Professional Documents
Culture Documents
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0095-1137/07/$08.00+0 doi:10.1128/JCM.02033-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.
Tinea capitis is of public health importance because of its transmissibility. Trichophyton violaceum and
Trichophyton soudanense, which are common causes of tinea capitis in parts of Africa and West Asia, have only
rarely been reported to cause dermatophytoses in the United States. We identifted 24 patients with 25 positive
cultures for T. violaceum or T. soudanense that were processed in a single hospital laboratory in Baltimore,
Dermatophytoses are infections of skin, hair, and nails result in significantly better outcomes (6). Griseofulvin doses
caused by species of the fungal genera Trichophyton, Micros- of up to 20 mg/kg/day for 8 weeks are currently utilized in
porum, and Epidermophyton. These infections are of public clinical practice (3, 14).
health importance because of their transmissibility from hu- The epidemiology of tinea capitis in the United States has
man to human or from animal to human. Tinea capitis in changed dramatically over the past century, possibly due in
particular remains a prevalent public health problem among part to the introduction of griseofulvin and the spread of der-
school-aged children in the United States; a recent study dem- matophyte species from South America to the United States.
onstrated that 13% of elementary school children in Cleveland, The predominant species causing tinea capitis in the United
Ohio, had positive scalp cultures for dermatophytic fungi (8). States during the first half of the 20th century was the an-
Sixty percent of these children were asymptomatic carriers (8). thropophilic species Microsporum audouinii (3). By the 1970s
Others have shown that the incidence of tinea capitis is in- to 1980s Trichophyton tonsurans, another anthropophilic der-
creasing. Lobato and colleagues found that the incidence rate matophyte, had become the most common cause of tinea cap-
in California for oral griseofulvin suspension prescriptions, a itis (21), and it now causes more than 95% of these infections
surrogate for tinea capitis, increased 84.2% from 1984 through in the United States (7). By contrast, species such as Tricho-
1993 (21). The increase in prescriptions among African-Amer- phyton violaceum and Trichophyton soudanense, which are com-
ican children during this time period was 209.7% (21). mon causes of tinea capitis in parts of Africa and West Asia (5,
Despite the availability of newer antifungal drugs, treatment 15, 24, 25, 35), have rarely been isolated from patients in the
of tinea capitis remains a challenge. Systemic antifungal ther- United States. Among 14,696 dermatophytes isolated from
apy is necessary to eradicate the disease, and currently only a patients at 54 locations throughout the United States from
single agent, griseofulvin, is approved by the U.S. Food and 1985 through 1987, only 12 were identified as T. violaceum and
Drug Administration. Although griseofulvin therapy is usually only 2 were identified as T. soudanense (31).
well tolerated, the drug may cause gastrointestinal side effects The present study was triggered by the identification of a
and must be administered for a period of several weeks, mak- cluster of T. violaceum and T. soudanense isolates recovered
ing successful treatment of young children potentially difficult. from multiple patients during the spring and early summer of
Researchers have also reported concerns about the emergence 2005 in the Mycology Laboratory of The Johns Hopkins Hos-
of clinical tolerance to griseofulvin. In a recent trial, initial pital (JHH) in Baltimore, Maryland. The goals of this retro-
rates of response to griseofulvin therapy at the recommended spective study were (i) to identify patients with positive cul-
dose of 11 mg/kg/day were only 52.2% at the end of 6 weeks of tures for these species from 2000 through June 2006, (ii) to
therapy and 57.0% at the end of 10 weeks of therapy (6). present pertinent mycological findings, and (iii) to describe the
Fluconazole at 6 mg/kg/day administered for 6 weeks did not epidemiology and characterize the clinical features of infec-
tions due to these organisms.
461
462 MAGILL ET AL. J. CLIN. MICROBIOL.
TABLE 1. Dermatophytes isolated by the JHH Mycology Laboratory, January 2000 through June 2006
No. of dermatophytes isolated in:
Species Total no. of
2006 dermatophytes isolated
2000 2001 2002 2003 2004 2005
(first 6 mo)
Trichophyton spp.
T. tonsurans 192 213 236 346 344 328 180 1,839
T. rubrum 23 19 39 78 80 64 35 338
T. mentagrophytes 0 2 8 12 9 12 4 47
T. violaceum 1 0 0 3 3 7 2 16
T. soudanense 0 0 0 0 2 0 7 9
Trichophyton sp., NOSa 0 1 1 5 2 8 5 22
Microsporum spp.
