Next Article in Journal
Resistance to Azoles in Candida parapsilosis Isolates from Spain Is Associated with an Impairment in Filamentation and Biofilm Formation
Previous Article in Journal
Gastrointestinal and Intra-Abdominal Mucormycosis in Non-Haematological Patients—A Comprehensive Review
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
JoF
Volume 11
Issue 4
10.3390/jof11040297
jof-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Characteristics of Chrysosporium spp. Pathogens Causing Skin Mycoses in Horses

by
Yelena Kukhar
1,
Gulshat Bailina
1,
Ainura Smagulova
1,2,3,
Rabiga Uakhit
1,2,3 and
Vladimir Kiyan
2,3,*
1
Research Platform of Agricultural Biotechnology, S. Seifullin Kazakh Agrotechnical Research University, Astana 010011, Kazakhstan
2
Laboratory of Biodiversity and Genetic Resources, National Center for Biotechnology, Astana 010011, Kazakhstan
3
Scientific Center for Biological Research, Astana 010011, Kazakhstan
*
Author to whom correspondence should be addressed.
J. Fungi 2025, 11(4), 297; https://doi.org/10.3390/jof11040297
Submission received: 26 February 2025 / Revised: 3 April 2025 / Accepted: 3 April 2025 / Published: 9 April 2025
(This article belongs to the Section Fungal Pathogenesis and Disease Control)
Browse Figures
Versions Notes

Abstract

:
Equine skin mycoses are a significant concern in Kazakhstan’s livestock industry due to the country’s historical livestock farming practices, the development of equestrian sports, and food traditions. Skin infections are among the most common fungal infections in horses. Emerging pathogens of equine dermatophytosis include keratinophilic Chrysosporium spp., which can degrade and metabolize keratin found in superficial tissues. This, combined with their thermotolerance, contributes to their pathogenicity. In this study, we investigated the biological properties and pathogenicity of two Chrysosporium strains isolated from equine skin lesions in northern and central Kazakhstan. Our findings showed that the Chrysosporium isolates caused a variety of clinically expressed skin lesions and exhibited cultural and morphological similarities to Trichophyton mentagrophytes. Genetic identification using ribosomal gene sequencing revealed 98.9% identity with Chrysosporium kreiselii and Chrysosporium zonatum sequences in both cases. The C. kreiselii strain caused pronounced skin lesions typical of classic dermatomycoses, demonstrated both keratinophilic and keratinolytic properties, and showed resistance to antifungal drugs. In contrast, the C. zonatum strain, which caused atypical lesions such as dandruff and seborrhea, was more sensitive to antifungal agents and exhibited keratinophilic properties. Our results highlight the emergence of new pathogenic Chrysosporium strains responsible for skin pathology in horses in Kazakhstan. We recommend that the identification of Chrysosporium skin infections in horses in Kazakhstan be followed by a comprehensive retrospective analysis of newly identified pathogens, including a full characterization of their pathogenicity.

