How Many Species Of Fungi Cause Disease In Animals

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• Published: 17 July 2020

Occurrence of various pathogenic and opportunistic fungi in peel diseases of domestic animals: a retrospective study

BMC Veterinary Inquiry volume 16, Article number:248 (2020) Cite this commodity

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Abstruse

Background

Fungal infection of animals or humans are common all over the world. Some of microorganisms similar fungi, be on the skin and can be transmitted onto other individuals, other animal species or even humans and cause pare infections. Moreover, they can be the causative agents of astringent generalized infections especially in immunocompromised individuals. The study aimed to evaluate the most frequent etiological agents of skin diseases and to compare the prevalence of beast fungal infections in Poland, and to hash out the possibility of transmission to humans in Poland.

Results

The obtained results are culture based. The fungi most oftentimes isolated from grouping of animals with skin lesions were Malassezia pachydermatis (29.fourteen%), and Candida yeasts (27.07%), and dermatophytes (23.five%), including Microsporum canis as majority of them (59.25%), and Trichophyton genus (40.7%), nigh of them T. mentagrophytes, while Malassezia pachydermatis represented (80%) of isolates in animals with otitis externa. In over 19% of positive fungal cultures obtained from external ear canals Candida yeasts, mainly C. albicans, were identified.

Conclusions

Dermatomycoses in companion animals are caused by both, mycelial fungi and yeasts. Most oft isolated were Malassezia pachydermatis and Candida spp. Dermatophytes (Trichophyton, Microsporum), were also cultured, but the total number of these isolates seems to subtract. We take not establish Cryptococcus neoformans in tested clinical samples.

Background

Human also every bit animate being mycoses are common all over the world. Multifariousness of ecology and physiological factors can contribute to the development of those diseases, east.grand. the quantity of fungal elements nowadays in the surroundings and the efficiency of the host allowed system [i,two,three,four]. The sources of fungi may also differ. The almost common road of infection is aerogenic, thus inhalation of fungal spores present in the air, is the frequent way to acquire the fungi. In such cases the infection starts in the respiratory system [ii, 3]. Other important site for fungal colonization and development of mycoses is the skin, which is the largest organ of the body and the first of protective barriers [3, v]. Its' major functions include protecting the organism from pathogens, preventing loss of moisture and the regulation of body temperature. Considered as an ecosystem, the skin is the ground for microbial communities of natural microbiota, positively influencing the residue between the health and the disease. The pilus coat, the scalp and the hairless skin are quite different niches. Studies characterizing the microbiota inhabiting these niches may answer the fundamental question about the breaking points between the normal colonization and the affliction [vi]. In recent years, many experiments take been conducted to examine the natural skin microbiome of salubrious skin in humans and some animals, especially companion animals [vi,7,viii]. Other studies were focused on the qualitative and quantitative changes of the microbiota in various skin diseases [9, 10]. Meason-Smith et al. [six], take performed the experiments aiming at label of fungal microbiota in dogs and evaluating the influence of body site and health status on the mycobiota. They have used side by side generation sequencing of ITS (Internal Transcribed Spacer) region and showed, that in general, mucosal sites have had reduced fungal diversity when compared to cutaneous mycobiota. But the composition of fungal species and their diverseness were more individual features of creature host than were associated with a particular site of the body. The taxonomic analysis revealed, that dominating phylum of fungi was Ascomycota, represented in majority by three genera: Alternaria, Cladosporium and Epicoccum, while the predominant genera among the Basidiomycota, were Cryptococcus and Malassezia [6]. The results of our previous investigation of good for you dogs mycobiota are basically compatible with these data [11].

Among the various fungi included in mycobiota [6, 8] there are genera classified as opportunistic microorganisms. However, even if about of the time opportunists are harmless, their virulence strongly depends on the wellness status of the host [one, 3, four]. Such species are also the of import etiological agents of various disorders in the group of individuals suffering from other diseases, undergoing surgical procedures or receiving prolonged antibody treatment and parenteral diet [5].

