Tinea capitis et barbae caused by Trichophyton tonsurans: A retrospective cohort study of an infection chain after shavings in barber shops

Tinea capitis is a highly contagious infectious disease caused by dermatophytes. In Central Europe, it is mainly caused by zoophilic dermatophytes, as, for example Microsporum (M) canis or Trichophyton (T) mentagrophytes and increasingly by anthropophilic fungi. T tonsurans was commonly related to the Tinea gladiatorum, where transmission occurred between infected persons or via contaminated floors.


| INTRODUC TI ON
Infections with the anthropophilic dermatophyte Trichophyton (T) tonsurans have been described worldwide, mainly in the context of martial arts and other contact sports 1 which require proximity between the athletes. Here, the pathogen regularly triggers local and supra-regional outbreaks of tinea corporis in sports clubs but also during competitions, which is why the disease caused by this dermatophyte is also called 'Tinea gladiatorum'. 2,3 Originally, T tonsurans was native to South East Asia and Australia. In the colonial period, it expanded to Central and South America, and from there, through both migration and international combat sports competitions, to Europe and the United States. 4 In the USA, Iran and Turkey, the prevalence of the 'Tinea gladiatorum' among wrestlers varies from 2.4% to 90.62% (average 34.29%). 5 As a trigger of tinea capitis, T tonsurans initially played a rather minor role in Europe, while in the USA, the Caribbean and, later, also in Great Britain, the pathogen has become the main cause of tinea capitis in children. 6,7 During the last decades, a decrease of the formerly prevalent pathogens Microsporum (M) canis and M audouinii in favour of T tonsurans was observed in Central Europe. An increase in infections with T tonsurans has been described, particularly in patients with a West African migration background, although T tonsurans is not the predominant cause of tinea capitis in West Africa. 8 This led to the assumption that an infection must have taken place outside the home countries.
However, it is still not conclusively clarified, why the overall prevalence of T tonsurans is increasing. One reason could be the therapeutic possibilities. As griseofulvin is the only approved systemic antifungal drug in childhood, it is commonly used to treat all forms of tinea capitis. Nevertheless, griseofulvin is more efficient in the treatment of infections with Microsporum species than Trichophyton species. It is possible that consequently an inadequate therapy led to the spread of T tonsurans. In addition, the niche could be occupied by the decreasing number of Microsporum species. To what extent mutations of the pathogen with increased virulence are present is yet to be proven. 8,9 The present work describes a new route of infection in our regions by a possible transmission of T tonsurans through contaminated hair cutting tools. Shaving with high potential for microtrauma could serve as an entry for the pathogen and, if the equipment is contaminated, could lead to an increased incidence of tinea capitis or barbae. Next to an accurate diagnostic and therapy, the detection of the mode of infection and the interruption of the chain of infection are therefore of great importance.

| Patients
The observation period was 2 years, from April 2018 to April 2020. The study was conducted in accordance with the Helsinki Declaration; patient-relevant diagnostics and therapy strictly followed the current guidelines. The authors confirm that the ethical policies of the journal, as noted on the journal's author guidelines page, have been adhered to.
In this period, 18 young, exclusively male patients with tinea capitis/barbae were presented dermatologically. In all cases, the skin lesions aroused a few days to a maximum of 2 weeks after receiving a haircut in a barber shop. The lesions appeared in the shaved/ combed regions of the scalp, neck and beard (Figures 1-4). 16

| Morphological detection of the dermatophyte
Microscopic examinations of epilated hair shaft material and removed skin scales were carried out in all patients by preparation using TEAH (Tetraethylammonium hydroxide, Merck, Darmstadt, Germany). In addition, suitable skin biopsies were taken from 4 patients using a punch biopsy. Numerous serial sections were stained using PAS (periodic acid-ship) reaction.

| Cultural detection of the dermatophyte
Intra-and perilesional, depilated hair (hair roots) and affected skin scales were taken from all patients for cultural, mycological diagnostics. The pathogens were cultivated on Sabouraud glucose agar containing gentamicin and chloramphenicol (Becton Dickinson, Heidelberg, Germany) and on Mycosel ® agar (Becton Dickinson, Heidelberg, Germany).
After sufficient growth of the pathogens, adhesive tape was applied to the respective colonies and the material adhering to it was stained with lactophenol blue on a cover glass. Direct microscopy of the samples was performed.

| Resistance testing of the dermatophyte
In order to evaluate the therapeutic possibilities of tinea capitis caused by T tonsurans, we carried out an in vitro resistance test for terbinafine on the samples of six randomly selected patients of our cohort. Thereby, we used a recently described modified breakpoint method. 12 We filled Petri dishes with Sabouraud glucose agar, which

| Morphological detection of the dermatophyte
Hair and skin scales were microscopically examined after incubation with TEAH. A highly variable number of hyphae were found in the different samples, which did not correlate with the clinical expression. All patient samples were positive for fungi.

| Resistance testing
After 7 days, all growth controls showed regular growth. In contrast, no fungal growth was detectable on the agar plates impregnated with terbinafine. The examination showed a completely inhibited growth (breakpoint <0.2 µg/ml) under terbinafine in all 6 cultures, so that an in vitro sensitivity of the T tonsurans isolates to terbinafine can be assumed.

