Review article

Epidemiological trends in skin mycoses worldwide

1 2 1
Blanka Havlickova, Viktor A. Czaika and Markus Friedrich
1
Global Clinical Development, Intendis GmbH, Berlin, Germany and 2Dermatology Out-patient Department, Department of Internal Medicine, Helios
Clinic Bad Saarow, Bad Saarow, Germany

Summary Fungal infections of the skin and nails are a common global problem. The high
prevalence of superficial mycotic infections shows that 20–25% of the world s
population has skin mycoses, making these one of the most frequent forms of
infection. Pathogens responsible for skin mycoses are primarily anthropophilic and
zoophilic dermatophytes from the genera Trichophyton (T.), Microsporum (M.) and
Epidermophyton (E.). There appears to be considerable inter- and intra-continental
variability in the global incidence of these fungal infections. Trichophyton rubrum,
T. interdigitale (mentagrophytes var. interdigitale), M. canis, M. audouinii, T. tonsurans and
T. verrucosum are the most common, but the attack rates and incidence of specific
mycoses can vary widely. Local socio-economic conditions and cultural practices can
also influence the prevalence of a particular infection in a given area. For example,
tinea pedis (athlete s foot) is more prevalent in developed countries than in emerging
economies and is likely to be caused by the anthropophilic germ T. rubrum. In poorer
countries, scalp infections (tinea capitis) caused by T. soudanense or M. audouinii are
more prevalent. This review summarises current epidemiological trends for fungal
infections and focuses on dermatomycosis of glabrous skin on different continents.

Key words: Skin mycoses, epidemiology, tinea, Trichophyton, Candida.

Introduction superficial fungal infections are relatively common in

tropical countries and are exacerbated by the wearing of
Fungal infections of the skin and nails form the most occlusive clothing. In addition, the frequency of derma-
numerous and widespread group of all mycoses. The tomycoses is greater in communities with low socioeco-
prevalence of superficial mycotic infections has risen to nomic status: crowded living conditions provide multiple
such a level in the last decades that skin mycoses now opportunities for skin-to-skin contact and close proximity
affect more than 20–25% of the world s population, to animals, while hygiene may be suboptimal. Moreover,
making them one of the most frequent forms of superficial skin infections show a low ten-dency to self
1
infections. The distribution of the dermatomycoses, their limitation, and absence of, or poor medical care further
aetiological agents and the predominating ana-tomical increases the epidemic spread of skin mycoses.
infection patterns vary with geographical loca-tion and a
1,2
wide range of environmental and cultural factors. Despite regional characteristics and predispositions for
Dermatophytes thrive at surface temperatures of 25–28 dermatophyte infections, the spectrum of dermato-phytes
LC and infection of human skin is supported by warm and is not static. Booming mass tourism, interna-tional sports
humid conditions. For these reasons, activities and increasing migration mean that less common
or forgotten species are being imported and disseminated.

Correspondence: Blanka Havlickova, Intendis GmbH, Max-Dohrn Straße 10,

Berlin, Germany.
This review attempts to summarise current epide-
E-mail: [email protected] miological trends for fungal infections. Its main focus is
on dermatomycosis of glabrous skin in different
Accepted for publication 8 July 2008 continents.

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2 Journal compilation 2008 Blackwell Publishing Ltd • Mycoses, 51 (Suppl. 4), 2–15
 Superficial dermatomycoses worldwide

Causative agents Table 1 Dominant species of dermatophytes according to clinical

localisation
Superficial fungi can be classified according to their usual
Condition Dominant species
habitat into anthropophilic, zoophilic and geo-philic
organisms. Tinea capitis (scalp) Trichophyton violaceum
T. tonsurans
Generally, anthropophilic fungi cause superficial der-
T. soudanense
matomycoses characterised by relatively low inflamma- Microsporum canis
tory activity because of an immunological arrangement M. audouinii
1,2
that exists between the fungus and its human host. Tinea pedis (feet) T. rubrum
Household dust may act as a reservoir of antropophilic T. mentagrophytes (var. interdigitale)
dermatophytes, preserving dermatophyte spores for years. Epidermophyton floccosum
Tinea cruris (groin) T. rubrum
T. mentagrophytes
Zoophilic germs are found in animals, but are also (var. interdigit et granulosum)
sporadically transmitted to humans by cats, dogs Tinea corporis T. rubrum
(Microsporum canis), guinea pigs and rabbits (Tricho- (arms, legs and trunk) M. canis
phyton mentagrophytes var. granulosum). T. tonsurans
Tinea unguium T. rubrum
Zoophilic germs can be referred to as cuddly toy
(finger-nails and toe-nails) T. mentagrophytes (var. interdigitale)
mycoses (because of the mode of infection in children and
adolescents) and have a high affinity to the hairy head of a
child. They are associated with highly inflammatory and
potentially highly contagious skin infections. Candida species are part of the transient or commensal
flora in specific regions of the body. They are opportu-
Geophilic fungi grow in the soil and only sporadically nistic pathogens that only become pathogenic to humans
2
infect humans. When they do, the result varies from high under particular systemic and local conditions.
to low inflammation. Strains of Microsporum gypseum, Candidiasis is predominantly a disease of the very old, the
the most common geophilic pathogen, cul-tured from very young and the very sick . In most cases, it is an
humans are more virulent than those from the soil, endogenous infection originating from the patient s own
accounting for occasional epidemic spread under flora and generally follows a shift in the existing host ⁄
appropriate conditions.
3 yeast relationship. Occasionally, a strain can spread
7
There are approximately 100 000 species of fungi between individuals or in hospitals.
distributed worldwide. The majority of fungal infections Tinea can be caused by obligatory pathogenic
seen in both temperate and tropical countries are dermatophytes such as M. canis or T. verrucosum. Non-
superficial infections of the skin. The most common dermatophytic moulds, such as Scopulariopsis brevicaulis
pathogens relevant in practice are dermatophytes, yeasts or Aspergillus species, can theoretically cause nail
and moulds. infections, albeit rarely.
There are approximately 40 different species of
dermatophytes, characterised by their capability to digest Clinical manifestations
keratin and divided among three genera: Trich-ophyton,
Microsporum and Epidermophyton. A majority of Most basic fungal skin infections are caused by derma-
superficial fungal infections of the skin are caused by five tophytes and the main clinical manifestations are detailed
or six species of dermatophyte, of which Trichophy-ton below.
4
rubrum is the most common.
The predominant species of dermatophytes vary Tinea pedis (athlete s foot)
according to their clinical localisation, as described in the
Clinical manifestations and global patterns of superficial This is a very common infection that occurs in one in five
fungal infections sections and listed in Table 1. The
5 adults and the incidence increases with age from
1
management of tinea of the glabrous skin, caused by adolescence. It occurs more frequently in people who
2
dermatophyte infections, is a common therapeutic wear occlusive shoes.
6
problem for dermatologists. However, unlike pathogenic It may be associated with several different fungi,
yeasts and non-dermatophytic moulds, these infections including yeasts, the most common being T. rubrum and T.
never disseminate systemically and therefore can never be interdigitale (formerly T. mentagrophytes var. interdig-
lethal. itale). During the past 30 years, the incidence of tinea

