This article reports the first verified cases of infection by Trichophyton bullosum in Africa since the description of the fungus, isolated in 1933 from the coat of horses in Tunisia and Mali. We found the fungus in cutaneous samples obtained from donkeys suffering from severe dermatitis with areas of alopecia and scaling in the surroundings of Cairo (Egypt). Fungal elements (arthroconidia and hyphae) were seen at the microscopy of material collected by skin scraping and digested in NaOH. Fungal colonies grown on various culture media were identified through PCR and sequencing of the ITS rDNA region. Since the original report in Africa and the Middle East, only a few cases have been reported thus far in humans in France and two cases in horses in the Czech Republic and Japan. Trichophyton bullosum seems thus an infrequent cause of dermatophytosis. However, the actual prevalence of this pathogen may be underestimated due to the similarity with T. verrucosum, a predominant cause of infection in cattle, occasionally found on horses and donkeys. Indeed, the two fungi can be distinguished only via molecular methods, which are poorly employed in epidemiological studies on equine and bovine dermatophytosis. The present study results add to our knowledge on the ecology of this poorly explored dermatophyte, supporting the concept that equines are the primary hosts of T. bullosum and confirming the presence of this pathogen in Africa. At the same time, these are the first unequivocally documented infections in donkeys due to T. bullosum.

Department of Botany Faculty of Science Charles University Benátská 2 Prague 2 12801 Czech Republic

Department of Veterinary Sciences University of Turin Largo Paolo Braccini 2 Grugliasco 10095 Italy

Laboratory of Fungal Genetics and Metabolism Institute of Microbiology of the Academy of Sciences of the Czech Republic v v i Vídeňská 1083 Prague 4 14220 Czech Republic

Zobrazit více v PubMed

Abarca M, Castellá G, Martorell J, Cabañes F (2017) Trichophyton erinacei in pet hedgehogs in Spain: occurrence and revision of its taxonomic status. Med Mycol 55:164–172 DOI

Abdalla W, Suliman E, Gabbar A (2005) A report on Trichophyton verrucosum in donkeys in the Sudan. Sudan J Vet Res 20:83–85

Ajello L, Georg LK (1957) In vitro hair cultures for differentiating between atypical isolates of Trichophyton mentagrophytes and Trichophyton rubrum. Mycopathologia 8:3–17

Alzubaidy TSN, Mohammed AJ, Al-Gburi AAH (2018) Comparison of two conventional methods for identification of dermatophyte fungi. Ibn AL-Haitham J Pure Appl Sci 31:21–30 DOI

Baert F, Stubbe D, D’hooge E, Packeu A, Hendrickx M (2020) Updating the taxonomy of dermatophytes of the BCCM/IHEM Collection according to the new standard: a phylogenetic approach. Mycopathologia 185:161–168 PubMed

Cafarchia C, Figueredo LA, Otranto D (2013) Fungal diseases of horses. Vet Microbiol 167:215–234 DOI

Chermette R, Ferreiro L, Guillot J (2008) Dermatophytoses in animals. Mycopathologia 166:385–405 DOI

Čmoková A, Kolařík M, Dobiáš R, Hoyer LL, Janouškovcová H, Kano R, Kuklová I, Lysková P, Machová L, Maier T, Mallátová N, Man M, Mencl K, Nenoff P, Peano A, Prausová H, Stubbe D, Uhrlaß S, Větrovský T, Wiegand C, Hubka V (2020) Resolving the taxonomy of emerging zoonotic pathogens in the Trichophyton benhamiae complex. Fungal Divers 104:333–387 DOI

Čmoková A, Rezaei-Matehkolaei A, Kuklová I, Kolařík M, Shamsizadeh F, Ansari S, Gharaghani M, Miňovská V, Najafzadeh MJ, Nouripour-Sisakht S, Yaguchi T, Zomorodian K, Zarrinfar H, Hubka V (2021) Discovery of new Trichophyton members, T. persicum and T. spiraliforme spp. nov., as a cause of highly inflammatory tinea cases in Iran and Czechia. Microbiol Spectr 9:e00284-e1221 DOI

