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Tinea corporis caused by Trichophyton benhamiae: report of the first case transmitted by guinea pig in Brazil Study conducted at the Private Practice, Barra da Tijuca, Rio de Janeiro, RJ, Brazil.

Dear Editor,

Trichophyton benhamiae (T. benhamiae) is an emerging zoophilic dermatophyte, an important causative agent of dermatophytosis in several parts of the world. It is transmitted mainly by guinea pigs (Cavia porcellus), and its identification is carried out by molecular and proteomic methods, in addition to morphological ones.

We report the first case of tinea corporis in a child living in Rio de Janeiro, Brazil, transmitted by a guinea pig.

A ten-year-old, healthy white female patient seeked medical care because two weeks before, she had presented with multiple, mildly pruritic lesions on the neck, submandibular region, left forearm, and right scapular region, ranging from 2‒6 cm in diameter (Fig. 1). She had been in contact with a guinea pig for one month which was initially healthy, but which developed a skin lesion after ten days.

Figure 1
Erythematous-desquamative, circinated, vesico-crusted plaques with well-defined edges. They show centrifugal growth and central clearing.

Direct mycological examination of the skin desquamation showed septate hyaline hyphae and arthroconidia (Fig. 2). Trichophyton benhamiae was isolated and identified by its macro- and micromorphological aspects (Fig. 3 A‒D) and by proteomic analysis (MALDI ToF-MS, Biomerieux, confidence level 99.9%).

Figure 2
Direct mycological examination: skin desquamation containing septate, branched hyaline hyphae and arthroconidia. KOH 40% (×100).

Figure 3
Trichophyton benhamiae. (A) Macromorphology of the colony showing a yellowish-beige, velvety surface with radial growth. (B) Back of the colony, bright yellow; (C and D) micromorphology, with septate, branched hyaline hyphae and rounded, pyriform microconidia, grouped in clusters or arranged laterally and at the ends of the hyphae. Lactophenol-cotton blue (×100 and ×400).

She started treatment with oral terbinafine, 250 mg/day, for four weeks, with complete resolution of the lesions (Fig. 4). The animal was treated by the veterinarian with clotrimazole cream, applied twice a day for two weeks, with improvement of the condition.

Figure 4
Complete resolution after 30 days of oral treatment.

Trichophyton benhamiae, first described by Ajello and Cheng in 1967,11 Ajello L, Cheng SL. The perfect state of Trichophyton mentagrophytes. Sabouraudia. 1967;5:230-4. is a zoophilic dermatophyte fungus that has gained global prominence in the last 20 years.22 Nenoff P, Uhrlaß S, Krüger C, Erhard M, Hipler UC, Seyfarth F, et al. Trichophyton species of Arthroderma benhamiae ‒ a new infectious agent in dermatology. J Dtsch Dermatol Ges. 2014;12:571-81.

The first case of infection in humans was published in 2002, in Japan.33 Kano R, Nakamura Y, Yasuda K, Watari T, Watanabe S, Takahashi H, et al. The first isolation of Arthroderma benhamiae in Japan. Microbiol Immunol. 1998;42:575-8. Since then, cases have been reported in Germany and other European countries, as well as in China and the Americas, and their prevalence has been increasing, especially in Germany, Switzerland, and Japan.44 Berlin M, Kupsch C, Ritter L, Stoelcker B, Heusinger A, Gräser Y. German-wide analysis of the prevalence and the propagation factors of the zoonotic dermatophyte Trichophyton benhamiae. J Fungi (Basel). 2020;6:161. Fratti et al., in a recent Swiss study that analyzed the prevalence of dermatophytes in different animals, showed that T. benhamiae was the most prevalent dermatophyte in guinea pigs, found in 48 of 50 animals,55 Fratti M, Bontems O, Salamin K, Guenova E, Monod M. Survey on dermatophytes isolated from animals in Switzerland in the context of the prevention of zoonotic dermatophytosis. J Fungi (Basel). 2023;9:253. data confirmed in another prevalence study carried out in Germany.44 Berlin M, Kupsch C, Ritter L, Stoelcker B, Heusinger A, Gräser Y. German-wide analysis of the prevalence and the propagation factors of the zoonotic dermatophyte Trichophyton benhamiae. J Fungi (Basel). 2020;6:161.

