Epidemiologic surveillance of cutaneous fungal

infection in the United States from 1999 to 2002

K. Wade Foster, MD, PhD,a Mahmoud A. Ghannoum, PhD,b and
Boni E. Elewski, MDa
Birmingham, Alabama, and Cleveland, Ohio
Background: Cutaneous fungal infections are common in the United States, and causative organisms
include dermatophytes, yeasts, and nondermatophyte molds. These organisms are in constant competition
for their particular environmental niche, often resulting in the emergence of one or more predominant
pathogens and displacement of other less competitive species. Changes in the incidence of fungal
pathogens can be followed from laboratory culture results of infected cutaneous tissues over time. These
data can be used to ascertain past and present trends in incidence, predict increases in antifungal resistance
and the adequacy of our current pharmacologic repertoire, and provide insight into future developments.
Objective: This study identifies epidemiologic trends and the predominant organisms causing superficial
fungal infections in the United States.
Methods: A total of 15,381 specimens were collected from clinically suspected tinea corporis, tinea cruris,
tinea capitis, tinea faciei, tinea pedis, tinea manuum, and finger and toe onychomycosis from 1999 through
2002. Specimens were submitted to the Center for Medical Mycology in Cleveland, Ohio, for fungal culture
and identification, and the incidence of each species was calculated.
Results: Dermatophytes remain the most commonly isolated fungal organisms except from clinically
suspected finger onychomycosis, in which case Candida species comprise 70% of isolates. Trichophyton
rubrum remains the most prevalent fungal pathogen, and increased incidence of this species was observed
in finger and toe onychomycosis, tinea corporis and tinea cruris, tinea manuum, and tinea pedis. As the
causal agent of tinea capitis, T tonsurans continues to increase in incidence, achieving near exclusionary
proportions in the United States.
Conclusion: Consideration of the current epidemiologic trends in the incidence of cutaneous fungal pathogens
is of key importance to investigational efforts, diagnosis, and treatment. (J Am Acad Dermatol 2004;50:748-52.)

ycotic infection of the skin can be caused

by dermatophytes, yeasts, and nondermatophyte molds, although dermatophytes are the most frequently encountered causative agent. Together, these organisms account for a
high number of office visits and treatment-related
expenses.1 Superficial fungal infections comprise a

From the Department of Dermatology, University of Alabama at

Birmingham School of Medicine,a and University Center for
Medical Mycology, Cleveland.b
Funding sources: None.
Conflicts of interest: None identified.
Accepted for publication May 12, 2003.
Reprint requests: M. A. Ghannoum, PhD, University Center for
Medical Mycology, 11100 Euclid Ave, Cleveland, OH 44106-5028.
E-mail: [email protected].
Published online February 18, 2004.
2004 by the American Academy of Dermatology, Inc.
0190-9622/$30.00
doi:10.1016/S0190-9622(03)02117-0

748

complex host-parasite relationship that is in constant

flux. Species compete to exploit an environmental
niche within a host population, often resulting in the
emergence of one or more predominant pathogens
and displacement of organisms with less adaptive
qualities.2,3 Changes in the incidence of a pathogen
affect the physicians ability to render a diagnosis
and can change the approach to treatment.4 Multiple
factors may affect the incidence of fungal pathogens
within a population. These include the geographic
area and climate, immunocompetence of the host, the
pathogenicity of the infectious agent, and the availability of medical treatment. This study provides insight
into recent trends in the incidence of fungal species
isolated from skin infections in the United States.

METHODS
A total of 15,381 patient samples including nail
clippings, subungual debris, hair, and skin scrapings
were collected at the Center for Medical Mycology in

Foster, Ghannoum, and Elewski 749

J AM ACAD DERMATOL
VOLUME 50, NUMBER 5

Fig 1. Incidence of cutaneous fungal species from 1999 to 2002. Values represent the
incidence of the 5 most common species isolated from finger onychomycosis (A), toe onychomycosis (B), tinea capitis (C), tinea corporis and tinea cruris (D), tinea manuum (E), and tinea
pedis (F). Tabular presentation of complete data sets for each body site is available online at
www.eblue.org.