Skin diseases, including various mycoses, are among nigh common diseases affecting mammals [12,13,14,15,xvi]. In daily veterinarian exercise, dermatoses of companion animals are also one of the most frequent reasons for visiting the clinic (Fig. 1a, b). Quite frequently the etiological agents are mycelial fungi such as dermatophytes and some moulds equally Alternaria spp. or Scopulariopsis spp. together with yeasts and yeast-like fungi. Skin lesions can exist besides associated with infections caused by dimorphic fungi, such as Histoplasma capsulatum, Blastomyces dermatitidis or Cryptococcus neoformans, which are known to exist pathogenic for both humans and animals, only usually occur in specific geographic regions [17,18,nineteen,20]. In some cases, localized fungal colonization of skin, peculiarly with opportunistic yeasts, may initiate persistent mycoses or can be the source of severe systemic fungal infections. The gamble of fungal infection and the development of mycoses increases notably in individuals, whose immunity is weakened by other infections (viral or bacterial), parasitic infestations, metabolic diseases, neoplasms or inherited immune disorders [21, 22]. Moreover, nearly of dermatophytes are able, as true pathogens, to impose the natural barriers of resistance and to spread to many individuals, causing the disease [fifteen].

Fig. 1

Beast'south dermatomycosis: a) Cattle ringworm, b) Skin lesions in dogs' dermatomycosis. (Photographs by I. Kaszak).

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The aim of this study was to assess the occurrence of fungal pare infections in animals in the years 2008–2018 in Poland, to analyse the most prevalent fungal species involved and to evaluate the hazard of their transmission to humans.

Results

The results of bacteriological exam were non analysed for the purposes of this publication. The percentage of positive mycological cultures was lower in animals with dermatitis than in animals with otitis externa - 38.eighteen% vs. 71.42%, respectively.

Out of the 2399 investigated cases of dermatitis, more than one-half of examined samples (61.eight%), were negative for fungal isolation. From the 916 (38.18%), positive cultures, the genus Malassezia (267 isolates), mainly M. pachydermatis (Fig. 2a) and Candida genus (248 cases), mainly C. albicans, were the most frequent amid yeast-like fungi, 29.14 and 27.07% respectively. In 23.5% cases (216 isolates), dermatophytes were diagnosed, with 128 strains of Microsporum spp. and the majority of them (59.25%) were identified as 1000. canis. The other 88 isolates (40.seven%), of dermatophytes belonged to the Trichophyton genus and most of them were T. mentagrophytes (Fig. iii). Other mycelial fungi were besides isolated, such as 127 strains of Alternaria spp. (13.86% of positive cultures), and 58 other mycelial fungi (half-dozen.33% of positive cultures, Aspergillus, Paeciliomyces or Penicilium) (Fig. three), included to the grouping of "Molds" for this study. During presented study the test of clinical materials revealed the presence of Alternaria moulds in 127 samples, sometimes as the only isolated fungi. All of these isolates were counted separately from other moulds because of the presence of hyphae and typical spores in skin scrapings (especially in samples from horses) (Fig .4a, b, c.). Moreover, during the direct microscopic examination of pilus samples, typical, proliferating poroconidia of Alternaria were seen together with hyphae fixed effectually the hair.

Fig. 2

Blastospores of: a) Malassezia pachydermatis and b) Malassezia globosa in directly smears from two cases of otitis externa in dogs. Methylene blue staining; calorie-free microscope × 1000.

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Fig. three

Mycological investigations of samples collected from animals with dermatitis. Colour bars represent indicated fungi and the number of isolates

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Fig. iv

Alternaria sp. in stratum corneum of equus caballus's skin: a) & b) proliferating spores, c) bondage of spores in horse epithelium. Slides prepared from skin scrapings: a) and b) Wet mounts; light microscope 400x; c) lactophenol cotton fiber blueish staining; calorie-free microscope 400x.

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From all 2936 samples collected from animals suffering from otitis externa, there were 2097 cultures (71.four%) positive for fungi. The virtually frequently isolated fungi was likewise Malassezia pachydermatis (1682 cases; 80.two%) (Fig. 2a). In several cases, during the microscopic investigation we take noticed the presence of typical for Grand. globosa round, budding cells (Fig. 2b), merely the attempts to abound these yeasts were unsuccessful. Routinely, for isolation of yeast the Sabouraud medium without supplementation of fatty acrid was used, so only the lipid-independent strains of Malassezia were able to abound. In the group of animals suffering from otitis externa the frequency of Candida yeasts isolation of was significantly lower – they were grown just in 415 cases (19.8%). Among Candida strains we have found mainly C. albicans, but too other species like C. krusei, C. glabrata and C. parapsilosis were infrequently isolated.

