Dermatophytoses are superficial and contagious infections caused by dermatophyte fungi. They are the most fre-quent  infectious  dermatosis  in  clinical  practice,  and  can  affect  the  skin,  hair  and  nails.  Its  correct  diagnosis  allows  the understanding of clinical, ecological and epidemiological aspects associated with these microorganisms. Clinical presentation is variable and depends on the habitat (human, animal or soil origin), virulence of the fungus and on the host’s immune status.We report the clinical case of a 62-year-old man with tinea corporis, which stands out for its exuberant clinical pres-entation and by the isolated agent, Trichophyton benhamiae (formerly known as Arthroderma benhamiae), an etiologi-cal agent of dermatophytosis that has not been scientifically reported in Portugal yet.info:eu-repo/semantics/publishedVersio

Sabino, R

Simões, H

Tavares, E

Ussene, E

Veríssimo, C

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CASOS CLÍNICOSTinea Corporis Caused by Trichophy-ton Benhamiae Transmitted by a Dog: First Case Report in Portugal Tinea Corporis Causada por Trichophyton Benhamiae de Transmissão Canina: Primeiro Relato em Portugal Ermelindo Tavares1*, Raquel Sabino2, Helena Simões2, Cristina Veríssimo2,  Esperança Ussene3 *Corresponding Author/Autor Correspondente:Ermelindo Tavares [tavares.ermelindo@gmail.com]Estrada Carlos Lima Costa Nº2, Povos, 2600-009 Vila Franca de Xira, PortugalORCID iD: 0000-0002-4590-3962ABSTRACTDermatophytoses are superficial and contagious infections caused by dermatophyte fungi. They are the most fre-quent infectious dermatosis in clinical practice, and can affect the skin, hair and nails. Its correct diagnosis allows the understanding of clinical, ecological and epidemiological aspects associated with these microorganisms. Clinical presentation is variable and depends on the habitat (human, animal or soil origin), virulence of the fungus and on the host’s immune status.We report the clinical case of a 62-year-old man with tinea corporis, which stands out for its exuberant clinical pres-entation and by the isolated agent, Trichophyton benhamiae (formerly known as Arthroderma benhamiae), an etiologi-cal agent of dermatophytosis that has not been scientifically reported in Portugal yet.KEYWORDS: Adult; Animals, Domestic; Arthrodermataceae; Dermatomycoses; Dogs; Tinea 1. Department of Dermatology and Venereology, Vila Franca de Xira Hospital, Vila Franca de Xira, Portugal. 2. Department of Infectious Diseases, National Reference Laboratory for Parasitic and Fungal Infections, National Institute of Health Dr. Ricardo Jorge, Lisbon, Portugal. 3. Department of Pathology, Vila Franca de Xira Hos-pital, Vila Franca de Xira, Portugal.Received/Recebido: 03/12/2020 - Accepted/Aceite: 07/01/2021 - Published online/Publicado online: 18/01/2021 - Published/Publicado: 31/03/2021 © Author(s) (or their employer(s)) and Gazeta Médica 2021. Re-use permitted under CC BY-NC. No commercial re-use. © Autor (es) (ou seu (s) empregador (es)) e Gazeta Médica 2021. Reutilização permitida de acordo com CC BY-NC. Nenhuma reutilização comercial.GAZETA MÉDICA Nº1 VOL. 8 · JANEIRO/MARÇO 2021 · 29CASOS CLÍNICOSRESUMOAs dermatofitoses ou tinhas (tinea do latim) são infeções superficiais e contagiosas causadas por fungos dermatófitos. São as dermatoses infeciosas mais frequentes na prática clínica, podendo afetar a pele, o cabelo e as unhas. O seu correto diag-nóstico permite compreender os aspetos clínicos, ecológicos e epidemiológicos relacionados com estes microrganismos.  A apresentação clínica é variável e depende do habitat (origem humana, animal ou solo), da virulência do fungo e do estado imunológico do hospedeiro. Relata-se o caso clínico de um homem de 62 anos com tinea corporis, que se destaca pela sua apresentação clínica exuberan-te e pelo agente isolado, Trichophyton benhamiae (anteriomente designado Arthroderma benhamiae), um agente etiológico de dermatofitose ainda sem relato científico em Portugal.  