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Journal compilation 2008 Blackwell Publishing Ltd • Mycoses, 51 (Suppl. 4), 2–15 3
B. Havlickova et al.

pedis has increased in the developed world and its Dermatophyte infection affecting nearly the entire
8
prevalence is around 10%. integument is named tinea corporis generalisata. A
One hand two feet syndrome is characterised by generalised dermatophytosis caused by T. rubrum can
dermatophyte infection of both feet and one hand and can occur as a result of mis-diagnosis or mis-treatment.
be found in patients with lower immunocompe-tence, such Misread tinea corporis generalisata caused by T. rubrum is
as diabetics. The condition is frequently associated with T. named tinea incognita .
rubrum.

Tinea cruris (ringworm of the groin)

Tinea unguium (onychomycosis, nail infections)
This presents as an itchy, red rash in the groin and
The causative agents of onychomycosis include derma- surrounding area and is commonly seen in young men
tophytes, Candida spp and non-dermatophytic moulds. 2
living in a warm climate. Tinea pedis can co-exist if the
Dermatophytes are most commonly responsible for infection is spread by scratching the feet and then the
onychomycosis in temperate western countries, whereas groin. Axillary infection can be seen as an analogous tinea
Candida and non-dermatophytic moulds are more pattern in woman. The most common agents are E.
frequently involved in countries with a hot and humid floccosum, T. mentagrophytes and T. rubrum.
9
climate.
Trichophyton rubrum is the most common dermato-
Tinea capitis (ringworm of the scalp)
phyte associated with onychomycosis, others include
T. interdigitale, Epidermophyton floccosum, T. violaceum, This is a dermatophyte infection of the scalp and hair and
M. gypseum, T. tonsurans, T. soudanense (considered by 2
tends to affect young children worldwide. Presen-tation
some to be an African variant of T. rubrum rather than a
depends on the aetiology and can be non-inflammatory,
full-fledged separate species) and the cattle ringworm inflammatory or black dot type. The non-inflammatory
2
fungus, T. verrucosum. Note that T. interdigitale is still form is most commonly caused by M. audouinii or M.
sometimes referred to as T. mentagrophytes var. interdig- ferrugineum and usually begins as a small erythematous
itale. The latter should be used to describe the zoophilic papule surrounding a single hair shaft, which spreads
form of the dermatophyte, and T. interdigitale used to centrifugally to other hairs. Scaling occurs and the hair
describe its anthropophilic form. Recent genetic research turns grey. The inflamma-tory type is usually associated
has shown that T. mentagrophytes var. granulosum is the with zoophilic or geophilic germs such as M. canis and M.
10
same as T. interdigitale. gypseum respectively. Black dot tinea capitis is caused by
2 T. tonsurans or T. violaceum. T. verrucosum is highly
Other causative agents include Candida spp. and non-
dermatophytic moulds, in particular members of the contagious and virulent and is the only dermatophyte able
genera Scytalidium (now Neoscytalidium), Scopulari- to thrive at 37 LC. Tinea capitis caused by T. verrucosum
opsis and Aspergillus. Scytalidium mainly affects people can result in irreversible scarring and alopecia. The
in the tropics, although it can persist if they move to more analogous clinical infection pattern in adults is sycosis
temperate areas. barbae, which corresponds to ring-worm in cattle. It is
Candida mainly causes proximal nail infections in widespread and a well-known occupational disease of
people whose hands are often submerged in water. Nail 2
cattle keepers.
infection caused by Candida subspecies – such as C.
albicans, C. parapsilosis and C. guilliermondii – is almost
always associated with paronychia. As a rule, C.
Candidiasis
parapsilosis appears concomitantly with T. interdigitale (T.
mentagrophytes var. granulosum) in nail infections. This is a diverse group of infections caused by members of
1
the genus Candida, especially C. albicans. These
Tinea corporis (ringworm on the trunk) organisms typically infect the skin, nails, mucous
membranes and gastrointestinal tract. Cutaneous and
This affects the trunk, often in exposed areas like the mucosal manifestations of candidiasis can be divided into
abdomen or limbs, causing red patches. It is more several distinct clinical syndromes (Table 2). Thirty years
common in children than in adults and occurs most ago, superficial fungal infections were common, but
2
frequently in hot climates. Dermatophytes of the genera systemic fungal infections were not as frequent as today.
Trichophyton and Microsporum are the most common The incidence of superficial and systemic fungal infection
causative agents. has been increasing because of the increasing

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 Superficial dermatomycoses worldwide

Table 2 Mucocutaneous Candida infections

Disease Clinical appearance Causative agent

Oral candidiasis Discrete white patches that may confluence on the buccal mucosa, Candida albicans
tongue, palate and gingivae
Vaginal and vulvovaginal candidiasis Thick vaginal discharge associated with burning, itching and occasional C. albicans; C.
dysuria
Balanitis Small papules or fragile papulopustules on the galns or in the coronal glabrata C. albicans
sulcus in men. Infection may spread to the scrotum and inguinal areas
Cutaneous candidiasis Pruritic, erythematous, macerated skin in the intertriginous area with C. albicans
satellite vesicopustules. Pustules break open leaving a red, macular
base with a collarette of easily detachable necrotic epidermis
Disseminated candidiasis Organs most commonly involved: lungs, spleen, kidneys, liver, heart and C. albicans, C. tropicalis,
brain C. lustaniae, C. krusei,
C. parapsilosis Candida
Chronic mucocutaneous candidiasis Chronic superficial infections of the skin, nails and oropharynx. Broad species
range of syndromes involved