Pathogenic dimorphic fungi as Blastomyces dermatitidis or Histoplasma capsulatum have not been establish in specimens nerveless during the ten-year menses.

Word

Our retrospective analysis was focused on the specimens from animals with clinical signs of skin diseases (otitis externa and various forms of dermatitis), and showed, that in 56.47% of examined animals, fungi belonging to dissimilar morphological groups were isolated. We have institute basidiomycetous and ascomycetous fungi including Malassezia and Candida yeasts, opportunistic moulds e.g. Alternaria, every bit well as typical dermatophytes. In the group of animals suffering from dermatitis, yeasts were discovered in 56.2% of positive cultures (Malassezia pachydermatis in 29.1%, Candida spp. in 27.1%, respectively), while dermatophytes were the etiological agents of skin disease in 23.v% of cases. The carriers of dermatophytes are cats and other companion animals such as rabbits, guinea pigs or dogs [15, 16]. Moreover, the brute'due south equipment, like brushes, collars, mattresses or resting places for dogs and cats can be the source of infection, because the spores of dermatophytes are highly resistant in the surroundings for long period of fourth dimension. Among all skin mycoses, dermatophytoses are zoonoses and may be transmitted from animals to humans. Clinical cases of dermatophytosis occurring simultaneously in animalsouth and its owner were described in literature, e.thou. Trichophyton rubrum infection coexisting in a human and in a hog [23], and in a dog [24], or microsporosis transmitted from cat to children [xiv].

Additionally, one of those who accept conducted this investigation, had experienced dermatophytosis after contact with the infected animals during sampling and with the clinical specimens during repeated diagnostic mycological procedures (Fig. v.). In this case Arthroderma benhamiae (the anamorph of Trichophyton mentagrophytes), was cultured from skin scrapings (information not published). Likewise, nosotros had noticed skin lesions typical for dermatophytosis on the forearm of a adult female owning the pet rabbit, from which we had isolated Microsporum canis. These findings complies with the literature data from several years describing Trichophyton mentagrophytes and Microsporum canis infections equally the most mutual etiological agents of human being dermatomycosis in Poland [25,26,27]. Among the Trichophyton genus, in few cases we have isolated geophilic Trichophyton terrestre (Arthroderma insingulare) besides. In our former study, focused on mycological screening, we didn't observe the presence of the dermatophytes' spores in the environments of healthy animals, their collars or dens [11], notwithstanding we cannot exclude these sources.

Fig. 5

Tinea manuum contracted by laboratory personnel.

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During our investigations we have cultured diverse moulds such as Aspergillus, Penicilium or Paeciliomyces. However, while culturing animals hair samples or skin swabs, the growth of such ecology moulds should be treated as the contaminations, because their multiple spores are nowadays in the air, especially in the stables, barns and creature rooms. They are widely distributed in the environment and deposited on the pilus glaze and skin surface of animals [28].