Cleveland, Ohio, from January 4, 1999, through September 4, 2002. Specimens were obtained from clinically suspected fungal infections of various body
sites including fingernail, toenail, body and groin,
head and scalp, face, hand, and foot by US podiatrists, dermatologists, and primary care physicians.
In all, 11 states were represented in the study: Alabama, California, Florida, Illinois, Michigan, Missouri, New York, Ohio, Pennsylvania, Tennessee,
and Texas. Specimens were submitted in a DermaPak (Microbiological Supply Co, Toddington, United
Kingdom) on Mycosel agar (BBL, Cockeysville, Md)
or on dermatophyte testing agar, as described.5 Primary isolation medium included Mycosel agar and
potato dextrose agar supplemented with chloramphenicol and gentamycin, as described.6 Cultures
were incubated at 30C for up to 28 days and
checked twice weekly for growth. Negative cultures
were confirmed after 4 weeks of no growth. Identi-

fication of dermatophyte isolates was on the basis of

microscopic morphology, urea testing, growth on
Trichophyton agars, and hair perforation assays.
Nondermatophyte molds were identified by microscopic morphology. Recovered yeasts were subjected to the germ tube test,6 analyzed using an
identification system (API 20C, bioMe rieux Inc,
Durham, NC),7 and checked for morphology in
cornmeal agar (BBL). All specimens were sent as
part of routine medical workup and analyses were
conducted retrospectively. The incidence of the 5
most common species from each body site is presented graphically (Fig 1). A more detailed analysis
is presented in a series of tables that can be accessed
online at www.eblue.org.

RESULTS
From fingernail debris, 674 isolates were obtained. The incidence of nondermatophyte molds

750 Foster, Ghannoum, and Elewski

decreased 5-fold from 1999 to 2002, yet the incidence of Candida species remained relatively constant, ranging from 70.3% to 75.8%. C albicans was
the predominant isolate, accounting for 47.9% to
54% of positive cultures (Fig 1, A). The incidence of
dermatophytes increased nearly 2-fold during the
study period, fueled by upward trends in the incidence of T rubrum. T rubrum was also the predominant dermatophyte, accounting for 90% of all fingernail-derived dermatophyte isolates in each of the
4 years analyzed.
From infected toenail debris, 3698 isolates were
obtained. The fungal isolates were diverse and included 29 species of nondermatophyte molds, 8
species of Candida, and 6 species of dermatophytes. As with finger onychomycosis, the incidence
of nondermatophyte molds decreased during the
study period, with a pronounced decline in the incidence of Fusarium species. In contrast to finger
onychomycosis, incidence of Candida species was
low, ranging from only 3.5% to 6.7%. Incidence of
dermatophytes ranged from 72.4% to 88.2% and
trended upward during the study period secondary
to increases in the incidence of T rubrum, the predominant dermatophyte (Fig 1, B). Analysis of combined (fingernail- and toenail-derived) data identified T rubrum as the predominant causative agent of
onychomycosis, with incidence ranging from 55.2%
in 1999 and increasing steadily to 72.8% in 2002.
Conversely, analysis of combined nail data showed
that Candida species accounted for a much smaller
fraction of onychomycosis, and a steady decline in
incidence from 18.9% in 1999 to 11.3% in 2002 was
observed.
From hair- and scalp-derived tissues, 775 isolates
were obtained. Nondermatophyte molds and Candida species were isolated in low abundance from
hair and scalp tissues, accounting for 5.4% and
1.6% of isolates, respectively. Dermatophytes
comprised the majority of isolates, with incidence
ranging from 94.6% to 99.7%. T tonsurans remains
the most commonly isolated pathogen, with incidence reaching 95.8% in 2002 (Fig 1, C). As with
tinea capitis, the predominant isolate from face-derived tissues was T tonsurans, with incidence ranging from 50% to 100% during the study period.
From body- and groin-derived tissues, 130 fungal
isolates were obtained. The incidence of nondermatophytes was low, ranging from 0% to 4%. The
incidence of Candida species was higher, but with
somewhat more erratic fluctuations from year to
year, ranging from 0% in 2001 to 23.5% in 2002.
Dermatophytes had the highest incidence throughout the study ranging from 76.5% to 96%. Although
several species of dermatophytes were isolated, the