1
incidence of severe diseases (e.g. malignancies or HIV- face and upper arms. P. orbiculare is also associated with
infection) or immunosuppressant therapies (sys-temic the development of seborrhoeic dermatitis.
1
steroids or chemotherapy). In normal popula-tions,
superficial skin candidiasis occurs because of a Global patterns of superficial fungal
combination of deficiency of the skin s barrier and an infections
endogenous yeast reservoir. Typically, Candida infection is
activated by antibiotic or steroid therapy. Obesity and The clinical appearance and the causative species of
diabetes mellitus are leading predisposing factors for superficial fungal infections vary with geographic region,
cutaneuos candidiasis. socioeconomic conditions and habits. Some species of
fungi exhibit worldwide distribution, whereas others are
restricted to particular continents or geo-graphic regions
Intertrigo 8
(Table 3).
Intertrigo is an inflammation of the body folds and can Trichophyton rubrum is the most common cause
result from bacterial, fungal or viral infection that has worldwide for tinea pedis, nail infection, tinea cruris and
developed at the site of broken skin, for example, the tinea corporis. Tinea pedis and onychomycosis are
4,11
chafing of warm, moist skin of the inner thighs and becoming more common.
genitalia, the armpits, under the breasts, the underside of More widespread travel (economic migration and mass
the belly, behind the ears and between the toes and fingers. tourism), increased ownership of companion
It occurs most frequently in overweight subjects,
diabetics, patients confined to bed, babies and those who Table 3 Distribution of anthropophilic species of fungi
use medical devices like artificial limbs that trap moisture
on the skin. Several skin diseases predispose to intertrigo, Worldwide
including dermatitis or inverse psoriasis. Candida albicans Epidermophyton floccosum
Microsporum audouinii
is the pathogen usually associated with intertrigo.
Trichophyton mentagrophytes var. interdigitale
T. rubrum T.
tonsurans
Geographically limited
Tinea versicolor (pityriasis versicolor) M. ferrungineum: Africa, India, E. Europe, Asia, S. America,
T. concentricum: Pacific Islands, Far East, India, Ceylon,
This is a common skin disease caused by the overgrowth N., Central and S. America,
of Pityrosporum orbiculare, also named Malassezia furfur. T. gourvilii: Central and W. Africa
Most adults harbour P. orbiculare on their skin; in a few T. megninii: Portugal, Sardinia
people, however, its presence results in a harmless skin T. schoenleinii: Europe, Mediterranean,
disease characterised by the development of either hypo-or Middle East, S. Africa, sporadically in US
T. soudanense: Central and W. Africa T.
hyperpigmented patches covered with fine scales on the
violaceum: Africa, Europe, Asia
upper trunk. It occurs less frequently on the neck,

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B. Havlickova et al.

animals, increased use of public sports facilities (espe- increases in those agents have been noted in the UK (T.
cially swimming pools), wearing occlusive training shoes, 14
tonsurans) and France (T. soudanense and M. audouinii).
the increasing incidence of diabetes mellitus and vascular Tinea capitis mostly affects children aged 3–7 years of
disease, such as arteriosclerosis and an ageing population both genders, but recently an increased incidence has been
are contributing factors to the devel-opment of 14
observed in adults and the elderly.
dermatomycoses in socially and economically developed Eastern Europe seems to be characterised by a
1
countries. These are to be seen in addition to dominance of tinea corporis and capitis caused by the
well-established risk factors such as familiar disposition, zoophilic germ M. canis and a related comparatively high
1,12,13
male gender, foot trauma and cigarette smoking. rate of infantile fungal infections. The effects of civil war
Studies in Europe, Asia and Africa indicate that in some European countries in the 1980s and 1990s
anthropophilic agents of scalp infections are being resulted in low standards of medical care and outbreaks of
eradicated in developed nations and are now more typical M. canis possibly related to increased numbers of feral
of countries with low socio-economic status. The domestic animals. The end of war and subsequent
exception is T. tonsurans-related tinea capitis and tinea improvement in standards of living has led to a decline in
corporis in North America. zoophyte infections and an increase in anthropophylic
In tropical and subtropical countries, infectious dis- dermatophyte infections.
eases of the skin are not just more prevalent than in central The incidence of the various fungal species identified in
Europe; they are more frequent and more distinctive. This different epidemiological studies is summarised in Table 4
is particularly true for certain areas in Asia (especially and a wider discussion follows.
India) and for the whole continent of Africa. Socio-
economic conditions tend to be poorer than in Europe and France. Tinea pedis shows an infectious agents pattern
the Americas and there are more problems with diagnosis comparable to the one in other states of developed Europe.
and therapy, but most of all, the humid and warm climatic Plantar dermatophytoses in association with onyxis and
conditions encourage the extensive skin mycoses. In intertrigo rank with leading fungal infections mainly
Africa, a large number of HIV infections favour certain caused by T. rubrum. In a large French study, relating to
fungal infections by reducing the cellular immunity frequency of plantar dermatophytosis, dermatophytes was
needed in the defence against fungi. isolated in 66.6% of patients with interdigital plantar
signs. Trichophyton rubrum was isolated most
15
The following sections look at the main types and frequently.
incidence of superficial fungal infections and their As mentioned above, there has been a significant
associated pathogens based on epidemiological studies (as increase in the incidence of tinea capitis in Europe,
these are the only data available because there is no including France. In the more rural regions, e.g. north-east
requirement to notify dermatophyte infections) by France, dermatophytoses is mostly caused by zoophilic
continent and country. dermatophyte fungi such as M. canis, T. ment-agrophytes
or T. verrucosum, whereas in urban areas, e.g. Paris, there
is a shift toward anthropophilic tinea capitis. Developed
Europe
urban regions of France as well as the UK are
Currently, the most important dermatophytes isolated in characterised by the largest overall increase in anthrop-
Europe are T. rubrum, M. canis, T. mentagrophytes var. ophilic tinea capitis infection. Besides T. tonsurans, T.
granulosum and T. verrucosum. Several of these are soudanense and M. audouinii are the main infectious
believed to have spread from the Mediterranean countries. agents causing tinea capitis. This pattern of anthropo-
Other dermatophytes such as M. audouinii, T. soudenense philic infections seems to be linked to immigration from
and T. violaceum (causing so-called immigration 14
sub-Saharan Africa or from the Caribbean.
mycoses), which are endemic in Africa and some parts of
Asia, are currently rarely isolated in Europe. However, United Kingdom. Tinea capitis-causing anthropophilic
their incidence may be expected to increase in the future species predominate also in the urban regions of the UK.
2
as a result of tourism and migration. Trichophyton tonsurans has been noted as the leading
Trichophyton rubrum is the most frequently isolated pathogen causing tinea capitis in the UK, comparable to
dermatophyte in cases of tinea corporis and cruris in Northern America. Other relevant anthropophilic fungi
developed European countries. There is also a shift include M. audouinii and M. rivalieri. The occurrence of
towards tinea capitis caused by anthropophilic dermato- these anthropophilic germ-induced infections is statis-
phytes in urban areas in Europe. The largest overall tically related to ethnic groups originating from Africa.

