Biology, Diagnosis and Treatment of Malassezia Dermatitis in Dogs and Cats Clinical Consensus Guidelines of the World Association for Veterinary Dermatology
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Vet Dermatol 2020; 31: 27–e4 DOI: 10.1111/vde.12809 Biology, diagnosis and treatment of Malassezia dermatitis in dogs and cats Clinical Consensus Guidelines of the World Association for Veterinary Dermatology Ross Bond* , Daniel O. Morris†, Jacques Guillot‡, Emmanuel J. Bensignor§ , David Robson¶, Kenneth V. Mason**, Rui Kano†† and Peter B. Hill‡‡ *Department of Clinical Sciences and Services, Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL9 7TA, UK †Department of Clinical Sciences and Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, 3900 Delancy Street, Philadelphia, PA 19104, USA ‡Ecole nationale vet erinaire d’Alfort, BioPole^ Alfort, EA 7380 Dynamyc, UPEC, EnvA, Maisons Alfort, Ile-de-France, France §Clinique Vet erinaire, 17 Boulevard des Filles du Calvaire, Paris 75003, France ¶Animal Skin and Ear Specialists, Melbourne Veterinary Specialist Centre, 70 Blackburn Road, Glen Waverley, Victoria 3150, Australia **Dermcare-vet PTY LTD, 7 Centenary Road, Slacks Creek, Queensland 4127, Australia ††Department of Veterinary Pathobiology, Nihon University College of Bioresource Sciences, 1866 Kameino, Fujisawa, Kanagawa 252-0880, Japan ‡‡Department of Veterinary Science, University of Adelaide, Adelaide, South Australia 5005, Australia Correspondence: Ross Bond, Department of Clinical Sciences and Services, Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire, AL9 7TA, UK. E-mail: [email protected] Background – The genus Malassezia is comprised of a group of lipophilic yeasts that have evolved as skin com- mensals and opportunistic cutaneous pathogens of a variety of mammals and birds. Objectives – The objective of this document is to provide the veterinary community and other interested parties with current information on the ecology, pathophysiology, diagnosis, treatment and prevention of skin diseases associated with Malassezia yeasts in dogs and cats. Methods and material – The authors served as a Guideline Panel (GP) and reviewed the literature available prior to October 2018. The GP prepared a detailed literature review and made recommendations on selected topics. The World Association of Veterinary Dermatology (WAVD) Clinical Consensus Guideline committee provided guidance and oversight for this process. The document was presented at two international meetings of veteri- nary dermatology societies and one international mycology workshop; it was made available for comment on the WAVD website for a period of six months. Comments were shared with the GP electronically and responses incorporated into the final document. Conclusions and clinical importance – There has been a remarkable expansion of knowledge on Malassezia yeasts and their role in animal disease, particularly since the early 1990’s. Malassezia dermatitis in dogs and cats has evolved from a disease of obscurity and controversy on its existence, to now being a routine diagnosis in general veterinary practice. Clinical signs are well recognised and diagnostic approaches are well developed. A range of topical and systemic therapies is known to be effective, especially when predisposing factors are identi- fied and corrected. Accepted 20 August 2019 Note: A shortened version of this review, comprising the summaries from each section, can be found at https://doi.org/10.1111/vde.12834. Sources of Funding: This study was self-funded. Conflicts of Interest: In the past five years, Ross Bond has received funding from or otherwise collaborated with Dechra Veterinary Prod- ucts, Bayer Animal Health, Ceva Animal Health, MSD Animal Health and Elanco. Daniel O. Morris has received honoraria, consulting fees and/or has collaborated with Pfizer Animal Health/Zoetis, Bayer, and Ceva Animal Health. Jacques Guillot has received funding from or otherwise collaborated with MSD Animal Health, Ceva Animal Health, Bayer Animal Health and Boehringer-Ingelheim. Emmanuel Bensignor has consulted and lectured for Elanco and Ceva Animal Health. David Robinson has received funding from or otherwise collaborated with MSD Animal Health, Virbac Animal Health and Elanco. Kenneth V. Mason is Managing Director of Dermcare-vet PTY LTD. Rui Kano has no conflicts of interest to declare. Peter B. Hill has received honoraria and consulting fees from Pfizer/Zoetis and Elanco/Novartis. Presented in draft form at the 2018 North American Veterinary Dermatology Forum, Maui, Hawaii, USA, the 2018 International Society for Human and Animal Mycology Malassezia Workshop, Utrecht, The Netherlands, and the 2018 European Society/College of Veterinary Der- matology Annual Congress in Dubrovnik, Croatia. © 2019 ESVD and ACVD, Veterinary Dermatology, 31, 27–e4. 