Review article

Epidemiological trends in skin mycoses worldwide

Blanka Havlickova,1 Viktor A. Czaika2 and Markus Friedrich1
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 supercial mycotic infections shows that 2025% of the worlds 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 specic mycoses can vary widely. Local socio-economic conditions and cultural practices can also inuence the prevalence of a particular infection in a given area. For example, tinea pedis (athletes 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
Fungal infections of the skin and nails form the most numerous and widespread group of all mycoses. The prevalence of supercial mycotic infections has risen to such a level in the last decades that skin mycoses now affect more than 2025% of the worlds population, making them one of the most frequent forms of infections.1 The distribution of the dermatomycoses, their aetiological agents and the predominating anatomical infection patterns vary with geographical location and a wide range of environmental and cultural factors.1,2 Dermatophytes thrive at surface temperatures of 2528 C and infection of human skin is supported by warm and humid conditions. For these reasons,

Correspondence: Blanka Havlickova, Intendis GmbH, Max-Dohrn Strae 10, Berlin, Germany. E-mail: blanka.havlickova@intendis.com Accepted for publication 8 July 2008

supercial fungal infections are relatively common in tropical countries and are exacerbated by the wearing of occlusive clothing. In addition, the frequency of dermatomycoses is greater in communities with low socioeconomic status: crowded living conditions provide multiple opportunities for skin-to-skin contact and close proximity to animals, while hygiene may be suboptimal. Moreover, supercial skin infections show a low tendency to self limitation, and absence of, or poor medical care further increases the epidemic spread of skin mycoses. Despite regional characteristics and predispositions for dermatophyte infections, the spectrum of dermatophytes is not static. Booming mass tourism, international sports activities and increasing migration mean that less common or forgotten species are being imported and disseminated. This review attempts to summarise current epidemiological trends for fungal infections. Its main focus is on dermatomycosis of glabrous skin in different continents.

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Supercial dermatomycoses worldwide

Causative agents
Supercial fungi can be classied according to their usual habitat into anthropophilic, zoophilic and geophilic organisms. Generally, anthropophilic fungi cause supercial dermatomycoses characterised by relatively low inammatory activity because of an immunological arrangement that exists between the fungus and its human host.1,2 Household dust may act as a reservoir of antropophilic dermatophytes, preserving dermatophyte spores for years. Zoophilic germs are found in animals, but are also sporadically transmitted to humans by cats, dogs (Microsporum canis), guinea pigs and rabbits (Trichophyton mentagrophytes var. granulosum). Zoophilic germs can be referred to as cuddly toy mycoses (because of the mode of infection in children and adolescents) and have a high afnity to the hairy head of a child. They are associated with highly inammatory and potentially highly contagious skin infections. Geophilic fungi grow in the soil and only sporadically infect humans.2 When they do, the result varies from high to low inammation. Strains of Microsporum gypseum, the most common geophilic pathogen, cultured from humans are more virulent than those from the soil, accounting for occasional epidemic spread under appropriate conditions.3 There are approximately 100 000 species of fungi distributed worldwide. The majority of fungal infections seen in both temperate and tropical countries are supercial infections of the skin. The most common pathogens relevant in practice are dermatophytes, yeasts and moulds. There are approximately 40 different species of dermatophytes, characterised by their capability to digest keratin and divided among three genera: Trichophyton, Microsporum and Epidermophyton. A majority of supercial fungal infections of the skin are caused by ve or six species of dermatophyte, of which Trichophyton rubrum is the most common.4 The predominant species of dermatophytes vary according to their clinical localisation, as described in the Clinical manifestations and global patterns of supercial fungal infections sections and listed in Table 1.5 The management of tinea of the glabrous skin, caused by dermatophyte infections, is a common therapeutic problem for dermatologists.6 However, unlike pathogenic yeasts and non-dermatophytic moulds, these infections never disseminate systemically and therefore can never be lethal.

Table 1 Dominant species of dermatophytes according to clinical localisation Condition Tinea capitis (scalp) Dominant species Trichophyton violaceum T. tonsurans T. soudanense Microsporum canis M. audouinii T. rubrum T. mentagrophytes (var. interdigitale) Epidermophyton occosum T. rubrum T. mentagrophytes (var. interdigit et granulosum) T. rubrum M. canis T. tonsurans T. rubrum T. mentagrophytes (var. interdigitale)

Tinea pedis (feet)

Tinea cruris (groin)

Tinea corporis (arms, legs and trunk) Tinea unguium (nger-nails and toe-nails)

Candida species are part of the transient or commensal ora in specic regions of the body. They are opportunistic pathogens that only become pathogenic to humans under particular systemic and local conditions. Candidiasis is predominantly a disease of the very old, the very young and the very sick. In most cases, it is an endogenous infection originating from the patients own ora and generally follows a shift in the existing host yeast relationship. Occasionally, a strain can spread between individuals or in hospitals.7 Tinea can be caused by obligatory pathogenic dermatophytes such as M. canis or T. verrucosum. Non-dermatophytic moulds, such as Scopulariopsis brevicaulis or Aspergillus species, can theoretically cause nail infections, albeit rarely.