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 Superficial dermatomycoses worldwide

Table 4 Summary of the European incidence of the most common mycoses identified in these epidemiological studies

Lange Monod Lehenkari Jeske Lupa

et al.26 Korstanje21 et al.23 Dolenc-Voljc37 et al.22 Prohic38 et al.27 et al.11
Microsporum canis 62 40.9 5 46.8 90.4 23.5
M. gypseum 5.3
M. equinum 0.7
M. cookei 0.14
Trichophyton mentagrophytes 24.5 26
T. mentagrophytes var. granulosum 21.6 30.9
T. mentagrophytes var. interdigitale 7.9 2.3 10.0
T. mentagrophytes var. mentagrophytes 11.4 4.9
T. mentagrophytes var. quinckeanum 6.0 6.9
T. rubrum 12 62.5 36.7 66 17.8 41.7
T. verrucosum 4.5 0.4
T. violaceum 29.6 1.9 3.7 0.1
T. tonsurans 6.8 10.4 2.3
T. terrestre 0.2
T. schoenleinii 2.3 2.4
Epidermophyton floccosum 6 7.7 7.4

All values are percentages.

Corresponding to the situation in Europe at large, tinea requirement to notify the disease mean that a further rise
capitis is a fungal infection that affects especially young in the number of cases in humans is to be expected.
children. This has been demonstrated in a study by Hay et
16
al.. The study shows tinea capitis in school children in Belgium and the Netherlands. In these countries, zoophilic
south east London and the importance of new guidance to dermatophytes are supplanting anthropophilic strains as
general practitioners on treatment. Tinea pedis and the cause of tinea capitis. Samples of scales, pus and hair
associated tinea capitis seem to be comparable with the collected from 435 patients with tinea capitis over a period
characteristics of developed Europe, with T. rubrum and T. 21
of 30 years have revealed that at the beginning of the
mentagrophytes var. interdigitale as the leading derma- period, T. verrucosum was found most frequently, but
tophytes. declined dramatically from the mid-1970s onwards. In
contrast, M. canis was found frequently over the years,
Germany. Trichophyton rubrum accounts for 80–90% of all rising from 9% to 11% of cases in the 1960s to >40% in
17
isolated strains in Germany. Trichophyton interdigitale (T. the 1990s. This change is associated with increased
mentagrophytes var. interdigitale) and E. floccosum are the mechanisation in farming and increased numbers of
second and third most frequently isolated agents and tinea households keeping companion animals. The frequency of
pedis and unguium are most frequently diagnosed. The T. violaceum has also increased significantly since the
German Mycologic Society estimates the prevalence of 1970s because of increased immigration from countries
onychomycosis to be 12.4%, whereas the incidence of tinea 21
such as Italy, Turkey, Morocco and Tunisia.
12
cruris has declined in the last 70 years.
Investigations in miners indicate that the incidence of Finland. Trichophyton rubrum was the most common
1
tinea pedis and tinea unguium is up to 72.9% , primarily species (66% of all positive cultures) isolated from 2101
because of their use of occlusive boots, the warm and 22
samples in northern Finland between 1982 and 1990; T.
humid environment in the mine and shared use of washing mentagrophytes was isolated from 815 samples (26%) and
17,18
facilities. E. floccosum from 193 samples (6%). T. verrucosum
Two studies of cases of tinea capitis have found that the caused an epidemic among cattle keepers in 1987–1990,
most prevalent causative agent of tinea capitis was causing 47 infections. Microsporum canis, T. terrestre and
M. canis, followed by T. tonsurans, T. violaceum and T. T. violaceum isolates were rare. The same species affected
19,20 both children and adults. Trichophyton rubrum and T.
mentagrophytes.
As a result of an immunisation programme against T. mentagrophytes (T. interdigitale) occurred most frequently
verrucosum in cattle, ringworm should have been (mostly as causative micro-organisms of foot infections)
eradicated in Eastern Germany. However, inconsistent in patients aged 41–45 years of age. Epidermophyton
immunisation of livestock and the removal of the floccosum usually affected the toes and ⁄ or the groin in

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B. Havlickova et al.