In addition to the guinea pig, transmission can occur through other animals, such as small rodents, rabbits, cats, dogs, and porcupines.22 Nenoff P, Uhrlaß S, Krüger C, Erhard M, Hipler UC, Seyfarth F, et al. Trichophyton species of Arthroderma benhamiae ‒ a new infectious agent in dermatology. J Dtsch Dermatol Ges. 2014;12:571-81.,66 Bartosch T, Frank A, Günther C, Uhrlaβ S, Heydel T, Nenoff P, et al. Trichophyton benhamiae and T. mentagrophytes target guinea pigs in a mixed small animal stock. Med Mycol Case Rep. 2018;23:37-42.,77 Peano A, Hubka V, Cavana P, Ottino C, Blandolino M, Min ARM, et al. Cases of dermatophytosis caused by Trichophyton benhamiae var. luteum and T. europaeum, newly described dermatophytes within the T. benhamiae complex. Vet Dermatol. 2022;33:440-5. The first and only case of tinea corporis caused by T. benhamiae, reported in Brazil, was transmitted by a cat.88 de Freitas RS, de Freitas THP, Siqueira LPM, Gimenes VMF, Bernard G. First report of tinea corporis caused by Arthroderma benhamiae in Brazil. Braz J Microbiol. 2019;50:985-7.

Berlin et al. concluded, in a study on the prevalence and dissemination factors of T. benhamiae, that guinea pigs can be asymptomatic carriers: 92.7% of the colonized animals did not have any apparent lesions.44 Berlin M, Kupsch C, Ritter L, Stoelcker B, Heusinger A, Gräser Y. German-wide analysis of the prevalence and the propagation factors of the zoonotic dermatophyte Trichophyton benhamiae. J Fungi (Basel). 2020;6:161.

Clinically, the lesions have an inflammatory nature, due to the fact that they are not adapted to human parasitism, manifesting themselves as tinea faciei, tinea corporis, tinea barbae, tinea capitis, Kerion celsi and tinea unguium.22 Nenoff P, Uhrlaß S, Krüger C, Erhard M, Hipler UC, Seyfarth F, et al. Trichophyton species of Arthroderma benhamiae ‒ a new infectious agent in dermatology. J Dtsch Dermatol Ges. 2014;12:571-81.,88 de Freitas RS, de Freitas THP, Siqueira LPM, Gimenes VMF, Bernard G. First report of tinea corporis caused by Arthroderma benhamiae in Brazil. Braz J Microbiol. 2019;50:985-7. It mainly affects children and adolescents through direct contact with domestic animals, but it can also appear in young adults and immunosuppressed patients.

The identification of the fungus is made by morphological characteristics, associated with proteomic and molecular techniques.22 Nenoff P, Uhrlaß S, Krüger C, Erhard M, Hipler UC, Seyfarth F, et al. Trichophyton species of Arthroderma benhamiae ‒ a new infectious agent in dermatology. J Dtsch Dermatol Ges. 2014;12:571-81.,44 Berlin M, Kupsch C, Ritter L, Stoelcker B, Heusinger A, Gräser Y. German-wide analysis of the prevalence and the propagation factors of the zoonotic dermatophyte Trichophyton benhamiae. J Fungi (Basel). 2020;6:161.,99 Sabou M, Denis J, Boulanger N, Forouzanfar F, Glatz I, Lipsker D, et al. Molecular identification of Trichophyton benhamiae in Strasbourg, France: a 9-year retrospective study. Med Mycol. 2018;56:723-34. The yellowish color observed in the macromorphological examination of the colony suggests Microsporum canis; however, the micromorphology is more suggestive of T. mentagrophytes, showing rounded or oval microconidia, grouped or implanted laterally in the hyphae. The laboratory technician suspicion is important for the correct identification of the colony, confirming it through molecular or proteomic characteristics, as in the reported case.22 Nenoff P, Uhrlaß S, Krüger C, Erhard M, Hipler UC, Seyfarth F, et al. Trichophyton species of Arthroderma benhamiae ‒ a new infectious agent in dermatology. J Dtsch Dermatol Ges. 2014;12:571-81.,1010 Frías-De-León MG, Martínez-Herrera E, Atoche-Diéguez CE, Cespón JLG, Uribe B, Arenas R, et al. Molecular identification of isolates of the Trichophyton mentagrophytes complex. Int J Med Sci. 2020;17:45-52.

