Introduction

Dermatophytes are a group of filamentous fungi prone to infect keratin-rich tissues, i.e., skin, nail and hair; this feature leading them to be designated as keratinolytic fungi.

The discovery of hyphae of dermatophytes in clinical materials of tinea in 1830s was the beginning of medical mycology study, which led to numerous great discoveries and rapid progress in the past century [1, 2]. Till today, it has been recognized that dermatophytoses are the most common fungal infections worldwide, affecting 20–25 % of the world population [3, 4]. An important perspective of dermatophytes is that they experienced great changes in the past 100 years [4, 5]. Factually, the evolution of dermatophytes is driven by their ecology, reproduction, host adaption and pathogenicity, as well as population migration and socioeconomic status.

Dermatophytoses, infections caused by dermatophytes, are also called ringworms or tinea and are usually clinically classified according to the infectious sites: tinea pedis and tinea manuum refer to dermatophytosis of the feet and hands, and tinea cruris to lesions of inguinal, pubic, perineal and perianal areas, whereas tinea corporis affects the glabrous skin excluding the above-mentioned areas, tinea unguium (onycomycosis) the nails, tinea barbae the facial area of beard men and tinea capitis the scalp [6]. Considering the similar fungal spectrum of tinea pedis, tinea manuum, tinea barbae, tinea corporis and onychomycosis, we can summarize all these diseases into two classes. The first class comprises all infections on glabrous skin and nails, with Trichophyton rubrum and Trichophyton interdigitale as the predominant pathogens, and the second class is the hair infection, with Microsporum canis, Trichophyton tonsurans and Trichophyton violaceum as the major pathogens, with variations in their respective frequency with geographic locations and population [4, 5]. In this article, we give an overview of dermatophyte evolution and then introduce the most common human/animal pathogenic dermatophytes. The aim is to get a comprehensive understanding of these organisms and prospect the trends of their changes in future.

History and Taxonomy Evolution of Dermatophytes

The first dermatophytic infection case, kerion, was recorded around 30 A.D in Roman and described as a suppurative infection on scalp, which suggested this organism has lived with human beings for thousands of years [1, 7]. However, due to lack of effective tools of observation, this kind of damage was named as tinea or ringworm because of its clinical appearance, but it was not related to microorganism. The etiological agent of tinea capitis, Trichophyton schoenleinii, was discovered around 1830s, in crust of favus by Robert Remark, Johann Lucas Schoenlein and David Gruby, which was regarded as the start of medical mycology [1, 7, 8]. In 1886, Paul Grawitz and Emile Duclaux isolated some dermatophytes in pure cultures independently [1, 8]. Henceforth, Microsporum audouinii, Trichophyton mentagrophytes, T. tonsurans and Epidermophyton floccosum were successively reported on either the basis of the appearance of clinical materials or described under the microscope [1, 2, 7]. At the beginning of the twentieth century, Raymond Sabouraud took advantage of the newly developed culture medium for isolation, identification and maintenance of dermatophytes, and established the taxonomic criteria for these fungi. He integrated the mycological and clinical aspects into a comprehensive concept, and classified the dermatophytes into four genera, Achorion, Microsporum, Trichophyton and Epidermophyton [1, 9, 11]. Due to his great contribution, Sabouraud was regarded as “the one man who truly revolutionized our concepts of dermatophytes and who immeasurably contributed to the development of medical mycology” [7]. Dermatophytes were described and categorized by their vegetative structure, their conidia and their anamorph/teleomorph state. The genus name Achorion was deleted in 1934 by Emmons, Sabouraud’s student, and the other three genera reserved till today [10, 11]. Due to the unstable characteristics and too much unrelated factors involved, a new genus/species was very easily reported; in 1935, Dodge introduced 118 species of dermatophytes in his book Medical Mycology which reflected at some extend the confusion of dermatophyte denomination at the first half of the twentieth century [1, 7]. In addition, some authentic strains are now missing, and precise taxonomy of the first reported species is not available today.