predominantly men aged 21–25 years. Overall, there was a (41.7%), T. mentagrophytes var. granulosum (30.9%), T.
slight increase in tinea pedis during the study period and a mentagrophytes var. interdigitale (10.0%), E. floccosum
decrease in tinea cruris. (7.4%) and T. mentagrophytes var. quinckeanum (6.9%).
The incidence of tinea pedis increased substantially
Switzerland. A survey of dermatophyte infections in the between 1994 and 1996.
Lausanne area during an 8-year period showed that 5–10%
of consultations in dermatology concern mycotic Russia. Several epidemiological studies confirm a higher
infections. Trichophyton rubrum was the most frequently number of toenail infections and a more frequent
isolated species (at 62.5%) followed by T. mentagrophytes occurrence of severe toenail diseases, including mixed
(24.5%) and M. canis (5.0%). Less frequent isolates fungal infections with yeasts and moulds, in Russia
included E. floccosum, M. langeroni, compared to developed countries in Western Europe. The
prevalence of tinea pedis has been reported as at up to
M.gypseum, T. soudanense, T. violaceum, T. verrucosum, 28
T. gourvili and T. tonsurans.
23 83% in the Russian population.
Khaldin et al. found that in the Russian Federation, T.
Italy. Panasiti et al. conducted a retrospective study of rubrum was the predominant causative agent of
dermatophytes causing superficial mycoses among dermatomycoses, accounting for 65–75% of cases,
24 whereas Candida spp. were commonly detected in skin
outpatients at one centre in Rome between 2002 and 2004. 29
fold infections.
With 3160 patients studied, the most frequently isolated
dermatophyte was M. canis, followed by M. audouinii. This These findings correlate with a study by Ja¨rv et al.
30
species was identified as an emerging species, being the concerning toenail onychomycosis in Estonia from 2004,
second most frequent aetiological agent of tinea capitis and in which nearly 70% of pathologic nail changes were
the fourth of tinea corporis in this study. It should be noted caused by dermatophytes, 10% by yeasts and 7% by
that in the Mediterranean region – especially in Italy – M. moulds. Trichophyton rubrum was the most-frequently
canis seems to be endemic in feral cats. isolated pathogen. Mixed infections were found in 6% of
patients. Furthermore, the incidence of tinea corporis and
30,31
Poland. A survey in Gdan´sk between 1984 and 1995 tinea faciei is also thought to be high.
showed that in 1544 patients, the most common types of Tinea pedis has been found not only in elderly or sick
dermatophytoses were tinea cutis glabrae (32.3%), tinea people but also in a significantly high degree in the
pedis (24%), onychomycosis (16.5%), tinea capitis working population. This is shown in a Russian study of
(11.7%), tinea inguinalis (8.9%) and tinea manus foot mycoses in workers at metallurgical plants. Trich-
25 ophyton rubrum (71.3%) and T. interdigitale (28.7%) were
(4.0%). Lange et al. reported that in children and
26
the main pathogens. 18.3% of patients had mixed
adolescents in Gdan´sk between 1999 and 2001, the infections with C. albicans. It was notable that Tricho-
most frequent pathogens identified were M. canis (62%) 32
phyton occurred as a complication in some cases.
and T. rubrum (12%) and the most common
Vakulova et al. have also reported a high incidence of
dermatophytoses were tinea cutis glabrae (42%) and tinea
fungal skin and nail infections caused by Candida ssp. in
capitis (30%) primarily due to M. canis. Glabrous skin 33
lesions were most frequent in children aged 8–15 years; Russian submariners.
the incidence of scalp lesions peaked in children aged 4–7 As in other parts of Eastern Europe, zoophilic infections
years and tinea pedis, mostly caused by T. rubrum and T. are more common in rural regions; M. canis, T. mentag-
mentagrophytes var. granulosum, was observed mainly in rophytes and T. verrucosum are the predominant zoophilic
adolescents (aged over 12 years). Onychomycosis was pathogens. The incidence of T. verrucosum and T.
34
highly uncommon in children and was caused mainly by mentagrophytes continued to rise until the late 1980s.
T. rubrum. Effective antimycotic therapy has reduced the number
Among 7393 dermatophytoses identified in central of trichophytoses in recent years. In Armenia, an
Poland during 1987–1996, there were 2204 (29.8%) cases epidemiological study showed a reduction in the number
35
27
of tinea cutis glabrae. Causative organisms included M. of trichophytosis patients.
canis (23.5%), T. mentagrophytes var. granulosum Favus caused by T. schoenleinii, T. violaceum or M.
(21.6%), T. rubrum (17.8%), T. tonsurans (10.4%), E. gypseum is now found only rarely, in areas with low social
36
floccosum (7.7%), T. mentagrophytes var. quinckeanum conditions.
(6.0%) and M. gypseum (5.3%). In the same population,
11
Lupa et al. reported 2025 (27.4%) cases of tinea pedis. Slovenia. Results from patients with suspected
Causative organisms included: T. rubrum dermatophytoses in Slovenia for the period 1995–2002

2008 The Authors

8 Journal compilation 2008 Blackwell Publishing Ltd • Mycoses, 51 (Suppl. 4), 2–15
 Superficial dermatomycoses worldwide

have shown that among 42 494 samples, M. canis was are also found in Asia, especially India. Trichophyton
isolated most frequently (46.8%) followed by T. rubrum concentricum causes tinea imbricata.
(36.7%), T. mentagrophytes var. interdigitale (7.9%) and The prevalence of tinea pedis in Asia is similar to that in
T. mentagrophytes var. mentagrophytes (4.9%). The most Europe (approx. 20%); it is also common in Australia.
common dermatophyte infections were tinea corporis, Tinea corporis and capitis are frequently found in children
37
onychomycosis, tinea pedis and tinea faciei. and adolescents.
The incidence of the various fungal species identi-fied
Bosnia and Herzegovina. Tinea capitis was found in 241 in epidemiological studies is summarised in Table 5 and
(34.1%) patients in Sarajevo between 1997 and 2006;
38 the significance for the prevalence of associated
causative agents were identified in 209 (29.6%) cases. dermatomyces in different countries is discussed below.
Zoophilic dermatophytes (91.8%) prevailed over
anthropophilic (7.2%) and geophilic (1.0%)
dermatophytes. Microsporum canis was isolated most Turkey. A study performed in a Turkish University
frequently (90.4%), followed by T. schoenleinii (2.4%) Hospital during 2001–2002 found the prevalence of
39
and T. violaceum (1.9%). Most patients were male dermatophytoses to be 7.34% (68 out of 926).
(56.5%) and aged under 10 years (52.6%). Zoophilic Trichophyton rubrum was the most frequently isolated
dermatophytes were most commonly recovered from dermatophyte (56%), followed by T. mentagrophytes
children and adolescents with tinea capitis, tinea corporis (38%), T. violaceum, T. verrucosum, M. canis and E.
and tinea faciei. Anthropophilic species were identified floccosum. Tinea pedis (47%) was the most common
mostly in adults with tinea pedis, onychomycosis and dermatophytosis, followed by tinea unguium (29%), tinea
tinea cruris. Interestingly, rates of M. canis infection inguinalis (15%), tinea corporis (7.4%) and tinea capitis
declined during the study period, while infections caused (1.6%).
by T. rubrum increased in frequency – possibly as the war S¸as¸maz et al. examined the frequency and spectrum of
came to an end and quality of life began to improve again. superficial fungal infections among 925 consecutive
Turkish soldiers admitted to the dermatology outpatient
40
clinic in Northern Cyprus. Superficial mycotic infec-
tions were found in 185 soldiers (20%), of whom 151
Asia and Australia
(61.6%) had dermatophytosis, 32 (17.3%) had tinea
In Asia, T. rubrum and T. mentagrophytes are the most versicolor and two (1.1%) had candidiasis. A similar study
commonly isolated pathogens, causing tinea pedis and was conducted among workers in a Turkish textile factory
41
unguium, as is the case in Europe. In contrast to Europe, – an important industry in that country. Superficial
the next most commonly isolated pathogen is T. mycoses were found in 73 (16.9%) workers; of these, 56
violaceum, the causative agent of tinea capitis and (76.7%) cases were dermatophytoses and eight (11.0%)
corporis. Microsporum ferrugineum and T. concentricum were pityriasis versicolor. No causative

