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Clinics in Dermatology (2010) 28, 197–201

Epidemiology of superficial fungal infections


Mahreen Ameen, MD
St. John's Institute of Dermatology, Guy's and St. Thomas' Hospitals NHS Trust, Westminster Bridge Rd, London SE1 7EH,
United Kingdom

Abstract Fungal infections of the skin, hair, and nails are common worldwide, and their incidence
continues to increase. The principal causative agents are dermatophytes, and their geographic
distribution is variable. This is reflected in the differing patterns of dermatophytoses seen in different
parts of the world. The epidemiology of dermatophyte infection has changed as a result of migration,
lifestyle, drug therapy, and socioeconomic conditions. This contribution discusses global patterns of
dermatophyte infection and the changing epidemiology of the causative agents.
© 2010 Elsevier Inc. All rights reserved.

Introduction variable, and there are some strong regional associations. For
example, M audouinii is the most prevalent pathogen in
Superficial mycoses are common worldwide. They are Africa overall; however, T violaceum infection is highly
believed to affect 20% to 25% of the world's population, and endemic in the horn of Africa as well as in North and South
the incidence continues to increase.1 They are predominantly Africa, and T soudanense infection in northwestern central
caused by dermatophytes, and the causative species vary with tropical Africa.7-9
geographic region. Some species are distributed worldwide, The epidemiology of dermatophyte infection is likely to
such as Trichophyton rubrum, T. mentagrophytes var. alter with changing patterns of migration, growth in tourism,
interdigitale, Microsporum canis, and Epidermophyton and changes in socioeconomic conditions. Dermatophytes
floccosum. Others have partial geographic restriction, such endemic to Asia and Africa, such as T soudanense,
as T schoenleinii (Eurasia, Africa), T soudanense (Africa), T violaceum, and M audouinii, have increased in frequency
T violaceum (Africa, Asia, and Europe), and T concentricum in Europe and North America as a result of migration.
(Pacific Islands, Far East, and India). Changes to the epidemiology of causative agents are also a
Most cases of tinea unguium, tinea cruris, tinea corporis, reflection of changing patterns of dermatophytosis. For
and tinea pedis are caused by T rubrum, which is the example, a century ago in Europe, tinea capitis was the
commonest dermatophyte in most developed countries2,3 as principal dermatophytosis, but tinea pedis became far more
well as in urban areas of some developing countries.4 common towards the late 20th century, and the incidence of
M canis is the predominant dermatophyte in Central and tinea capitis decreased.
Southern Europe as a result of the high rate of tinea capitis. In Few studies have investigated the etiology of superficial
Asia, T rubrum and T mentagrophytes are the most fungal infections in the developing world, and consequently,
commonly isolated dermatophytes, and as in Europe, this there is less knowledge of any changes to their epidemiol-
is as a result of the high prevalence of tinea pedis and tinea ogy. It is difficult to ascertain reliably the overall incidence
unguium.5,6 In Latin America, Africa, and the Middle East, and prevalence of the various skin diseases caused by
the pattern of dermatophyte infection is a much more superficial mycoses in different parts of the world because
studies of one region of the country may not be a true
representation of the overall disease pattern of that country;
E-mail address: mahreenameen@hotmail.com. furthermore, incidence and prevalence figures may only be

0738-081X/$ – see front matter © 2010 Elsevier Inc. All rights reserved.
doi:10.1016/j.clindermatol.2009.12.005
198 M. Ameen