1. Introduction

Fungal infections in horses are generally categorized into superficial mycoses, cutaneous mycoses, subcutaneous infections, and deep (or systemic) mycoses. Cutaneous mycoses are typically localized on the surface of the skin and hooves, such as dermatophytosis and onychomycosis [1,2], and can significantly impact the performance and financial value of the horse [3]. This is especially true for sport horses, as well as horses in Kazakhstan and other countries that are intended for slaughter for food purposes.
Due to the historical characteristics of livestock farming, Kazakhstan’s territory serves as a natural reservoir for classical mycoses in farm animals [4,5,6]. For centuries, breeding and draft horses, cattle, and sheep have been moved from the southern regions to the northern parts of the country or to the highlands (dzhailau) during the summer, and back in the fall. The lack of a system for the treatment and prevention of dermatophytosis has led to the widespread dissemination of pathogens throughout Kazakhstan [4].
The main causative agents of equine dermatophytosis are Trichophyton equinum, Microsporum equinum, Trichophyton mentagrophytes, Microsporum gypseum, Microsporum canis, and T. verrucosum [7,8,9,10,11,12,13]. In addition to dermatomycetes, other fungi responsible for equine diseases include Aspergillus, Alternaria, and yeast fungi [2,14,15]. Among the most common causative agents of superficial mycoses in horses are yeasts belonging to the genus Malassezia [16].
The spectrum of pathogens causing fungal skin infections in horses is expanding and includes mold fungi and yeasts from genera such as Aspergillus, Alternaria, Chaetomium, Phoma, Penicillium, Cladosporium, Candida, Sporothrix, Geotrichum, Scedosporium, Scopulariopsis, and other representatives [7,13,14,17,18,19,20,21]. This expansion is associated with factors such as global climate change, cosmopolitanism, zoonotic potential, physical inactivity, decreased immune function, and others [2,22,23,24]. The isolation of Chrysosporium spp. mold fungi from horses with adiaspiromycosis, corneal lesions, keratitis, and skin mycoses have also been described [25,26,27]. Pathogenic Chrysosporium-related fungi (PCRF) have emerged in recent decades as significant pathogens causing mycoses in both captive and free-living reptiles. The recognized pathogenicity of these fungi, along with the high mortality rate in reptiles, makes PCRF a potential threat to other animal groups as well [28].
According to the literature, Chrysosporium spp. can cause systemic, subcutaneous, and superficial mycoses in humans and various animals, including horses. The genus Chrysosporium belongs to the family Onygenaceae, order Onygenales, class Eurotiomycetes, and phylum Ascomycota. This genus includes about 100 species [29], which are commonly found in the environment, soil, aquatic sediments, as well as on the skin, hair, and nails of animals and humans, and the feathers of birds [30,31,32]. The ability of Chrysosporium spp. to degrade and assimilate keratin from superficial tissues classifies them as opportunistic pathogens of cutaneous mycoses and contributes to their pathogenicity [33,34]. Furthermore, the presence of thermotolerance in several keratinophilic Chrysosporium spp. further supports their potential pathogenicity [35].
A steady increase in the incidence of Chrysosporium spp. infections has been reported in reptiles, causing infectious dermatitis and fatal infections [36,37], as well as in warm-blooded animals, including chickens [38], cats [29], dogs [39,40,41,42], horses [26,27], and other animals. The isolation of Chrysosporium spp. from soil, animal hair, or bird feathers has been frequently reported [30,31,43,44,45].
In India, keratinophilic fungi of the genus Chrysosporium, including C. indicum (26.4%), C. tropicum (11.1%), C. aphanoascus (2.5%), and C. arthroderma tuberculatum (3.4%) [46], have been identified in wild birds and domestic fowls. Additionally, 28 isolates of Chrysosporium spp. were found in chickens on the mainland and Nansei Island in Japan [38]. In Germany, a clinical and mycological examination of 500 combs from adult hens yielded 11 isolates of C. georgiae [47].
Chrysosporium infections in other animals have been reported much less frequently [29]. Soil-dwelling Chrysosporium spp. may be responsible for pulmonary disease in burrowing rodents [48] or cases of adiaspiromycosis with lymph node involvement in wild rabbits (Oryctolagus cuniculus) [49]. C. keratinophilum was identified in cultures of seven Bennett’s wallabies (Macropus rufogriseus rufogriseus) suffering from onychodystrophy, onychomadesis, and severe swelling of the digits on the claws [26].
Chrysosporium spp. has been reported isolated from domestic animals [39,40,41,42,43,44]. It was identified as the etiologic agent in one of 10 dogs in Australia [39]. Chrysosporium spp. was confirmed as the cause of fungal keratitis in one of 11 dogs [41]. It was also detected in needle aspirates from the iliac lymph nodes and spleen of a German shepherd in Australia [42]. In Turkey, superficial skin lesions caused by Chrysosporium spp. were found in two Persian cats and their owner, who lived in the same household [43]. C. articulatum was isolated from a cat in Poland with dermatophytosis that resembled that of Trichophyton spp. [29]. Chrysosporium spp. was also isolated from a horse with a corneal ulcer, stromal abscess, and severe diffuse non-ulcerative keratitis [25]. Two other cases of Chrysosporium spp. detection in equine biomaterial were associated with the isolation of the pathogen from horse hair [28,50].
Particular attention should be paid to cases of incorrect diagnosis and pathogen identification in skin mycoses, especially with the emergence of the new pathogen Chrysosporium spp., which shares cultural and morphological similarities with classical dermatophytosis pathogens, particularly T. mentagrophytes [23,51,52].
The development of a treatment regimen for skin mycoses caused by Chrysosporium requires careful attention. The treatment regimens described for warm-blooded animals with superficial mycosis caused by Chrysosporium spp. in horses are typically associated with the local use of antifungal drugs, diet, and rest [25,41,42]. In Kazakhstan, treatment of opportunistic skin mycosis is still evolving. No data on the detection of Chrysosporium spp. pathogens in horses from Kazakhstan have been found. Generally, information on opportunistic mycoses in Kazakhstan remains fragmentary [53,54,55,56,57], and many opportunistic pathogens are not confirmed by the latest taxonomy [58,59] or genomic analysis [60,61]. This underscores the need for reliable identification of opportunistic pathogens in horses with skin lesions, determining their sensitivity to antimycotics, and developing treatment recommendations for farmers, animal owners, and veterinarians.
The aim of this scientific research was to identify the causative agents of mycosis in horses in northern Kazakhstan and confirm their taxonomic classification. The main objectives of the research are to determine the types of mycosis-causing agents in horses of various purposes in northern Kazakhstan, analyze the occurrence of Chrysosporium spp. as a pathogenic agent in the context of global and local research, and describe the taxonomic classification of new causative agents of equine dermatomycosis in Kazakhstan.