Table 5 Summary of the Asian incidence

of the most common mycoses identified in Prohic C¸ elik E Lari Tao-Xiang Kim Singal
these epidemiological studies et al.38 et al.41 et al.42 et al.46 et al.49 et al.43 Min48
Microsporum canis 1.5 15.1 65
M. audounii 34
M. gypseum 7.5 3
Trichophyton mentagrophytes 38 42.9 11.3 29.4 3
T. rubrum 56 57.1 13.2 43.9
T. verrucosum 1.5 5.7 3
T. violaceum 1.5 28.3 38 18
T. tonsurans 9 9
T. schoenleinii 10
T. asahii 62.1
T. mucoides 20.3
T. inkin 14.9
Epidermophyton floccosum 1.5 15.1
Candida spp. 14.0

All values are percentages.

2008 The Authors

Journal compilation 2008 Blackwell Publishing Ltd • Mycoses, 51 (Suppl. 4), 2–15 9
B. Havlickova et al.

agent could be identified in nine (12.3%) workers. T. found in rural communities of this region tend to be
rubrum (57.1%) and T. mentagrophytes (42.9%) were two different from those found in other regions in the country,
of the most frequently isolated dermatophytes. The study indicating that dermatophytes in former rural societies
emphasised that textile workers should be considered as a 47
must have migrated extremely slowly. In developed
risk group for superficial mycoses, especially tinea pedis. cities in China, as in Europe, zoophilic dermatophytes are
becoming the most important pathogens in the context of
tinea capitis. In 600 cases in Shanghai between 1993 and
Iran. The characteristics of dermatophytoses among 2002, M. canis was identified as the main pathogen in 65%
children in an area south of Tehran were reported by Lari of cases. The anthropophilic dermatophytes T. violaceum
et al. 382 children aged £16 years with suspected (18%) and T. tonsurans (9%) were also important
48
dermatophytic lesions were examined between 1999 and species.
42
2001. The incidence rate of dermatophytoses was 6.6 per
100 000 person-years. Trichophyton violaceum (28.3%), Korea. Tinea pedis is the most common dermatomycosis
M. canis (15.1%), E. floccosum (15.1%), T. rubrum in Korea and Kim et al. have shown that the most common
(13.2%), T. mentagrophytes (11.3%), M. gypseum (7.5%) infectious agents in foot mycoses are T. rubrum, other
49
and T. verrucosum (5.7%) were the most frequent isolates. Trichosporon spp. and Candida spp. Jang et al. have
Tinea capitis (39.6%) was the most common reported that the prevalence of tinea corporis is increasing
dermatophytosis, followed by tinea corporis (30.2%), 50
in Korea, but that it varies according to life style and
tinea faciei (18.9%) and tinea manuum (7.5%). regional characteristics. Dermatophytes were isolated in
73 out of 105 cases of tinea corporis; T. rubrum (58 cases),
India. In northern India, anthropophilic dermatophytes are T. mentagrophytes (eight cases) and M. canis (five cases)
the predominant pathogens causing tinea capitis. In a were the most common causative agents.
study of 153 consecutive patients with tinea capitis, 90%
of the patients were aged less than 15 years; 75%
belonged to poor socio-economic groups and 19% had a Singapore. Cutaneous fungal infections are common in
family history of tinea capitis. Trichophyton violaceum Singapore. Between 1999 and 2003, 12 903 cases of
(38%), M. audouinii (34%), T. schoenleinii (10%) and T. superficial fungal infections were seen at the National Skin
tonsurans (10%) were the most commonly isolated 51
Centre. A majority of patients (72.3%) were male. The
43
pathogens. most common conditions were tinea pedis (27.3%),
Tinea capitis caused by T. violaceum is endemic in pityriasis versicolor (25.2%) and tinea cruris
south India. A study conducted in 1978 suggested that (13.5%). Tinea capitis is uncommon in Singapore.
trauma to the scalp caused by ritual shaving may be one Trichophyton rubrum was the most prevalent fungal
explanation for this. Twenty one cases of tinea capitis pathogen isolated, except in cases of tinea pedis, where T.
were found in boys aged 10–17 years in Purasawalkam, interdigitale was the most frequently isolated organism.
Madras, who were shaved consecu-tively by the same Candida infections were common (n = 1430) and were
44 manifested as candidal intertrigo. The incidence of
barber. The razors were cleaned only in soap and water.
onychomycosis has increased over the past 5 years.
Unlike in Europe, tinea pedis is comparatively rare in Dermatophytes remain the most commonly isolated fungal
India, especially in the poorer areas. As in Europe, the pathogens isolated in toenail onychomycosis, whereas
most important causative agents are T. rubrum, T. Candida spp. accounted for the majority of isolates in
interdigitale and E. floccosum.
45 fingernail onychomycosis.