J AM ACAD DERMATOL
MAY 2004

predominant pathogens were T rubrum and T tonsurans (Fig 1, D). The incidence of T rubrum increased during the study period, comprising 32% of
isolates in 1999 and increasing to 47% in 2002. Conversely, T tonsurans accounted for 30.1% and only
17.7% of isolates in 1999 and 2002, respectively.
A total of 40 isolates were obtained from the
hand. An abrupt decrease in the incidence of nondermatophyte molds from 21.4% in 1999 to 0%
thereafter was observed. The incidence of Candida
species was variable, ranging from 6.7% to 33.3%
during the study period. Dermatophyte incidence
trended upward, from 64.4% in 1999 to 80% in 2002,
secondary to increases in the incidence of T rubrum,
the most common isolate (Fig 1, E).
From foot-derived tissues, 189 fungal isolates
were obtained. Both nondermatophytes and Candida species had relatively low incidence, whereas
dermatophytes accounted for 86.2% to 100% of isolates. T rubrum was the most common isolate, and
the incidence of this species increased steadily during the study period (Fig 1, F).

DISCUSSION
Analysis of finger and toe onychomycosis in this
study showed an inverse relationship between T
rubrum and Candida species. In finger onychomycosis, Candida species have high incidence and T
rubrum has relatively low incidence. In toe onychomycosis, the opposite is true. The high incidence of
Candida species in finger onychomycosis has been
noted previously, albeit not to the degree present in
this study. Work conducted in The Netherlands confirmed analogous roles for T rubrum and Candida
species in onychomycosis, with C albicans accounting for 58.5% and 6.4% of finger and toe onychomycosis, respectively.8 Similarly, in the United Kingdom, T rubrum and Candida species accounted for
39% and 58% of fingernail- and 80% and 1% of
toenail-derived isolates, respectively.9 In Canada,
the organisms causing toe onychomycosis were
90.5% dermatophyte and 1.7% Candida species,
whereas the corresponding organisms causing finger onychomycosis were 70.8% and 29.2%, respectively.10 The incidence of Candida species in finger
onychomycosis in the current study ranged from
70.3% to 75.8%, somewhat higher than that noted by
other groups. Although these observations are intriguing, the data are difficult to interpret for a number of reasons, including the lack of clinical correlation and microscopic observation and the
possibility that the high incidence of Candida observed in this study represents only secondary infection.11 Furthermore, recent studies have demonstrated that Candida species, particularly C

J AM ACAD DERMATOL
VOLUME 50, NUMBER 5

parapsilosis and C albicans, are capable of hand

colonization without causing apparent disease.12
Further study of this phenomenon is required before
definitive conclusions may be drawn.
The incidence of organisms causing tinea capitis
varies according to region.2 Studies conducted in
The Netherlands identified multiple causative species including T rubrum and T mentagrophytes, but
T verrucosum, T schonleinii, T violaceum, and
Microsporum canis were most common, accounting
for 25.3%, 24%, 17.3%, and 14.4% of infections, respectively. T tonsurans was not isolated in this
study.8 In Germany, the predominant organism
causing tinea capitis is M canis, accounting for
54% of infections, and the incidence of T tonsurans was 4%.13 In contrast to Western Europe,
T tonsurans remains the predominant causative
agent in North America and currently accounts for
95% of tinea capitis in the United States. The observations reported here are in general agreement
with previous studies conducted in the United States
and Canada, showing that T tonsurans accounts for
88.1% and 76% of tinea capitis, respectively.3,5 In
addition to the recent increases in the incidence of
T tonsurans in tinea capitis in this country, studies in
Canada report a more rapidly increasing incidence
initially observed at only 9% in 1985 but climbing to
76% in 1996.3 The nearly exclusive role of T tonsurans in tinea capitis and its increasing incidence in
tinea faciei in this study highlight the success of this
organism as a pathogen.
Of isolates obtained from the groin and body,
T rubrum, T tonsurans, and Candida species accounted for 32% to 60%, 17.7% to 34.3%, and 24%
of isolates, respectively. Although these results are in
general agreement with previous Canadian and US
studies,3,5 the incidence gap between T rubrum and
T tonsurans has widened in the United States since
1999. Compared with previous studies conducted in
the United States where T rubrum and C albicans
accounted for 20.3% and 47.9% of isolates, respectively,5 we observed a decrease in the incidence of
C albicans and an increase in the incidence of
T rubrum, reaching 47% in 2002. These observations
taken together indicate an increasingly important
role for T rubrum in tinea corporis and tinea cruris.
T rubrum, continues to play a significant role in
tinea manuum and tinea pedis as well, accounting
for 80% and 82.9% of isolates, respectively, in 2002.
The incidence of T rubrum in tinea manuum and
tinea pedis continues to rise in the United States but
is still noticeably less than that observed in Canada,
where it has achieved near exclusionary proportions.3