Since 1980s, molecular methods made taxonomy of organisms much more plausible and clear. Yvonne Graser, Koichi Makimura, Sybren de Hoog and others dedicated great contribution to this work, and in 2011 the Amsterdam Declaration on Fungal Nomenclature was adopted promoting the idea of “one fungus one name” to clarify the nomenclature of fungi though this new system still keeps some limits [12–14]. Many molecular methods were applied for strain or species identification and taxonomy of dermatophytes, e.g., random amplification of polymorphic DNA (RAPD), PCR fingerprinting, amplified fragment length polymorphism (AFLP), microsatellite markers, single-strand conformation polymorphism (SSCP) and sequencing of one or multiple loci [13]. Factually, taxonomy of these fungi will change inevitably with the development of scientific techniques and keeps dynamic at present [14]. In the newly taxonomic tree, Sybren de Hoog et al. (unpublished data) classifies dermatophytes into six clades based on multilocus genetic analysis, Trichophyton, Epidermophyton, Nannizzia, Microsporum, Lophophyton and Arthroderma.

Evolution of Dermatophytes Before 1980s

The spectrum of dermatophytes has experienced great evolution in the first half of the twentieth century and changed by geography and population. From 1930 to 1950, M. audouinii and T. schoenleinii were the predominant agents of tinea capitis in British islands, Northern and Western Europe and America, while T. mentagrophytes was the main agent for tinea pedis and tinea corporis [15]. It is worth noting that frequency of tinea pedis increased dramatically along with the global migration after the World War II. In contrast, frequency of tinea capitis has declined greatly due to the advent of griseofulvin in the mid of 1950s and improved hygiene [4, 5]. Trichophyton rubrum was very rare in Europe before 1940s [15].

Since 1950s, the frequency of M. audouinii and T. schoenleinii in British islands, North and Western Europe declined along with an increased frequency of M. canis, T. mentagrophytes and T. verrucosum, the latter became the most important agent isolated from scalp. In North America, T. tonsurans took the place of M. audouinii as the most common agent for tinea capitis followed by M. canis [15–17], and T. rubrum expanded, together with T. mentagrophytes and E. floccosum, as a common cause of superficial fungal disease worldwide, except infections on scalp [15, 18]. Etiology of dermatophytosis in Australia was much similar to that of North America except that M. audouninii was rarely reported in Australia. It is thought that its spread was prevented by M. canis [15, 19].

Differences in the dermatophyte spectrum for tinea capitis were observed in Mediterranean countries and Eastern Europe, where M. canis, T. mentagrophytes, T. violaceum and T. schoenleinii acted as the major agents, changing with areas [15, 16, 18].

Few original reports could be reviewed before 1960s for Africa, Asia and Middle East. Between 1960s and 1970s, E. floccosum, M. ferrugineum, T. violaceum and T. schoenleinii were highly popular in these areas as the main causes of scalp ringworm yet their respective frequency varied by regions [15, 20, 21].

Epidemiology of Dermatophytoses Since 1980s

In recent 30 years, the spectrum of dermatophytes showed slower evolution though some changes keep happening. Table 1 lists some of the large studies reported since 1980.

Table 1 Epidemiology of dermatophytes worldwide since 1980s
Full size table

Trichophyton rubrum almost presents as the predominant species for tinea on skin and nails worldwide. Trichophyton mentagrophytes ranks the second and even shows as the most common agent in some countries like Venezuela, Iran and Croatia [22–24]. Epidermophyton floccosum, T. tonsurans, T. violaceum, M. canis, M. audouinii and M. ferrugineum are also responsible for some proportions of tinea corporis and onychomycosis in some areas of the world. Epidermophyton floccosum, which disappeared for many areas, accounted for 16–40 % of cases in Tehran, Iran [23, 25, 26], whereas M. audouinii, T. soudanense and T. schoenleinii are still popular in Africa [27–29].