During the menstruation of 10 years, among the mycelial fungi isolated from cases of cutaneous infections was also Alternaria spp. In many laboratories, growth of Alternaria colonies is treated as typical civilization contamination with saprophytic fungi, because they are widely distributed in the environs and colonizing diverse plants or causing their diseases [29]. Alternaria spores are present in the air, soil and water or on the surface of human and animal skin [6, 11, 29]. However, in veterinarian medicine, infections due to moulds such as Alternaria alternata, peculiarly in horses, every bit well as hypersensitivities noted frequently in pet animals, have get an emerging clinical problem. Despite Alternaria does non belong to keratinolytic fungi, proliferating fungal elements present in the tissues suggest, that information technology may be responsible for peel damage. Considering the increasing number of cases in which this fungus was found equally the simply agent in pare lesions [30], information technology should exist noticed that the growing mycelium may mechanically harm the neighbouring tissues. In our do, nosotros have isolated Alternaria fungi in 13.8% of positive cultures and we have seen in microscopic slides prepared directly from skin scrapings, that poroconidia of Alternaria were able to germinate and produce hyphae in stratum corneum. In Poland, such reports were thin until 2013, when Dworecka-Kaszak [31] has described spores of Alternaria proliferating in the pare scrapings and has isolated information technology as the sole causative agent of fungal dermatitis in horse. In the same year, Tyczkowska-Sieroń and Głowacka [32], have described dermatomycoses in two Shetland ponies and Beagle canis familiaris, in which Alternaria tenuissima was the etiological agent. In the international veterinary literature cutaneous fungal granulomas occurring in horses take been described for years. Many authors have noted the cases of equine dermatitis, in which Alternaria fungi were institute in samples obtained by biopsy of pare nodules [30, 33, 34]. In some clinical samples of this study Alternaria was isolated from as the only infectious amanuensis, causing skin lesions characteristic for dermatomycoses, as reported before [30]. Alternaria alternata has been recorded as a common indoor allergen, causing different hypersensitivity reactions in humans, sometimes leading to asthma [29, 35, 36]. Although, serious infections in the immunocompetent hosts are rare. This fungus may cause opportunistic infections in immunocompromised patients, especially in those undergoing solid organ or bone marrow transplantation [36]. Fungi of Alternaria spp. were too noted as the causative agents of ocular mycosis and onychomycosis connected either with the steroids therapy or mail service traumatic disorders [36]. Additionally, their presence in the foodstuff (e.g. in crops, vegetables, fruits) is very mutual.

Our analysis of specimens obtained from animals with clinical symptoms of dermatitis did not reveal cases of infections acquired by dimorphic fungi, as these obligate pathogens are endemic for other geographic regions. Even though, in that location were clinical cases of histoplasmosis reported in European countries (Austria, Italy, Turkey) [37, 38] or cryptococcosis [20], presented retrospective study has confirmed, that they are unremarkably not found in companion animals in Poland.

Abreast mycelial fungi, nosotros accept too reported the isolation of the genus Malassezia. These yeasts are found in dissimilar pare regions of healthy man skin [8], and are also present on heathy skin of dogs [6]. Traditionally, the lipid-dependent species were thought to occur only on human skin, while Grand. pachydermatis was assumed to exist restricted to animals skin and in item carnivores [39]. It is suspected, that other Malassezia species, like M. globosa or M. sympodialis or fifty-fifty lipid-dependent strains of Thou. pachydermatis could be involved in developing of otitis in dogs, but we were not able to cultivate them [40, 41]. Mentioned species were also isolated from the skin of healthy cats [39, 42]. Although most of the time these yeasts are opportunistic in nature, it may go pathogenic with any alteration in the peel microbiota, disorders of the host defense mechanisms or the imbalance of homeostasis [39, 43,44,45]. Also dermatitis caused past flea bites, especially when accompanied past hypersensitivity reaction, together with nutrient hypersensitivity or atopy, likewise as antimicrobial or corticosteroid therapy, may facilitate proliferation of these yeasts [39]. Additionally in that location are some canine breeds with college run a risk of developing malasseziosis e.g. West Highland White Terriers, Basset Hounds, Beagles, Springer and Cocker Spaniels or Boxers [39, 43,44,45]. In cats, Malassezia infections are more limited and ordinarily are associated with other underlying or concurrent illness such as retro-viral infections [39]. Malassezia yeasts, especially M. pachydermatis, were also isolated from wild pinnipeds and ferrets, foxes, bears or other animal species such equally pigs, horses and also from birds. They were also noted in literature as the etiological agents of infections of such "exotic" host species as rhinoceroses, dromedaries, okapis or elephants [39]. M. pachydermatis are still the about common fungal agent contributing to otitis externa and other types of dermatitis in domestic animals, particularly in dogs, what has been described by others and confirmed in this report [39, 44, 46,47,48]. Nosotros have isolated this species from over 80% of positive fungal cultures of ear swabs taken from the otitis externa cases. Our observations of fungal diversity in clinical specimens obtained from the dogs with diverse cutaneous hypersensitivities are also congenial with the experiments of Meason-Smith and her group [6]. They have showed, that Malassezia colonization of ear canals of allergic dogs were significantly more arable, than in salubrious individuals [6]. Fig.2a and b, take shown the direct microscopic slides prepared from the samples taken from external ear culvert of two dissimilar dogs suffering from otitis externa. In one canis familiaris, likewise as in many others, the well-nigh frequent etiological agent - M. pachydermatis - was identified, while in second private we establish One thousand. globosa blastospores, what was consequent with the literature data showing the occurrence of this species in the ear canal of dogs. These opportunistic yeasts are of increasing importance in human and animal diseases [8, nine, 49, 50]. Malassezia pachydermatis has been described as the cause of sporadic bloodstream infections (BSI), especially in neonates with depression birth weight and in premature infants. Most cases of fungal BSI are noted in patients with whatever intravenous catheters. Other factors increasing the take chances of BSI is mechanical ventilation and steroid and antibiotic treatment [49]. Cases of life-threatening fungemia in humans have been attributed to Malassezia pachydermatis, for which dogs are a natural host. In some cases, the sources of homo infections have been traced to pet dogs endemic by healthcare workers [46, 47].