China. Tao-Xiang et al. conducted a 1-year analysis of

dermatomycoses in the Lanzhou district of northwestern Japan. In an epidemiological investigation to determine the
46
China. In 1443 suspected fungal infections, the fungi prevalence and circumstances of untreated and
unsuspected tinea pedis and onychomycosis, the
were isolated in 221 cases, the most frequent being T.
prevalence of occult tinea pedis was 25%. Fifty nine per
rubrum (43.9%) T. mentagrophytes (29.4%) and Candida 52
spp. (14.0%). The incidence of tinea pedis, cent of those patients had tinea unguium simultaneously.
onychomycosis and tinea manuum was 38.7%, 27.8% and
13.5% respectively.
Tinea capitis of children, primarily caused by T. Australia. In Australia, there is a high incidence of tinea
violaceum, is common in western China. Strains pedis. In a randomised sample of 2491 students with

2008 The Authors

10 Journal compilation 2008 Blackwell Publishing Ltd • Mycoses, 51 (Suppl. 4), 2–15
 Superficial dermatomycoses worldwide

53 Table 6 Summary of the African incidence of the most common mycoses

confirmed tinea pedis an age- and gender-adjusted
identified in these epidemiological studies
prevalence of 5.2% was found; increasing with age from
2.1% in 4–6 year-old to 9.7% in 16–18 year-old Hay Enweani Ellabib Abu-Elteen
individuals. A higher proportion of males (6.0%) had tinea et al.55 et al.58 et al.60 & Malek61
pedis than females (4.3%). Trichophyton mentagrophytes Microsporum canis 8 11.1
and T. rubrum were the most common dermatophytes M. audouinii 46.8 46.8
isolated on culture. Only 20 isolates of T. violaceum, M. gypseum 0.5
associated with tinea capitis and tinea corporis, have been Trichophyton mentagrophytes 25.5 25.5 3 32.7
54 T. rubrum 21.3 28.6
identified in a 32-year period in Melbourne. As observed
T. verrucosum 14 2.0
in Europe and America, infection seems to occur almost T. violaceum 44 1.0
exclusively in African immigrants, not in the indigenous T. tonsurans 2.1
population. T. schoenleinii 4.0
Epidermophyton floccosum 4.3 7 20.1
Candida spp. 10
Africa
All values are percentages.
Fungal infections are among the most commonly
diagnosed skin diseases in Africa. Both the pathogen
spectrum and the clinical manifestations are totally dence of the various fungal species are summarised in
different from those seen in Europe. The anthropophilic Table 6.
dermatophyte T. audouinii is the most prevalent patho-
gen, together with T. violaceum and T. soudanense. South Africa. The incidence of dermatoses in 246 adults
Trichophyton gourvilii is an endemic, partly geographi- with HIV at a South African clinic was studied over a
cally restricted, anthropophilic dermatophyte, and its 56
period of 1 year. The most common cutaneous disease
predominance in tinea capitis is characterised by patches manifestation was herpes zoster (19%) and tinea corporis
of grey hair. The black dot type, caused by the endotrichus was found in 7% of patients. Opportunistic fungal
fungi T. tonsurans and T. violaceum (also endemic in infections, such as candidiasis, were present at 3%. In 100
Africa), is widespread. Favus, caused by T. schoenleinii, children (mean age of 4.6 years) in Kwa-Zulu ⁄ Natal,
has occasionally been observed. This pathogen was a dermatologists identified T. violaceum in 90% of positive
widespread trigger of family epidemics in Europe in the cultures, making it probably the most common cause of
18th century. Today, it has almost disappeared from 57
tinea capitis in South Africa. The most common clinical
developed European countries but is found in the densely manifestation was the black dot type, seen in 50% of
populated areas of Africa. Trichophyton soudanense seems patients.
to be a common cause of tinea capitis in north-western
tropical Africa. Tricho-phyton rubrum and T. Nigeria. A total of 188 (13.4%) mycotic infections were
mentagrophytes are less common and are associated with identified in a study among 1400 school children in
tinea corporis and, in particu-lar, tinea cruris (or tinea 58
Ekpoma, Nigeria. The causative agents included M.
axillaris in women). In 2005, Hay et al. estimated the audouinii in 88 cases (46.8%), T. mentagrophytes in 48
overall incidence of tinea in Sub-Saharan Africa to be 78 (25.5%), T. rubrum in 40 (21.3%), T. tonsurans in 4
55
million. Notably, tinea pedis and unguium are very (2.1%) and E. floccosum in 8 (4.3%) patients.
uncommon in rural areas in Africa – probably because of
the lack of risk factors. A large part of the population Malawi. In a survey conducted between 1987 and 1989,
walks bare foot; diabetes mellitus and adipositas are rare 59
Po¨nnighaus et al. looked at the spectrum of derma-
in these areas. tophytes in a northern Malawi population. Between 1.5%
Tinea faciei and barbae are caused by dermatophytes, and 2.5% of the population were diagnosed with tinea
including M. gypseum and M. ferrugineum. In some faciei, corporis or cruris. The authors noted the rarity of T.
regions of Africa, T. rubrum is rare. rubrum (around 1%) and the predominance of M.
Besides dermatophytoses, pityriasis versicolor is a audouinii (57%) in this part of Africa. Epidermophyton
typical dermatological diagnosis for African adolescents. floccosum was the most common isolate (56%) from the
Humidity seems to favour this endogenic infection. genital area.
Europeans travelling to Africa often develop this disease.
Candida infections are also highly prevalent given the Libya. In a study of the prevalence of skin infections and
high incidence of HIV infections. Some data on inci- their causative agents in 1180 patients with a

2008 The Authors

Journal compilation 2008 Blackwell Publishing Ltd • Mycoses, 51 (Suppl. 4), 2–15 11
B. Havlickova et al.