Clinical manifestations
Most basic fungal skin infections are caused by dermatophytes and the main clinical manifestations are detailed below.
Tinea pedis (athletes foot)

This is a very common infection that occurs in one in ve adults and the incidence increases with age from adolescence.1 It occurs more frequently in people who wear occlusive shoes.2 It may be associated with several different fungi, including yeasts, the most common being T. rubrum and T. interdigitale (formerly T. mentagrophytes var. interdigitale). During the past 30 years, the incidence of tinea

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pedis has increased in the developed world and its prevalence is around 10%.8 One hand two feet syndrome is characterised by dermatophyte infection of both feet and one hand and can be found in patients with lower immunocompetence, such as diabetics. The condition is frequently associated with T. rubrum.
Tinea unguium (onychomycosis, nail infections)

Dermatophyte infection affecting nearly the entire integument is named tinea corporis generalisata. A generalised dermatophytosis caused by T. rubrum can occur as a result of mis-diagnosis or mis-treatment. Misread tinea corporis generalisata caused by T. rubrum is named tinea incognita.
Tinea cruris (ringworm of the groin)

The causative agents of onychomycosis include dermatophytes, Candida spp and non-dermatophytic moulds. Dermatophytes are most commonly responsible for onychomycosis in temperate western countries, whereas Candida and non-dermatophytic moulds are more frequently involved in countries with a hot and humid climate.9 Trichophyton rubrum is the most common dermatophyte associated with onychomycosis, others include T. interdigitale, Epidermophyton occosum, T. violaceum, M. gypseum, T. tonsurans, T. soudanense (considered by some to be an African variant of T. rubrum rather than a full-edged separate species) and the cattle ringworm fungus, T. verrucosum.2 Note that T. interdigitale is still sometimes referred to as T. mentagrophytes var. interdigitale. The latter should be used to describe the zoophilic form of the dermatophyte, and T. interdigitale used to describe its anthropophilic form. Recent genetic research has shown that T. mentagrophytes var. granulosum is the same as T. interdigitale.10 Other causative agents include Candida spp.2 and non-dermatophytic moulds, in particular members of the genera Scytalidium (now Neoscytalidium), Scopulariopsis and Aspergillus. Scytalidium mainly affects people in the tropics, although it can persist if they move to more temperate areas. Candida mainly causes proximal nail infections in people whose hands are often submerged in water. Nail infection caused by Candida subspecies such as C. albicans, C. parapsilosis and C. guilliermondii is almost always associated with paronychia. As a rule, C. parapsilosis appears concomitantly with T. interdigitale (T. mentagrophytes var. granulosum) in nail infections.
Tinea corporis (ringworm on the trunk)

This presents as an itchy, red rash in the groin and surrounding area and is commonly seen in young men living in a warm climate.2 Tinea pedis can co-exist if the infection is spread by scratching the feet and then the groin. Axillary infection can be seen as an analogous tinea pattern in woman. The most common agents are E. occosum, T. mentagrophytes and T. rubrum.
Tinea capitis (ringworm of the scalp)

This is a dermatophyte infection of the scalp and hair and tends to affect young children worldwide.2 Presentation depends on the aetiology and can be noninammatory, inammatory or black dot type. The non-inammatory form is most commonly caused by M. audouinii or M. ferrugineum and usually begins as a small erythematous papule surrounding a single hair shaft, which spreads centrifugally to other hairs. Scaling occurs and the hair turns grey. The inammatory type is usually associated with zoophilic or geophilic germs such as M. canis and M. gypseum respectively. Black dot tinea capitis is caused by T. tonsurans or T. violaceum. T. verrucosum is highly contagious and virulent and is the only dermatophyte able to thrive at 37 C. Tinea capitis caused by T. verrucosum can result in irreversible scarring and alopecia. The analogous clinical infection pattern in adults is sycosis barbae, which corresponds to ringworm in cattle. It is widespread and a well-known occupational disease of cattle keepers.2
Candidiasis

This affects the trunk, often in exposed areas like the abdomen or limbs, causing red patches. It is more common in children than in adults and occurs most frequently in hot climates.2 Dermatophytes of the genera Trichophyton and Microsporum are the most common causative agents.

This is a diverse group of infections caused by members of the genus Candida, especially C. albicans.1 These organisms typically infect the skin, nails, mucous membranes and gastrointestinal tract. Cutaneous and mucosal manifestations of candidiasis can be divided into several distinct clinical syndromes (Table 2). Thirty years ago, supercial fungal infections were common, but systemic fungal infections were not as frequent as today. The incidence of supercial and systemic fungal infection has been increasing because of the increasing

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Table 2 Mucocutaneous Candida infections Disease Oral candidiasis Vaginal and vulvovaginal candidiasis Balanitis Cutaneous candidiasis Clinical appearance Discrete white patches that may conuence on the buccal mucosa, tongue, palate and gingivae Thick vaginal discharge associated with burning, itching and occasional dysuria Small papules or fragile papulopustules on the galns or in the coronal sulcus in men. Infection may spread to the scrotum and inguinal areas Pruritic, erythematous, macerated skin in the intertriginous area with satellite vesicopustules. Pustules break open leaving a red, macular base with a collarette of easily detachable necrotic epidermis Organs most commonly involved: lungs, spleen, kidneys, liver, heart and brain Chronic supercial infections of the skin, nails and oropharynx. Broad range of syndromes involved Causative agent Candida albicans C. albicans; C. glabrata C. albicans C. albicans

Disseminated candidiasis

Chronic mucocutaneous candidiasis

C. albicans, C. tropicalis, C. lustaniae, C. krusei, C. parapsilosis Candida species

incidence of severe diseases (e.g. malignancies or HIV-infection) or immunosuppressant therapies (systemic steroids or chemotherapy).1 In normal populations, supercial skin candidiasis occurs because of a combination of deciency of the skins barrier and an endogenous yeast reservoir. Typically, Candida infection is activated by antibiotic or steroid therapy. Obesity and diabetes mellitus are leading predisposing factors for cutaneuos candidiasis.
Intertrigo

face and upper arms.1 P. orbiculare is also associated with the development of seborrhoeic dermatitis.

