Identification of Malassezia species as part of normal skin and ear canal microbiota in horses

Rubiela Castañeda Salazar; Diana M. Rodríguez Sandoval; Adriana P. Pulido-Villamarín; Melva Y. Linares Linares; Olimpo J. Oliver Espinosa

doi:10.17533/udea.rccp.v33n1a01

Authors

Rubiela Castañeda Salazar Pontifical Xavierian University
Diana M. Rodríguez Sandoval Pontifical Xavierian University
Adriana P. Pulido-Villamarín Pontifical Xavierian University
Melva Y. Linares Linares Pontifical Xavierian University
Olimpo J. Oliver Espinosa National University of Colombia

DOI:

https://doi.org/10.17533/udea.rccp.v33n1a01

Keywords:

culture, ear canal, horses, identification, Malassezia, normal microbiota, PCR, skin, yeast

Abstract

Background: The yeasts of the genus Malassezia are considered part of the normal skin microbiota in humans and animals. In horses, several species of the genus Malassezia have been reported in different areas of the skin and ear canal. Objective: Isolate, characterize and identify the different species belonging to the genus Malassezia isolated from the ear canal and skin of equine patients with no dermatological lesions that were referred to the large animal clinic of veterinary teaching hospital at the National University of Colombia. Methods: 22 horses were evaluated and sampled. Eighty-two samples were obtained by swabbing either the ear canals (left and right), skin areas of prepuce, mammary gland and inguinal region. The samples were examined by cytological evaluation and were cultured on modified Dixon’s agar and phenotypic and molecular identification were performed for yeast colonies. Results: Fourteen yeast isolates were obtained from the 82 samples. Biochemical identification determined that 50% (n=7) were Malassezia spp., 35.7% (n=5) were identified as Candida spp. and 14.3% (n=2) as Cryptococcus spp. Using molecular tests, the Malassezia species were M. slooffiae(28.6%) and M. nana (57.1%); only one isolate was classified as Trichosporo asahii. Conclusion: M. nana and M. slooffiae were identified as part of the normal ear canal and skin microbiota in the evaluated horses. The observed prevalence of Malassezia spp. was 18.2% (n=4/22) in this study sample.

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Author Biographies

Rubiela Castañeda Salazar, Pontifical Xavierian University

Department of Microbiology, Faculty of Sciences, Agricultural Research Unit (UNIDIA) - Line of Epidemiology and Animal Health, Pontifical Xavierian University, Bogotá, Colombia.

Diana M. Rodríguez Sandoval, Pontifical Xavierian University

Department of Microbiology, Faculty of Sciences, Agricultural Research Unit (UNIDIA) - Line of Epidemiology and Animal Health, Pontifical Xavierian University, Bogotá, Colombia.

Adriana P. Pulido-Villamarín, Pontifical Xavierian University

Department of Microbiology, Faculty of Sciences, Agricultural Research Unit (UNIDIA) - Line of Epidemiology and Animal Health, Pontifical Xavierian University, Bogotá, Colombia.

Melva Y. Linares Linares, Pontifical Xavierian University

Department of Microbiology, Faculty of Sciences, Agricultural Research Unit (UNIDIA) – Line of Epidemiology and Animal Health, Pontifical Xavierian University, Bogotá, Colombia.

Olimpo J. Oliver Espinosa, National University of Colombia

Department of Animal Health, Faculty of Veterinary Medicine and Zootechnics, National University of Colombia, Bogotá, Colombia.

References

Aldrovandi AL, Osugui L, Coutinho SDA. Is Malassezia nana the main species in horses’ ear canal microbiome?. Braz J Microbiol 2016; 47:770–774. 10.1016/j.bjm.2016.04.017

Arenas R. Micología Médica Ilustrada. 5th ed. México: Mc Graw Hill; 2008. ISBN: 978-607-15-1125-6

Ashbee H. Update on the genus Malassezia. Med Mycol2007; 45:287-303. 10.1080/13693780701191373

Cabañes J, Theelen B, Castellá G, Boekhout T. Two new lipi-dependent Malassezia species from domestic animals. FEMS Yeast Res 2007; 7(6):1064-1076. 10.1111/j.1567-1364.2007.00217.x

Cabañes F, Vega S, Castellá G. Malassezia cuniculi sp. nov., a novel yeast species isolated from rabbit skin. Med Mycol 2011; 49:40–48. https://doi.org/10.3109/13693786.2010.493562

Cafarchia C & Otranto D. Association between phospholipase production by Malassezia pachydermatis and skin lesions. J Clin Microbiol 2004; 42(10):4868–4869. 10.1128/JCM.42.10.4868-4869.2004

Cafarchia C, Gasser RB, Figueredo LA, Latrofa MF, Otranto D. Advances in the identification of Malassezia. Mol Cell Probe 2011; 25:1-7. 10.1016/j.mcp.2010.12.003

