The enzymatic and antifungal profiles of dermatophytes play an important role in causing infections in humans and animals. This study aimed to assess the virulence factors produced by Microsporum canis strains, in vitro antifungal profile and the relationship between virulence, antifungal profile and occurrence of lesions in animals and humans. A total of 100 M. canis strains from humans with tinea corporis (n = 10) and from animals presenting (n = 64) or not (n = 26) skin lesions was employed to evaluate phospholipase (Pz), hemolytic (Hz), lipase (Lz), catalase (Ca), and thermotolerance (GI) activities. In addition, in vitro antifungal profile was conducted using the CLSI broth microdilution method. A statistically significant difference (p < 0.05) in Lz and Ca values was revealed among strains from hosts with and without lesions. Voriconazole, terbinafine, and posaconazole were the most active drugs followed by ketoconazole, griseofulvin, itraconazole, and fluconazole in decreasing activity order. The significant positive correlation between azole susceptibility profile of M. canis and virulence factors (i.e., hemolysin and catalase) suggest that both enzyme patterns and antifungal susceptibility play a role in the appearance of skin lesions in animals and humans.

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

Department of Veterinary Pathology and Microbiology University of Nigeria 410001 Nsukka Nigeria

Dipartimento di Medicina Veterinaria Università degli Studi Aldo Moro 70010 Bari Italy

Faculty of Veterinary Sciences Bu Ali Sina University 6517658978 Hamedan Iran

Laboratory of Fungal Genetics and Metabolism Institute of Microbiology of the Academy of Sciences 14220 Prague Czech Republic

Zobrazit více v PubMed

Pier A.C., Moriello K.A. Parasitic relationship between Microsporum canis and the cat. Med. Mycol. 1998;36:271–275. PubMed

Aly R., Hay R.J., Palacio A.D., Galimberti R. Epidemiology of tinea capitis. Med. Mycol. 2000;38:183–188. doi: 10.1080/mmy.38.s1.183.188. PubMed DOI

Cafarchia C., Romito D., Sasanelli M., Lia R., Capelli G., Otranto D. The epidemiology of canine and feline dermatophytosis in southern Italy. Mycoses. 2004;47:508–513. doi: 10.1111/j.1439-0507.2004.01055.x. PubMed DOI

Cafarchia C., Romito D., Capelli G., Guillot J., Otranto D. Isolation of Microsporum canis from the hair coat of pet dogs and cats belonging to owners diagnosed with M. canis tinea corporis. Vet. Dermatol. 2006;17:327–331. doi: 10.1111/j.1365-3164.2006.00533.x. PubMed DOI

Patel G.A., Schwartz R.A. Tinea capitis: Still an unsolved problem? Mycoses. 2011;54:183–188. doi: 10.1111/j.1439-0507.2009.01819.x. PubMed DOI

Silveira-Gomes F., Oliveira E.F.D., Nepomuceno L.B., Pimentel R.F., Marques-da-Silva S.H., Mesquita-da-Costa M. Der-matophytosis diagnosed at the evandro chagas institute, Pará, Brazil. Braz. J. Microbiol. 2013;44:443–446. PubMed PMC

Moriello K.A., Coyner K., Paterson S. Diagnosis and treatment of dermatophytosis in dogs and cats: Clinical Consensus Guidelines of the World Association for Veterinary Dermatology. Vet. Dermatol. 2017;28:266–e68. doi: 10.1111/vde.12440. PubMed DOI

Monod M. Secreted Proteases from Dermatophytes. Mycopathologia. 2008;166:285–294. doi: 10.1007/s11046-008-9105-4. PubMed DOI

Gnat S., Łagowski D., Nowakiewicz A. Major challenges and perspectives in the diagnostics and treatment of dermatophyte infections. J. Appl. Microbiol. 2020;129:212–232. doi: 10.1111/jam.14611. PubMed DOI

Cafarchia C., Figueredo L.A., Coccioli C., Camarda A., Otranto M. Enzymatic activity of Microsporum canis and Trichophyton mentagrophytes from breeding rabbits with and without skin lesions. Mycoses. 2011;55:45–49. doi: 10.1111/j.1439-0507.2010.01997.x. PubMed DOI

Elavarashi E., Kindo A.J., Rangarajan S. Enzymatic and Non-Enzymatic Virulence Activities of Dermatophytes on Solid Media. J. Clin. Diagn. Res. 2017;11:DC23–DC25. doi: 10.7860/JCDR/2017/23147.9410. PubMed DOI PMC

Chinnapun D. Virulence factors involved in pathogenicity of dermatophytes. Walailak J. Sci. Tech. 2015;12:573–580.

