Dermatophytoses or tineas are superficial cutaneous infections caused by a group of fungi called dermatophytes, which invade keratinized tissues such as skin, hair or nails.

Epidermophyton, Microsporum and Trichophyton were the genera covering all dermatophytes, but in the last years, a new taxonomy was proposed and more genera were included: Trichophyton, Epidermophyton, Nannizzia, Microsporum, Lophophyton, Arthroderma, Ctenomyces, Guarromyces and Paraphyton1. These fungi can be divided into three major groups according to the reservoir and the transmission: anthropophilic, zoophilic or geophilic.

Tinea capitis is especially frequent in children and is caused by an invasion of dermatophytes, mainly Trichophyton and Microsporum genera, into the hair follicles and the skin of the scalp.

The epidemiology of the tinea capitis varies according to geographical and socioeconomic factors and evolves over time. In Europe and North America, anthropophilic Microsporum audouinii, Trichophyton schonleinii, Trichophyton violaceum and Trichophyton tonsurans were the most common species in the 19th century. It changed in the 20th because of using griseofulvin and hygiene improvement, so zoophilic Microsporum canis became the main tinea capitis species in Europe2–4.

Although zoophilic dermatophytes still prevail, lately, a change has been noticed in the incidence of major causative agents5,6. An increase in tinea capitis due to anthropophilic African species (Microsporum audouinii and Trichophyton soudanense) and Caribbean species (Trichophyton tonsurans) of dermatophytes has been reported from the main capitals in Europe, North America and the Middle East3. This pattern of infection appears to be linked to immigration from Africa and the Caribbean7,8.

The present retrospective study aimed to analyse the epidemiology, clinical and mycological features of anthropophilic tinea capitis in children of our health area. Our second objective was to evaluate the type of treatment used and the obtained response.

We designed a single-center retrospective observational study that included children who were diagnosed with tinea capitis at our hospital, in northwestern Spain, between 2004 and 2019. A retrospective database analysis was performed on the medical records of children with tinea capitis and positive mycologic cultures for anthropophilic species who were attended in the paediatric dermatology consultation of our department.

Samples were collected by scraping the infected area using a sterile scalpel. Specimens were examined by fluorescent microscopy using 20% potassium hydroxide and Calcofluor white stain (Remel, San Diego, CA, USA). Whenever ectothrix and endothrix phenomena were observed, it was used to help fungal identification. Clinical specimens were cultured on two different Sabouraud Dextrose Agar, one with chloramphenicol and cycloheximide and another one with chloramphenicol and gentamicin (BD, Franklin Lakes, NJ, USA), both incubated at 30 °C for at least four weeks. Isolates were subcultured on rice grains to demonstrate pigment formation. Urease activity was studied through Christensen’s Urea Agar (BD), and in vitro hair perforation test was performed in sterile prepubertal human hair to analyse the presence of perforating organs. Final identification was achieved by combining the above mentioned with colony microscopic examination with Lactophenol cotton blue stain (Remel) by an experienced medical microbiologist. No genomic analysis was performed.

Data were coded and entered into the computer and analyzed using SPSS Statistics. We carried out a descriptive analysis of the variables included in the study; quantitative variables were expressed as a mean ± standard deviation (SD), and qualitative variables were reflected as the absolute value and percentage.

A narrative review was also performed. Potentially relevant studies were identified through a literature search for articles published until 26 July 2019 using PubMed database. The searches were limited to English and Spanish articles. References within retrieved articles were also reviewed to identify missing information in the primary research.

We included 24 children who were under 12 years, the minimum age was 1 year. The mean age was 4,88 years and +- SD 2,86.

Eighteen patients (75%) were males while only six (25%) were females. We observed a total of twenty (83,3%) cases in patients born in Africa or whose parents were from Africa (Ethiopia, Nigeria, Senegal, Equatorial Guinea and Burundi) in comparison with only one (4,2%) from South America (Dominican Republic) and three (12,5%) from Spain. A total of five patients (20,8%) were adopted and all of them were born in Africa.

Twelve children (50%) went on a trip to Africa a few months before the symptoms began. Only two cases had contact with other family members with tinea. There were not any animal contact. We found just one patient (4,2%) with a co-dermatophytose and it was tinea faciei.

Clinically, thirteen patients (54,2%) presented non-scarring alopecia, seventeen (70,8%) scaly patches, eight (33,3%) crusts and six (25%) pustules. Neither of the cases were diagnosed as kerion nor presented systemic symptoms.