Cafarchia C, Figueredo L, Otranto D. Fungal diseases of horses. Vet Microbiol 2013; 167:215-34. 10.1016/j.vetmic.2013.01.015

Coutinho S. Malassezia pachydermatis: enzymes production in isolates from external ear canal of dogs with and without otitis. Arq Bras Med Vet Zootec 2005; 57(2):149-153. http://dx.doi.org/10.1590/S0102-09352005000800003

Crespo M, Abarca M, Cabañes F. Occurrence of Malassezia spp. in horses and domestic ruminants. Mycoses 2002; 45:333–337. https://doi.org/10.1046/j.1439-0507.2002.00762.x

Crespo V, Crespo M, Gómez E. Diagnóstico de laboratorio de las levaduras del género Malassezia. Piel 2008a; 23(10):570-576. 10.1016/S0213-9251(08)75801-5

Crespo V, Gómez E, Crespo M. La pitiriasis versicolor y las levaduras del género Malassezia . Actas Dermosifiliogr 2008b; 99:764-771. 10.1016/S0001-7310(08)74956-1

Gaitanis G, Prokopios M, Hantschke M, Bassukas I, Velegrakid A. The Malassezia Genus in Skin and Systemic Diseases. Clin Microbiol Rev 2012; 25:106–141. 10.1128/CMR.00021-11

Gaitanis G, Robert V, Velegraki A. Verifiable single nucleotide polymorphisms of the internal transcribed spacer 2 region for the identification of 11 Malassezia species. J Dermatol Sci 2006; 43:214–217. 10.1016/j.jdermsci.2006.03.013

Gaitanis G, Velegraki A, Frangoulis E, Mitroussia A, Tsigonia A. Identification of Malassezia species from patient skin scales by PCR-RFLP. Clin Microbiol Infec 2002; 8:162-173. https://doi.org/10.1046/j.1469-0691.2002.00383.x

Gemmer C, De Angelis Y, Theelen B, Boekhout T, Dawson T. Fast, noninvasive method for molecular detection and differentiation of Malassezia yeast species on human skin and application of the method to dandruff microbiology. J Clin Microbiol 2002; 40(9):3350–3357. 10.1128/jcm.40.9.3350-3357.2002

Giusiano G. Malassezia: Estado del conocimiento y perspectivas en su estudio. Rev Argent Microbiol 2006; 38:41-48. Available from: http://www.redalyc.org/articulo.oa?id=213016797012

Guého-Kellermann E, Boekhout T, Begerow D. Biodiversity, Phylogeny and Ultrastructure. In: Boekhout T, Guého E, Mayser P, Velegraki A, editors. Malassezia and the skin. Science and Clinical Practice. Germany: Springer-Berlin, Heidelberg, 2010. p. 17-63. ISBN: 978-3-642-03616-3

Guého E, Midgley G, Guillot J. The genus Malassezia with description of four new species. Anton Leeuw Int JG 1996; 69:337-355. Avaliable from: https://www.ncbi.nlm.nih.gov/pubmed/8836432

Hernández J. Caracterización molecular de especies del género Malassezia . Tesis de Doctorado. 2005. Facultad de Veterinaria, Universidad Autónoma de Barcelona, España. Available from: https://www.tdx.cat/bitstream/handle/10803/5600/jjhe1de1.pdf?sequence=1&isAllowed=y

Higgins JC, Pusterla N. Fungal Pneumonia in Horses. Clin Tech Equine Pract 2006; 5:218-224. https://doi.org/10.1053/j.ctep.2006.03.017

Hirai A, Kano R, Makimura K, Duarte E, Hamdam J et al. Malassezia nana, a novel lipid-dependent yeast species isolated from animals. Int J Syst Evol Micr 2004; 54:623-627. 10.1099/ijs.0.02776-0

Hurtado-Suárez A, Pulido-Villamarín A, Linares-Linares M, Suárez-Fernández L, Castañeda-Salazar R, Rodríguez-Bocanegra MX. Caracterización fenotípica de aislamientos de Malassezia spp. de origen canino. Rev MVZ Córdoba 2016; 21(3):5535-5546. http://dx.doi.org/10.15381/rivep.v28i3.13350

Juntachai W, Oura T, Murayama SY &Kajiwara S. The lipolytic enzymes activities of Malassezia species. Med Mycol 2009; 47:477-484. 10.1080/13693780802314825

Kaneko T, Makimura k, Abe M, Shiota R, Nakamura Y, Kano R, Hasegawa A, Sugita T, Shibuya S, Watanabe S, Yamaguchi H, Abe S, Okamura N. Revised Culture-Based System for Identification of Malassezia Species. J Clin Microbiol 2007; 45(11):3737–3742. 10.1128/JCM.01243-07