Some Candida yeasts, specially C. albicans, are endogenic saprophytes, but their role as the opportunistic pathogen is likewise known and described. Together with Cryptococcus neoformans these yeasts are one of the near important etiological agents of opportunistic systemic mycoses particularly in immunocompromised patients, who would like otherwise not be infected.

Examples of medical conditions connected with immunosuppression include AIDS, alteration or translocation of normal microbiota acquired by antibiotics, immunosuppressive therapy and metastatic cancer or astringent surgical procedures. In companion animals, the incidence of Candida systemic mycoses is not so loftier, simply the function of these yeasts as causative agent of other mycoses has increased. The medical conditions increasing the susceptibility of animals such as dogs or cats for candydosis are briefly the same as in humans, including diabetes, other endocrinal disorders and neoplastic diseases [21, 51]. There are too suggestions, that these yeasts may play a role in atopic dermatitis (AD) in humans past influencing the product of IgE, but it is notwithstanding not thoroughly explained or proved [9].

In our Mycology lab. Candida yeasts are isolated oftentimes, mostly from mucous membranes of various animals [21]. Nosotros have also observed their growth from skin swabs and scrapings or from ear canal swabs. During reported 10-year period, we have identified Candida strains, mainly C. albicans in 27.1% of positive fungal cultures in dermatitis cases and 19.eight% of positive fungal cultures in otitis externa cases. Amid others, C. krusei, C. glabrata or C. parapsilosis, were isolated too. In this written report, we have also shown that the number of Candida isolates obtained from companion animals maybe comparable or even like with the number of Malassezia isolates. Our findings may indicate, that fungi from Candida genus are important factors of dermatitis in animals, including immunocompetent individuals.

Conclusions

• Dermatomycoses in companion animals are caused past both mycelial fungi and yeasts.

• Among the animals with dermatitic lesions, yeasts and yeast-like fungi from Malassezia and Candida genera, were the most frequent fungal etiological agents.

• In more than 20% of positive cultures, dermatophytes were identified, by and large belonging to Microsporum genus, while Trichophyton were less common.

• We have noted the increasing tendency of Alternaria spp. isolation from clinical cases of dermatitis. These fungi should be considered as the causative agents of peel mycoses, basing on the presence of their proliferating spores in the pare samples every bit the sole organism.

• Malassezia pachydermatis was isolated in over 80% of otitis externa cases in dogs and remains the most frequent etiological agent of this disease. In this group of animals Candida yeasts were revealed in less than twenty% of cases, what makes them the 2nd causative agent.

• During the 10 twelvemonth period there were no clinical cases of dermatomycosis caused by Histoplasma capsulatum or Cryptococcus neoformans in the region of Mazovia, Poland.

Methods

A total of 5335 specimens, such as hair, skin scrapings, peel or ear swabs were investigated during a 10 years period 2007 to 2016 for fungal infection at the Microbiology Lab from Section of Preclinical Sciences, Faculty of Veterinarian Medicine, Warsaw University of Life Sciences-SGGW, Poland. The clinical specimens were obtained from 4150 dogs, 689 cats, 88 rodents and 274 riding horses, xi birds (e.yard. parrots, decorative pigeons), and 123 other pet animals (e.g. reptiles and mammals), and divided in 2 groups; 2399 from animals with dermatitis and 2936 from animals with otitis externa. The group of animals with otitis externa was consisted exclusively of dogs and cats. All clinical samples were tested routinely past microscopic examination of direct slide and culturing on Sabouraud Medium (with and/or without cycloheximide). Results were calculated basing on the cultures. All fungal isolates were divided according to their morphology in the group of mycelial fungi (including moulds and dermatophytes), or yeasts and yeast-like fungi. Identification of mycelial fungi was based on the morphology of their colonies and micromorphology of spore and hyphae. Additional techniques, such as Riddel'southward microculture or pilus perforation test, were also applied. In some cases, for identification of called dermatophytes strains, genetic analyses were used. For all of the yeast isolates biochemical and physiological backdrop were analysed with API Candida and/or ID32C microtests (BioMerieux, France) urease and germ tube tests.

