Diagnostic and epidemiological analysis of Trichophyton benhamiae infection on an alpaca (Vicugna pacos) farm in Poland


Diagnostic procedure
Infection source
Trichophyton benhamiae

How to Cite

Łagowski, D., Gnat, S., Nowakiewicz, A., Osińska, M., & Zięba, P. (2021). Diagnostic and epidemiological analysis of Trichophyton benhamiae infection on an alpaca (Vicugna pacos) farm in Poland. Veterinaria Italiana, 57(4), 319–327. https://doi.org/10.12834/VetIt.1967.10530.2


Alpacas (Vicugna pacos) are growing in popularity and are increasingly being presented for veterinary care. Literature reports indicate that dermatophytosis occurring in alpacas accounted for about 3% of dermatological diagnoses. However, there are no reports regarding species of dermatophytes associated with alpacas and reservoirs of infection. In this study, we investigate the diagnosis and epidemiological origin procedure and the virulence enzymes activities of Trichophyton benhamiae isolates obtained from alpacas from a breeding farm. Identification was carried out traditionally by correlating clinical manifestations with micro- and macroscopic examination, and molecular differentiation methods based on Internal Transcribed Spacer (ITS) sequences. Epidemiological analysis was carried out on the basis of Melting Point PCR (MP -PCR) and Amplified Fragment Lenght Polymorphism (AFLP) genotyping. The production of virulence factors was evaluated phenotypically using specific test media. The results obtained from diagnostic tests indicated that the etiological factor of dermatophytosis is T. benhamiae. The same species was also isolated from cowsheds and insects. The MP-PCR and AFLP analyses indicated high invariability of the genomes of the strains isolated from the animals, cowsheds, and insects. In conclusion, animal husbandry outside the natural ecological niche may increase predisposition to dermatophytosis. The treatment of animals alone is insufficient, one should be aware that only elimination of all fungal sources is a long-term success and the key point of therapy.


Bartosch T., Agnes F., Günther C., Silke Uhrlaß, Heydel T., Nenoff P., Baums C. & Schrödl W. 2019. Trichophyton Benhamiae and T. Mentagrophytes Target Guinea Pigs in a Mixed Small Animal Stock. Med Mycol Case Rep, 23, 37–42.

Brasch J., Beck-Jendroschek V., Voss K., Uhrlass S. & Nenoff P. 2016. Arthroderma benhamiae strains in Germany : Morphological and physiological characteristics of the anamorphs. Hautarzt, 67,700–705.

Brasch J. & Wodarg S. 2015. Morphological and Physiological Features of Arthroderma Benhamiae Anamorphs Isolated in Northern Germany. Mycoses, 58, 93–98.

Brillowska-Dabrowska A., Sogaard Nielsen S.,Vedel Nielsen H. & Arendrup M.C. 2010. Optimized 5-Hour Multiplex PCR Test for the Detection of Tinea Unguium: Performance in a Routine PCR Laboratory. Med Mycol, 48, 828–831.

Brillowska-Dabrowska A., Saunte D.M. & Arendrup M.C. 2007. Five-Hour Diagnosis of Dermatophyte Nail Infections with Specific Detection of Trichophyton Rubrum. J Clin Microbiol, 45,1200–1204.

Contet-Audonneau N. & Leyer C. 2010. Émergence d’un Dermatophyte transmis par le cochon d’Inde et proche de Trichophyton Mentagrophytes var. Erinacei: T. Mentagrophytes var. Porcellae. J Mycologie Médicale, 20, 321–325.

Costa G. L. & de Oliveira P. C. 1998. Penicillium Species in Mosquitoes from Two Brazilian Regions. J Basic Microbiol, 38, 343–347.

D’Alterio G. L., Knowles T. G., Eknaes E. I., Loevland I. E. & Foster A. P. 2006. Postal Survey of the Population of South American Camelids in the United Kingdom in 2000/01. Vet Rec, 158, (3), 86-90.

Dalis J. S., Kazeem H.M., Kwaga J. K. P. & Kwanashie C.N. 2014. An Outbreak of Ringworm Caused by Trichophyton Verrucosum in a Group of Calves in Vom, Nigeria. Afr J Microb Res, 8,783–787.