2. Materials and Methods

2.1. Search Strategy

A systematic review and meta-analysis were conducted in accordance with the recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA). A comprehensive database search was performed using PubMed and the Cochrane Library. The search was limited to English-language articles published between 1964 and 2024.

2.2. Research Area and Period

In accordance with the set objectives, we analyzed the pathogens of equine skin mycoses in the northern and central regions of Kazakhstan. Sampling was conducted in three northern regions (Akmola, Kostanay, and North Kazakhstan) and one central region (Karaganda). The study was carried out in the laboratories of the Scientific and Production Platform of Agricultural Biotechnology at Saken Seifullin Kazakh Agrotechnical Research University and the Laboratory of Biodiversity and Genetic Resources of the National Biotechnology Center.

2.3. Study Design and Populations

Commercial horses were kept on free grazing, while racehorses and sport horses were housed in individual stalls with controlled grazing. Sampling was conducted in late September to early October. A total of 21 biomaterial samples were collected from animals suspected of being infected or ill, with samples taken from the affected areas on the head and body of the horses. Special attention was given to the affected hair and the presence of skin scales along the edges of the lesions. Scrapings of the dense, white, floury contents from the affected areas were taken with a scalpel at the center of the lesion until the wound surface appeared, following biosafety protocols and humane treatment practices for animals. After collecting samples from the skin and hair, a primary screening was conducted using microscopy to detect the presence of fungal mycelium and spores. Samples were collected using methods approved by the local ethics committee of Seifullin Kazakh Agrotechnical Research University (Protocol No. 2, dated 03 November 2022). The study adhered to the requirements of the International Guiding Principles for Biomedical Research Involving Animals and the European Convention for the Protection of Vertebrate Animals used for Experimental and Other Scientific Purposes [61].

2.4. Microbiological Research

Primary isolation of pathogens was performed on Sabouraud media: Sabouraud dextrose agar and Sabouraud medium supplemented with chloramphenicol (Titan Biotech Ltd., Delhi, India) to inhibit the growth of extraneous bacterial biota. Cultivation was carried out at 28 °C for 12–15 days. Pure cultures were isolated on Sabouraud medium without the addition of antimycotics. Inoculation was performed using three passages in a triangular pattern along the diameter of the Petri dishes [62]. Microscopic analysis of the morphological structures of the micromycetes was conducted using a trinocular transmitted light microscope (AxioScope A1, Zeiss, Oberkochen, Germany) at a magnification of ×40 [63].