27 WAVD cannot be held responsible for errors or any consequences arising from the use of information contained in this article. Readers need to bear this in mind and be aware of the prescribing laws pertaining to their own countries. Bond et al. Table of Contents 1 Introduction 3 2 The genus Malassezia. General properties, phylogeny, genomic studies and 3 species of relevance to veterinary medicine 3 Historical aspects of Malassezia yeasts as skin pathogens in dogs and cats 5 4 Ecology and epidemiology 7 5 Pathogenesis: virulence attributes amongst Malassezia yeasts 9 6 Pathogenesis: immunological responses to Malassezia yeasts and their 11 clinical relevance in diagnosis/therapy 7 Predisposing factors for development of Malassezia dermatitis 14 8 Quantification of Malassezia populations on canine and feline skin by cytology 15 and culture 9 Diagnostic methods: molecular and mass spectrometry identification of 19 yeasts in culture and skin 10 Histopathological features of canine and feline Malassezia dermatitis 20 11 Antifungal susceptibility testing and resistance 21 12 Clinical presentations in dogs 24 13 Clinical presentations in cats 26 14 Summary of the diagnostic approach 27 15 Therapy 28 16 Prevention of Malassezia-associated skin diseases in dogs and cats 32 17 Malassezia yeasts as zoonotic agents 34 References 35 Supporting Information 46 28 © 2019 ESVD and ACVD, Veterinary Dermatology, 31, 27–e4. WAVD Consensus Guidelines Malassezia dermatitis (Section 15.2). Given the general paucity of high quality 1 Introduction trials in this field, consensus views from the panel of Scientists have been grappling with the complexity of the authors have also been incorporated. Thus, our conclud- genus Malassezia and their associated diseases for dec- ing summary of therapeutic options is a combination of ades. Their relevance to companion animal veterinary evidence base and consensus of opinion.2 Finally, in the practitioners first became apparent in the context of spirit of a “one health” approach, the zoonotic potential canine otitis externa in the 1950’s, whereas their role in of these yeasts is reviewed. canine dermatitis was not established until more recently. Malassezia dermatitis is now recognised as a common 2 The genus Malassezia. General skin disorder in canine practice, although it is encountered properties, phylogeny, genomic studies more occasionally in feline practice. and species of relevance to veterinary The commissioning of this review by the World Associ- medicine ation for Veterinary Dermatology (WAVD) is timely, given the marked advances in our understanding of these lipo- Malassezia yeasts form a well-defined and unique clus- philic yeasts as a consequence of significant scientific ter of lipophilic fungi living almost exclusively on the endeavour, not least the sequencing of the genomes of skin and mucosal sites of warm-blooded vertebrates. the majority of the recognised species. Molecular biologi- The genus Malassezia (Baillon) is usually considered as cal techniques have transformed the taxonomy of the a monophyletic taxon in the phylum Basidiomycota and genus from two species in 1989 to 18 species at the time subphylum Ustilaginomycotina, a highly diversified of publication, in the process explaining, at a stroke, many group of more than 1,500 species of plant pathogens.3 of the painstaking observations of phenotypic variation Molecular analysis has confirmed that the genus Malas- made by generations of mycologists. sezia is deeply rooted in the Ustilaginomycotina with a This is the second WAVD consensus document on sister relationship to Ustilaginomycetes and Exobasid- superficial veterinary mycoses, following on from one for iomycetes.4 As a consequence, it was proposed that dermatophytosis.1 Whilst the headline title of our review the genus should be assigned as its own class, Malas- is “diagnosis and treatment”, the complexity of Malasse- seziomycetes.4 During the last decade, the analysis of zia dermatitis in dogs and cats requires a wider-ranging the genome of Malassezia yeasts has allowed a better review. Unlike the dermatophytes, which visit and poten- understanding of how these fungi, whose ancestors tially infect the non-immune host, Malassezia yeasts are were most probably plant or soil residents, manage to commensal organisms, forming a reservoir of potential survive and develop in the cutaneous ecosystem and pathogens in the stratum corneum or mucosae, that may how they interact with other members of the cutaneous induce disease whenever the homeostatic balance of microbiota. In 2007 the first genome sequence of a yeast virulence, on the one hand, and host immunity, on Malassezia species (M. globosa) was published.5 A few the other, is disrupted in favour of the yeast. years later, a similar analysis was performed for M. Our review includes a full description