The agents of tinea capitis showed much obvious geographic changes. Microsporum canis is the leading agent of tinea capitis in most parts of Europe and Asia. Trichophyton tonsurans presents as the predominant cause of tinea capitis in North/South America and the United Kingdom [15, 30, 31], and T. violaceum, T. schoenleinii, M. ferrugineum and M. audouinii are still epidemic in Africa, Eastern Europe and Asia [15, 32–36].

Population mobility, the advent of new antifungal agents, popularization of leather shoes and sneakers, improvement of human hygiene are responsible for this shift in the dermatophyte spectrum [4, 37]. Ping et al. [32] reported a big shift from anthropophiles to zoophiles in the past 60 years in China.

Dermatophytes, Related Diseases and History Evolution

Concerning their natural habitat, host preference and transmission route, dermatophytes can be divided into anthropophilic, zoophilic and geophilic species. Generally speaking, anthropophilic dermatophytes which are characterized by human to human transmission are geographically limited except for T. rubrum, which is most frequently isolated in developing countries and usually associated with low socioeconomic status [4, 5]. By contrast, zoophilic species which are related to pet feeding and farming work increase dramatically nowadays and show a global distribution, especially in Europe and Asia [5]. Microsporum canis and T. mentagrophytes are the major pathogenic species belonging to this category. Geophilic dermatophytes grow in soil and sporadically infect humans, with Microsporum gypseum as the most common pathogen for human in this group [4].

Numerous reports about the epidemiology of dermatophytoses have been published in recent years (Table 1). Reports from Europe are more numerous than those from Asia, Africa, America and Australia. However, we can speculate that superficial fungal infections are more prevalent in Africa and Asia due to the ecological diversity in tropical/subtropical areas and low socioeconomic status. However, the lack of research groups about dermatophytes, professional technicians and limit of laboratory diagnosis are the major limitations for epidemiological research in most developing countries.

Trichophyton rubrum Trichophyton rubrum is the leading etiological agent of most superficial infections on skin and nails. Interestingly, this species is relatively new to human beings compared to the other main dermatophytes [38]. It was described by Castellani in 1910 and named as Epidermophyton rubrum firstly and then changed to T. rubrum by Sabouraud in 1911 [7, 10]. The first clinical case due to this organism, corresponding to tinea pedis, was reported in 1927, in the USA [7]. Microsatellite analysis suggested that it originated from Africa, followed by the emergence of a new genotype in Asia with subsequent spread of this genotype over Europe and the United States by population expansion and immigration around the Second World War [39, 40]. It has since become the most common etiologic agent of tinea corporis, tinea pedis and tinea manuum, tinea cruris, tinea unguium (onychomycosis) and subcutaneous dermatophytosis (Majochii granuloma), representing about 50–80 % of these infections [4, 41, 42]. Trichophyton rubrum seldom infects hair due to its incompetence of invading into follicle and hair.

A broad spectrum of species close to T. rubrum was nominated in the history, including Trichophyton megninii, Trichophyton balcaneum, Trichophyton rodhainii, Trichophyton kuryangei, Trichophyton circonvolutum, Trichophyton fischeri, Trichophyton fluviomuniense, Trichophyton glabrum, Trichophyton gourvilii, Trichophyton kanei, Trichophyton pedis, Trichophyton raubitschekii, Trichophyton soudanense, Trichophyton violaceum and Trichophyton yaoundei, which revealed high sequence homology by molecular analysis, and are now summarized into a generic term, Trichophyton rubrum complex [38, 40]. This complex can be divided into two groups according to Graser et al. [38, 39]: Trichophyton rubrum clade (representative member is Trichophyton rubrum Castellani) and Trichophyton violaceum clade (representative member is Trichophyton violaceum). The former group is related to the infections of skin and nails, whereas the latter is recovered from scalp infections with endothrix-type hair invasion [38]. Trichophyton rubrum sibling species are anthropophilic, transmitting from human to human by direct or indirect contact, and usually induce chronic, mild inflammation. The classical species, T. rubrum, has a global distribution, without preference of gender, race and age [43]. However, it prefers warm and humid climates and more easily infects outdoor and hard working population, which explains why in most epidemiological reports males exceed females and more cases are reported from tropical and subtropical countries [6].

