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Manoyan M.G., Gursheva A.S., Gabuzyan N.A., Panin A.N. Dermatophytoses of animals in the Russian regions: etiological structure and sensitivity of pathogens to antifungal drugs. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2024, Vol. 59, № 2, p. 342-354.
(how to cite this article)

doi:10.15389/agrobiology.2024.2.342eng

UDC: 619:579.62

Acknowledgements:
Supported financially by the Russian Science Foundation, grant No. 22-26-00206, https://rscf.ru/project/22-26-00206/

 

DERMATOPHYTOSES OF ANIMALS IN THE RUSSIAN REGIONS: ETIOLOGICAL STRUCTURE AND SENSITIVITY OF PATHOGENS TO ANTIFUNGAL DRUGS

M.G. Manoyan ✉, A.S. Gursheva, N.A. Gabuzyan, A.N. Panin

All-Russian State Center for Quality and Standardization of Medicines and Feeds for Animals, 5, Zvenigorodskoe sh., Moscow, 123022 Russia, e-mail mycology@vgnki.ru (✉ corresponding author), a.gursheva@vgnki.ru, n.gabuzyan@vgnki.ru, alexanderpanin5083@gmail.com

ORCID:
Manoyan M.G. orcid.org/0000-0001-6347-413X
Gabuzyan N.A. orcid.org/0009-0004-5155-1766
Gursheva A.S. orcid.org/0009-0006-5562-5501
Panin A.N. orcid.org/0000-0002-6001-6739

Final revision received August 14, 2023
Accepted October 23, 2023

 

Systematic monitoring of the etiological structure of animal dermatomycoses allows tracking their incidence, prevalence, changes in the composition of pathogenic species, and identification of previously unidentified etiological agents. In the Russian Federation, knowledge about the incidence of dermatophytoses in agricultural and domestic animals and on the sensitivity of their causative agents to antifungal drugs is scant. In the presented study, we assessed the incidence of dermatophytoses in animals, identified the main etiological agents, and evaluated their sensitivity to the antifungal drugs approved for use in Russia. The purpose of the work is to identify the prevalence of the main etiological agents of dermatophytoses and determine their sensitivity to commonly used antifungal drugs. Of 851 samples of clinical materials collected in 27 Russian regions from farm and domestic animals, 311 isolates (36.54 %) were identified as dermatophytes of the genera Microsporum (M. canis, M. gypseum, M. nanum) and Trichophyton (T. verrucosum, T. mentagrophytes, T. equinum). This indicates high prevalence of microscopic fungi in the clinical materials. We assessed the sensitivity of 125 isolates to antifungal drugs terbinafine, ketoconazole, and enilconazole. Of M. canis isolates, 6.4 % were resistant to terbinafine, 5.6 % to ketoconazole and to enilconazole, of M. gypseum, 0.9 % were resistant to terbinafine, 4.9 % to ketoconazole, and 4.5 % to enilconazole. Of T. verrucosum isolates, 2.6 % were resistant to terbinafine, 0.9 % to ketoconazole, and 0 % to enilconazole, of T. mentagrophytes, 4.2 % were resistant to terbinafine, 3.2 % to ketoconazole and to enilconazole, of T. equinum, 0.7 % were resistant to terbinafine, 0.4 % to ketoconazole and 0.2 % to enilconazole. These data will serve to develop a methodology for systematic assessing the risks of the spread of resistant fungal pathogen species common to humans and animals.

Keywords: dermatophytes, sensitivity, antifungal drug, terbinafine, ketoconazole, enilconazole, farm animals, domestic animals.

 