Cafarchia C., Romito D., Coccioli C., Camarda A., Otranto M. Phospholipase activity of yeasts from wild birds and possible implications for human disease. Med. Mycol. 2008;46:429–434. doi: 10.1080/13693780701885636. PubMed DOI

Schaller M., Borelli C., Korting H.C., Hube B. Hydrolytic enzymes as virulence factors of Candida albicans. Mycoses. 2005;48:365–377. doi: 10.1111/j.1439-0507.2005.01165.x. PubMed DOI

Mohammadi F., Ghasemi Z., Familsatarian B., Salehi E., Sharifynia S., Barikani A., Mirzadeh M., Hosseini M.A. Relationship between antifungal susceptibility profile and virulence factors in Candida albicans isolated from nail specimens. Rev. Soc. Bras. Med. Trop. 2020;53:e20190214. doi: 10.1590/0037-8682-0214-2019. PubMed DOI PMC

Mawby D.I., Whittemore J.C., Fowler L.E., Papich M.G. Comparison of absorption characteristics of oral reference and compounded itraconazole formulations in healthy cats. J. Am. Vet. Med. Assoc. 2018;252:195–200. doi: 10.2460/javma.252.2.195. PubMed DOI

Bueno J.G., Martinez C., Zapata B., Sanclemente G., Gallego M., Mesa A.C. In vitro activity of fluconazole, itraconazole, voriconazole and terbinafine against fungi causing onychomycosis. Clin. Exp. Dermatol. 2009;35:658–663. doi: 10.1111/j.1365-2230.2009.03698.x. PubMed DOI

Aneke C.I., Rhimi W., Otranto D., Cafarchia C. Synergistic Effects of Efflux Pump Modulators on the Azole Antifungal Susceptibility of Microsporum canis. Mycopathology. 2020;185:1–10. doi: 10.1007/s11046-019-00419-7. PubMed DOI

Hsiao Y.-H., Chen C., Han H.S., Kano R. The first report of terbinafine resistance Microsporum canis from a cat. J. Vet.-Med. Sci. 2018;80:898–900. doi: 10.1292/jvms.17-0680. PubMed DOI PMC

Aneke C.I., Otranto D., Cafarchia C. Therapy and Antifungal Susceptibility Profile of Microsporum canis. J. Fungi. 2018;4:107. doi: 10.3390/jof4030107. PubMed DOI PMC

Fernández-Torres B., Carrillo-Muñoz A., Ortoneda M., Pujol I., Pastor F.J., Guarro J. Interlaboratory evaluation of the Etest® for antifungal susceptibility testing of dermatophytes. Med. Mycol. 2003;41:125–130. PubMed

Abastabar M., Jedi A., Guillot J., Ilkit M., Eidi S., Hedayati M.T., Shokohi T., Ghazvini R.D., Rezaei-Matehkolaei A., Katiraee F., et al. In vitro activities of 15 antifungal drugs against a large collection of clinical isolates of Microsporum canis. Mycoses. 2019;62:1069–1078. doi: 10.1111/myc.12986. PubMed DOI

Ghannoum M. Azole Resistance in Dermatophytes: Prevalence and Mechanism of Action. J. Am. Podiatr. Med. Assoc. 2015;106:79–86. doi: 10.7547/14-109. PubMed DOI

Cafarchia C., Gasser R.B., Figueredo L.A., Weigl S., Danesi P., Capelli G., Otranto D. An improved molecular diagnostic assay for canine and feline dermatophytosis. Med. Mycol. 2013;51:136–143. doi: 10.3109/13693786.2012.691995. PubMed DOI