M. canis 3 3 9 5 7 10 3 40
M. gypseum 0 0 2 1 1 0 0 4
Microsporum sp., NOS 0 0 0 0 2 0 0 2
Dermatophyte, NOS 0 0 2 2 5 0 1 10
positive for dermatophytes from 1 January 2000 through 30 June 2006. The organisms accounted for 1.5% of all dermatophytes. This dif-
database search included fungal cultures of skin, hair, and nail specimens col-
ference was statistically significant (P = 0.001; Fisher’s exact
lected from inpatient and outpatient locations. We excluded cultures performed
as part of the College of American Pathologists Survey and cultures from un- test). By the first half of 2006, T. violaceum and T. soudanense
identified locations. accounted for almost 4% of all dermatophytes, and T. soudane-
The JHH Institutional Review Board approved the study. Because some of the nse was the second most common dermatophyte isolated from
positive cultures for T. violaceum and T. soudanense came from a non-JHH- scalp and hair specimens (following T. tonsurans).
affiliated community clinic that submitted its specimens to JHH for processing,
we also sought and received approval from the clinic’s Council on Clinical
Seventy-two percent (18/25) of T. violaceum and T. soudane-
Operations for participation of the clinic in this study. Available medical records nse isolates were cultured from scalp or hair specimens, and
were reviewed for patients with positive cultures for T. violaceum or T. soudanense the remainder were cultured from skin specimens (6/25; 24%)
during the study period. The data collected included age, sex, race, country of or nail specimens (1/25; 4%). The median number of days of
origin, duration of U.S. residence at the time of positive culture, diagnosis, incubation until growth was noted in culture was 11 (range, 5
treatment, and outcome. Data were entered manually onto case report forms and
then entered into a Microsoft Access 2000 database. Descriptive statistics were
to 21). Although the numbers are small, T. violaceum took
calculated. approximately twice as long to grow in culture (median, 13.5
Specimen processing and organism identiftcation. Dermatophytic fungi recov- days; range, 5 to 21 days) as T. soudanense (median, 7 days;
ered from clinical specimens at JHH were identified to the species level. Myco- range, 6 to 21 days) (P = 0.03; Wilcoxon rank sum test).
logical studies used to identify dermatophytes, including T. violaceum and T.
soudanense, were colony morphology, microscopic morphology, resistance to
Mycological characteristics of T. violaceum and T. soudane-
cycloheximide, urease activity, and, when necessary, growth on media with and nse. T. violaceum isolates were slow-growing, with waxy, gla-
without thiamine. Patient isolates were compared to published descriptions of brous, wrinkled colonies. Colonies were a distinctive, deep,
these organisms (29). purple-red and sometimes had a white, waxy fringe. Over time,
some cultures became fluffy and lost their characteristic colony
morphology. Colony morphology and microscopic characteris-
RESULTS
tics of T. violaceum (for example, lack of sporulation) may
Dermatophytes isolated by the JHH Mycology Laboratory, overlap with those of Trichophyton rubrum.
January 2000 to June 2006. Between 1 January 2000 and 30 T. soudanense isolates were also slow-growing. Colonies
June 2006, the electronic database search yielded 7,804 skin, were flat, with a suede-like texture, a spidery edge, and a
hair, and nail specimens that were submitted to the JHH My- distinctive yellow or orange-yellow color. Over time, the colo-
cology Laboratory for fungal culture. Of these, 2,334 (29.9%) nies became folded and pleomorphic. Microscopically, no
were positive for dermatophytes. Total numbers of dermato- conidia were seen. Reflexive branching, in which the hypha
phytes isolated by the JHH Mycology Laboratory between 1 bends back toward the inoculum site, was seen. This species
January 2000 and 30 June 2006 are presented in Table 1. may overlap with Microsporum ferrugineum. Colony color on
Throughout the study period, the most commonly cultured mycobacterial Lowenstein-Jensen medium may allow for dif-
dermatophyte was T. tonsurans. During the period from 2000 ferentiation of the two species; T. soudanense has brownish-
to 2002, T. violaceum and T. soudanense accounted for 0.13% black colonies, whereas M. ferrugineum produces yellow colo-
of all dermatophytes isolated by the laboratory, whereas during nies. Characteristic features of T. violaceum and T. soudanense
the period from 2003 through the first half of 2006, these two are presented in standard mycology textbooks (19, 21, 27).