Georg LK, Camp LB (1957) Routine nutritional tests for the identification of dermatophytes. J Bacteriol 74:113–121 DOI

Heidemann S, Monod M, Gräser Y (2010) Signature polymorphisms in the internal transcribed spacer region relevant for the differentiation of zoophilic and anthropophilic strains of Trichophyton interdigitale and other species of T. mentagrophytes sensu lato. Brit J Dermatol 162:282–295 DOI

Hubka V, Barrs V, Dudová Z, Sklenář F, Kubátová A, Matsuzawa T, Yaguchi T, Horie Y, Nováková A, Frisvad J (2018a) Unravelling species boundaries in the Aspergillus viridinutans complex (section Fumigati): opportunistic human and animal pathogens capable of interspecific hybridization. Persoonia 41:142–174 DOI

Hubka V, Nováková A, Jurjević Ž, Sklenář F, Frisvad JC, Houbraken J, Arendrup MC, Jørgensen KM, Siqueira JP, Gené J, Kolařík M (2018b) Polyphasic data support the splitting of Aspergillus candidus into two species; proposal of Aspergillus dobrogensis sp. nov. Int J Syst Evol Microbiol 68:995–1011 DOI

Hubka V, Peano A, Cmokova A, Guillot J (2018c) Common and emerging dermatophytoses in animals: well-known and new threats. In: Seyedmousavi S, de Hoog GS, Guillot J, Verweij PE (eds) Emerging and Epizootic Fungal Infections in Animals. Springer, Cham, pp 31–79 DOI

Kane J, Smitka C (1978) Early detection and identification of Trichophyton verrucosum. J Clin Microbiol 8:740–747 DOI

Kano R, Kawasaki M, Mochizuki T, Hiruma M, Hasegawa A (2012) Mating genes of the Trichophyton mentagrophytes complex. Mycopathologia 173:103–112 DOI

Kano R, Yoshida E, Yaguchi T, Hubka V, Anzawa K, Mochizuki T, Hasegawa A, Kamata H (2014) Mating type gene (MAT1-2) of Trichophyton verrucosum. Mycopathologia 177:103–112 DOI

Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166 DOI

Knottenbelt D (2005) Skin disorders of donkeys. In: Matthews N, Taylor T (eds) Veterinary Care of Donkeys. International Veterinary Information Service, Ithaca, NY

Kosanke S, Hamann L, Kupsch C, Garcia SM, Chopra A, Gräser Y (2018) Unequal distribution of the mating type (MAT) locus idiomorphs in dermatophyte species. Fungal Genet Biol 118:45–53 DOI

Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34:772–773 PubMed

Le Barzic C, Cmokova A, Denaes C, Arné P, Hubka V, Guillot J, Risco-Castillo V (2021) Detection and control of dermatophytosis in wild European hedgehogs (Erinaceus europaeus) admitted to a french wildlife rehabilitation centre. J Fungi 7:74 DOI

Lebasque J (1933) Les champignons des teignes du cheval et des bovidés. Dissertation, Faculté des Sciences de Paris

Lebasque J (1934) Recherches morphologiques et biologiques sur les Trichophyton mégasporés du cheval et du boeuf. Ann Parasitol 12:418–444

Lysková P, Dobiáš R, Čmoková A, Kolařík M, Hamal P, Šmatláková K, Hušek J, Mencl K, Na M, Poláčková Z, Krnácová A, Palkovičová K, Jablonská D, Macháčová J, Drlík Z, Bázsóová D, Jaworská P, Svobodová L, Hubka V (2021) An outbreak of Trichophyton quinckeanum zoonotic infections in the Czech Republic transmitted from cats and dogs. J Fungi 7:684 DOI