Vermout S., Tabart J., Baldo A., Mathy A., Losson B., Mignon B. Pathogenesis of Dermatophytosis. Mycopathologia. 2008;166:267–275. doi: 10.1007/s11046-008-9104-5. PubMed DOI

Döğen A., Gümral R., Ilkit M. Haemolytic and co-haemolytic (CAMP-like) activity in dermatophytes. Mycoses. 2014;58:40–47. doi: 10.1111/myc.12269. PubMed DOI

Tamayo D., Muñoz J.F., Almeida A.J., Puerta J.D., Restrepo Á., Cuomo C.A., McEwen J.G., Hernández O. Paracoccidioides spp. catalases and their role in antioxidant defense against host defense responses. Fungal Genet. Biol. 2017;100:22–32. doi: 10.1016/j.fgb.2017.01.005. PubMed DOI PMC

Hellgren L., Vincent L. Lipolytic activity of some dermatophytes. J. Med. Microbiol. 1980;13:155–157. doi: 10.1099/00222615-13-1-155. PubMed DOI

Lopez-Martinez R., Manzano-Gayosso P., Miert M., Mendez-Tovar L.J., Hernandez-Hernandez F. Exoenzimes de der-matofitos aislados de tinas agudas y cronicas. Rev. Latin. Am. Microbiol. 1994;36:17–20. PubMed

Gnat S., Łagowski D., Nowakiewicz A., Zięba P. Phenotypic characterization of enzymatic activity of clinical dermatophyte isolates from animals with and without skin lesions and humans. J. Appl. Microbiol. 2018;125:700–709. doi: 10.1111/jam.13921. PubMed DOI

Muhsin T.M., Aubaid A.H., Al-Duboon A.H. Extracellular enzyme activities of dermatophytes and yeast isolates on solid media. Mycoses. 1997;40:465–469. doi: 10.1111/j.1439-0507.1997.tb00186.x. PubMed DOI

Viani F.C., Dos Santos M., Paula C.R., Larson C.E., Gambale W. Production of extracellular enzymes by Microsporum canis and their role in its virulence. Med. Mycol. 2001;39:463–468. doi: 10.1080/mmy.39.5.463.468. PubMed DOI

Stoytcheva M., Montero G., Zlatev R., Leon J.A., Gochew V. Analytical methods for lipase activity determination: A re-view. Curr. Anal. Chem. 2012;8:400–407. doi: 10.2174/157341112801264879. DOI

Aktas E., Yıgıt N. Hemolytic activity of dermatophytes species isolated from clinical specimens. J. Med. Mycol. 2015;25:e25–e30. doi: 10.1016/j.mycmed.2014.10.014. PubMed DOI

Almeida-Paes R., de Oliveira L.C., Oliveira M.M.E., Gutierrez-Galhardo M.C., Nosanchuk J.D., Zancopé-Oliveira R.M. Phenotypic Characteristics Associated with Virulence of Clinical Isolates from the SporothrixComplex. BioMed. Res. Int. 2015;2015:1–10. doi: 10.1155/2015/212308. PubMed DOI PMC

Fernández-Torres B., Carrillo A.J., Martín E., Del Palacio A., Moore M.K., Valverde A., Serrano M., Guarro J. In Vitro Activities of 10 Antifungal Drugs against 508 Dermatophyte Strains. Antimicrob. Agents Chemother. 2001;45:2524–2528. doi: 10.1128/AAC.45.9.2524-2528.2001. PubMed DOI PMC

Perea S., Fothergill A.W., Sutton D.A., Rinaldi M.G. Comparison of In Vitro Activities of Voriconazole and Five Established Antifungal Agents against Different Species of Dermatophytes Using a Broth Macrodilution Method. J. Clin. Microbiol. 2001;39:385–388. doi: 10.1128/JCM.39.1.385-388.2001. PubMed DOI PMC

