Dermatophytosis, Trends in Epidemiology and Diagnostic Approach
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Curr Fungal Infect Rep DOI 10.1007/s12281-015-0231-4 CLINICAL MYCOLOGY LAB ISSUES (K LAGROU, SECTION EDITOR) Dermatophytosis, Trends in Epidemiology and Diagnostic Approach Marie-Pierre Hayette1 & Rosalie Sacheli 1 # Springer Science+Business Media New York 2015 Abstract Dermatophytes are amongst the most common fun- Introduction gal agents causing superficial skin infections. The epidemiolo- gy of dermatophytosis has changed during the last century Dermatophytes are a group of filamentous fungi referred to as under the influence of socioeconomic factors, modern life, in- the ringworm fungi. They are keratinolytic and invade tensification of travel, migration of populations from the south- keratinized tissues causing mostly superficial infections in- ern to the northern hemisphere. As result, Trichophyton rubrum volving the skin, hair and nails. They are amongst the most has become the most frequent species worldwide, causing common causes of skin disease in the world, and the real mainly tinea pedis and tinea unguium, while Microsporum prevalence is probably underestimated. Onychomycosis is canis is still the main agent in tinea corporis and capitis in the most common nail disorder in adults causing about 50 % Mediterranean countries. However, the prevalence of of all nail diseases. Large-scale studies on onychomycosis anthropophilic dermatophytes causing tinea capitis in young conducted in the US and Canada in the late 1990s showed a children is increasing overall in the big cities of Europe and prevalence rate of 14 % [1]and8%[2], respectively. In America, causing epidemics and becoming a public health con- Europe, the prevalence rate is even more variable: 2.7 % in cern. This review summarizes the current status of dermato- the UK [3] and Spain [4], 8.4 % in Finland [5], 12.4 % in phyte infection in Europe, Africa, Asia and America and gives Germany [6••] and 16.8 % in France in a more recent study an overview of the most recent molecular methods currently [7]. The Achilles project, the largest survey on foot disease available for the laboratory diagnosis of dermatophytosis. undertaken in Europe, conducted in 20 European countries during 1997–1998, showed a particularly high prevalence of fungal foot disease and onychomycosis which accounted for Keywords Dermatophytosis . Dermatophytes . Tinea 40.6 % and 28 %, respectively (data extracted from study II, epidemiology . Molecular methods . Diagnosis including clinical and mycological examination of patients consulting a dermatologist) [8]. This survey was divided into two studies: in the first, patients visiting a general practitioner or a dermatologist were clinically checked for foot disease, and in the second, only patients visiting a dermatologist were examined for foot disease and a sample taken for culture. However, patients consulting a dermatologist for foot disease This article is part of the Topical Collection on Clinical Mycology Lab Issues were not excluded from the study, creating an inclusion bias, in contrast to north American studies which excluded this * Marie-Pierre Hayette population [1, 2]. [email protected] Dermatophytosis or infections due to dermatophytes are called tinea according to the site of infection as for example tinea corporis, involving the arms, trunk and legs, tinea capitis 1 National Reference Center for Mycosis, Department of Clinical Microbiology, University Hospital of Liège, Domaine du Sart Tilman (TC), involving the scalp, and tinea pedis involving the foot. B23, Avenue de l’Hôpital, 1, 4000 Liège, Belgium In some cases, a misdiagnosis followed by inappropriate Curr Fungal Infect Rep topical use of corticosteroids results in an atypical clinical Trends in Epidemiology presentation (tinea incognito) making the diagnosis more dif- ficult. Complications such as bacterial secondary infection Evolution of Dermatophytosis in European Countries and allergies can also complicate an unrecognized chronic tinea [9, 10]. Depending on the climate and culture, the picture During the last 100 years, the dermatophyte spectrum has can differ: tinea pedis and onychomycosis are the most prev- markedly changed over the world with differences depending alent clinical forms in Western countries while TC and tinea on the geographic area and other factors such as immigration. corporis are the most frequent forms in tropical areas. For a The most common dermatophytosis and dermatophytes in- few years, small epidemics of TC due to anthropophilic der- volved according to the country are summarised in matophytes have been emerging in different European coun- Table 1. In central and northern Europe, the example of Ger- tries [11, 12]. many, which has been widely reviewed by Seebacher et