PALAVRAS-CHAVE: Adulto; Animais Domésticos; Arthrodermataceae; Cão; Dermatomicoses; TinhaINTRODUCTIONDermatophytes are keratinophilic filamentous fungi that cause skin, nail and hair infections in animals and humans. Those infections are designated as dermato-phytosis, ringworm (Latin - tinea) or even as epidermo-phytosis. In what concerns to taxonomy, dermatophytes are now classified in seven genera: Trichophyton (T.), Ep-idermophyton, Microsporum (M.), Nannizzia, Paraphyton, Lophophyton and Arthroderma (A.). The genus Tricho-phyton is the most frequently isolated in man. Accord-ing to their habitat, dermatophytes are classified into anthropophilic fungi (infecting almost exclusively the man, with mild or even absent inflammatory reaction), zoophilic (infecting animals and, accidentally, man, with moderate to severe inflammatory reaction) and geophilic (found predominantly in the soil, infecting hu-mans and animals, with moderate to severe inflammato-ry reaction).1,2A. benhamiae (basonym) is a zoophilic dermatophyte whose main reservoir is the guinea pig, in which it can cause hair and nail infections. The first case of dermato-phytosis in humans caused by this specie was reported in Japan in 2002. Since then, it has been isolated in skin, hair and nail dermatophytosis in Northern Europe and the American continent. For many years, this fungus was considered as a Trichophyton species and integrated in the T. mentagrophytes complex.2-5 In the work published in 2017 by de Hoog et al,1 based on the sequencing of the ribosomal DNA, this microorganism was renamed as T. benhamiae.CASE REPORTA 62-year-old man, Caucasian, carpenter, with obesi-ty and dyslipidemia treated with atorvastatin was ob-served in the dermatology consultation due to an ery-thematous and scaly dermatosis with three weeks of evolution. On March 20th, 2020 (day zero) he referred direct contact with a portuguese podengo dog (Canis lupus familiaris) that presented a wound on its left pos-terior leg. On March 30th, 2020 (day 10 post-contact) he noticed the appearance of erythematous papules and pustules on the upper and lower limbs that increased in diameter resulting in round and oval scaly cutaneous plaques with vesicles and pustules on the periphery and blisters that quickly ruptured releasing a purulent exu-date. The lesions were pruritic, and the patient had no complaints regarding other organs and systems. The animal was not taken to the vet for clinical evaluation. Its wound was washed at home with 0.4% sodium hy-pochlorite solution with complete resolution in 14 days. The patient denied contact with other pets.By the day the patient was observed in our department (day 31 post-contact) the dermatological examination revealed, in the right leg, a dermatosis characterized by an erythematous, scaly plaque, with more than 10 cm diameter, with an annular border with vesicles and pustules and slightly scaly center. More than ten round and oval plaques with 3 to 5 cm diameter with erythe-matous and violet edges were also observed. The major-ity of them are coalescent and cutaneous detachment and blisters with purulent exudate content were also detected (Fig. 1). In the thighs and forearms, five erythe-matous, round and oval plaques, with 1 to 2 cm diameter were also present. No lesions were found in the scalp, face and nails. The overall examination was normal. The hypothesis of diagnosis was tinea corporis.Incisional biopsy was performed in the right leg for his-tological examination and direct immunofluorescence (DIF). The first was compatible with tinea corporis, with 30 · GAZETA MÉDICA Nº1 VOL. 8 · JANEIRO/MARÇO 2021CASOS CLÍNICOSAB CFIGURE 1.  Tinea corporis: clinical features. Erythematous plaque with desquamated center, annular and circular rim containing vesicles and pustules on the right leg (A, B). Blister with purulent exudate (B). Round and oval plate and skin detachment (A-C).ABFIGURE 2.  