Drouot S., Mignon B., Fratti M., Roosje P. & Monod M. 2009. Pets as the Main Source of Two Zoonotic Species of the Trichophyton Mentagrophytes Complex in Switzerland, Arthroderma Vanbreuseghemii and Arthroderma Benhamiae. Vet Dermatol, 20,13–18.

Figueredo L. A., Cafarchia C., Camarda A., Coccioli C. & Otranto D. 2011. Enzymatic Activity of Microsporum Canis and Trichophyton Mentagrophytes from Breeding Rabbits with and without Skin Lesions. Mycoses, 55, 45–49.

Foster A., Jackson A. & D’Alterio G. L. 2007. Skin Diseases of South American Camelids. In Practice, 29, 216–223.

Gilliam M. D., Prest B. & Morton H. L. 1974. Fungi Isolated from Honey Bees, Apis Mellifera, Fed 2,4-D and Antibiotics. J Invertebrate Pathol, 24, 213–217.

Gnat S., Nowakiewicz A., Ziółkowska G.,Trościańczyk A, Majer-Dziedzic B. & Zięba P. 2017. Evaluation of Growth Conditions and DNA Extraction Techniques Used in the Molecular Analysis of Dermatophytes. J Applied Microbiol, 122,1368–1379.

Gnat S., Łagowski D., Nowakiewicz A., Trościańczyk A. & Zięba P. 2018. Infection of Trichophyton Verrucosum in Cattle Breeders, Poland: A 40-Year Retrospective Study on the Genomic Variability of Strains. Mycoses, 61,681–90.

Gnat S., Łagowski D., Nowakiewicz A., Trościańczyk A. & Zięba P. 2018. Tinea Corporis by Microsporum Canis in Mycological Laboratory Staff: Unexpected Results of Epidemiological Investigation. Mycoses, 61,945–953.

Gnat S., Łagowski D., Nowakiewicz A., Trościańczyk A. & Zięba P. 2019. The Host Range of Dermatophytes, It Is at All Possible? Phenotypic Evaluation of the Keratinolytic Activity of Trichophyton Verrucosum Clinical Isolates. Mycoses, 62, 274–283.

Gnat S., Łagowski D., Nowakiewicz A., Trościańczyk A. & Zięba P. 2018. Phenotypic Characterization of Enzymatic Activity of Clinical Dermatophyte Isolates from Animals with and without Skin Lesions and Humans. J Applied Microbiol, 125,700–709.

Gnat S., Łagowski D., Nowakiewicz A., Trościańczyk A. & Zięba P. 2019. Host- and Pathogen-Dependent Susceptibility and Predisposition to Dermatophytosis. J Med Microbiol, 68, 823–836.

Gnat S., Nowakiewicz A. & Zięba P. 2019. Taksonomia Dermatofitów – Systemy Klasyfikacyjne Się Zmieniają, Problemy Identyfikacyjne Pozostają Te Same. Postępy Mikrobiologii, 58, 49–58.

Gräser Y., Kuijpers A. F., Presber W. & de Hoog G. S. 2000. Molecular Taxonomy of the Trichophyton Rubrum Complex. J Clin Microbiol, 38, 3329–3336.

Halsby K. D., Twomey F., Featherstone C., Foster A., Walsh A., Hewitt K. & Morgan D. 2017. Zoonotic Diseases in South American Camelids in England and Wales. Epidemiol Infect, 145, 1037–1043.

Hiruma J., Kano R., Harada K., Monod M., Hiruma M., Hasegawa A. & Tsuboi R. 2015. Occurrence of Arthroderma Benhamiae Genotype in Japan. Mycopathologia, 179, 219–223.

Hiruma J., Ogawa Y. & Hiruma M. 2015. Trichophyton Tonsurans Infection in Japan: Epidemiology, Clinical Features, Diagnosis and Infection Control. J Dermatol, 42, 245–249.

Hoog G. S., Guarro J., Gené J. & Figueras M. 2000. Atlas of Clinical Fungi. 2nd ed. Utrecht, Netherlands, Centraalbureau voor Schimmelcultures (CBS).