Global patterns of supercial fungal infections

The clinical appearance and the causative species of supercial fungal infections vary with geographic region, socioeconomic conditions and habits. Some species of fungi exhibit worldwide distribution, whereas others are restricted to particular continents or geographic regions (Table 3).8 Trichophyton rubrum is the most common cause worldwide for tinea pedis, nail infection, tinea cruris and tinea corporis. Tinea pedis and onychomycosis are becoming more common.4,11 More widespread travel (economic migration and mass tourism), increased ownership of companion
Table 3 Distribution of anthropophilic species of fungi Worldwide Epidermophyton occosum Microsporum audouinii Trichophyton mentagrophytes var. interdigitale T. rubrum T. tonsurans Geographically limited M. ferrungineum: Africa, India, E. Europe, Asia, S. America, T. concentricum: Pacic Islands, Far East, India, Ceylon, N., Central and S. America, T. gourvilii: Central and W. Africa T. megninii: Portugal, Sardinia T. schoenleinii: Europe, Mediterranean, Middle East, S. Africa, sporadically in US T. soudanense: Central and W. Africa T. violaceum: Africa, Europe, Asia

Intertrigo is an inammation of the body folds and can result from bacterial, fungal or viral infection that has developed at the site of broken skin, for example, the chang of warm, moist skin of the inner thighs and genitalia, the armpits, under the breasts, the underside of the belly, behind the ears and between the toes and ngers. It occurs most frequently in overweight subjects, diabetics, patients conned to bed, babies and those who use medical devices like articial limbs that trap moisture on the skin. Several skin diseases predispose to intertrigo, including dermatitis or inverse psoriasis. Candida albicans is the pathogen usually associated with intertrigo.
Tinea versicolor (pityriasis versicolor)

This is a common skin disease caused by the overgrowth of Pityrosporum orbiculare, also named Malassezia furfur. Most adults harbour P. orbiculare on their skin; in a few people, however, its presence results in a harmless skin disease characterised by the development of either hypoor hyperpigmented patches covered with ne scales on the upper trunk. It occurs less frequently on the neck,

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animals, increased use of public sports facilities (especially swimming pools), wearing occlusive training shoes, the increasing incidence of diabetes mellitus and vascular disease, such as arteriosclerosis and an ageing population are contributing factors to the development of dermatomycoses in socially and economically developed countries.1 These are to be seen in addition to well-established risk factors such as familiar disposition, male gender, foot trauma and cigarette smoking.1,12,13 Studies in Europe, Asia and Africa indicate that anthropophilic agents of scalp infections are being eradicated in developed nations and are now more typical of countries with low socio-economic status. The exception is T. tonsurans-related tinea capitis and tinea corporis in North America. In tropical and subtropical countries, infectious diseases of the skin are not just more prevalent than in central Europe; they are more frequent and more distinctive. This is particularly true for certain areas in Asia (especially India) and for the whole continent of Africa. Socio-economic conditions tend to be poorer than in Europe and the Americas and there are more problems with diagnosis and therapy, but most of all, the humid and warm climatic conditions encourage the extensive skin mycoses. In Africa, a large number of HIV infections favour certain fungal infections by reducing the cellular immunity needed in the defence against fungi. The following sections look at the main types and incidence of supercial fungal infections and their associated pathogens based on epidemiological studies (as these are the only data available because there is no requirement to notify dermatophyte infections) by continent and country.
Europe

increases in those agents have been noted in the UK (T. tonsurans) and France (T. soudanense and M. audouinii).14 Tinea capitis mostly affects children aged 37 years of both genders, but recently an increased incidence has been observed in adults and the elderly.14 Eastern Europe seems to be characterised by a dominance of tinea corporis and capitis caused by the zoophilic germ M. canis and a related comparatively high rate of infantile fungal infections. The effects of civil war in some European countries in the 1980s and 1990s resulted in low standards of medical care and outbreaks of M. canis possibly related to increased numbers of feral domestic animals. The end of war and subsequent improvement in standards of living has led to a decline in zoophyte infections and an increase in anthropophylic dermatophyte infections. The incidence of the various fungal species identied in different epidemiological studies is summarised in Table 4 and a wider discussion follows. France. Tinea pedis shows an infectious agents pattern comparable to the one in other states of developed Europe. Plantar dermatophytoses in association with onyxis and intertrigo rank with leading fungal infections mainly caused by T. rubrum. In a large French study, relating to frequency of plantar dermatophytosis, dermatophytes was isolated in 66.6% of patients with interdigital plantar signs. Trichophyton rubrum was isolated most frequently.15 As mentioned above, there has been a signicant increase in the incidence of tinea capitis in Europe, including France. In the more rural regions, e.g. northeast France, dermatophytoses is mostly caused by zoophilic dermatophyte fungi such as M. canis, T. mentagrophytes or T. verrucosum, whereas in urban areas, e.g. Paris, there is a shift toward anthropophilic tinea capitis. Developed urban regions of France as well as the UK are characterised by the largest overall increase in anthropophilic tinea capitis infection. Besides T. tonsurans, T. soudanense and M. audouinii are the main infectious agents causing tinea capitis. This pattern of anthropophilic infections seems to be linked to immigration from sub-Saharan Africa or from the Caribbean.14 United Kingdom. Tinea capitis-causing anthropophilic species predominate also in the urban regions of the UK. Trichophyton tonsurans has been noted as the leading pathogen causing tinea capitis in the UK, comparable to Northern America. Other relevant anthropophilic fungi include M. audouinii and M. rivalieri. The occurrence of these anthropophilic germ-induced infections is statistically related to ethnic groups originating from Africa.