Lysková P, Hubka V, Petřičáková A, Dobiáš R, Čmoková A, Kolařík M (2015) Equine dermatophytosis due to Trichophyton bullosum, a poorly known zoophilic dermatophyte masquerading as T. verrucosum. Mycopathologia 180:407–419 DOI

Nenoff P, Uhrlaß S, Krüger C, Erhard M, Hipler UC, Seyfarth F, Herrmann J, Wetzig T, Schroedl W, Gräser Y (2014) Trichophyton species von Arthroderma benhamiae – a new infectious agent in dermatology. J Dtsch Dermatol Ges 12:571–582 PubMed

Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274 DOI

Philpot C (1967) The differentiation of Trichophyton mentagrophytes from T. rubrum by a simple urease test. Med Mycol 5:189–193 DOI

Pchelin IM, Zlatogursky VV, Rudneva MV, Chilina GA, Rezaei-Matehkolaei A, Lavnikevich DM, Vasilyeva NV, Taraskina AE (2016) Reconstruction of phylogenetic relationships in dermatomycete genus Trichophyton Malmsten 1848 based on ribosomal internal transcribed spacer region, partial 28S rRNA and beta-tubulin genes sequences. Mycoses 59:566–575 DOI

Rochette F, Engelen M, Vanden Bossche H (2003) Antifungal agents of use in animal health–practical applications. J Vet Pharmacol Ther 26:31–53 DOI

Sabou M, Denis J, Boulanger N, Forouzanfar F, Glatz I, Lipsker D, Poirier P, Candolfi E, Letscher-Bru V (2018) Molecular identification of Trichophyton benhamiae in Strasbourg, France: a 9-year retrospective study. Med Mycol 56:723–734 DOI

Sitterle E, Frealle E, Foulet F, Cabaret O, Cremer G, Guillot J, Delhaes L, Botterel F (2012) Trichophyton bullosum: a new zoonotic dermatophyte species. Med Mycol 50:305–309 DOI

Sklenář F, Jurjević Ž, Houbraken J, Kolařík M, Arendrup MC, Jørgensen KM, Siqueira JPZ, Gené J, Yaguchi T, Ezekiel CN, Pereira CS, Hubka V (2021) Re-examination of species limits in Aspergillus section Flavipedes using advanced species delimitation methods and proposal of four new species. Stud Mycol.  https://doi.org/10.1016/j.simyco.2021.100120 DOI

Suh S-O, Grosso KM, Carrion ME (2018) Multilocus phylogeny of the Trichophyton mentagrophytes species complex and the application of matrix-assisted laser desorption/ionization–time-of-flight (MALDI-TOF) mass spectrometry for the rapid identification of dermatophytes. Mycologia 110:118–130 DOI

Suleiman EA, Abdalla WG, Ahmed AH, Abdelgabar MA (2017) Isolation and molecular characterization of dermatophytes in donkeys. Int J Trop Dis Health 26:1–8 DOI

Symoens F, Jousson O, Packeu A, Fratti M, Staib P, Mignon B, Monod M (2013) The dermatophyte species Arthroderma benhamiae: intraspecies variability and mating behaviour. J Med Microbiol 62:377–385 DOI

Ungo-kore HY, Ehinmidu JO, Onaolapo JA, Olonitola OS (2021) Molecular characterisation and phylogenetic analysis of dermatophytic fungi isolated from tinea capitis in Northwest Nigeria using sequence of the 28S rRNA. Microbiol Res 12:646–655 DOI

Watanabe R, Furuta H, Ueno Y, Nukada T, Niwa H, Shinyashiki N, Kano R (2021) First isolation of Trichophyton bullosum from a horse with dermatophytosis in Japan. Med Mycol Case Rep 32:81–83 DOI

White SD, Bourdeau PJ, Brément T, Vandenabeele SI, Haspeslagh M, Bruet V, Sloet van Oldruitenborgh-Oosterbaan MM (2019) Skin disease in donkeys (Equus asinus): a retrospective study from four veterinary schools. Vet Dermatol 30:247-e276 DOI

White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, J. SJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, 315–322