Availability of data and materials

The datasets used and/or analysed during the current study are bachelor from the authors on reasonable request.

Abbreviations

ITS:

Internal transcribed spacer

AIDS:

Acquired immunodeficiency syndrome

KOH + DMSO:

Potassium hydroxide and dimethylsulphoxide used for Moisture Mount technique, a process in which potassium hydroxide is used to dissolve keratin in pare and reveal fungal elements under the microscope

BSI:

Bloodstream infections

AD:

Atopic dermatitis

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Acknowledgments

The authors thanks: 1) Beata Kowalkowska for her technical help.

two) Ilona Kaszak, DVM for the permission to use ii photographs No 1a, 1b and her consent for their publication.

Funding

At that place was no funding for researches.

Participation of B. Dworecka-Kaszak every bit the speaker in the Clinical Microbiology Briefing series, 26.10–29.10.2017, Paris, France was supported by KNOW- Leading National Enquiry Centre Scientific Consortium, Healthy Animal-Safe Nutrient.

MJ. Biegańska and I. Dąbrowska did not attended this Conference and did not receive any funding.

Author information

Authors and Affiliations

1. Warsaw University of Life Sciences, Kinesthesia of Veterinary Medicine, Ciszewskiego 8, 02-784, Warsaw, Poland

   Bożena Dworecka-Kaszak, Małgorzata J. Biegańska & Iwona Dąbrowska

Contributions

BDK, MJB designed the piece of work. BDK, ID, MJB analyzed and interpreted obtained results. All authors wrote and revised the paper. ID and MJB edited the paper. All authors read and approved both the initial and final manuscript.

Corresponding author

Correspondence to Małgorzata J. Biegańska.

Ideals declarations

Ethics approval and consent to participate

This piece of work does non contain any studies with man participants performed past any of the authors. The man patient with dermatomycosis caused from animals, described in this study accept granted the written permission for using the photograph of the clinical signs of the disease in this publication.

During the studies there were no animals used for the experiments. The animals mentioned in the work were brought as the patients and treated in various veterinary clinics in Mazovia region. All medical procedures applied to them were in accordance with loftier professional standards and ethics of the veterinary practitioners. All applicative international, national, and institutional guidelines for the care of animals were followed. The authors received simply the clinical samples and investigated them in accordance with the ethical standards.

Consent for publication

Written Consent of Ilona Kaszak DVM to publish her photographs No. 1a, b was obtained before submitting this publication.

Written permission was granted for using the photograph of the clinical signs of human dermatomycosis in this publication.

Competing interests

a. The upshot was partially presented on Clinical Microbiology Conference series, 26.10–29.ten.2017, Paris, France. Participation of B. Dworecka-Kaszak every bit the speaker in the mentioned briefing was supported by KNOW- Leading National Inquiry Center Scientific Consortium, Healthy Animal-Safe Food.

b. B.D.K. declare no other conflict of involvement

c.K.J.B and I. D declare that they have no conflict of interest.

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Dworecka-Kaszak, B., Biegańska, Thou.J. & Dąbrowska, I. Occurrence of various pathogenic and opportunistic fungi in skin diseases of domestic animals: a retrospective study. BMC Vet Res sixteen, 248 (2020). https://doi.org/10.1186/s12917-020-02460-x

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• Received: 30 May 2019

• Accepted: 06 July 2020

• Published: 17 July 2020

• DOI : https://doi.org/10.1186/s12917-020-02460-x

Keywords

• Animals
• Dermatomycosis
• Etiological agents
• Fungi
• Otitis externa
• Transmission

Source: https://bmcvetres.biomedcentral.com/articles/10.1186/s12917-020-02460-x

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