Trichophyton benhamiae: An Emerging Pathogen in Europe
Abandoning the previously accepted nomenclature of an asexual state, i.e., T. mentagrophytes, and a sexual state, i.e., Arthroderma benhamiae (see above), resulted in situation that no name combined in Trichophyton was available for A.
benhamiae despite its clear phylogenetic position within Trichophyton clade (Fig. 3.3). This combination was introduced recently (de Hoog et al. 2017), but during the last decade, the species was usually designated A. benhamiae or “Trichophyton sp. anamorph of A. benhamiae” in the literature. Originally, the sexual state of this species was induced by crossing of two isolates designated by authors as “T. mentagrophytes var. granulosum” which originated from a dog and a man with dermatophytosis in the USA (Ajello and Cheng 1967). Consequently, the identification of isolates designated as A. benhamiae before the molecular era is commonly doubtful and can comprise quite broad spectrum of currently accepted species, i.e., T. benhamiae s. str., T. erinacei, T. mentagrophytes, and some less common related species (Fig. 3.3). Isolates designated as “African race of A. benhamiae” represent an independent monophyletic entity related to T. bullosum rather than to T. benhamiae (Fig. 3.3). However, mating compatibility between “African race of A. benhamiae” and T. benhamiae (also called American-European race) was observed in vitro (Takashio 1974). The mating groups were indicated as “races” because no morphological differences could be observed between strains from different continents.Guinea pigs represent the main host reservoir (Fig. 3.6) in Europe (Drouot et al. 2009; Kraemer et al. 2013; Hubka et al. 2014b); infections occasionally occur also in dogs (mostly USA), pigs (USA), and cats (Belgium) or various rodents (rabbits, chinchilla, mouse, rat, porcupine, degus) (Ajello and Cheng 1967; Takahashi et al. 2008; Takeda et al.
2012; Symoens et al. 2013; Sieklucki et al. 2014; Hiruma et al. 2015; Overgaauw et al. 2017). Our knowledge on spectrum of hosts worldwide supported by molecular data is still insufficient. Based on sequence data, it seems that the majority of infections in guinea pigs is caused by T. benhamiae, to a less extent by T. mentagrophytes and rarely by M. canis; in contrast T. mentagrophytes is a frequent pathogen in rabbits followed by M. canis and T. benhamiae (Arabatzis et al. 2006; Frealle et al. 2007; Drouot et al. 2009; Heidemann et al. 2010; Sun et al. 2010; Cafarchia et al. 2012; Symoens et al. 2013). The prevalence of T. benhamiae in various animals probably differs significantly in different geographic areas, and these infections seem to be associated with different genotypes or subpopulations, respectively (Cmokova 2015). A small outbreak of dermatophytosis due to T. benhamiae was reported in Canadian porcupines (Erethizon dorsatum), a close relative of the guinea pig, housed in a Japanese zoo (Takahashi et al. 2008). A case of infection in Cape porcupine (Hystrix africaeaustralis) and a man who handled animals (Marais and Olivier 1965) were reported from Southern Africa.Trichophyton benhamiae has been reported and confirmed by molecular methods in many European countries, the USA, and Japan. The prevalence and distribution in rodents is largely unknown due to fact that the pathogens were usually identified as T. mentagrophytes across published studies. It was determined that the prevalence of dermatophytosis in guinea pigs in Germany was 38.1% of which 91.6% infections were caused by species from T. mentagrophytes complex (Kraemer et al. 2012; Kraemer et al. 2013) in agreement with an older study which found prevalence 37% (Weiβ et al. 1979). A recent study revealed more than 90% prevalence of T. benhamiae in guinea pigs from pet shops in Germany, 9% of which showed visible symptoms (Kupsch et al. 2017). The prevalence in Switzerland was 38.1%, and T.