Currently, the most important dermatophytes isolated in Europe are T. rubrum, M. canis, T. mentagrophytes var. granulosum and T. verrucosum. Several of these are believed to have spread from the Mediterranean countries. Other dermatophytes such as M. audouinii, T. soudenense and T. violaceum (causing so-called immigration mycoses), which are endemic in Africa and some parts of Asia, are currently rarely isolated in Europe. However, their incidence may be expected to increase in the future as a result of tourism and migration.2 Trichophyton rubrum is the most frequently isolated dermatophyte in cases of tinea corporis and cruris in developed European countries. There is also a shift towards tinea capitis caused by anthropophilic dermatophytes in urban areas in Europe. The largest overall

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Supercial dermatomycoses worldwide

Table 4 Summary of the European incidence of the most common mycoses identied in these epidemiological studies Lange et al.26 Microsporum canis M. gypseum M. equinum M. cookei Trichophyton mentagrophytes T. mentagrophytes var. granulosum T. mentagrophytes var. interdigitale T. mentagrophytes var. mentagrophytes T. mentagrophytes var. quinckeanum T. rubrum T. verrucosum T. violaceum T. tonsurans T. terrestre T. schoenleinii Epidermophyton occosum 62 Monod et al.23 5 Lehenkari et al.22 Jeske et al.27 23.5 5.3 0.7 0.14 21.6 2.3 6.0 17.8 0.4 3.7 10.4 30.9 10.0 6.9 41.7 0.1 2.3 0.2 7.4 Lupa et al.11

Korstanje21 40.9

Dolenc-Voljc37 46.8

Prohic38 90.4

24.5 7.9 4.9 62.5 4.5 29.6 6.8 2.3 36.7

26

11.4 12

66 1.9

2.4 6 7.7

All values are percentages.

Corresponding to the situation in Europe at large, tinea capitis is a fungal infection that affects especially young children. This has been demonstrated in a study by Hay et al..16 The study shows tinea capitis in school children in south east London and the importance of new guidance to general practitioners on treatment. Tinea pedis and associated tinea capitis seem to be comparable with the characteristics of developed Europe, with T. rubrum and T. mentagrophytes var. interdigitale as the leading dermatophytes. Germany. Trichophyton rubrum accounts for 8090% of all isolated strains in Germany.17 Trichophyton interdigitale (T. mentagrophytes var. interdigitale) and E. occosum are the second and third most frequently isolated agents and tinea pedis and unguium are most frequently diagnosed. The German Mycologic Society estimates the prevalence of onychomycosis to be 12.4%, whereas the incidence of tinea cruris has declined in the last 70 years.12 Investigations in miners indicate that the incidence of tinea pedis and tinea unguium is up to 72.9%1, primarily because of their use of occlusive boots, the warm and humid environment in the mine and shared use of washing facilities.17,18 Two studies of cases of tinea capitis have found that the most prevalent causative agent of tinea capitis was M. canis, followed by T. tonsurans, T. violaceum and T. mentagrophytes.19,20 As a result of an immunisation programme against T. verrucosum in cattle, ringworm should have been eradicated in Eastern Germany. However, inconsistent immunisation of livestock and the removal of the

requirement to notify the disease mean that a further rise in the number of cases in humans is to be expected. Belgium and the Netherlands. In these countries, zoophilic dermatophytes are supplanting anthropophilic strains as the cause of tinea capitis. Samples of scales, pus and hair collected from 435 patients with tinea capitis over a period of 30 years21 have revealed that at the beginning of the period, T. verrucosum was found most frequently, but declined dramatically from the mid-1970s onwards. In contrast, M. canis was found frequently over the years, rising from 9% to 11% of cases in the 1960s to >40% in the 1990s. This change is associated with increased mechanisation in farming and increased numbers of households keeping companion animals. The frequency of T. violaceum has also increased signicantly since the 1970s because of increased immigration from countries such as Italy, Turkey, Morocco and Tunisia.21 Finland. Trichophyton rubrum was the most common species (66% of all positive cultures) isolated from 2101 samples in northern Finland between 1982 and 1990;22 T. mentagrophytes was isolated from 815 samples (26%) and E. occosum from 193 samples (6%). T. verrucosum caused an epidemic among cattle keepers in 19871990, causing 47 infections. Microsporum canis, T. terrestre and T. violaceum isolates were rare. The same species affected both children and adults. Trichophyton rubrum and T. mentagrophytes (T. interdigitale) occurred most frequently (mostly as causative micro-organisms of foot infections) in patients aged 4145 years of age. Epidermophyton occosum usually affected the toes and or the groin in

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predominantly men aged 2125 years. Overall, there was a slight increase in tinea pedis during the study period and a decrease in tinea cruris. Switzerland. A survey of dermatophyte infections in the Lausanne area during an 8-year period showed that 510% of consultations in dermatology concern mycotic infections. Trichophyton rubrum was the most frequently isolated species (at 62.5%) followed by T. mentagrophytes (24.5%) and M. canis (5.0%). Less frequent isolates included E. occosum, M. langeroni, M. gypseum, T. soudanense, T. violaceum, T. verrucosum, T. gourvili and T. tonsurans.23 Italy. Panasiti et al. conducted a retrospective study of dermatophytes causing supercial mycoses among outpatients at one centre in Rome between 2002 and 2004.24 With 3160 patients studied, the most frequently isolated dermatophyte was M. canis, followed by M. audouinii. This species was identied as an emerging species, being the second most frequent aetiological agent of tinea capitis and the fourth of tinea corporis in this study. It should be noted that in the Mediterranean region especially in Italy M. canis seems to be endemic in feral cats. sk between 1984 and 1995 Poland. A survey in Gdan showed that in 1544 patients, the most common types of dermatophytoses were tinea cutis glabrae (32.3%), tinea pedis (24%), onychomycosis (16.5%), tinea capitis (11.7%), tinea inguinalis (8.9%) and tinea manus (4.0%).25 Lange et al. reported that in children and sk between 1999 and 2001,26 the adolescents in Gdan most frequent pathogens identied were M. canis (62%) and T. rubrum (12%) and the most common dermatophytoses were tinea cutis glabrae (42%) and tinea capitis (30%) primarily due to M. canis. Glabrous skin lesions were most frequent in children aged 815 years; the incidence of scalp lesions peaked in children aged 47 years and tinea pedis, mostly caused by T. rubrum and T. mentagrophytes var. granulosum, was observed mainly in adolescents (aged over 12 years). Onychomycosis was highly uncommon in children and was caused mainly by T. rubrum. Among 7393 dermatophytoses identied in central Poland during 19871996, there were 2204 (29.8%) cases of tinea cutis glabrae.27 Causative organisms included M. canis (23.5%), T. mentagrophytes var. granulosum (21.6%), T. rubrum (17.8%), T. tonsurans (10.4%), E. occosum (7.7%), T. mentagrophytes var. quinckeanum (6.0%) and M. gypseum (5.3%). In the same population, Lupa et al.11 reported 2025 (27.4%) cases of tinea pedis. Causative organisms included: T. rubrum