Saunte D.M., Simmel F., Frimodt-Moller N., Stolle L.B., Svejgaard E.L., Haedersdal M., Kloft C., Arendrup M.C. In Vivo Efficacy and Pharmacokinetics of Voriconazole in an Animal Model of Dermatophytosis. Antimicrob. Agents Chemother. 2007;51:3317–3321. doi: 10.1128/AAC.01185-06. PubMed DOI PMC

Barchiesi F., Arzeni D., Camiletti V., Simonetti O., Cellini A., Offidani A.M., Scalise G. In Vitro Activity of Posaconazole against Clinical Isolates of Dermatophytes. J. Clin. Microbiol. 2001;39:4208–4209. doi: 10.1128/JCM.39.11.4208-4209.2001. PubMed DOI PMC

Badali H., Mohammadi R., Mashedi O., De Hoog G.S., Meis J.F. In vitrosusceptibility patterns of clinically importantTrichophytonandEpidermophytonspecies against nine antifungal drugs. Mycoses. 2015;58:303–307. doi: 10.1111/myc.12315. PubMed DOI

De Hoog G.S., Guarro J., Gené J., Figueras M.J. Atlas of Clinical Fungi. 2nd ed. Amer Society for Microbiology; Utrecht, The Netherlands: 2000.

Hubka V., Nováková A., Jurjević Ž., Sklenář F., Frisvad J.C., Houbraken J., Arendrup M.C., Jørgensen K.M., Siqueira J.P., Gené J., et al. Polyphasic data support the splitting of Aspergillus candidus into two species; proposal of Aspergillus dobrogensis sp. nov. Int. J. Syst. Evol. Microbiol. 2018;68:995–1011. doi: 10.1099/ijsem.0.002583. PubMed DOI

Hubka V., Barrs V., Dudová Z., Sklenář F., Kubátová A., Matsuzawa T., Yaguchi T., Horie Y., Nováková A., Frisvad J., et al. Unravelling species boundaries in the Aspergillus viridinutans complex (section Fumigati): Opportunistic human and animal pathogens capable of interspecific hybridization. Persoonia Mol. Phylogeny Evol. Fungi. 2018;41:142–174. doi: 10.3767/persoonia.2018.41.08. PubMed DOI PMC

Price M.F., Wilkinson I.D., Gentry L.O. Plate method for detection of phospholipase activity in Candida albicans. Med. Mycol. 1982;20:7–14. doi: 10.1080/00362178285380031. PubMed DOI

Boechat J.S., Oliveira M.M.E., Almeida-Paes R., Gremião I.D.F., Machado A.C.D.S., Oliveira R.D.V.C., Figueiredo A.B.F., Rabello V.B.D.S., Silva K.B.D.L., Zancopé-Oliveira R.M., et al. Feline sporotrichosis: Associations between clinical-epidemiological profiles and phenotypic-genotypic characteristics of the etiological agents in the Rio de Janeiro epizootic area. Memórias Inst. Oswaldo Cruz. 2018;113:185–196. doi: 10.1590/0074-02760170407. PubMed DOI PMC

Aneke C.I., Rhimi W., Pellicoro C., Cantacessi C., Otranto D., Cafarchia C. The best type of inoculum for testing the antifungal drug susceptibility of Microsporum canis: In vivo and in vitro results. Mycoses. 2020;63:711–716. doi: 10.1111/myc.13090. PubMed DOI

Fernandez-Torres B., Cabanes F.J., Carrillo-Munoz A.J., Esteban A., Inza I., Abarca L., Guarro J. Collaborative Evaluation of Optimal Antifungal Susceptibility Testing Conditions for Dermatophytes. J. Clin. Microbiol. 2002;40:4121–4125. doi: 10.1128/JCM.40.11.3999-4003.2002. PubMed DOI PMC

Ghannoum M.A., Chaturvedi V., Espinel-Ingroff A., Pfaller M.A., Rinaldi M.G., Lee-Yang W., Warnock D.W. Intra- and inter-laboratory study of a method for testing the antifungal susceptibilities of dermatophytes. J. Clin. Microbiol. 2004;42:2977–2979. doi: 10.1128/JCM.42.7.2977-2979.2004. PubMed DOI PMC