2.5. Biochemical Research

To study the biochemical properties of the isolated fungal cultures, Giss media containing lactose, glucose, sucrose, maltose, and mannitol were used [64]. Christensen agar with 40% urea was employed to test urease activity [65]. Proteolytic activity of the isolated fungi was assessed using skim milk agar. Additionally, nutrient gelatin was used to detect proteolytic activity based on gelatin liquefaction [66]. Columbia nutrient medium with 5% sheep blood agar was used to evaluate the hemolytic activity of the fungi [67]. Keratinolytic properties were assessed using the classic hair perforation test, following standard mycological procedures [55]. Antifungal susceptibility was determined using the CLSI method [68], as described by the authors [69].

2.6. Genetic Research

To confirm the accuracy of the cultural and morphological identification, genetic identification of the micromycetes was subsequently performed through ribosomal gene sequencing. Genomic DNA was extracted from five-day-old colonies using the method described by Kukhar et al. (2013) [70]. The procedure for isolating micromycete genomic DNA involved growing the biomass on solid nutrient media for 5–10 days, depending on the colony growth pattern. A colony fragment was separated from the substrate, transferred to a mortar, and 300 μL of 2% CTAB (2% CTAB, 1.4 M NaCl, 20 mM EDTA, 500 mM Tris-HCl, made up to 50 mL with distilled water) was added, followed by incubation with Proteinase K for 14–16 h at 65 °C. DNA extraction continued using the standard phenol-chloroform method [71].
Genotyping was performed using a Bio-Rad T100 thermal cycler (Bio-Rad, Hercules, CA, USA). PCR was carried out in a total reaction volume of 25 μL containing 5 μL of 5× buffer (Promega), 1 μL of dNTPs (20 mM), 1.5 μL of MgCl2 (25 mM), 0.25 U (5 U/μL) of Taq DNA polymerase, 2 μL of primers (20 pmol/μL), and 2 μL of genomic DNA (50 ng/μL). The amplification program included an initial denaturation at 95 °C for 3 min, followed by 35 cycles of denaturation at 95 °C (15 s), annealing at 59 °C (30 s), extension at 72 °C (45 s), and a final extension at 72 °C for 10 min in a SimpliAmp™ Thermal Cycler (Thermo Fisher Scientific, Waltham, MA, USA).
Following amplification, PCR products were electrophoresed on 1.5% agarose gels buffered with 0.5× TBE (4.5 mM Tris, 4.5 mM boric acid, and 1 mM EDTA, pH 8) and stained with ethidium bromide using primers ITS1 (5′-TCGGTAGGTGAACCTGCGG-3′) and ITS4 (5′-CCTCCGCTTATTGATATGC-3′) [72]. PCR products were purified enzymatically using ExoI and SAP, and sequences were determined by cycle sequencing. Sequencing was performed with the BigDye® Terminator v3.1 Cycle Sequencing Kit (Applied Biosystems Thermo Fisher Scientific, Carlsbad, CA, USA), following the manufacturer’s instructions, and fragment separation was performed using an IonTorrent automated genetic sequencer (Applied Biosystems Thermo Fisher Scientific, Carlsbad, CA, USA). For comparative analysis, sequences of Chrysosporium zonatum strains (OW987038.1, OW986965.1, OW986863.1, KY290545.1) and Chrysosporium kreiselii (MN862059.1), published in GenBank (https://blast.ncbi.nlm.nih.gov/Blast.cgi, accessed on 22 December 2024), were used.

2.7. Bioinformatics Analysis

For the multiple sequence alignment, the MUSCLE (Multiple Sequence Comparison by Log-Expectation) method was employed. Following the alignment, a phylogenetic analysis was conducted utilizing the maximum likelihood mathematical algorithm implemented in MEGA v. 11 software [73]. The species Agaricus candussoi (accession number NR158351) was chosen as the outgroup, providing a clear basis for rooting and enhancing the interpretation of the evolutionary pathways observed in the analysis.