(41.7%), T. mentagrophytes var. granulosum (30.9%), T. mentagrophytes var. interdigitale (10.0%), E. occosum (7.4%) and T. mentagrophytes var. quinckeanum (6.9%). The incidence of tinea pedis increased substantially between 1994 and 1996. Russia. Several epidemiological studies conrm a higher number of toenail infections and a more frequent occurrence of severe toenail diseases, including mixed fungal infections with yeasts and moulds, in Russia compared to developed countries in Western Europe. The prevalence of tinea pedis has been reported as at up to 83% in the Russian population.28 Khaldin et al. found that in the Russian Federation, T. rubrum was the predominant causative agent of dermatomycoses, accounting for 6575% of cases, whereas Candida spp. were commonly detected in skin fold infections.29 These ndings correlate with a study by Ja rv et al. concerning toenail onychomycosis in Estonia from 2004,30 in which nearly 70% of pathologic nail changes were caused by dermatophytes, 10% by yeasts and 7% by moulds. Trichophyton rubrum was the most-frequently isolated pathogen. Mixed infections were found in 6% of patients. Furthermore, the incidence of tinea corporis and tinea faciei is also thought to be high.30,31 Tinea pedis has been found not only in elderly or sick people but also in a signicantly high degree in the working population. This is shown in a Russian study of foot mycoses in workers at metallurgical plants. Trichophyton rubrum (71.3%) and T. interdigitale (28.7%) were the main pathogens. 18.3% of patients had mixed infections with C. albicans. It was notable that Trichophyton occurred as a complication in some cases.32 Vakulova et al. have also reported a high incidence of fungal skin and nail infections caused by Candida ssp. in Russian submariners.33 As in other parts of Eastern Europe, zoophilic infections are more common in rural regions; M. canis, T. mentagrophytes and T. verrucosum are the predominant zoophilic pathogens. The incidence of T. verrucosum and T. mentagrophytes continued to rise until the late 1980s.34 Effective antimycotic therapy has reduced the number of trichophytoses in recent years. In Armenia, an epidemiological study showed a reduction in the number of trichophytosis patients.35 Favus caused by T. schoenleinii, T. violaceum or M. gypseum is now found only rarely, in areas with low social conditions.36 Slovenia. Results from patients with suspected dermatophytoses in Slovenia for the period 19952002

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have shown that among 42 494 samples, M. canis was isolated most frequently (46.8%) followed by T. rubrum (36.7%), T. mentagrophytes var. interdigitale (7.9%) and T. mentagrophytes var. mentagrophytes (4.9%). The most common dermatophyte infections were tinea corporis, onychomycosis, tinea pedis and tinea faciei.37 Bosnia and Herzegovina. Tinea capitis was found in 241 (34.1%) patients in Sarajevo between 1997 and 2006;38 causative agents were identied in 209 (29.6%) cases. Zoophilic dermatophytes (91.8%) prevailed over anthropophilic (7.2%) and geophilic (1.0%) dermatophytes. Microsporum canis was isolated most frequently (90.4%), followed by T. schoenleinii (2.4%) and T. violaceum (1.9%). Most patients were male (56.5%) and aged under 10 years (52.6%). Zoophilic dermatophytes were most commonly recovered from children and adolescents with tinea capitis, tinea corporis and tinea faciei. Anthropophilic species were identied mostly in adults with tinea pedis, onychomycosis and tinea cruris. Interestingly, rates of M. canis infection declined during the study period, while infections caused by T. rubrum increased in frequency possibly as the war came to an end and quality of life began to improve again.
Asia and Australia

are also found in Asia, especially India. Trichophyton concentricum causes tinea imbricata. The prevalence of tinea pedis in Asia is similar to that in Europe (approx. 20%); it is also common in Australia. Tinea corporis and capitis are frequently found in children and adolescents. The incidence of the various fungal species identied in epidemiological studies is summarised in Table 5 and the signicance for the prevalence of associated dermatomyces in different countries is discussed below. Turkey. A study performed in a Turkish University Hospital during 20012002 found the prevalence of dermatophytoses to be 7.34% (68 out of 926).39 Trichophyton rubrum was the most frequently isolated dermatophyte (56%), followed by T. mentagrophytes (38%), T. violaceum, T. verrucosum, M. canis and E. occosum. Tinea pedis (47%) was the most common dermatophytosis, followed by tinea unguium (29%), tinea inguinalis (15%), tinea corporis (7.4%) and tinea capitis (1.6%). S as maz et al. examined the frequency and spectrum of supercial fungal infections among 925 consecutive Turkish soldiers admitted to the dermatology outpatient clinic in Northern Cyprus.40 Supercial mycotic infections were found in 185 soldiers (20%), of whom 151 (61.6%) had dermatophytosis, 32 (17.3%) had tinea versicolor and two (1.1%) had candidiasis. A similar study was conducted among workers in a Turkish textile factory an important industry in that country.41 Supercial mycoses were found in 73 (16.9%) workers; of these, 56 (76.7%) cases were dermatophytoses and eight (11.0%) were pityriasis versicolor. No causative