confirmed mycotic infection, tinea corporis was diagnosed and vector, leading to specific clinical presentations and
62
in 45.9% of cases (85% in children aged less than 15). compliance difficulties for treatment.
Other conditions included pityriasis versicolor (27.8%), American teams have taken T. tonsurans infections to
candidiasis (13.4%) and tinea pedis (8.1%). Trichophyton Europe and Asia. This is another example of traditionally
violaceum was the most common aetiological agent, geographically confined pathogens spreading to new areas.
responsible for 44% (300 cases) of dermatophyte Conversely, T. violaceum and T. soudanense, which are
infections. Malassezia furfur was found in 27.8% of cases, causes of tinea capitis in parts of Africa and West Asia,
T. rubrum in 13.8%, C. albicans in 10%, M. canis in 8.1%, have only rarely been reported to cause dermatophytoses
60 in the USA. However, sporadic cases provide evidence for
E. floccosum in 6.6% and T. mentagrophytes in 3.1%.
the emergence of these organisms as a result of changing
63
population demographics.
Jordan. The Zarqa district of Jordan has an industrialised
area surrounded by farms and villages; the climate is
relatively hot and semi-arid. The most common USA. An epidemiological survey of superficial fungal
dermatophytes isolated were T. mentagrophytes, E. 64
diseases found that T. rubrum was the most commonly
floccosum, T. rubrum and M. canis. Tinea pedis (35% of isolated dermatophyte species. Trichophyton tonsurans
all cases) and cruris (10%) are found more frequently was more common in tinea capitis, and equally common in
during the summer months, whereas tinea capitis (23% of tinea corporis and cruris. Dermatophytes appeared in
all cases), corporis (10%) and unguium (22%) are more approximately 95% of tinea pedis isolates and 82% of
61
frequent during the spring and winter. There is evidence onychomycosis isolates. Candida albicans (7%) and non-
that the increasing prevalence of T. rubrum is because of dermatophyte moulds (11%) played only a minor role in
immigration from Mediterranean countries. Tinea pedis onychomycosis. These findings were in general agreement
(caused by T. mentagrophytes) is most prevalent in older with other major epidemiological studies performed
farmers. Tinea capitis is more common in children and outside the USA and confirm that dermatophyte fungi are
more common in girls because girls tend to have long hair, responsible for most superficial fungal infections.
which facilitates contact and spread of fungal species.
Foster et al. carried out a survey of cutaneous fungal
65
infections between 1999 and 2002. Dermatophytes were
Americas the most commonly isolated fungal organisms, except
suspected finger onychomycosis caused by Candida spp.
The most commonly observed fungal species in the Trichophyton rubrum was the most prevalent fungal
Americas are T. rubrum, T. tonsurans and T. mentagro- pathogen (70%) and increased incidence of this species
phytes. Some data on the frequency of the various fungal was observed in finger and toenail onychomycosis, tinea
species are summarised in Table 7. corporis and tinea cruris, tinea manuum and tinea pedis.
A dramatic increase in T. tonsurans infections has been
8
reported in the USA. The term tinea corporis gladiatorum In the first half of the 20th century, the predominant
was created because T. tonsurans has high attack rates in causative agent of tinea capitis was the anthropophilic
teams of wrestlers, high-level judo players and in other species M. audouinii. By the 1980s, however, T. tonsurans
combat sports. This may be because of a unique fungal had become the most common cause and today, more than
aetiology and the nature of the reservoir 65
95% of tinea capitis cases are because of T. tonsurans.

Table 7 Summary of the incidence of the most common mycoses Canada. The incidence of T. tonsurans in confirmed tinea
66
identified in epidemiological studies in the Americas capitis cases increased from 9% in 1985 to 76% in 1996.
Prior to this, the more common agents were
Brilhante et al.68 Welsh et al.69
T. verrucosum, M. canis and M. audouinii. This infection
Microsporum canis 7 7.1 pattern is most common in children of both genders under
Trichophyton mentagrophytes 6.2 23.7 14 years of age. Subjects are significantly more likely to
T. rubrum 49.6 45
live in urban than in rural areas.
T. tonsurans 34.4 21
Epidermophyton floccosum 2.5
Brazil. A 5-year study examined dermatophytoses in 137
All values are percentages. children below the age of 12 with clinically

2008 The Authors

12 Journal compilation 2008 Blackwell Publishing Ltd • Mycoses, 51 (Suppl. 4), 2–15
 Superficial dermatomycoses worldwide

67
diagnosed tinea. Male children aged 2–12 years were the increasing prevalence of obesity and diabetes mellitus and
most often affected. Tinea capitis (78 cases, 56.9%), an ageing population. Microsporum canis is a prevalent
mainly caused by M. canis (46 cases), was the most agent of tinea capitis in the developed world and this
common clinical form, followed by tinea corporis (43 could be related to mass tourism to endemic regions (such
cases, 31.3%) mainly caused by T. rubrum (17 cases) and as the Mediterranean area) and the close association
tinea cruris (10 cases, 7.2%) caused by T. rubrum (five between humans and companion animals.
cases). In another study with 2297 patients with suspected
68 Several dermatophyte species are geographically
clinical lesions of dermatophytosis, 534 (23.2%) patients
were tested positive for dermatophytes. Trichophyton limited. Trichophyton violaceum is endemic in certain
rubrum (49.6%), T. tonsurans (34.4%), M. canis (7%) and parts of Eastern Europe, Africa, Asia and South America,
T. mentagrophytes (6.2%) were the most prevalent but not in North America. Trichophyton soudanense is a
species. Correlating the species with the anatomical common and endemic cause of tinea capitis in north-
localisation revealed that T. tonsurans was the most western tropical Africa and West Asia. The sporadic
frequent isolate in scalp lesions (73.9%), whereas T. appearance of both in Western Europe and the USA
rubrum was the main species involved in body lesions provides evidence for the ongoing evolution of dermato-
(72.8%). phytosis epidemiology in relation to international travel,
immigration and shifts in population demographics.
Mexico. Welsh et al. have published data from Monterrey
involving 2397 cases of dermatophytosis from superficial
69
Conflict of interest
cutaneous lesions between 1978 and 1990. Seven
hundred and twenty-six (30.2%) cases of tinea pedis, 613 Dr B Havlickova and Dr M Friedrich are employees of
(25.6%) of tinea unguium, 441 (18.4%) of tinea capitis, Intendis GmbH; Dr V Czaika has a consultancy agreement
395 (16.4%) of tinea corporis and 222 (9.3%) of tinea with Intendis GmbH.
cruris were observed. The most commonly isolated
dermatophytes were
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