REFERENCES

  1. Moskaluk A.E., VandeWoude S. Current topics in dermatophyte classification and clinical diagnosis. Pathogens, 2022, 11(9): 957 CrossRef
  2. Moretti A., Agnetti F., Mancianti F., Nardoni S., Righi C., Moretta I., Morganti G., Papini M. Dermatophytosis in animals: epidemiological, clinical and zoonotic aspects. Giornale Italiano di Dermatologia e Venereologia, 2013, 148(6): 563-572.
  3. Paryuni A.D., Indarjulianto S., Widyarini S. Dermatophytosis in companion animals: a review. Veterinary World, 2020, 13(6): 1174-1181 CrossRef
  4. Sylvén K.R., Bergefur A.L., Jacobson M., Wallgren P., Selling L.E. Dermatophytosis caused by trichophyton mentagrophytes complex in organic pigs. Acta Veterinaria Scandinavica, 2023, 65(1): 32 CrossRef
  5. Pontes Z.B., Oliveira A.C., Guerra F.Q., Pontes L.R., Santos J.P. Distribution of dermatophytes from soils of urban and rural areas of cities of Paraiba State, Brazil. Revista do Instituto de Medicina. Tropical de Sao Paulo, 2013, 55(6): 377-383 CrossRef
  6. Jartarkar S.R., Patil A., Goldust Y., Cockerell C.J., Schwartz R.A., Grabbe S,, Goldust M. Pathogenesis, immunology and management of dermatophytosis. Journal of Fungi (Basel), 2021, 8(1): 39 CrossRef
  7. Martinez-Rossi N.M., Peres N.T.A., Bitencourt T.A., Martins M.P., Rossi A. State-of-the-art dermatophyte infections: epidemiology aspects, pathophysiology, and resistance mechanisms. Journal of Fungi (Basel), 2021, 7(8): 629 CrossRef
  8. Seyedmousavi S., Bosco S.M.G., de Hoog S., Ebel F., Elad D., Gomes R.R., Jacobsen I.D., Jensen H.E., Martel A., Mignon B., Pasmans F., Piecková E., Rodrigues A.M., Singh K., Vicente V.A., Wibbelt G., Wiederhold N.P., Guillot J. Fungal infections in animals: a patchwork of different situations. Medical Mycology, 2018, 56(suppl_1): 165-187 CrossRef
  9. Cabañes F.J., Abarca M.L., Bragulat M.R., Castellá G. Seasonal study of the fungal biota of the fur of dogs. Mycopathologia, 1996, 133(1): 1-7 CrossRef
  10. Boehm T.M.S.A., Mueller R.S. Dermatophytosis in dogs and cats — an update. Tierarztl Prax Ausg K Kleintiere Heimtiere, 2019, 47(4): 257-268 CrossRef
  11. Cabañes F.J., Gallo M.G., Mancianti F., Tampieri M.P., Pinter L., Mignon B., Tomsíková A., Fabiková R., Weber A., Payá M.J., Cutuli M.T. Survey of cat and dog dermatophytosis in Europe. The ECMM working group report. “Trends in Medical Mycology”. Proceedings of the 9th Congress of the ECMM and 7th Trends in Invasive Fungal Infections. Bologna, 2003: 49-54.
  12. Moriello K.A., Coyner K., Paterson S., Mignon B. Diagnosis and treatment of dermatophytosis in dogs and cats: clinical consensus guidelines of the World Association for Veterinary Dermatology. Veterinary Dermatology, 2017, 28(3): 266-268 CrossRef
  13. Kottferová L., Molnár L., Čonková E., Major P., Sesztáková E., Szarková A., Slivková M., Kottferová J. Fungal flora in asymptomatic pet guinea pigs and rabbits. Animals (Basel), 2022, 12(18): 2387 CrossRef
  14. Chang C.C., Wechtaisong W., Chen S.Y., Cheng M.C., Chung C.S., Lin L.S., Lien Y.Y., Tsai Y.L. Prevalence and risk factors of zoonotic dermatophyte infection in pet rabbits in northern Taiwan. Journal of Fungi (Basel), 2022, 8(6): 627 CrossRef 
  15. Monod M., Fratti M., Mignon B., Baudraz-Rosselet F. Dermatophytes transmis par les animaux domestiques [Dermatophytes transmitted by pets and cattle]. Rev. Med. Suisse., 2014, 10(424): 749-753.
  16. Rambozzi L., Meneguz P.G., Molinar Min A.R., Pasquetti M., Peano A. Concurrent chorioptic mange and dermatophytosis in dairy goats: case report. Veterinary Sciences, 2022, 9(12): 677 CrossRef
  17. Chermette R., Ferreiro L., Guillot J. Dermatophytoses in animals. Mycopathologia, 2008, 166(5-6): 385-405 CrossRef
  18. Weitzman I., Summerbell R.C. The dermatophytes. Clin. Microbiol. Rev., 1995, 8(2): 240-259 CrossRef