Foster, Ghannoum, and Elewski 751

This work identifies both annual changes and

even broader trends in the incidence of cutaneous
fungal pathogens that span or even extend beyond
the length of this study. Monitoring the incidence of
these species enables the detection of emerging organisms and allows for assessment of the adequacy
of current pharmacologic regimens. Emerging species with increased resistance to mainstay antifungal
agents must prompt testing of novel therapeutic
drugs or drug combinations. Two types of resistance
are currently recognized. The first of these, termed
clinical resistance, denotes a lack of clinical response to an antifungal agent, likely secondary to
low circulating levels of drug, noncompliance with
therapeutic regimens, or immunosuppression. The
other type of antifungal resistance, in vitro resistance, is manifest in organisms with increased minimum inhibitory concentration values and is classified as either primary, denoting an innate resistance
to the pharmacologic agent, or secondary, indicating
an acquired resistance to a drug.14 Acquired resistance is becoming more common in individuals who
are immunosuppressed, lack the ability to effectively
clear infections, and in whom the selective pressures
of multiple antifungal agents are at work.14 Dermatophyte resistance to antifungal agents has been
previously demonstrated. Specifically, griseofulvinresistant T rubrum has been obtained from clinical
sources and induced in the laboratory setting after
mutagenesis.15,16 Moreover, increased minimum inhibitory concentration values for griseofulvin, ketoconazole, and itraconazole have been observed in
subsets of T rubrum and T interdigitale.17 As with
dermatophytes, triazole-resistant Candida species,
including C glabrata, C albicans, and C krusei,14,18
and nondermatophyte molds exhibiting single- or
multi-drug resistance are becoming increasingly
prevalent.19,20 These observations taken together
emphasize the growing problem of antifungal resistance, predict future increases in severity, and underscore the importance of continued epidemiologic
surveillance.
In conclusion, these data reiterate the continued
predominance of dermatophytes as the principal
pathogens in cutaneous fungal infections. T rubrum
remains the most prevalent pathogen, and increased
incidence of this organism was observed in finger
and toe onychomycosis, tinea corporis and tinea
cruris, tinea manuum, and tinea pedis. High incidence of Candida species was documented in finger
onychomycosis, but necessitates clinical correlation
and further study. As the causal agent of tinea capitis, T tonsurans continues its expansion to near
exclusionary proportions in the United States and
exhibits parallel increases in incidence in tinea fa-