In Asia, T. rubrum and T. mentagrophytes are the most commonly isolated pathogens, causing tinea pedis and unguium, as is the case in Europe. In contrast to Europe, the next most commonly isolated pathogen is T. violaceum, the causative agent of tinea capitis and corporis. Microsporum ferrugineum and T. concentricum

Table 5 Summary of the Asian incidence of the most common mycoses identied in these epidemiological studies Microsporum canis M. audounii M. gypseum Trichophyton mentagrophytes T. rubrum T. verrucosum T. violaceum T. tonsurans T. schoenleinii T. asahii T. mucoides T. inkin Epidermophyton occosum Candida spp.

Prohic C elik E Lari Tao-Xiang Kim Singal et al.38 et al.41 et al.42 et al.46 et al.49 et al.43 Min48 1.5 15.1 7.5 11.3 13.2 5.7 28.3 34 3 3 3 38 9 10 62.1 20.3 14.9 1.5 15.1 14.0 65

38 56 1.5 1.5

42.9 57.1

29.4 43.9

18 9

All values are percentages.

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B. Havlickova et al.

agent could be identied in nine (12.3%) workers. T. rubrum (57.1%) and T. mentagrophytes (42.9%) were two of the most frequently isolated dermatophytes. The study emphasised that textile workers should be considered as a risk group for supercial mycoses, especially tinea pedis. Iran. The characteristics of dermatophytoses among children in an area south of Tehran were reported by Lari et al. 382 children aged 16 years with suspected dermatophytic lesions were examined between 1999 and 2001.42 The incidence rate of dermatophytoses was 6.6 per 100 000 person-years. Trichophyton violaceum (28.3%), M. canis (15.1%), E. occosum (15.1%), T. rubrum (13.2%), T. mentagrophytes (11.3%), M. gypseum (7.5%) and T. verrucosum (5.7%) were the most frequent isolates. Tinea capitis (39.6%) was the most common dermatophytosis, followed by tinea corporis (30.2%), tinea faciei (18.9%) and tinea manuum (7.5%). India. In northern India, anthropophilic dermatophytes are the predominant pathogens causing tinea capitis. In a 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 family history of tinea capitis. Trichophyton violaceum (38%), M. audouinii (34%), T. schoenleinii (10%) and T. tonsurans (10%) were the most commonly isolated pathogens.43 Tinea capitis caused by T. violaceum is endemic in south India. A study conducted in 1978 suggested that trauma to the scalp caused by ritual shaving may be one explanation for this. Twenty one cases of tinea capitis were found in boys aged 1017 years in Purasawalkam, Madras, who were shaved consecutively by the same barber. The razors were cleaned only in soap and water.44 Unlike in Europe, tinea pedis is comparatively rare in India, especially in the poorer areas. As in Europe, the most important causative agents are T. rubrum, T. interdigitale and E. occosum.45 China. Tao-Xiang et al. conducted a 1-year analysis of dermatomycoses in the Lanzhou district of northwestern China.46 In 1443 suspected fungal infections, the fungi were isolated in 221 cases, the most frequent being T. rubrum (43.9%) T. mentagrophytes (29.4%) and Candida spp. (14.0%). The incidence of tinea pedis, onychomycosis and tinea manuum was 38.7%, 27.8% and 13.5% respectively. Tinea capitis of children, primarily caused by T. violaceum, is common in western China. Strains

found in rural communities of this region tend to be different from those found in other regions in the country, indicating that dermatophytes in former rural societies must have migrated extremely slowly.47 In developed 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 2002, M. canis was identied as the main pathogen in 65% of cases. The anthropophilic dermatophytes T. violaceum (18%) and T. tonsurans (9%) were also important species.48 Korea. Tinea pedis is the most common dermatomycosis in Korea and Kim et al. have shown that the most common infectious agents in foot mycoses are T. rubrum, other Trichosporon spp. and Candida spp.49 Jang et al. have reported that the prevalence of tinea corporis is increasing in Korea,50 but that it varies according to life style and regional characteristics. Dermatophytes were isolated in 73 out of 105 cases of tinea corporis; T. rubrum (58 cases), T. mentagrophytes (eight cases) and M. canis (ve cases) were the most common causative agents. Singapore. Cutaneous fungal infections are common in Singapore. Between 1999 and 2003, 12 903 cases of supercial fungal infections were seen at the National Skin Centre.51 A majority of patients (72.3%) were male. The most common conditions were tinea pedis (27.3%), pityriasis versicolor (25.2%) and tinea cruris (13.5%). Tinea capitis is uncommon in Singapore. Trichophyton rubrum was the most prevalent fungal pathogen isolated, except in cases of tinea pedis, where T. interdigitale was the most frequently isolated organism. Candida infections were common (n = 1430) and were manifested as candidal intertrigo. The incidence of onychomycosis has increased over the past 5 years. Dermatophytes remain the most commonly isolated fungal pathogens isolated in toenail onychomycosis, whereas Candida spp. accounted for the majority of isolates in ngernail onychomycosis. Japan. In an epidemiological investigation to determine the prevalence and circumstances of untreated and unsuspected tinea pedis and onychomycosis, the prevalence of occult tinea pedis was 25%. Fifty nine per cent of those patients had tinea unguium simultaneously.52 Australia. In Australia, there is a high incidence of tinea pedis. In a randomised sample of 2491 students with

