborrheic and atopic dermatitis for tinea capitis has long been an issue of clinical significance in pediatric dermatology, with recent recognition in adults.29 Consequently, we concur with other researchers that clinicians observing adult seborrhea, alopecia areata, and scalp folliculitis should entertain tinea capitis in their differential diagnosis. HIV infection has been implicated in previously reported cases of adult tinea capitis, although adult cases have been reported in African patients in the absence of HIV infection.30 Six of the 8 patients in the French report4 were immunocompromised (2 with lymphoma, 1 HIV positive, 1 with psoriasis on therapy, 1 with thrombocythemia). However, only 1 of our patients was known to be immunocompromised. Thus, we do not believe that HIV infection, AIDS, or other manifestations of immune compromise are responsible for all cases of tinea capitis. Based on our cases and the report of both HIV30 and non-HIV25 infected adults with tinea capitis in Africa, it seems likely that endemic pathogens causing tinea capitis in the general population are more responsible for the rise of adult disease in this population. The incidence of tinea capitis has been reported to account for 12% of all childhood skin disorders in Africa.18 Because 25% of the African population is estimated to have HIV infection, it would not be surprising that many African tinea capitis cases would be seen in HIV-infected individuals. Reports from Nigeria before the HIV epidemic demonstrated few adult tinea capitis cases, with only 2 out of 58 patients being older than age 25. More recently, there has been a rise in the overall adult incidence of tinea capitis on the African continent and in tinea capitis cases in adult immigrants from Africa.17,31 Whether these observations are related to the HIV epidemic is unknown. The incidence of tinea capitis has been reported to be as high as 12.19% in a population.18 It is likely that our adult cases reflect the recent overall rise in tinea capitis of more than 200% in African American children2 and the African American community. The carrier rate is known to be higher in adult female caretakers than in male caretakers and can approach 30% for cases caused by T tonsurans.31-33 Some authors5 have hypothesized that there is a hormonal basis for adult tinea based on endocrinologic evaluation. In their analysis, 12 cases showed altered hormonal patterns. Compounding matters further are hair care practices in African Americans, including less shampooing, which has some spore-removal benefits, and traction hair styling, which can allow easier fungal
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access to the impaired hair shaft. Sharma et al34 have recently shown that hair care plays a minimal role in development of disease in children; rather, exposure to index cases is the factor most likely to be associated with the development of disease. Most probably, the incidence in women worldwide is related to a combination of being the primary caretaker of children with disease, high-level exposure from the background population, and hair care practices.31-33
CONCLUSION Tinea capitis may be rising in African American women, and this rise is likely to escalate. The worldwide prevalence in women is undoubtedly the result of a number of gender-specific factors (eg, their role as primary caretakers of children with disease and hair care practices) as well as high-level exposure from the background population. It will become more important for practitioners to perform scalp cultures on adult African American women with any signs of persistent seborrhea or alopecia. REFERENCES 1. Elewski BE. Tinea capitis: a current perspective. J Am Acad Dermatol 2000; 42:1-20. 2. Lobato MN, Vugia DJ, Frieden IJ. Tinea capitis in California children: a population-based study of a growing epidemic. Pediatrics 1997;99:551-4. 3. Pomeranz AJ, Sabnis SS, McGrath GJ, Esterly NB. Asymptomatic dermatophyte carriers in the households of children with tinea capitis. Arch Pediatr Adolesc Med 1999;153:483-6. 4. Cremer G, Bournerias I, Vandemeleubroucke E, Houin R, Revuz J. Tinea capitis in adults: misdiagnosis or reappearance? Dermatology 1997;194:8-11. 5. Aste N, Pau M, Biggio P. Tinea capitis in adults. Mycoses 1996;39:299-301. 6. Romano C. Tinea capitis in Siena, Italy. An 18-year survey. Mycoses 1999;42:559-62. 7. Chao S-C, Hsu MM-L. Trichophyton tonsurans infection in Tainan area. J Formos Med Assoc 1994;93:697-701. 8. Lee JY-Y, Hsu M-L. Tinea capitis in adults in southern Taiwan. Int J Dermatol 1991;30:572-5. 9. Neil G, Hanslo D, Bucimazza S, Kibel M. Control of the carrier state of scalp dermatophytes. Pediatr Infect Dis 1990;9:57-8. 10. Maraki S, Tselentis Y. Survey on the epidemiology of Microsporum canis infections in Crete, Greece over a 5-year period. Int J Dermatol 2000;39:21-4. 11. Nowicki R. Dermatophytoses in Gdansk area, Poland: a 12-year survey. Mycoses 1996;39:399-402. 12. Rudolph AH. The diagnosis and treatment of tinea capitis due to Trichophyton tonsurans. Int J Dermatol 1985;24:426-31. 13. Seale ER, Richardson JB. Trichophyton tonsurans: a follow-up of treated and untreated cases. Arch Dermatol 1960;81:87-94.