752 Foster, Ghannoum, and Elewski

ciei. Diagnosis, treatment, and investigational efforts

should include consideration of these recent data.
We thank Nancy Isham and Debbie Yearick for their
efforts collecting the data and Judy Warner for her competent advice on fungal culture and identification.
REFERENCES
1. Smith ES, Fleischer AB, Feldman SR, Williford PM. Characteristics
of office-based physician visits for cutaneous fungal infections:
an analysis of 1990 to 1994 national ambulatory medical care
survey data. Cutis 2002;69:191-8, 201-2.
2. Gupta AK, Summerbell RC. Tinea capitis. Med Mycol 2000;38:
255-87.
3. Gupta AK, Summerbell RC. Increased incidence of Trichophyton
tonsurans tinea capitis in Ontario, Canada between 1985 and
1996. Med Mycol 1998;36:55-60.
4. Gupta AK, Einarson TR, Summerbell RC, Shear NH. An overview
of topical antifungal therapy in dermatomycoses: a North American perspective. Drugs 1998;55:645-74.
5. Kemna ME, Elewski BE. A US epidemiologic survey of superficial
fungal diseases. J Am Acad Dermatol 1996;35:539-42.
6. Ghannoum MA, Hajjeh RA, Scher R, Konnikov N, Gupta AK, Summerbell R, et al. A large-scale North American study of fungal
isolates from nails: the frequency of onychomycosis, fungal distribution, and antifungal susceptibility patterns. J Am Acad Dermatol 2000;43:641-8.
7. Salkin IF, Land GA, Hurd NJ, Goldson PR, McGinnis MR. Evaluation of YeastIdent and Uni-Yeast-Tek yeast identification systems. J Clin Microbiol 1987;25:624-7.
8. Korstanje MJ, Staats CC. Fungal infections in the Netherlands:
prevailing fungi and pattern of infection. Dermatology 1995;
190:39-42.
9. Clayton YM. Clinical and mycological diagnostic aspects of onychomycoses and dermatomycoses. Clin Exp Dermatol 1992;17
(Suppl 1):37-40.

J AM ACAD DERMATOL
MAY 2004

10. Gupta AK, Jain HC, Lynde CW, MacDonald P, Cooper EA, Summerbell RC. Prevalence and epidemiology of onychomycosis in
patients visiting physicians offices: a multicenter Canadian survey of 15,000 patients. J Am Acad Dermatol 2000;43:244-8.
11. Daniel CR III, Elewski BE. Candida as a nail pathogen in healthy
patients. J Miss State Med Assoc 1995;36:379-81.
12. Saiman L, Ludington E, Dawson JD, Patterson JE, Rangel-Frausto
S, Wiblin RT, et al. Risk factors for Candida species colonization of
neonatal intensive care unit patients. Pediatr Infect Dis J 2001;
20:1119-24.
13. Tietz HJ, Czaika V, Ulbricht HM, Sterry W. Tinea capitis in Germany: a survey in 1998. Mycoses 1999;42 (Suppl 2):73-6.
14. Fidel PL Jr, Vazquez JA, Sobel JD. Candida glabrata: review of
epidemiology, pathogenesis, and clinical disease with comparison to C albicans. Clin Microbiol Rev 1999;12:80-96.
15. Artis WM, Odle BM, Jones HE. Griseofulvin-resistant dermatophytosis correlates with in vitro resistance. Arch Dermatol 1981;
117:16-9.
16. Fachin AL, Maffei CM, Martinez-Rossi NM. In vitro susceptibility
of Trichophyton rubrum isolates to griseofulvin and tioconazole:
induction and isolation of a resistant mutant to both antimycotic drugs; mutant of Trichophyton rubrum resistant to griseofulvin and tioconazole. Mycopathologia 1996;135:141-3.
17. Goh CL, Tay YK, Ali KB, Koh MT, Seow CS. In vitro evaluation of
griseofulvin, ketoconazole, and itraconazole against various
dermatophytes in Singapore. Int J Dermatol 1994;33:733-7.
18. Rubin AI, Bagheri B, Scher RK. Six novel antimycotics. Am J Clin
Dermatol 2002;3:71-81.
19. Wolf DG, Falk R, Hacham M, Theelen B, Boekhout T, Scorzetti G,
et al. Multidrug-resistant Trichosporon asahii infection of nongranulocytopenic patients in three intensive care units. J Clin
Microbiol 2001;39:4420-5.
20. Denning DW, Venkateswarlu K, Oakley KL, Anderson MJ, Manning NJ, Stevens DA, et al. Itraconazole resistance in Aspergillus
fumigatus. Antimicrob Agents Chemother 1997;41:1364-8.

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