3. Results

3.1. Data Analysis

An analysis of the literature shows that in recent years, Chrysosporium spp. have increasingly been identified as opportunistic pathogens in various invasive systemic and deep non-invasive diseases, as well as in rhinosinusitis and subcutaneous or superficial mycoses in animals and birds (Table 1).
In animals, Chrysosporium spp. is most commonly reported to infect cold-blooded animals (various species of snakes, crocodiles, and other reptiles). Cases of Chrysosporium spp. being isolated as pathogens have also been recorded in warm-blooded animals. We found only three publications on the detection of Chrysosporium spp. from the skin, mucous membranes, or hair of horses.

3.2. Clinical Signs and Microbiological Study Results

During our research, in accordance with the set objectives, a total of 90 samples were collected from horses in the northern and central regions of the Republic of Kazakhstan (Table 2).
As shown in Table 2, the total number of positive samples was 68.9% (62 samples). In 31.1% of cases, no pathogen growth was detected in the total number of samples. As a result of the cultural mycological analysis of the biological material, fungi were isolated from 62 samples. Of the total isolates, 14.4% were classical dermatophytes, while 85.6% were opportunistic fungi, including 77.8% mold fungi and 7.8% yeast strains.
A total of 90 isolates were obtained from the positive samples, and 26 fungal taxa were identified at the genus level (Figure 1).
In the mycobiota of skin lesions of horses with various purposes, filamentous fungi of the genus Aspergillus dominated, comprising 49% of the total. The breakdown of Aspergillus species was as follows: Aspergillus spp.—12.3%, A. protuberus—7.8%, A. chevalieri—5.6%, A. amstelodami—10.0%, A. pseudoglaucus—7.8%, A. cristatus—3.3%, A. minutus—1.1%, and A. flavus—1.1%. Other common species included A. alternata—7.8%, Penicillium notatum—6.6%, and Mucor indicus—6.7%. Additionally, several yeast species were identified: Rhodotorula mucilaginosa—3.3%, yeasts of the genus Candida—4.5%, and Aureobasidium pullulans—1.1%. Among keratinophilic fungi, T. mentagrophytes was isolated—12.2%, Microsporum spp.—1.1%, and Chrysosporium spp.—2.2%. In total, keratinophilic fungi accounted for 15.5%.
During our scientific research on the identification of dermatophytosis pathogens in horses in the Northern and Central regions of Kazakhstan, we found that some horses exhibited various skin lesions. Some of these lesions showed clinical similarities to those characteristics of classic dermatomycosis, while others presented uncharacteristic signs (Figure 2). The lesions were located on the muzzle, neck, and body of the animals, with the majority of the detected lesions on the muzzle. The lesions were primarily small, white, and mealy, measuring 1–2 cm in diameter. The alopecia zones on the facial areas of the horses’ heads were characterized by lesions measuring 2.0 × 0.9 cm, with clear, even, oval-shaped borders. The skin within the affected area appeared hyperemic (Figure 2).
As shown in Figure 2, the lesions on the commercial horse (Figure 2A) resembled classic dry trichophytosis, characterized by a white powdery surface. The flaking areas on the racehorse’s body (Figure 2B) were clinically identified as dry dermatitis with dandruff formation, though seborrhea remains questionable.
Primary isolation and characterization of the pathogens revealed the presence of various types of colonies. During the initial isolation from samples, fluffy brown colonies with black pigment formation were observed, along with whitish to light beige colonies that formed pigmentation foci ranging from yellowish to orange and resembled dermatophyte colonies morphologically.
When analyzing pure cultures, attention was given to the color of both the front and back sides of the colonies, substrate pigmentation, and the shape and surface of the colonies (Figure 3).
Colonies of pure cultures from strains No. 15.23.7H and No. 9.23.6H, which resemble dermatophytes, are uniform and exhibit distinct zonality: a powdery raised center, a fluffy growing edge, and a light yellow or pale orange pigment on the reverse side of the colony, although they differ in size (Figure 3). Cultural and morphological identification suggested that the white colonies with straw-yellow and orange-brown pigments correspond to dermatophyte colonies of the genus Trichophyton. The morphological similarity of the strain colony to typical colonies of T. mentagrophytes, along with the presence of microstructures such as twisted, colorless, thin, smooth or branched septate mycelium with chlamydospores and microconidia in characteristic single or cluster-like formations (Figure 3C,E), allowed for the identification of this pathogen as T. mentagrophytes.
In contrast, the pure culture of primary heterogeneous brown colonies from sample No. 15.23.7.1H differed significantly (Figure 3). These colonies had a brown color on the front, a black pigment on the reverse side, did not stain the substrate, and were identified by cultural and morphological characteristics as fungi of the genus Alternaria. Microscopic analysis of strain No. 15.23.7.1H revealed the presence of dark brown mycelium and conidia characteristic of Alternaria alternata (Figure 3D).
The obtained sequence was analyzed using BLAST (Stable release 2.16.0+[1], 25 June 2024) with the NCBI database, which revealed 98.9% identity in both cases with the sequences of C. kreiselii and C. zonatum. Phylogenetic analysis was performed on the obtained data for the Chrysosporium strains. The final dataset contained 1898 positions. Two isolates from this study (marked with red circles), designated as C. zonatum isolate KZ 09-23-6H and C. kreiselii isolate 15-23-7H, grouped with their respective reference species (C. zonatum and C. kreiselii), confirming their taxonomic placement. Agaricus candussol (NR 158351.1) served as an outgroup species, providing evolutionary context. Other fungal species also formed a separate clade with their related sequences. Low node support is evident, indicating a moderate but weak level of clustering. The phylogenetic tree of species evolution, constructed using the maximum likelihood algorithm, is presented in Figure 4.
After analyzing the obtained results, the nucleotide sequence of C. kreiselii was deposited in the GenBank database under accession number PQ796874, and that of C. zonatum was deposited under accession number PV034795.
Thus, isolates from horses with dermatological lesions, initially diagnosed as Trichophyton spp. infection, were identified by sequencing as Chrysosporium spp., which are generally considered non-pathogenic fungi.