Fungal cultures were positive for Trichophyton soudanense in eleven cases (45,8%), Microsporum audouinii in five patients (20,8%), Trichophyton tonsurans in three (12,5%), Trichophyton violaceum in also three (12,5%), Trichophyton megnini in one (4,2%) and Trichophyton rubrum in also one (4,2%).

Microsporum audouinii and Trichophyton soudanense were more common in patients with a recent trip to Africa.

Twenty-two patients (91,7%) received oral treatment. Griseofulvin was used in thirteen patients (54,2%), terbinafine in five (20,8%) and itraconazole in one case (4,2%). In three patients (12,5%), all with positive cultures for Microsporum audouinii, a treatment with terbinafine was initiated but after eight weeks without improvement it was changed to griseofulvin.

Twenty patients (83,3%) received topical antifungals (ketoconazole). Two cases (8,3%) only had topical treatment; in these patients, who were 3 and 5 years, topical antifungals were initiated empirically and achieved a complete clinical healing before the fungal culture result. No patient had a relapse during the follow-up that lasted more than 6 months.

Tinea capitis, or scalp ringworm, is more common in children. It has been seen that incidence is highest in males between three and seven years, so as we found in our cases.

Although zoophilic dermatophytes remain the predominant cause of tinea capitis in Spain, an increase in tinea capitis due to anthropophilics Microsporum audouinii, Trichophyton soudanense, Trichophyton violaceum and Trichophyton tonsurans has been reported2,9. European capitals, like London or Paris, have reported Trichophyton tonsurans as the main responsible for tinea capitis10,11, so did North America12. In contrast, Microsporum audouinii and Trichophyton soudanense were the most common in our series. This pattern of infection appears to be linked to immigration from Africa: Trichophyton violaceum is the major agent of tinea capitis in the North and East of Africa and Trichophyton soudanense and Microsporum audouinii predominate in the Western and Central regions of the African continent13–15. In our area, most of the immigration comes from Morocco and Senegal.

In our series, three children born in Spain of Spanish parents had tinea capitis due to anthropophilic species; in two cases Trichophyton soudanense was observed and Trichophyton tonsurans in one. We believe the infection in these native children probably occurred at their schools since there were similar cases in the area, in children of similar age and these patients had not taken any trips nor did they have any affected relatives. The situation was notified but there was not any follow-up in the schools.

Non-scarring alopecia and scaly patches were the predominant clinical presentation in our cases. None of the cases were diagnosed as kerion nor presented systemic symptoms. Delay in diagnosis in tineas caused by anthropophilic species may increase the risk of transmission to other family members3 and spread to other areas of the skin. In our study, two cases were developed in siblings and one patient had tinea faciei and tinea capitis at the same time.

A 2016 Cochrane review of systemic antifungal therapy for tinea capitis in children reveals that although griseofulvin or terbinafine are both effective, complete healing is superior with griseofulvin (6-12 weeks) in those cases due to Microsporum species and with terbinafine (6 weeks) in those caused by Trichophyton species without differences in adherence and with reasonable safety profile16. In our study, griseofulvin and terbinafine were used in tinea capitis treatment in both Microsporum and Trichophyton cases with good results. In three patients with tinea capitis due to Microsporum audouinii, no improvement was obtained after eight weeks of terbinafine treatment, so it was changed to griseofulvin. This resistance to terbinafine of Microsporum audouinii infections is frequently encountered and underestimated3. Topical antifungals are useful as an adjuvant treatment to eradicate viable spores in the scalp and to reduce the risk of transmission at the start of systemic treatment; ketoconazole or ciclopirox olamine can be used17.

To conclude, tinea capitis is more common in male children between three and seven years. Although zoophilic dermatophytes remain the predominant cause of tinea capitis in Spain, anthropophilic dermatophytes are becoming even more important in our community. Trichophyton soudanense and Microsporum audouinii were the most common in our series. Although this pattern of infection appears to be linked directly to immigration from Africa, we saw three native cases, two by Trichophyton soudanense and one by Trichophyton tonsurans, with probable transmission in schools. The easier transmission of anthropophilic rather than zoophilic dermatophytes could predict a rise in the incidence of tinea capitis, if diagnosis is poorly recognized or delayed, and it can become a public health problem.