  19. Nenoff P., Handrick W., Krüger C., Vissiennon T., Wichmann K., Gräser Y., Tchernev G. Dermatomycoses due to pets and farm animals: neglected infections? Hautarzt, 2012, 63(11): 848-858 CrossRef
  20. Moriello K.A. Dermatophytosis. In: Feline dermatology. C. Noli, S. Colombo (eds.). Springer, Cham, 2020: 265-296 CrossRef
  21. Nair S.S., Abhishek, Saini S., Chandana M.S., Sharun K., Athira V., Thomas P., Kumar B., Chaturvedi V.K. Dermatophytosis caused by Nannizzia nana (Microsporum nanum): a comprehensive review on a novel pathogen. Brazilian Journal of Microbiology, 2023, 54(1): 509-521 CrossRef
  22. Carter M.E. Microsporum gypseum isolated from ringworm lesions in a horse. New Zealand Veterinary Journal, 1966, 14(7): 92-93 CrossRef
  23. Murmu S., Debnath C., Pramanik A.K., Mitra T., Jana S., Dey S., Banerjee S., Batabyal K. Detection and characterization of zoonotic dermatophytes from dogs and cats in and around Kolkata. Veterinary World, 2015, 8(9): 1078-1082 CrossRef
  24. Sacheli R., Adjetey C., Darfouf R., Harag S., Huynen P., Meex C., Descy J., Melin P., Arrese J., Hayette M.P. A one-year survey of Microsporum audouinii infections in Belgium: epidemiological and genotypic characterization. Clin. Microbiol. Infect., 2016, 22(3): 285.E9-285.E17 CrossRef
  25. Kieliger S., Glatz M., Cozzio A., Bosshard P.P. Tinea capitis and tinea faciei in the Zurich area — an 8-year survey of trends in the epidemiology and treatment patterns. Journal of the European Academy of Dermatology and Venereology, 2015, 29(8): 1524-1529 CrossRef
  26. Donghi D., Hauser V., Bosshard P.P. Microsporum audouinii tinea capitis in a Swiss school: assessment and management of patients and asymptomatic carriers. Med. Mycol., 2011, 49: 324-328 CrossRef
  27. Pozdnyakova O.N., Makhnovets E.N., Reshetnikova T.B., Nemchaninova O.B.Epidemiologiya zooantropofil’nykh dermatomikozov v gorode Novosibirske. Problemy meditsinskoy mikologii, 2003, 5(2): 64. 
  28. de Hoog G.S., Guarro J., Gené J., Ahmed S., Al-Hatmi A.M.S., Figueras M.J., Vitale R.G. Atlas of clinical fungi, 4th edition. Hilversum, 2020.
  29. Fakhretdinova Kh.S., Medvedeva E.A., Burkhanova N.R., Gushchina R.T. Dinamika dermatomikozov v Respublike Bashkortostan v 1998-2003 gg. Problemy meditsinskoy mikologii, 2004, 6(2): 124-125 (in Russ.).
  30. Nussipov Y., Markabayeva A., Gianfaldoni S., Tchernev G., Wollina U., Lotti J., Roccia M.G., Fioranelli M., Lotti T. Clinical and epidemiological features of dermatophyte infections in Almaty, Kazakhstan. Open Access Macedonian Journal of Medical Sciences, 2017, 5(4): 409-413 CrossRef
  31. Khismatullina Z.R., Al’khashash S., Aydybaeva M.G., Dagkhamin I. Klinicheskie proyavleniya zooantroponoznoy trikhofitii. Sovremennye problemy nauki i obrazovaniya, 2020, 5: 145 CrossRef (in Russ.).
  32. Fattahi A., Shirvani F., Ayatollahi A., Rezaei-Matehkolaei A., Badali H., Lotfali E., Ghasemi R., Pourpak Z., Firooz A. Multidrug-resistant Trichophyton mentagrophytes genotype VIII in an Iranian family with generalized dermatophytosis: report of four cases and review of literature. International Journal of Dermatology, 2021, 60(6): 686-692 CrossRef
  33. Gnat S., Łagowski D., Nowakiewicz A., Dyląg M., Osińska M. Complementary effect of mechanism of multidrug resistance in Trichophyton mentagrophytes isolated from human dermatophytoses of animal origin. Mycoses, 2021, 64(5): 537-549 CrossRef
  34. Adimi P., Hashemi S.J., Mahmoudi M., Mirhendi H., Shidfar M.R., Emmami M., Rezaei-Matehkolaei A., Gramishoar M., Kordbacheh P. In-vitro activity of 10 antifungal agents against 320 Dermatophyte strains using microdilution method in Tehran. Iranian Journal of Pharmaceutical Research, 2013, 12(3): 537-545.
  35. Hsiao Y.H., Chen C., Han H.S., Kano R. The first report of terbinafine resistance Microsporum canis from a cat. Journal of Veterinary Medical Science, 2018, 80(6): 898-900 CrossRef