The treatment of choice for extensive cases is oral terbinafine. In isolated lesions, topical therapy with azoles, terbinafine, or cyclopiroxolamine is indicated, with excellent response.22 Nenoff P, Uhrlaß S, Krüger C, Erhard M, Hipler UC, Seyfarth F, et al. Trichophyton species of Arthroderma benhamiae ‒ a new infectious agent in dermatology. J Dtsch Dermatol Ges. 2014;12:571-81.

The clinician must be aware of new species of fungi as etiological agents of cutaneous mycoses, especially in children, due to the current diversification of domestic animals in contact with humans. The laboratory technician needs to be prepared to suspect and identify new species of fungi as etiological agents of cutaneous mycoses, especially infections caused by T. benhamiae, in which the usual morphological identification is not so characteristic. It is up to the veterinarian to advise animal owners about the possibility of the transmission of cutaneous mycoses to those who live with them.

The integration of different specialties and laboratory support is invaluable for a favorable patient outcome.

  • Financial support
    None declared.
  • Study conducted at the Private Practice, Barra da Tijuca, Rio de Janeiro, RJ, Brazil.

References

  • 1
    Ajello L, Cheng SL. The perfect state of Trichophyton mentagrophytes. Sabouraudia. 1967;5:230-4.
  • 2
    Nenoff P, Uhrlaß S, Krüger C, Erhard M, Hipler UC, Seyfarth F, et al. Trichophyton species of Arthroderma benhamiae ‒ a new infectious agent in dermatology. J Dtsch Dermatol Ges. 2014;12:571-81.
  • 3
    Kano R, Nakamura Y, Yasuda K, Watari T, Watanabe S, Takahashi H, et al. The first isolation of Arthroderma benhamiae in Japan. Microbiol Immunol. 1998;42:575-8.
  • 4
    Berlin M, Kupsch C, Ritter L, Stoelcker B, Heusinger A, Gräser Y. German-wide analysis of the prevalence and the propagation factors of the zoonotic dermatophyte Trichophyton benhamiae. J Fungi (Basel). 2020;6:161.
  • 5
    Fratti M, Bontems O, Salamin K, Guenova E, Monod M. Survey on dermatophytes isolated from animals in Switzerland in the context of the prevention of zoonotic dermatophytosis. J Fungi (Basel). 2023;9:253.
  • 6
    Bartosch T, Frank A, Günther C, Uhrlaβ S, Heydel T, Nenoff P, et al. Trichophyton benhamiae and T. mentagrophytes target guinea pigs in a mixed small animal stock. Med Mycol Case Rep. 2018;23:37-42.
  • 7
    Peano A, Hubka V, Cavana P, Ottino C, Blandolino M, Min ARM, et al. Cases of dermatophytosis caused by Trichophyton benhamiae var. luteum and T. europaeum, newly described dermatophytes within the T. benhamiae complex. Vet Dermatol. 2022;33:440-5.
  • 8
    de Freitas RS, de Freitas THP, Siqueira LPM, Gimenes VMF, Bernard G. First report of tinea corporis caused by Arthroderma benhamiae in Brazil. Braz J Microbiol. 2019;50:985-7.
  • 9
    Sabou M, Denis J, Boulanger N, Forouzanfar F, Glatz I, Lipsker D, et al. Molecular identification of Trichophyton benhamiae in Strasbourg, France: a 9-year retrospective study. Med Mycol. 2018;56:723-34.
  • 10
    Frías-De-León MG, Martínez-Herrera E, Atoche-Diéguez CE, Cespón JLG, Uribe B, Arenas R, et al. Molecular identification of isolates of the Trichophyton mentagrophytes complex. Int J Med Sci. 2020;17:45-52.

Publication Dates

  • Publication in this collection
    31 May 2024
  • Date of issue
    2024

History

  • Received
    21 May 2023
  • Accepted
    30 June 2023
  • Published
    24 Feb 2024
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