3.3. Study on the Pathogenicity of Isolated Strains

To confirm the pathogenicity of potential opportunistic strains, enzymatic activity, including activity against keratin, was assessed. Analysis of the enzymatic activity of C. kreiselii strain No. 15.23.7H and C. zonatum strain No. 9.23.6H, isolated from horse biomaterial samples, revealed that both isolates were capable of breaking down glucose, mannitol, maltose, sucrose, lactose, and urea. C. kreiselii No. 15.23.7H showed higher saccharolytic activity, though it was inferior to C. zonatum No. 9.23.6H only in glucose degradation. Proteolytic enzyme activity toward gelatin and hemoglobin was observed in C. zonatum No. 9.23.6H. Neither strain broke down milk casein (Figure 5).
When determining the nature of growth on media enriched with keratin, both isolates demonstrated the ability of the micromycetes to assimilate this protein, as evidenced by an increase in colony diameter and visible growth of both surface and deep mycelium (Figure 6).
As shown in Figure 6, colonies of Chrysosporium spp. strains on nutrient dextrose Sabouraud agar enriched with keratin had a larger diameter compared to colonies growing on regular Sabouraud agar, which served as the control. This result indicates the presence of keratinophilic properties in C. kreiselii No. 15.23.7H and C. zonatum No. 9.23.6H.
In the hair perforation test, the analyzed Chrysosporium spp. strains exhibited keratinolytic properties. More pronounced keratinolytic activity was observed in C. kreiselii №15.23.7H, which manifested as abundant mycelial growth on the hair surface (Figure 7A), damage to the hair cuticle externally visible as surface erosion (Figure 7B), loosening or thinning of the hair, and noticeable keratinolysis, with visible damage resembling “pegs” (Figure 7C).