al. Dermatophytes are divided into three closely related [21••] and Nenoff et al. [16••], shows that the predominance of genera: Epidermophyton, Trichophyton and Microsporum. E. floccosum and M. audouinii as causal agents of tinea The main characteristic of these fungi, with the exception corporis and TC, respectively, in the 1920s has been progres- of keratinophily, is their membership of a group that de- sively replaced by that of T. rubrum which since the 1950s has pends on their normal habitat: geophilic dermatophytes are been the most prevalent dermatophyte in Europe, causing naturally present in the soil, zoophilic in animals, and mainly tinea pedis and tinea unguium. This species has anthropophilic in humans. The fungal pathogens that infect evolved since the nineteenth century as a cause of chronic humans belong mostly to the second and third groups, tinea corporis from the endemic areas in South Asia [22]. geophilic dermatophytes being more rarely involved in Since the 1950s it has progressively replaced anthropophilic human disease. Zoophilic and anthropophilic dermato- T. interdigitale as the aetiological agent in tinea pedis and phytes evolved from a geophilic origin, with the unguium throughout Europe [21••]. This trend is particularly anthropophilic dermatophytes being the most highly spe- marked in northern Europe. A retrospective study performed cialized group. They rarely infect other animals and they in Stockholm (Sweden) found that T. rubrum was the main are also restricted to some body parts. Some species in- causal agent of fungal skin infections being associated with cluding Microsporum audouinii, Trichophyton tonsurans 83 % of infections [23]. In a large survey performed by the and T. soudanense mostly cause TC and are rarely isolated Mycology Reference Laboratory, Bristol, UK, from 1980 to from other body sites. Other species are responsible most- 2005, T. rubrum was the most frequently isolated dermato- ly for onychomycosis; these include T. rubrum which is phyte (70 % in 2005), followed by T. interdigitale (20.8 %) the main agent, followed by T. interdigitale. Finally, [24]. In Germany this species is responsible for 91 % of Epidermophyton floccosum infects only the skin. onychomycosis [16••]. In Belgium, T. rubrum has been iso- The dermatophytes normally develop in the dead part of lated from nails in 76 % of onychomycosis and T. interdigitale keratinized tissue of the stratum corneum, within and around in about 22 % (personal data, Belgian National Reference hair and in the nails [13••]. In these tissues, growth is asso- Center, Liège; 2012 annual report). In Poland, T. rubrum ciated with the production of hyphae and arthroconidia, this and T. mentagrophytes represented 90 % of all dermatophytes characteristic being used as a diagnostic feature. The patho- isolated from superficial fungal infections for the period genicity of dermatophytes is associated to different factors 2005–2010 with, however, a less marked predominance of including the production of keratinolytic enzymes [14, 15], a T. rubrum [25]. In a survey in Slovakia conducted during the genetic predisposition and the presence of host factors period 1994–1999T. rubrum accounted for 81.61 % of all [16••]. Numerous host factors have been associated with dermatophytes isolated [26]. tinea pedis and onychomycosis such as circulatory disorders, This predominance of T. rubrum suggests a great capacity diabetes mellitus, ichthyosis, psoriasis, disorders affecting of this species to spread as attested by the findings of recent cellular immunity, to the extent that onychomycosis is now molecular studies showing that some strains of T. rubrum have considered to be a predictor of diabetic foot syndrome [17]. a significantly higher capacity to spread than others [27]. The The prevalence of onychomycosis in diabetics is higher than most common source of infection is the private bath that is in the normal population, with high prevalence rates of, for contaminated by family members, with vertical transmission example, 20 % in Denmark (20 %) and 51 % in Japan [18, being more common than horizontal transmission [16••]. 19]. Indeed, due to the increasing number of diabetics in the However, other factors may explain the rise of this species. world [20], it is likely that the prevalence of onychomycosis First, the evolution of a life-style marked by the increasing use and tinea pedis will continue to rise in the future. of sports facilities including public pools, fitness studios and This review considers the recent changes in epidemiology martial arts facilities where the main sources of transmission and the new diagnostic tools applied to the laboratory diagno- are changing rooms, showers and mats. Another factor is the sis of dermatophytes. use of occlusive footwear which causes humidity leading