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14. Kligman AM. The pathogenesis of tinea capitis due to Microsporum audouinii and Microsporum canis. I. Gross observations following the inoculation of humans. J Invest Dermatol 1952;18:231-45. 15. Pipkin JL. Tinea capitis in adult and adolescent. Arch Dermatol 1952;66:9-40. 16. Van Hecke E, Meysman L.Tinea capitis in an adult (Microsporum canis). Mykosen 1980;23:607-8. 17. Grin EI. Epidemiology and control of ringworm of the scalp. Pan American Health Organization: International Symposium on Mycoses; Washington 1970. p. 149-56. 18. Malhotra YK, Garg MP, Kanwar AJ, Nagrajan S. A study of tinea capitis in Libya (Benghazi). Sabouradia 1979;17:181-3. 19. Ridley CM.Tinea capitis in an elderly woman. Clin Exp Dermatol 1979;4:247-9. 20. Bronson DM, Desai DR, Barsky S, Foley SM. An epidemic of infection with Trichophyton tonsurans revealed in a 20-year survey of fungal infection in Chicago. J Am Acad Dermatol 1983;8:32230. 21. Ive FA.The carrier stage of tinea capitis in Nigeria. Br J Dermatol 1966;78:219-21. 22. Marchisio VF, Preve L, Tullio V. Fungi responsible for skin mycoses in Turin (Italy). Mycoses 1996;39:141-150. 23. Cuetara MS, del Palacio A, Pereiro M, Amor E, Alvarez C, Noriega AR. Prevalence of undetected tinea capitis in a school survey in Spain. Mycoses 1997;40:131-7. 24. Hebert AA, Head ES, MacDonald EM. Tinea capitis caused by Trichophyton tonsurans. Pediatr Dermatol 1985;2:219-23. 25. Soyinka F. Epidemiologic study of dermatophyte infections in Nigeria (clinical survey and laboratory investigations). Mycopathologia 1978;63:99-103. 26. Stratigos AJ, Stern R, Gonzalez E, Johnson RA, O’ Connell JO, Dover JS. Prevalence of skin disease in a cohort of shelter-based homeless men. J Am Acad Dermatol 1999;41:197-202. 27. Bargman H, Kane J, Baxter M-L, Summerbell RC. Tinea capitis due to Trichophyton rubrum in adult women. Mycoses 1995;38: 231-4. 28. Vannini P, Guadagni R, Palleschi GM, Difonzo EM, Panconesi E. Tinea capitis in the adult: two case studies. Mycopathologia 1986;96:53-7. 29. Honig PJ, Smith LR. Tinea capitis masquerading as atopic or seborrheic dermatitis. J Pediatr 1979;94:604-5. 30. Lateur N, Andre J, De Mabubeuge J, Poncin M, Song M. Tinea capitis in two black African adults with HIV infection. Br J Dermatol 1999;140:722-4. 31. Fuller LC, Child FC, Higgens EM. Tinea capitis in south-east London: an outbreak of Trichophyton tonsurans infection. Br J Dermatol 1997;136:132-48. 32. Vargo K, Cohen BA. Prevalence of undetected tinea capitis in household members of children with disease. Pediatrics 1993; 92:155-7. 33. Babel DE, Rogers AL, Beneke ES. Evaluation of the adult carrier state in juvenile tinea capitis caused by Trichophyton tonsurans. J Am Acad Dermatol 1989;21:1209-12. 34. Sharma V, Silverberg NB, Howard R,Tran CT, Laude TA, Frieden IJ. Do hair care practices affect the acquisition of tinea capitis? A case-control study. Arch Pediatr Adolesc Med 2001;155:818-21.