Korniłłowicz-Kowalska T., Kitowski I. & Iglik H. 2013. Geophilic Dermatophytes and Other Keratinophilic Fungi in the Nests of Wetland Birds. Acta Mycologica, 46, 83–107.

Leibner-Ciszak J., Dobrowolska A., Krawczyk B., Kaszuba A. & Staczek P. 2010. Evaluation of a PCR Melting Profile Method for Intraspecies Differentiation of Trichophyton Rubrum and Trichophyton Interdigitale. J Med Microbiol, 59,185–192.

Mayser P. & Budihardja D. 2013. A Simple and Rapid Method to Differentiate Arthroderma Benhamiae from Microsporum Canis. J German Soc Dermatol, 11, 322–327.

Moriello K., Kimberly A. C., Paterson S. & Mignon B. 2017. Diagnosis and Treatment of Dermatophytosis in Dogs and Cats. Vet Dermatol, 28, 266-268.

Nakamura Y., Kano R., Nakamura E., Saito K., Watanabe S. & Hasegawa A. 2002. Case Report. First Report on Human Ringworm Caused by Arthroderma Benhamiae in Japan Transmitted from a Rabbit. Mycoses, 45,129–131.

Nenoff P., Uhrlass S., Kruger C., Erhard M., Hipler U., Seyfarth F., Herrmann J., Wetzig T., Schroedl W. & Graser Y. 2014. Trichophyton Species of Arthroderma Benhamiae - a New Infectious Agent in Dermatology. J German Soc Dermatol, 12, 571–581.

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.

Scott D. W., Vogel J. W., Fleis R. I., Miller W. H. Jr. & Smith M. C. 2011. Skin Diseases in the Alpaca (Vicugna Pacos): A Literature Review and Retrospective Analysis of 68 Cases (Cornell University 1997-2006). Veterinary Dermatology, 22,2–16.

Sharma R., S. Hoog S. C., Presber W. & Gräser Y. 2007. A Virulent Genotype of Microsporum Canis is Responsible for the majority of Human Infections. J Medical Microbiol, 56, 1377–1385.

Shehata A. S., Mukherjee P. K., Aboulatta H. N., I el-Akhras A., Abbadi S. H. & Ghannoum M. A. 2008. Single-Step PCR Using (GACA)4 Primer: Utility for Rapid Identification of Dermatophyte Species and Strains. J Clin Microbiol, 46, 2641–2645.

Sieklucki U., Oh S. & Hoyer L. L. 2014. Frequent Isolation of Arthroderma Benhamiae from Dogs with Dermatophytosis. Vet Dermatol, 25, 39-e14.

Takahashi H., Takahashi-kyuhachi H., Takahashi T., Yarita K., Takayama A., Inomata T., Sano A., Nishimura K. & Kame K. 2008. An Intrafamilial Transmission of Arthroderma Benhamiae in Canadian Porcupines (Erethizon Dorsatum) in a Japanese Zoo. Med Mycol, 46,465–473.

Twomey D. F., Nicholson G. R., Watson E. N. & Foster A. P. 2014. Review of Laboratory Submissions from New World Camelids in England and Wales (2000-2011). Vet J, 200, 51–59.

White T. J., Bruns T., Lee S. & Taylor J. 1990. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In PCR Protocols: A Guide to Methods and Applications (M.A. Innis, D.H. Gelfand, J.J.Shinsky & T.J.White, eds.). San Diego, Academic Press, 315–322.

Ysquierdo Ch.A., Olafson P. U. & Thomas D. 2017. Fungi Isolated From House Flies (Diptera: Muscidae) on Penned Cattle in South Texas. J Med Entomol, 54, 705–711.

Zarrin M.,Vazirianzadeh B., Shams S. S., Mahmoudabadi A. Z. & Rahdar M. 2007. Isolation of Fungi from housefly (Musca Domestica) in Ahwaz, Iran. Pakistan J Med Sci, 23, 917–919.

Copyright (c) 2022 Veterinaria Italiana