  36. Afshari M.A., Shams-Ghahfarokhi M., Razzaghi-Abyaneh M. Antifungal susceptibility and virulence factors of clinically isolated dermatophytes in Tehran, Iran. Iranian Journal of Microbiology, 2016, 8(1): 36-46.
  37. Hryncewicz-Gwóźdź A., Kalinowska K., Plomer-Niezgoda E., Bielecki J., Jagielski T. Increase in resistance to fluconazole and itraconazole in Trichophyton rubrum clinical isolates by sequential passages in vitro under drug pressure. Mycopathologia, 2013, 176(1-2): 49-55 CrossRef
  38. Manoyan M., Sololov V., Gursheva A., Panin A. Sensitivity of isolated dermatophyte strains to antifungal drugs in the Russian Federation. Journal of Fungi, 2019, 5(4): 95 9th Trends in Medical Mycology Held on 11-14 October 2019, Nice, France: P034 CrossRef
  39. Ilhan Z., Karaca M., Ekin I.H., Solmaz H., Akkan H.A., Tutuncu M. Detection of seasonal asymptomatic dermatophytes in Van cats. Braz. J. Microbiol., 2016, 47(1): 225-230 CrossRef
  40. Hernandez-Bures A., Pieper J.B., Bidot W.A., O’Dell M., Sander W.E., Maddox C.W. Survey of dermatophytes in stray dogs and cats with and without skin lesions in Puerto Rico and confirmed with MALDI-TOF MS. PLoS ONE, 2021, 16(9): e0257514 CrossRef
  41. Segal E., Elad D. Human and zoonotic dermatophytoses: epidemiological aspects. Front Microbiol., 2021, 12: 713532 CrossRef
  42. Beck W., Clark H.H. Zoophile Dermatophyten als Epizoonoseerreger und ihre Bedeutung in der Dermatologie [Zoophilic dermatophytes as epizoonoses pathogens and their significance to dermatology]. Hautarzt, 1998, 49(6): 457-461 CrossRef
  43. Dworecka-Kaszak B., Biegańska M.J., Dąbrowska I. Occurrence of various pathogenic and opportunistic fungi in skin diseases of domestic animals: a retrospective study. BMC Vet. Res., 2020, 16(1): 248 CrossRef
  44. Radentz W.H. Fungal skin infections associated with animal contact. Am. Fam. Physician., 1991, 43(4): 1253-1256.
  45. Dalis J.S., Kazeem H.M., Kwaga J.K.P., Kwanashie C.N. Prevalence and distribution of dermatophytosis lesions on cattle in Plateau State, Nigeria. Veterinary World, 2019, 12(9): 1484-1490 CrossRef 
  46. Rossel’khoznadzor. Gosudarstvennaya informatsionnaya sistema v oblasti veterinarii VetIS [State information system in veterinary medicine VetIS]. Available: https://vetrf.ru/. No date (in Russ.).
  47. Bhattacharya S., Esquivel B.D., White T.C. Overexpression or deletion of ergosterol biosynthesis genes alters doubling time, response to stress agents, and drug susceptibility in Saccharomyces cerevisiae. mBio, 2018, 9(4): e01291-18. CrossRef
  48. Pierson C.A., Eckstein J., Barbuch R., Bard M. Ergosterol gene expression in wild-type and ergosterol-deficient mutants of Candida albicans. Med. Mycol., 2004, 42(4): 385-389 CrossRef
  49. Ryder N.S. Terbinafine: mode of action and properties of the squalene epoxidase inhibition. Br. J. Dermatol., 1992, 126(Suppl 39): 2-7 CrossRef
  50. Ryder N.S., Dupont M.C. Inhibition of squalene epoxidase by allylamine antimycotic compounds. A comparative study of the fungal and mammalian enzymes. Biochem. J., 1985, 230(3): 765-770 CrossRef
  51. Gupta A.K., Kohli Y. In vitro susceptibility testing of ciclopirox, terbinafine, ketoconazole and itraconazole against dermatophytes and nondermatophytes, and in vitro evaluation of combination antifungal activity. Br. J. Dermatol., 2003, 149(2): 296-305 CrossRef
  52. Aneke CI, Rhimi W, Hubka V, Otranto D, Cafarchia C. Virulence and Antifungal Susceptibility of Microsporum canis Strains from Animals and Humans. Antibiotics, 2021, 10(3): 296 CrossRef
  53. Manoyan M.G., Sokolov V.V., Gursheva A.S., Gabuzyan N.A., Panin A.N. Uspekhi meditsinskoy mikologii, 2019. 20: 431-436 (in Russ.).   

 

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