Tinea corporis: histopathological features. Acanthosis, compact hyperkeratosis, orthokeratosis and neutrophils are ob-served in the epidermis and perivascular lymphocytic inflamma-tion is observed in the dermis (A) (hematoxylin and eosin staining, 10x). Hyphae (black arrows) are present in the stratum corneum (B) (periodic acid-Schiff staining, 40x).observation of acanthosis, compact hyperkeratosis, fo-cal orthokeratosis, few neutrophils and hyphae (positive reaction with periodic acid-Schiff staining) in the stra-tum corneum and a mild chronic superficial perivascular lymphocytic inflammation with few eosinophils in the dermis (Fig. 2). The DIF examination was negative. The bacteriological culture of the purulent exudate did not reveal any pathogens. Skin scales were collected for mycological examination, revealing spores in the direct examination with KOH 30%. Sample was inoculated onto Sabouraud dextrose agar (SDA) with chloramphenicol 0.05%, Sabouraud broth with chloramphenicol 0.05% and mycosel agar and incubated at 27ºC for three weeks. The obtained culture revealed a white cottony colony with yellowish reverse with morphological characteristics compatible with T. benhamiae (Fig. 3). Identification was obtained by MALDI-TOF MS (MAtrix-assisted laser desorption/ionization time-of-flight mass spectrometry) with a confidence level of 99.9%. Confirmation was done by molecular method. Total genomic DNA was extracted from purified colonies. The internal transcribed spacer (ITS) region of ribosomal DNA (rDNA) was amplified using the primer set ITS1 and ITS4. Sequencing was performed and nucleotide sequences were edited using the program Chromas 2 and aligned using the program CLUSTAL X2. The obtained sequence was compared with sequences deposited in the NCBI and Westerdijk Fungal Biodiversity Institute – KNAW databases, result-ing in identification of T. benhamiae (97% homology). The obtained sequence was deposited in GenBank with the accession number MT956947 and the isolated strain is referenced as Tb2020HVFX. Treatment was instituted using oral terbinafine 250 mg/day, four weeks and diflucortolone valerate 0.1% + isoconazole nitrate 1% cream twice a day, one week, fol-lowed by omoconazole nitrate 1% cream once a day, two weeks. Complete remission was observed at the end of the treatment period.GAZETA MÉDICA Nº1 VOL. 8 · JANEIRO/MARÇO 2021 · 31CASOS CLÍNICOSDISCUSSIONTo the best of the authors’ knowledge, this is the first report on dermatophytosis caused by T. benhamiae in Portugal. T. benhamiae is a zoophilic fungus and is an etiologic agent of tinea corporis, faciei, manuum and capitis. This specie causes moderate to severe inflammatory skin re-action in man, in particular in children, teenagers and im-munocompromised patients. Its natural reservoir is the guinea pig, but it is occasionally isolated from rabbits, dogs and cats. The infection is usually found in these an-imals and in persons who adopt them as pets. The first report of ringworm caused by this species was from Ja-pan. Subsequently, cases in Northern Europe and South America have been emerging.1-5The taxonomic classification of fungi has undergone ma-jor changes in recent decades. For several years, classi-fication was based on clinical, morphological and phys-iological features of the isolates. As such, T. benhamiae was initially considered as part of the T. mentagrophytes complex and was classified as A. benhamiae (anamorph). However, the development and improvement of mo-lecular methods based on the sequencing of ribosomal DNA led to a huge revolution in fungal taxonomy, in par-ticular in dermatophytes.2,6,7Identification of T. benhamiae is a complex laboratorial process. As such, the definitive diagnosis must be ob-tained by combining several techniques, namely conven-tional mycological methods (direct examination, culture followed by colonies’s macroscopic and microscopic observation and enzymatic profile), molecular method-ologies and technologies based on protein profile (MAL-DI-TOF MS).2,5 Conventional methods do not allow, in some cases, the differentiation between morphological-ly similar dermatophytes.Two phenotypes have been described for T. benhamiae: yellow and white. In the first, the colonies grow slowly, A BFIGURE 3.   