| Therapy and progress
After confirmation of the diagnosis of tinea capitis/barbae, oral antifungal therapy with terbinafine 250 mg or weight-adapted with terbinafine 125 mg once per day for at least 28 (Figures 3 and 4).

| DISCUSS ION
Anamnestically and clinically, the frequent occurrence of tinea capi-

| T tonsurans in the course of time
As early as 1952, an increasing prevalence of tinea capitis was reported in the USA, whose main cause was considered to be T tonsurans. 13 In Germany, at that time, the zoophilic dermatophytes caused the majority of tinea capitis. In Southern and Western Europe (among others in England, Belgium and the Netherlands), the number of anthropophilic pathogens had already increased. 14 In 1997, Fuller et al 15 declared tinea capitis caused by T tonsurans to be a 'major health problem' in South East London. Thus, tinea capitis also gained more importance in Europe. Currently, the number of tinea capitis caused by anthropophilic pathogens is still increasing in Germany due to T violaceum and T soudanense and especially T tonsurans. 16 As an anthropophilic dermatophyte, T tonsurans usually triggers a rather low inflammatory reaction in the skin in contrast to zoophilic dermatophytes. 14 However, the dermatophyte may sometimes lead to pustular, purulent abscessing and also hyperkeratotic lesions with the danger of secondary complications such as cicatrisation (Figures 3 and 4). 17 In its classic form, the 'black dots' tinea capitis, the hair is weakened by the pathogen, breaks off and appears as a black dot on the scalp. 18 However, none of our patients presented this variant. 4 patients presented a rather untypical, highly inflammatory course. The clinical picture was similar to that of a severe folliculitis or impetigo, leading to an increased risk of misdiagnosis and consequently to an inadequate therapy. 19 It is therefore of great importance, especially in ambiguous cases, to carry out a detailed diagnosis, which, in addition to a precise anamnesis, always requires microscopy of the native preparation, the preparation of a culture and, if necessary, the biopsy of a suitable skin lesion. 20 Microscopically, numerous spores can usually be detected in affected hairs; a so-called endothrix growth pattern is observed, in which an invasion of the hair shaft takes place, making the pathogen almost invisible to wood light. 21 It is interesting to note that in our patients the number of microscopically visible spores did not correlate with the severity of the disease, so that even in pronounced foci on the scalp, sometimes only a few spores could be found.
Histopathological investigation is a helpful diagnostic supplement in special questions, diagnostically challenging and ambiguous cases as well as highly inflammatory courses to find a rapid diagnosis. Essential for the detection of fungi is the skin biopsy, taken from a suitable lesion. Sufficient hair shafts should be embedded in the biopsy so that the endothrix growth of T tonsurans can be detected. All patients in our cohort were informed about an increased risk of infecting more persons, mainly within their families. Since transmission through physical contact and the use of common hair clippers and towels could not be avoided completely, patients were encouraged to use only their own hygiene products.

| Dermatophytes on hair dressing tools
A Stockholm study showed that mostly migrants from West Africa were more likely to be affected by tinea capitis, mainly caused by T violaceum. The common use of hairdressing tools, mostly combs and razors, was suspected to be a potential way of transmission. 25 In a further study, conducted in a West African suburb, a random sampling of household combs, brushes and hair clippers showed a contamination of more than 70% with the anthropophilic dermatophytes T soudanense and M audouinii. Tinea capitis particularly affected school children in the village. 26 The high prevalence of tinea capitis may also be due to the cultural use of certain hair practices (braiding, use of shared hair rubbers, shared brushes), especially among children. This correlates with the high incidence of the same pathogens within a family. Selective immune tolerance and variable sebum composition are also discussed. 27 On the other hand, Sharma et al 28 did not find a high incidence of T tonsurans when using certain hair practices, so that this way of transmission must be regarded critically and depends on the context.

| Therapy and hygiene
Only griseofulvin is approved for systemic antifungal therapy in children, but since 2018 it has no longer been available in Germany and can only be obtained from international pharmacies. 20 However, only about half of all infections with T tonsurans are successfully treated by the application of griseofulvin. 34 Terbinafine in a weightadapted dosage is more effective to treat infections with T tonsurans.
In our in vitro resistance testing, the growth of the pathogens could be completely inhibited under terbinafine; a terbinafine resistance is not detectable. This is significant regarding the increasing clinical and in vitro terbinafine resistance of Indian T mentagrophytes genotype VIII strains. 35 It should be noted that the drug has no approval for children in Germany and can only be used in the context of an individual therapeutic trial ('off label use') after the parents have been informed accordingly. In order to interrupt the chain of infection, a mycological co-examination of the contact persons is urgently indicated, as well as the initiation of a topical, antimycotic therapy in case of asymp- disinfection of used haircutting tools should become a daily routine.
It is not yet clear why the incidence of T tonsurans has increased so rapidly in Europe in recent years and decades. It is assumed that the pathogen can easily pass from one organism to another in close communities. 38 Since asymptomatic carriers only become negative after approximately 2-12 months, the question is whether they should receive additional therapy to interrupt the chain of infection. Since tinea capitis is considered to be the most infectious form of all tinea diseases, T tonsurans is to be classified as an 'emerging pathogen' due to the increasing incidence of this dermatophytosis in Europe.

ACK N OWLED G EM ENTS
This research received no specific grant from any funding agency in the public, commercial or not-for-profit-sectors.