VOL. 45, 2007 TRICHOPHYTON SPP. IN BALTIMORE, MD 463
TABLE 2. Clinical features, treatment, and outcome of T. violaceum and T. soudanense infections
Oral antifungal Topical antifungal Treatment
Subject Diagnosis Organism Oral antifungal dose Outcome
treatment treatment duration
not yet completed therapy and three were lost to follow-up. All was sending its specimens to JHH during the entire duration of
subjects with tinea capitis were 12 years of age or younger. the study period (B. Filburn, personal communication). We
Four patients had tinea corporis (two children and two adults), believe that increased immigration to the Baltimore area from
and one adult patient had onychomycosis. Among the 19 pa- regions where T. violaceum and T. soudanense are endemic
tients for whom a clinical diagnosis was available, 3/15 patients may be a more likely explanation for the observed increase in
infected with T. violaceum (20%) had a dermatophytosis other isolation of these species. Although publicly accessible immi-
than tinea capitis (2 patients with tinea corporis involving the gration data specific to the Baltimore metropolitan area are
face and 1 patient with onychomycosis), and 2/4 patients in- limited, data from the U.S. Census Bureau indicate that the
fected with T. soudanense (50%) had tinea corporis involving number of individuals born in Africa who entered the United
the extremities and/or the trunk. Of note, the only patient States and established residence in Baltimore City has in-
noted to have relapsed in this series was a child with tinea creased over the past few decades (33). For example, 534
capitis due to T. violaceum who initially received a low dose of African-born individuals entered the United States prior to
griseofulvin and developed recurrent disease 1.5 years later. 1980 and established residence in Baltimore City, compared to
Although the source of the dermatophyte infection was un- 828 African-born individuals entering the United States be-
known for most patients, two of the adult patients were re- tween 1980 and 1989 and 2,329 African-born individuals en-
these regions and have characteristic clinical findings. Since 10. Gupta, A. K., P. Adam, N. Dlova, C. Lynde, S. Hofstader, N. Morar, J.
Abookar, and R. C. Summerbell. 2001. Therapeutic options for the treat-
these species are rarely seen in the United States and usually ment of tinea capitis caused by Trichophyton species: griseofulvin versus the
fail to produce micro- or macroconidia, definitive identification new oral antifungal agents, terbinafine, itraconazole and fluconazole. Ped.
may in some cases require molecular methods (20). Molecular Dermatol. 18:433–438.
11. Gupta, A. K., N. Dlova, P. Taborda, N. Morar, V. Taborda, C. W. Lynde, N.
taxonomy studies also suggest that T. soudanense (as well as Konnikov, M. Borges, N. Raboobee, R. C. Summerbell, P. Adam, S. L. R.
other infrequently encountered species, such as T. gourvilii and Hofstader, and J. Abookar. 2000. Once weekly fluconazole is effective in
T. yaoundei) is conspecific with T. violaceum, although their children for the treatment of tinea capitis: a prospective, multicentre study.
Br. J. Dermatol. 142:965–968.
phenetics differ (9). A more recent study using a microsatellite 12. Hällgren, J., B. Petrini, and C.-F. Wahlgren. 2004. Increasing tinea capitis
marker has suggested that T. soudanense is actually more prevalence in Stockholm reflects immigration. Med. Mycol. 42:505–509.
closely related to T. rubrum than to T. violaceum (26). These 13. Heikkilä, H., and S. Stubb. 2004. Ringworm of the scalp among immigrants
in Finland. Acta Derm. Venereol. 84:333–334.
evolutionary relationships are interesting and require further 14. Huang, D. B., L. Ostrosky-Zeichner, J. J. Wu, K. R. Pang, and S. K. Tyring.
study, probably necessitating sequencing of multiple regions. 2004. Therapy of common superficial fungal infections. Dermatol. Ther.
17:517–522.
Our findings provide evidence for the ongoing evolution of 15. Jahangir, M., I. Hussain, K. Khurshid, and T. S. Haroon. 1999. A clinico-
dermatophytosis epidemiology related to international travel etiologic correlation in tinea capitis. Int. J. Dermatol. 38:275–278.
and shifts in population demographics, although our study is 16. Jha, B. N., V. K. Garg, S. Agrawal, B. Khanal, and A. Agarwalla. 2006. Tinea
461
468 MAGILL ET AL. J. CLIN. MICROBIOL.
HASIL
Dermatofit terisolasi oleh laboratorium Mikologi
JHH, Januari 2000 untuk Juni 2006. Antara 1 Januari 2000
dan 30 Juni 2006, pencarian database elektronik menghasilkan 7,804
kulit, rambut, dan kuku spesimen yang diserahkan ke cology JHH
My-laboratorium budaya jamur. Ini, 2,334 (29,9%) yang positif
untuk dermatofit. Jumlah total dermato-phytes terisolasi oleh
laboratorium Mikologi JHH antara 1 Januari 2000 dan 30 Juni 2006
disajikan dalam tabel 1. Sepanjang masa studi, dermatofit umumnya
berbudaya adalah T. tonsurans. Selama periode 2000-2002, T.
violaceum dan T. soudanense menyumbang 0.13% dari semua
dermatofit terisolasi oleh laboratorium, sedangkan selama periode
dari 2003 melalui pertama setengah dari 2006, ini dua
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