representative of the population sampled, which may have America from Central America and the Caribbean in the
associated risk factors for infection. 1950s, and within a decade, it had established itself in urban
Knowledge of the predominant causative species provides regions.13 A survey from Chicago demonstrated its emer-
a clearer understanding of risk factors for superficial fungal gence from the mid-1950s.15 A similar pattern emerged in
infections and future epidemiologic trends. Improvements in Canada, and by the mid-90s, the incidence of T tonsurans in
living conditions have generally been associated with a urban regions had increased by more than eightfold within
decline in zoophilic dermatophyte and an increase in only a decade and was responsible for almost 80% of all
anthropophilic dermatophyte infections. The epidemiology cases of tinea capitis.16
of tinea capitis and tinea pedis (together with onychomy- In the rest of the Americas, the principal agents of tinea
cosis) has undergone the most radical changes and will capitis are M canis and T tonsurans. In the southern region
therefore be discussed in detail. Epidemiologic changes in of Brazil, M canis is responsible for 60% of cases.17 In the
the prevalence of tinea corporis, tinea cruris, tinea manuum, northeast, however, T tonsurans accounted for 74% of cases
and tinea faciei have been less extensively studied. Their and M canis for just a fraction of cases of tinea capitis.18 In
prevalence and the dermatophytes responsible for causing Mexico, M canis is the commonest agent, followed by
them may reflect local trends in tinea capitis and tinea pedis, T tonsurans.19 In Peru, M canis is the most common.20
which may be the source of infection. In Europe, M canis remains the commonest agent for
In Western Europe, T rubrum is the most frequently tinea capitis overall. Its incidence is increasing, and it is the
isolated dermatophyte in cases of tinea corporis and tinea dominant agent in southern Europe, with countries such as
cruris. T rubrum is also the most common cause of tinea Austria, Spain, Italy, and Greece reporting the highest
pedis and tinea unguium, which may act as a reservoir of numbers and proportions of M canis cases.21-23 Hungary,
infection predisposing to tinea corporis or cruris through Germany, and Poland also report high incidences of M canis
autoinoculation. Anthropophilic tinea capitis is often asso- tinea capitis.24-26 Its main reservoir of infection is cats.
ciated with tinea corporis, and T tonsurans may therefore There has been a significant increase in and shift toward
become an important agent of tinea corporis in the future. An anthropophilic tinea capitis cases, with marked increases in
example of the association between tinea capitis and tinea T tonsurans infection in several European cities. In
corporis has occurred in Libya, where T violaceum is Amsterdam, Madrid, Birmingham, and London, it has now
responsible for almost half of all cases of tinea corporis7 and already established itself or is an emerging dominant agent
is probably a reflection of the high prevalence of T violaceum for tinea capitis.27-30 In Birmingham, T tonsurans repre-
tinea capitis in the population.10 sented 36%, 56%, and 72% of all cases of tinea capitis in
1991, 1992, and 1993, respectively.28 By 2002 in London,
more than 60% of tinea capitis cases were due to
Tinea capitis T tonsurans,30 and a more recent United Kingdom study
collating the reports from several centers demonstrated that
Tinea capitis is the dermatophytosis whose epidemiology T tonsurans comprised 83% of cases of tinea capitis.2
has perhaps changed the most significantly, especially in Increasing numbers of previously nonendemic dermato-
Western countries. In many parts of the world, tinea capitis is phytes have been detected in African immigrants, such as
the most common superficial mycosis in children of school T soudanense in Austria and the United Kingdom, and
age. After the advent of oral griseofulvin in the late 1950s T violaceum in Greece and Italy.2,12,23,31 In France, in
and improvements in surveillance, there was a marked particular in Paris, the main anthropophilic dermatophytes
decline in its incidence in developed countries.11 In recent are those that originate from Africa, such as T soudanense
decades, however, its incidence has dramatically increased, and M audouinii,32 although there have been epidemics of
and significant changes have occurred in the dermatophytes T tonsurans infection. In the Netherlands, Sweden, and
responsible for infection. In the late 19th and early 20th Belgium, there have been increases in M canis tinea capitis,
centuries, M audouinii, followed by M canis, was the main but there are also increases of anthropophilic tinea capitis
causative agent in Western and Mediterranean Europe, caused by T violaceum, T soudanense, and T tonsurans,
whereas T schoenleinii was the predominant agent in Eastern which is a reflection of immigration patterns, particularly
Europe.12 Anthropophilic dermatophytes, in particular from East Africa.29,33,34
T tonsurans, have now emerged as the dominant agents in The most common species responsible for tinea capitis in
many regions. T tonsurans has worldwide distribution and Australia and New Zealand are M canis and T tonsurans.
causes principally tinea capitis, but it may also cause tinea M canis was previously the dominant agent, but the incidence
corporis and tinea unguium. of T tonsurans infection has steadily increased.35 In addition
In the United States of America, T tonsurans is now since the early 1990s, T soudanense, T violaceum, and
responsible for up to 50% of all dermatophyte infections and M audouinii tinea capitis have been increasingly reported
90% of cases of tinea capitis, replacing Microsporum spp as in children who have immigrated from East Africa, in
the principal agent of tinea capitis.13,14 T tonsurans is particular, with evidence for transmission of these agents to
believed to have entered the southwestern United States of local populations.36,37
Epidemiology of superficial fungal infections 199