T. benhamiae. Macroscopic appearance (mycosel agar): yellowish reverse (A). Microscopic feature (toluidine blue staining, x10): micronidia are present and no spiral hyphae are observed (B). have pleated mycelium and have an orange-yellow re-verse. In SDA media, no macroconidia or spiral hyphae are found and microconidia are rare. The main differ-ential diagnosis is M. canis, which has also yellowish colonies and present thick walled macronidia with 6-12 cells and thin septa. The white phenotype shows fast growing, sprayed, flocose colonies with yellow, orange or brown reverse color. Spiral hyphae are present in some cases and many spherical or clavated microconid-ia are observed; macroconidia are fewer, clavated and cigar-shaped, with 3-8 cells with smooth and thin walls. The main differential diagnosis is T. mentagrophytes, which present several spherical microconidia, spiral hy-phae and clavated, cigar-shaped macroconidia.8-13The diagnosis of dermatophytosis is usually clinical. However, based on clinical presentation there is no differentiation between lesions caused by T. benhamiae and other dermatophytes, particularly the zoophilic one. Therefore, the confirmation of T. benhamiae should be obtained with the methods mentioned above. Further-more, complementary diagnostic methods such as his-tology, cutaneous DIF and bacteriological examination can be extremely important in the exclusion of other infectious and non-infectious dermatoses namely num-mular and stasis eczema, impetigo, subacute cutaneous lupus erythematosus, Hansen’s disease, pemphigus, granuloma annulare, psoriasis and erythema annulare centrifugum.14Topical antifungals are the first-line treatment for local-ized and non-complicated tinea corporis and faciei and should be applied for at least two weeks until complete clearance of the infection. Cases of extensive tinea cor-poris, tinea manuum, capitis, unguium and barbae require topical and systemic treatment. Oral terbinafine, itra-conazole and fluconazole are generally effective alter-natives. Adverse effects with different levels of severity may occur. The duration of the treatment depends on the location and extent of the infection, varying between one and six weeks. Associations of topical antifungals and steroids are important in cases of moderate or se-vere inflammation. They should be used with caution and for a short period to avoid striae, skin atrophy and secondary bacterial infections. The remaining treat-ment is carried out with topical antifungal alone. Pref-erence should be given to low-potency topical steroids, particularly in the face and skin folds. The use of system-ic steroids occurs in cases of tinea capitis with severe in-flammation (Kerion celsi).14In conclusion, the adoption of peculiar species as pets may have serious public health implications. T. benham-32 · GAZETA MÉDICA Nº1 VOL. 8 · JANEIRO/MARÇO 2021CASOS CLÍNICOSiae is an example of that, with an increasing recognition as agent of zoophilic ringworm. As in Northern Europe, the prevalence of this infection in Portugal is very likely to increase. Therefore, it is essential to consider pets as a potential source of infections and to treat them appro-priately together with their owners in order to avoid re-currences, interpersonal and inter-animal transmission. RESPONSABILIDADES ÉTICASCONFLITOS DE INTERESSE: Os autores declaram a inex-istência de conflitos de interesse na realização do pre-sente trabalho.FONTES