Kindo AJ, Sophia SKC, Kalyani J, Anandan S. Identification of Malassezia species. Indian J Med Microbi 2004; 22(3):179-181. Available from: http://www.ijmm.org/text.asp?2004/22/3/179/11214

Ko, JH; Lee, YW; Choe, YB and Ahn, KJ. Epidemiologic study of Malassezia yeast in patients with Malassezia folliculitis by 26S rDNA PCR-RFLP analysis. Ann Dermatol 2011; 23(2):177-184. 10.5021/ad.2011.23.2.177

Lorch JM, Palmer JM, Vanderwolf KJ, Schmidt KZ, Verant ML, Weller TJ, Blehert DS. Malasseszia vespert ilionis sp. nov.: a new cold-tolerant species of yeast isolated from bast. Persoonia. Mol. Phylog. Evol. Fungi 2018; 41(1): 56-70 http://dx.doi.org/10.3767/persoonia.2018.41.04

Nardoni S, Merildi V, Frangioni S, Ariti G, Verin R, Vannucci P, Mancianti F. Isolation and characterization of Malassezia spp. in healty swine of different breeds. Vet Microbiol 2010; 141:155-158. 10.1016/j.vetmic.2009.07.033

NCBI. National Center for Biotechnology Information. Basic Local Alignment Search Tool. [Access date: January 10th, 2014].Available from: http://blast.ncbi.nlm.nih.gov/Blast.cgi.

Ortiz G, Carmen M, Alfonso J. Carrillo M, y Paya M. Producción de fosfolipasa y proteinasa en cepas de Malassezia pachydermatisaisladas de perros con otitis y sin otitis. Rev Iberoam Micol 2013; 30(4):235–238. http://dx.doi.org/10.16/j.riam.2013.01.006

Paterson S. Identification of Malassezia from a horse’s skin case report. Equine Vet. Educ 2002; 14(3):121-125. https://doi.org/10.1111/j.2042-3292.2002.tb00152.x

Pini G, Faggi E. Extracellular phospholipase activity of Malassezia strains isolated from individuals with and without dermatological disease. Rev Iberoam Micol 2011; 28(4):179-182. 10.1016/j.riam.2011.05.002.

Pulido A, Castañeda R, Linares M, Mercado M. Diagnóstico clínico-microbiológico de otitis externa en caninos de Bogotá – Colombia. Rev MVZ Córdoba 2010; 15(3):2215-2222. https://doi.org/10.21897/rmvz.308

Resusta A, Sánchez A, Gil J. Fundamentos básicos para el diagnóstico micológico. Rev Iberoam Micol 2007. ISBN: 978-84- 611-8776-8. Available from: http://www.guia.reviberoammicol.com/

Różański P, Ślaska B, Różańska D. Current status of prevalence of yeast-like fungi in the environment of horses bred in Poland. Ann Anim Sci 2013; 13(2): 365–374. https://doi.org/10.2478/aoas-2013-0016

Salah BI, Makni F, Cheikhrouhou F, Neji S, Sellami H, Ayadi A. Les levures du genere Malassezia: pathologie, milieux d’isolement et d’identification. Malassezia species: Pathology, isolation and identification media. J Mycol Med 2010; 20:53-60. 10.1016/j.mycmed.2009.11.006

Sgorbini M, Barsotti G, Nardoni S, Mancianti F, Rossi S, Corazza M. Fungal Flora of Normal Eyes in Healthy Newborn Foals Living in the Same Stud Farm in Italy. J Equine Vet Sci 2008; 28(9):540-543. 10.1016/j.jevs.2008.07.018

Shokri H. Occurrence and distribution of Malassezia species on skin and external ear canal of horses. Mycoses 2016; 59:28-33. 10.1111/myc.12430

Sugita T, Takashima M, Kodama M, Tsuboi R, Nishikawa A. Description of a new yeast species Malassezia japonica and its detection in patients with atopic dermatitis and healthy subjects. J Clin Microbiol 2003; 41:4695-4699. 10.1128/JCM.41.10.4695-4699.2003

White SD. Equine Bacterial and Fungal Diseases: A Diagnostic and Therapeutic Update. Clin Tech Equine Pract 2005; 4:302-310. https://doi.org/10.1053/j.ctep.2005.10.004

White, SD, Vandenabeele, S.I., Drazenovich, N.L, Foley, J.E. Malassezia species isolated from the intermammary and preputial fossa areas of horses. J Vet Intern Med 2006; 20:395–398. 10.1892/0891-6640(2006)20[395:msifti]2.0.co;2

Zia M, Mirhendi H, Toghyani, M. Detection and identification of Malassezia species in domestic animals and aquatic birds by PCR-RFLP. Iran J Vet Res 2015; 16(1):36-41. PMID: 27175148. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4789237/