Skip to main content

Advertisement

SpringerLink
Log in

Re-discovery of Trichophyton bullosum in North Africa as a cause of severe dermatophytosis in donkeys

  • Original Article
  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Availability of data and material

The fungal isolates are publically available in the culture collection CCF (Culture Collection of Fungi, Department of Botany, Charles University, Prague, Czech Republic). The DNA sequences obtained in this study were deposited into the GenBank database (www.ncbi.nlm.nih.gov).

References

  • 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

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

Download references

Acknowledgements

We are grateful to Radek Zmítko for the help with graphical adjustments of analysis outputs. We thank Pavlína Lysková and Lenka Zídková for their assistance and advice.

Funding

The contribution of Vit Hubka was supported by the Charles University Research Centre program no. 204069 and Czech Academy of Sciences Long-term Research Development Project [RVO: 61388971].

Author information

Authors and Affiliations

  1. Department of Veterinary Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco (Turin), 10095, Italy

    Andrea Peano & Sara Arnoldi

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

    Adéla Čmoková & Vit Hubka

  3. 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

    Adéla Čmoková & Vit Hubka

Authors
  1. Andrea Peano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sara Arnoldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adéla Čmoková
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vit Hubka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vit Hubka.

Ethics declarations

Consent for publication

All co-authors agreed with this submission.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Below is the link to the electronic supplementary material.

Supplementary file1 (TIF 49086 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peano, A., Arnoldi, S., Čmoková, A. et al. Re-discovery of Trichophyton bullosum in North Africa as a cause of severe dermatophytosis in donkeys. Folia Microbiol 67, 265–275 (2022). https://doi.org/10.1007/s12223-021-00930-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12223-021-00930-9

Search

Navigation