Trichophyton mentagrophytes. Trichophyton mentagrophytes was discovered by David Gruby in tinea barbae, and named later as Microsporum mentagrophytes by Robin (1853), but then transferred to the Trichophyton genus by Blanchard (1896) [7]. Gruby [7] also recognized its ectothrix forms of hair invasion. Trichophyton mentagrophytes presents a global distribution with no bias of climate, race and regions. After T. rubrum, T. mentagrophytes/T. interdigitale is the second causative agent of tinea corporis and onychomycosis in most countries. However, in southwestern Iran and Venezuela, the frequency of T. mentagrophytes/T. interdigitale is significantly higher, these species being more common than T. rubrum, acting as the leading causative agents of superficial fungal infections [22, 23]. Additionally, T. mentagrophytes can invade hair and follicles, causing black dot and kerion type of tinea capitis. It is also the major pathogen for tinea faciei and tinea barbae, accounting for 70 % of cases in some reports [23, 44].

Trichophyton mentagrophytes sibling species form the most polymorphic group within dermatophytes, which comprises at least four clades, i.e., T. interdigitale (with no known teleomorph), T. mentagrophytes (with the teleomorph Arthroderma vanbreuseghemii), Trichophyton simii (with the teleomorph Arthroderma simii), Trichophyton erinacei (with no known teleomorph) and Arthroderma benhamiae. Among these species, T. interdigitale is the only one anthropophilic, the others being zoophilic or geophilic [45, 46]. Due to their variable pleomorph and limited resolution capability, these siblings make confusion to mycologist and clinical doctors and are usually summarized into the T. mentagrophytes complex in practice. Multilocus genetic analysis might clarify this dilemma in near future and bring us clear taxonomy of dermatophytes.

Microsporum canis. Microsporum canis was reported in 1902 by Bodin as Microsporum lanosum and its name was changed to Microsporum canis by Sabouraud in 1908 [7, 47]. It is a zoophilic species with a worldwide distribution. A wide variety of lower animals and cats and dogs are the main reservoir. The etiology of tinea capitis experienced great evolution since the 1950s from T. schoenleinii and M. audouinii to M. canis and T. tonsurans [5, 48]. Nowadays, M. canis is the predominant agent for tinea capitis, highly widespread in Asia, Mediterranean countries and Central Europe [5, 49]. In Chinese megacities, i.e., Beijing, Guangzhou and Chongqing, M. canis accounts for 80 % of all cases of tinea capitis [32]. While, the epidemiology of tinea capitis in Africa and some less-developed regions in Asia, i.e., Iran and northern west China, appears to sustain an old transmission route of human to human mode, with the spread of a broad spectrum of anthropophilic species [32, 50]. Microsporum audouinii, T. violaceum, M. ferrugineum and T. soudanense remain endemic as the major agents of tinea capitis, notably in Kenya, Malawi, Ethiopia and Nigeria [50, 51]. Along with the immigrations, reappearance of M. audouinii and T. violaceum has been reported in Europe recently, and they have been confirmed by molecular fingerprinting to come from African countries and spread to some European countries by human contact (see below) [52].

Microsporum audouinii. Microsporum audouinii was firstly discovered by David Gruby in 1843 in clinical samples and named in 1902 [7]. It is commonly regarded as an anthropophilic dermatophyte. However, rare isolation came from animal and soil indeed [53, 54]. This fungus had a worldwide distribution, highly epidemic in the nineteenth century, generally found in prepubescent children, causing tinea corporis and tinea capitis. Due to it is high sensitivity to griseofulvin, it was almost eliminated after 1950s. Currently it is only isolated in Africa and some parts of Europe and Asia. In some African countries, i.e., Nigeria [27] and countries in West Africa [28], it even acts as the leading organism of superficial fungal diseases. However, reappearance of M. audouinii was reported in Belgium and Germany recently [52, 55], as well as in the Zurich area of Switzerland [44], as a result of Africa immigration into Europe (see above introduction of Microsporum canis).