DE FINANCIAMENTO: Não existiram fontes ex-ternas de financiamento para a realização deste artigo.CONFIDENCIALIDADE DOS DADOS: Os autores declar-am ter seguido os protocolos da sua instituição acerca da publicação dos dados de doentes. CONSENTIMENTO: Consentimento do doente para publicação obtido.PROVENIÊNCIA E REVISÃO POR PARES: Não comissio-nado; revisão externa por pares.ETHICAL DISCLOSURES CONFLICTS OF INTEREST: The authors have no conflicts of interest to declare.FINANCING SUPPORT: This work has not received any contribution, grant or scholarship.CONFIDENTIALITY OF DATA: The authors declare that they have followed the protocols of their work center on the publication of data from patients.PATIENT CONSENT: Consent for publication was ob-tained. PROVENANCE AND PEER REVIEW: Not commissioned; externally peer reviewed.REFERENCES1. de Hoog GS, Dukik K, Monod M, Packeu A, Stubbe D, Hen-drickx M, et al. Toward a novel multilocus phylogenetic taxon-omy for the dermatophytes. Mycopathologia. 2017;182:5-31. doi:10.1007/s11046-016-0073-9. 2. 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. doi:10.1093/mmy/myx100.3. Mochizuki T, Kawasaki M, Ishizaki H, Kano R, Hasegawa A, Tosaki H, et al. Molecular epidemiology of Arthroderma ben-hamiae an emerging pathogen of dermatophytoses in Japan, by polymorphisms of the non-transcribed spacer region of the ribosomal DNA. J Dermatol Sci. 2001;27:14-20. doi:10.1016/S0923-1811(01)00101-3. 4. El-Heis S, Borman AM, Szekely A, Godfrey KM. Tinea Corporis Caused by Arthroderma Benhamiae in a Child. Clin Exp Der-matol. 2016;41:955-7. doi:10.1111/ced.12966.5. Nakamura Y, Kano R, Nakamura E, Saito K, Watanabe S, Hasegawa A. Case Report. First report on human ringworm caused by Arthroderma benhamiae in Japan transmitted from a rabbit. Mycoses. 2002;45:129-131. doi:10.1046/j.1439-0507.2002.00732.x.6. Heidemann S, Monod M, Graser Y. Signature polymorphisms in the internal transcribed spacer region relevant for the dif-ferentiation of zoophilic and anthropophilic strains of Tricho-phyton interdigitale and other species of T. mentagrophytes sensu lato. Br J Dermatol. 2010;162:282-95. doi:10.1111/j.1365-2133.2009.09494.x.7. Kawasaki M. Verification of a taxonomy of dermatophytes based on mating results and phylogenetic analyses. Med My-col. 2011;52:291-95. doi:10.3314/mmj.52.291.8. Symoens F, Jousson O, Packeu A, Fratti M, Staib P, Mignon B, et al. The dermatophyte species Arthroderma benhamiae: in-traspecies variability and mating behaviour. J Med Microbiol. 2013;62:377-85. doi:10.1099/jmm.0.053223-0.9. Contet-Audonneau N, Leyer C. Emergence of a dermato-phyte contracted from guinea pig and close to Trichophyton mentagrophytes var. erinacei: T. mentagrophytes var. por-cellae. J Med Mycol. 2010;20:321-5. doi:10.1016/j.myc-med.2010.08.001.10. Khettar L, Contet-Audonneau N. Cochon d’Inde et der-matophytose. Ann Dermatol Venereol. 2012;139:631-5. doi:10.1016/j.annder.2012.05.007.11. Hiruma J, Kano R, Harada K, Monod M, Hiruma M, Hasega-wa A, et al. Occurrence of Arthroderma benhamiae genotype in Japan. Mycopathologia. 2015;179:219-23. doi:10.1007/s11046-014-9839-0.12. Monod M, Fratti M, Mignon B, Baudraz-Rosselet F. Dermato-phytes transmis par les animaux domestiques. Rev Med Suisse. 2014;10:749-53. 13. Nenoff P, Uhrlaß S, Kruger 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. doi:10.1111/ddg.12390.14. Elewski BE, Hughey LC, Sobera JO, Hay R. Fungal diseases (Cap. 77). In: Bolognia JL, Jorizzo JL, Rapini LP, editors. Der-matology. 3rd ed. London: Elsevier; 2012. pag: 1251-84.GAZETA MÉDICA Nº1 VOL. 8 · JANEIRO/MARÇO 2021 · 33

Tinea Corporis Causada por Trichophyton Benhamiae de Transmissão Canina: Primeiro Relato em Portugal

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Tinea Corporis Causada por Trichophyton Benhamiae de Transmissão Canina: Primeiro Relato em Portugal

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