The incidence of tinea capitis in Asia has decreased in oils, which may adhere to and retain spores, may also
recent decades as a result of improved sanitary and increase the risk of spread.51 Some authors have concluded
socioeconomic conditions. Anthropophilic dermatophytes that the mechanism of spread and reasons for the emergence
are the predominant agent of tinea capitis in India: In the of T tonsurans tinea capitis are still unclear and remain
North, T violaceum and M audouinii are the dominant speculative.12 In addition, T tonsurans can exist as an
agents, followed by T schoenleinii and T tonsurans,38 and in asymptomatic carrier state in children, acting as a reservoir of
the South, T violaceum is the principal infective agent.39 In infection, which may explain its rapid increase in prevalence
Eastern Nepal, where tinea capitis accounts for only 4.6% of in several populations.51
all dermatophyte infections, T violaceum is responsible for
49%.40 In the rural regions of Western China, T violaceum
and T schoenleinii are the commonest species,41 whereas in Tinea pedis and onychomycosis
developed cities, such as Shanghai, the predominant species
are M canis, followed by T violaceum and T tonsurans.42 Tinea pedis and onychomycosis are becoming more
T violaceum, T soudanense, and to a lesser extent, common as a result of changes in lifestyle, including
M audouinii and M langeronii, are the main dermatophytes increased urbanization, the use of communal bathing
responsible for tinea capitis in sub-Saharan Africa. In facilities, and occlusive footwear. The increasing incidence
general, T violaceum is the principal agent in North and of diabetes and HIV infection are also important contribu-
East Africa, and T soudanense in Central Africa; however, tory factors.52 Certain occupations (miners, soldiers) and
there are exceptions, and the pattern is likely to be far more recreational activities (marathon runners) place participants
variable. In South Africa, T violaceum is the commonest at a higher risk of tinea pedis.53-55 In Europe, there has been
cause of tinea capitis in the province of KwaZulu Natal and a dramatic increase in the incidence of both tinea pedis and
was isolated in 90% of cases.8 In neighboring Mozambique, onychomycosis since the end of World War II, which has
however, where the prevalence of tinea capitis is 12%, been attributed to the return of soldiers from the Far East.56
M audouinii was isolated in 88% of cases.43 In Ethiopia, The prevalence of tinea pedis and onychomycosis is now
where up to 60% of children are affected by tinea capitis, more than 50% in Northern and Central Europe and
T violaceum is the dominant agent.9 In central Nigeria, approximately 25% in the Mediterranean.57 Tinea pedis is
T soudanense is the dominant dermatophyte responsible for much more common than onychomycosis. Some studies
one-third of cases.44 In the Ivory Coast, T soudanense and suggest that the population prevalence of onychomycosis in
M langeronii were the most prevalent etiologic agents, in Western societies ranges from 2% to 8%58,59; however,
63.6% and 31.3% of cases respectively. In Guinea, another there appear to be large variations in prevalence, with
West African country where T soudanense and M audouinii reports of 4.1% in Denmark,60 8.0% in Canada,61 and
had been the principal agents several decades ago, 12.4% in Germany.62
T violaceum is now responsible for 57% of cases.45 Onychomycosis is caused by dermatophytes, nonderma-
In the Middle East, T violaceum is responsible for most tophyte molds, and yeasts. Dermatophytes are the main
cases of tinea capitis, accounting for 83% of cases in the causative agent in temperate climates, and Candida and
West Bank of Israel and for 39% in Iraq.46,47 In Libya, nondermatophyte molds in tropical regions. 1 Overall,
T violaceum it is responsible for 64% of cases and M canis is dermatophytes are most commonly implicated, accounting
responsible for 25%. 10 In Saudi Arabia, where the for 90% of toenail infections and 50% of fingernail
prevalence of tinea capitis is 22%, the principal causative infections, and T rubrum is responsible for most cases
agent is M canis.48 In Kuwait, M canis is the predominant worldwide.52 The predominant dermatophytes causing tinea
dermatophyte isolated in 62.5% of cases, followed by pedis are T rubrum, followed by T mentagrophytes var
T violaceum in 19.3% and T tonsurans in 13.1%.49 interdigitale and E floccosum. In 2005, these dermatophytes
Several studies have demonstrated that T tonsurans comprised 90% of isolations in the United Kingdom.2
infection has had a significant effect on the changing T rubrum accounts for 66% of all isolated strains in Finland
epidemiology of tinea capitis globally. It appears to have a for 80% to 90% in Germany.57,63 As a consequence of the
predilection for Afro- American and Afro-Caribbean chil- marked increased prevalence of tinea pedis and onychomy-
dren in both North America and Europe.30,50 A study in cosis, T rubrum is now the principal dermatophyte in many
London demonstrated that 91% of T tonsurans tinea capitis European countries.
occurred in Afro-Caribbean children.30 In Amsterdam, In the United States of America, T rubrum is the second
too, children from the Afro-Caribbean community were most common dermatophyte after T tonsurans. Tinea pedis
primarily affected.29 and tinea unguium are also common in the rest of the
The emergence of T tonsurans infection in developed Americas, comprising 30% and 25%, respectively, of all
countries has been attributed to low socioeconomic status, superficial dermatophytoses in Mexico, for example.64 In
crowded living conditions, and the sharing of combs.30 The Australia and Asia too, increased incidences of tinea pedis
practice of tight braiding, which may expose the stratum and onychomycosis have resulted in prevalences of tinea
corneum of scalp skin to fungal spores, and the application of pedis that are comparable to that of Europe, and similarly,
200 M. Ameen

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