10

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Supercial dermatomycoses worldwide

conrmed tinea pedis53 an age- and gender-adjusted prevalence of 5.2% was found; increasing with age from 2.1% in 46 year-old to 9.7% in 1618 year-old individuals. A higher proportion of males (6.0%) had tinea pedis than females (4.3%). Trichophyton mentagrophytes and T. rubrum were the most common dermatophytes isolated on culture. Only 20 isolates of T. violaceum, associated with tinea capitis and tinea corporis, have been identied in a 32-year period in Melbourne.54 As observed in Europe and America, infection seems to occur almost exclusively in African immigrants, not in the indigenous population.
Africa

Table 6 Summary of the African incidence of the most common mycoses identied in these epidemiological studies Hay Enweani Ellabib Abu-Elteen et al.55 et al.58 et al.60 & Malek61 Microsporum canis M. audouinii 46.8 M. gypseum Trichophyton mentagrophytes 25.5 T. rubrum T. verrucosum T. violaceum T. tonsurans T. schoenleinii Epidermophyton occosum Candida spp. 8 46.8 25.5 21.3 3 14 44 2.1 4.3 7 10 4.0 20.1 0.5 32.7 28.6 2.0 1.0 11.1

Fungal infections are among the most commonly diagnosed skin diseases in Africa. Both the pathogen spectrum and the clinical manifestations are totally different from those seen in Europe. The anthropophilic dermatophyte T. audouinii is the most prevalent pathogen, together with T. violaceum and T. soudanense. Trichophyton gourvilii is an endemic, partly geographically restricted, anthropophilic dermatophyte, and its predominance in tinea capitis is characterised by patches of grey hair. The black dot type, caused by the endotrichus fungi T. tonsurans and T. violaceum (also endemic in Africa), is widespread. Favus, caused by T. schoenleinii, has occasionally been observed. This pathogen was a widespread trigger of family epidemics in Europe in the 18th century. Today, it has almost disappeared from developed European countries but is found in the densely populated areas of Africa. Trichophyton soudanense seems to be a common cause of tinea capitis in north-western tropical Africa. Trichophyton rubrum and T. mentagrophytes are less common and are associated with tinea corporis and, in particular, tinea cruris (or tinea axillaris in women). In 2005, Hay et al. estimated the overall incidence of tinea in Sub-Saharan Africa to be 78 million.55 Notably, tinea pedis and unguium are very uncommon in rural areas in Africa probably because of the lack of risk factors. A large part of the population walks bare foot; diabetes mellitus and adipositas are rare in these areas. Tinea faciei and barbae are caused by dermatophytes, including M. gypseum and M. ferrugineum. In some regions of Africa, T. rubrum is rare. Besides dermatophytoses, pityriasis versicolor is a typical dermatological diagnosis for African adolescents. Humidity seems to favour this endogenic infection. Europeans travelling to Africa often develop this disease. Candida infections are also highly prevalent given the high incidence of HIV infections. Some data on inci-

All values are percentages.

dence of the various fungal species are summarised in Table 6. South Africa. The incidence of dermatoses in 246 adults with HIV at a South African clinic was studied over a period of 1 year.56 The most common cutaneous disease manifestation was herpes zoster (19%) and tinea corporis was found in 7% of patients. Opportunistic fungal infections, such as candidiasis, were present at 3%. In 100 children (mean age of 4.6 years) in Kwa-Zulu Natal, dermatologists identied T. violaceum in 90% of positive cultures, making it probably the most common cause of tinea capitis in South Africa.57 The most common clinical manifestation was the black dot type, seen in 50% of patients. Nigeria. A total of 188 (13.4%) mycotic infections were identied in a study among 1400 school children in Ekpoma, Nigeria.58 The causative agents included M. audouinii in 88 cases (46.8%), T. mentagrophytes in 48 (25.5%), T. rubrum in 40 (21.3%), T. tonsurans in 4 (2.1%) and E. occosum in 8 (4.3%) patients. Malawi. In a survey conducted between 1987 and 1989, Po nnighaus et al.59 looked at the spectrum of dermatophytes in a northern Malawi population. Between 1.5% and 2.5% of the population were diagnosed with tinea faciei, corporis or cruris. The authors noted the rarity of T. rubrum (around 1%) and the predominance of M. audouinii (57%) in this part of Africa. Epidermophyton occosum was the most common isolate (56%) from the genital area. Libya. In a study of the prevalence of skin infections and their causative agents in 1180 patients with a

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B. Havlickova et al.

conrmed mycotic infection, tinea corporis was diagnosed in 45.9% of cases (85% in children aged less than 15). Other conditions included pityriasis versicolor (27.8%), candidiasis (13.4%) and tinea pedis (8.1%). Trichophyton violaceum was the most common aetiological agent, responsible for 44% (300 cases) of dermatophyte infections. Malassezia furfur was found in 27.8% of cases, T. rubrum in 13.8%, C. albicans in 10%, M. canis in 8.1%, E. occosum in 6.6% and T. mentagrophytes in 3.1%.60 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 dermatophytes isolated were T. mentagrophytes, E. occosum, T. rubrum and M. canis. Tinea pedis (35% of all cases) and cruris (10%) are found more frequently during the summer months, whereas tinea capitis (23% of all cases), corporis (10%) and unguium (22%) are more frequent during the spring and winter.61 There is evidence that the increasing prevalence of T. rubrum is because of immigration from Mediterranean countries. Tinea pedis (caused by T. mentagrophytes) is most prevalent in older farmers. Tinea capitis is more common in children and more common in girls because girls tend to have long hair, which facilitates contact and spread of fungal species.
Americas