benhamiae was confirmed in all mycologically positive samples (Drouot et al. 2009); the prevalence of dermatophytosis in guinea pigs across pet shops in the Netherlands was 16.8% (88% of cases were caused by T. benhamiae) that corresponds to 27.3% of pet shops which sell infected but mostly asymptomatic animals (Overgaauw et al. 2017). The retrospective analysis of the activity of a veterinary laboratory from 2010 to 2012 in France demonstrated that dermatophytes were isolated from 41.2% of 148 pet rodents (guinea pigs, rats, mice, hamsters, and chinchillas) and 38.2% of 76 pet rabbits (Guillot et al. 2016). In guinea pigs, T. benhamiae was predominant, whereas T. mentagrophytes was most frequently isolated from other rodents and from rabbits. In contrast, low prevalence (3.5%) of T. mentagrophytes was detected among guinea pigs in Belgium (Vangeel et al. 2000), and no Trichophyton spp. were isolated among 200 pet guinea pigs in Italy (d'Ovidio et al. 2014). The lack of reports of T. benhamiae from guinea pigs in the USA (a country of origin) is obvious, and guinea pig was determined as a source of infection only in one human case of dermatophytosis (Ajello and Cheng 1967). Although epizootic episodes in guinea pigs colonies and laboratory guinea pigs attributed to T. mentagrophytes have been described in the USA (Menges and Georg 1956; Pombier and Kim 1975) and other countries (Rush-Munro et al. 1977; McAller 1980), the identity of the pathogen is unclear in the context of recent taxonomic changes. More recently T. benhamiae was confirmed by molecular data in Iran at relatively low frequencies (Abastabar et al. 2013; Ansari et al. 2016; Rezaei-Matehkolaei et al. 2016) contrasting to its absence in the past studies.Trichophyton benhamiae causes 2.9% of all human dermatophytoses in Germany (Uhrlaβ et al. 2015) and 7.2% in the Czech Republic (Hubka et al. 2014b). Consequently, it is the most important agent of dermatophytosis transmitted from animals in the Czech Republic and causes 22.9% of all infections on glabrous skin and 29.2% of tinea capitis infections; median age of all patients was 12, and women comprised 71% of patients (Hubka et al.
2014b; Hamal et al. 2016). Current status of T. benhamiae infection in Japan, the USA, and other countries is almost unknown due to insufficient surveillance and lack of epidemiological studies supported by molecular-based identification. In contrast to Europe, rabbits seem to be a major reservoir of T. benhamiae in Japan; 78% of published Japanese cases were reported in women; median age of patients was 26 (Kimura et al. 2015). The infection in guinea pigs does not show any gender predisposition, but the young individuals are more frequently affected and symptomatic, whereas adult animals are mostly symptomless. In symptomatic guinea pigs, the infection manifests as alopecia with scaling and crusting located predominantly on the head, less frequently on the other body parts (Drouot et al. 2009; Kraemer et al. 2012, 2013; Overgaauw et al. 2017).With respect to the current epidemiological situation, it is clear that T. benhamiae is a new emerging pathogen in human clinical material in Europe and Japan. This fact is surprising because guinea pig breeding has a long tradition in these regions, and T. benhamiae has been documented among guinea pigs in the past, but the clinical cases in human were absent or very rare. Before widespread dispersal of T. benhamiae in Europe, sporadic cases of human and guinea pig infections caused usually by “yellow-pigmented isolates” which macroscopically resembled M. canis were reported from different countries. First cases due to T. benhamiae in Switzerland were dated in 2002 (Fumeaux et al. 2004), and similarly, first isolates from French cases were collected between 2002 and 2008 (Frealle et al. 2007; Contet-Audonneau and Leyer 2010; Charlent 2011; Khettar and Contet-Audonneau 2012). The first cases were observed in Germany and Czech Republic before 2010, and the pathogen became rapidly epidemic during following years (Hubka et al. 2014b; Nenoff et al. 2014; Skorepova et al. 2014; Uhrlaβ et al. 2015). In Japan, the species was first isolated in 1996 from an infected rabbit (Kano et al. 1998); the human cases were reported in following years (Nakamura et al. 2002) and summarized by Kimura et al. (2015). Because T. benhamiae became common in companion animals of Japan, increasing number of infections can be expected there.
3.8.2