Trichophyton violaceum. Trichophyton violaceum is another important species within the T. rubrum complex. Conversely to T. rubrum, it is geographically limited and mainly causes tinea capitis. This organism also originated from Africa and then became popular in Europe and Asia at the late nineteenth and the early twentieth century. It became an important agent of tinea capitis in Africa, Europe and Asia, as well as T. schoenleinii and M. ferrugineum. In China, T. violaceum accounted for 28.8 % of cases of tinea capitis, while T. schoenleinii and M. ferrugineum were the causal agents in 44.7 and 20.7 % of the cases during a 30-year period, from 1956 to 1985 [33]. Since then, its frequency decreased rapidly and it was replaced by M. canis in most of its once popular areas [32, 33]. Nowadays, it remains in some African countries, Eastern Europe, Middle East and South and West China. Nevertheless, an increasing occurrence of T. violaceum infections, as the predominant pathogen for tinea capitis, was reported in Milan (Italy) [34]. Foreigners from Africa are usually regarded as the infectious source. However, excluding Africa and Europe, amounts of cases have been reported in Middle East, Northwest and Southern China [25, 32, 33]. In Southern cities of China, Nanchang and Shanghai, T. violaceum ranks the first and the second pathogen for tinea capitis, respectively [32, 35]. In addition to tinea capitis, T. violaceum can infect skin and nails, causing tinea corporis, tinea pedis, tinea manuum, tinea cruris and onychomycosis.

Trichophyton tonsurans. Trichophyton tonsurans was firstly described by David Gruby as causing an endothrix form of hair invasion [7]. However, it is the Swedish scientist, Malmsten who named it in 1845 [10]. This anthropophilic dermatophyte has a worldwide distribution, but with frequency variations from continent to continent nowadays. This organism is mainly popular in North America (Canada, the USA), the United Kingdom and Western Europe, infecting hair and causing black dot tinea capitis, as well as infecting skin causing tinea corporis. Additionally, T. tonsurans may be recovered from the scalp of asymptomatic carriers and is the etiological agent for small outbreaks of tinea corporis and tinea capitis among kindergartens, health centers, family members and sports clubs [56–58].

Conclusions

The fungal biota of superficial infections varies not only geographically but also historically. In the past 100 years, dermatophytes experience great evolution worldwide. Those which were highly popular among human beings around 1930 and 1940s, e.g., T. schoenleinii, M. audouinii, E. floccosum and M. ferrugineum, are being disappearing from most countries and limited to some less-developed countries. Trichophyton tonsurans shows an upward trend in America and Europe, but its frequency still remains low in developing countries [15, 30, 33]. Zoophilic dermatophytes, mainly M. canis, gradually increased since the twentieth century, mainly because of the petting popularization [33]. Microsporum canis is the most common dermatophyte isolated from animals, followed by T. mentagrophytes, M. gypseum and T. verrucosum [59, 60].

In addition, a new feature of superficial fungal infections nowadays should be mentioned, that is the gradually increased frequency of yeast and yeast-like skin infections in tropical and subtropical countries, while dermatophytoses decrease continually, together with the increased frequency of hospital-acquired infections along with the increased number of immunocompromised patients since the late 1900s [41].

Changes in life style will inevitably promote a shift in the spectrum of fungal biota responsible for skin infections. It can be speculated that, due to the improvement of hygiene, generalization of animals quarantine and modern lifestyle, these organisms will shift from zoophilic (M. canis and T. mentagrophyes) to anthropophilic species (T. rubrum, T. tonsurans and T. violaceum), which transmit in a hidden way and cause mild inflammation. Many attempts have been made to eliminate dermatophytes and factually achieved great contributions indeed [5, 32, 33]. Interdisciplinary cooperations are needed to control this kind of disease and achieve maximum results, including efforts from public health organization, accurate diagnosis from clinical works, governmental intervention and social surveillance.