and vector, leading to specic clinical presentations and compliance difculties for treatment.62 American teams have taken T. tonsurans infections to Europe and Asia. This is another example of traditionally geographically conned pathogens spreading to new areas. Conversely, T. violaceum and T. soudanense, which are causes of tinea capitis in parts of Africa and West Asia, have only rarely been reported to cause dermatophytoses in the USA. However, sporadic cases provide evidence for the emergence of these organisms as a result of changing population demographics.63 USA. An epidemiological survey of supercial fungal diseases64 found that T. rubrum was the most commonly isolated dermatophyte species. Trichophyton tonsurans was more common in tinea capitis, and equally common in tinea corporis and cruris. Dermatophytes appeared in approximately 95% of tinea pedis isolates and 82% of onychomycosis isolates. Candida albicans (7%) and non-dermatophyte moulds (11%) played only a minor role in onychomycosis. These ndings were in general agreement with other major epidemiological studies performed outside the USA and conrm that dermatophyte fungi are responsible for most supercial fungal infections. Foster et al. carried out a survey of cutaneous fungal infections between 1999 and 2002.65 Dermatophytes were the most commonly isolated fungal organisms, except suspected nger onychomycosis caused by Candida spp. Trichophyton rubrum was the most prevalent fungal pathogen (70%) and increased incidence of this species was observed in nger and toenail onychomycosis, tinea corporis and tinea cruris, tinea manuum and tinea pedis. In the rst half of the 20th century, the predominant causative agent of tinea capitis was the anthropophilic species M. audouinii. By the 1980s, however, T. tonsurans had become the most common cause and today, more than 95% of tinea capitis cases are because of T. tonsurans.65 Canada. The incidence of T. tonsurans in conrmed tinea capitis cases increased from 9% in 1985 to 76% in 1996.66 Prior to this, the more common agents were T. verrucosum, M. canis and M. audouinii. This infection pattern is most common in children of both genders under 14 years of age. Subjects are signicantly more likely to live in urban than in rural areas. Brazil. A 5-year study examined dermatophytoses in 137 children below the age of 12 with clinically

The most commonly observed fungal species in the Americas are T. rubrum, T. tonsurans and T. mentagrophytes. Some data on the frequency of the various fungal species are summarised in Table 7. A dramatic increase in T. tonsurans infections has been reported in the USA.8 The term tinea corporis gladiatorum was created because T. tonsurans has high attack rates in teams of wrestlers, high-level judo players and in other combat sports. This may be because of a unique fungal aetiology and the nature of the reservoir

Table 7 Summary of the incidence of the most common mycoses identied in epidemiological studies in the Americas Brilhante et al.68 Microsporum canis Trichophyton mentagrophytes T. rubrum T. tonsurans Epidermophyton occosum 7 6.2 49.6 34.4 Welsh et al.69 7.1 23.7 45 21 2.5

All values are percentages.

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Supercial dermatomycoses worldwide

diagnosed tinea.67 Male children aged 212 years were the most often affected. Tinea capitis (78 cases, 56.9%), mainly caused by M. canis (46 cases), was the most common clinical form, followed by tinea corporis (43 cases, 31.3%) mainly caused by T. rubrum (17 cases) and tinea cruris (10 cases, 7.2%) caused by T. rubrum (ve cases). In another study with 2297 patients with suspected clinical lesions of dermatophytosis,68 534 (23.2%) patients were tested positive for dermatophytes. Trichophyton rubrum (49.6%), T. tonsurans (34.4%), M. canis (7%) and T. mentagrophytes (6.2%) were the most prevalent species. Correlating the species with the anatomical localisation revealed that T. tonsurans was the most frequent isolate in scalp lesions (73.9%), whereas T. rubrum was the main species involved in body lesions (72.8%). Mexico. Welsh et al. have published data from Monterrey involving 2397 cases of dermatophytosis from supercial cutaneous lesions between 1978 and 1990.69 Seven hundred and twenty-six (30.2%) cases of tinea pedis, 613 (25.6%) of tinea unguium, 441 (18.4%) of tinea capitis, 395 (16.4%) of tinea corporis and 222 (9.3%) of tinea cruris were observed. The most commonly isolated dermatophytes were T. rubrum (45%), T. mentagrophytes (23.7%), T. tonsurans (21%), M. canis (7.1%) and E. occosum (2.5%). Most cases of fungal infections were observed in the warmest months of the year and were equally distributed among men and women, except for tinea cruris, which was more prevalent in men.

increasing prevalence of obesity and diabetes mellitus and an ageing population. Microsporum canis is a prevalent agent of tinea capitis in the developed world and this could be related to mass tourism to endemic regions (such as the Mediterranean area) and the close association between humans and companion animals. Several dermatophyte species are geographically limited. Trichophyton violaceum is endemic in certain parts of Eastern Europe, Africa, Asia and South America, but not in North America. Trichophyton soudanense is a common and endemic cause of tinea capitis in northwestern tropical Africa and West Asia. The sporadic appearance of both in Western Europe and the USA provides evidence for the ongoing evolution of dermatophytosis epidemiology in relation to international travel, immigration and shifts in population demographics.

Conict of interest
Dr B Havlickova and Dr M Friedrich are employees of Intendis GmbH; Dr V Czaika has a consultancy agreement with Intendis GmbH.

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Conclusion
Most mycoses are caused by fungi that reside in nature, but there appears to be a considerable interand intra-continental variability in the incidence of fungal infections throughout the world. Furthermore different geographical locations favour different infection patterns. Trichophyton rubrum, T. interdigitale (mentagrophytes var. interdigitale), M. canis, M. audouinii, T. tonsurans and T. verrucosum account for most dermatophytoses globally, but the attack rates and incidence of specic mycoses can vary widely. The highest incidence of T. rubrum was reported in Europe, whereas T. mentagrophytes was more commonly reported in Asia. Increasingly frequent tinea pedis caused by T. rubrum and T. interdigitale (mentagrophytes var. interdigitale) infection seems to be a characteristic of highly developed countries with booming sport and tness facilities,

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