3.4. Antifungal Drug Susceptibility

Analysis of the susceptibility of fungal strains isolated from horses to antifungal drugs showed that the C. kreiselii strain 15.23.7H (Figure 8A), isolated from a racehorse in the Karaganda region, is resistant to almost all antifungal drugs, while the C. zonatum strain 9.23.6H is susceptible to all drugs except Fluconazole (Figure 8B). The A. alternata strain No. 15.23.7.1H (Figure 8C), isolated in association with C. kreiselii 15.23.7H, is susceptible to Ketoconazole, weakly sensitive to Nystatin, and Clotrimazole (Figure 8).
The C. kreiselii 15.23.7H strain is resistant to Nystatin, Amphotericin, and Fluconazole, and shows weak sensitivity to Clotrimazole and Ketoconazole. The C. zonatum 9.23.6H strain, isolated from a racehorse in the Karaganda region, showed weak sensitivity to Amphotericin, was sensitive to Nystatin and Ketoconazole, and resistant to Clotrimazole and Fluconazole.

4. Discussion

During the initial isolation of pathogens from 543 samples of biological material from domestic and wild animals in Northern Kazakhstan, conducted between 2012 and 2022, the predominant micromycetes were opportunistic mold fungi (50.2%), including Mucor spp., Penicillium spp., Aspergillus spp., Alternaria spp., Chaetomium spp., Eurotium spp., Phoma spp., Trichoderma spp., Lecanicillium psalliotae, Scopulariopsis brevicaulis, and others. Dermatophytes of the genera Trichophyton spp. and Microsporum spp. were detected in only 17.1% of cases. Yeasts of the genera Candida spp., Rhodotorula spp., and Exophiala spp. were isolated in only 5.1% of cases. In 27.6% of cases, no growth of micromycetes was observed in the biomaterial samples, or bacterial growth was noted. In the regions of Northern Kazakhstan and Western Siberia in Russia, a shift toward an increase in the number of opportunistic microorganisms was observed. Of the total number of identified micromycetes, 23.6% were classic causative agents of dermatomycosis, 69.3% were opportunistic causative agents of mold mycoses, and 7% were causative agents of yeast mycoses [97,98]. Our data are consistent with those of other researchers who have reported an increase in the proportion of opportunistic pathogens worldwide [2,7,13,14,15,16,17,18,19,20,21,99,100,101,102].
An analysis of the literature on cases of cutaneous mycoses caused by Chrysosporium spp. revealed reports of cutaneous infections in humans [99,100,101,102], reptiles, both wild and captive [74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,103,104], chickens [37], dogs [40], kangaroos [43], and cats [30,97]. Publications also describe the isolation of Chrysosporium spp. from horse hair [28,51]. To date, there have been no reports on the detection of Chrysosporium spp. in biomaterial or cases of cutaneous mycoses caused by Chrysosporium spp. in farm, wild, or domestic animals in Kazakhstan. However, when isolating pathogens from wild, farm, and domestic animals in Kazakhstan between 2023 and 2025, the authors of this article identified the emergence of new opportunistic microorganisms—representatives of the mold mycobiota, including Chrysosporium spp., Corynascus novoguineensis, and Lachnum controversum [105].
A racehorse from central Kazakhstan was found to have skin lesions similar to those characteristics of classic dermatomycosis. A farm horse from northern Kazakhstan showed uncharacteristic lesions, such as dandruff and seborrheic lesions.
Primary fungal cultures of pathogens isolated from the affected horses resembled dermatophytes and were thus cultured as pure strains. Colonies of two strains of Chrysosporium spp., isolated from the biomaterial of racehorses and farm horses, were initially identified based on their primary cultural and morphological features as dermatophytes of the genus Trichophyton. Moreover, the cultural, morphological, and biochemical characteristics of these colonies were consistent with T. mentagrophytes. The search for microconidia and macroconidia was challenging, as their formation was not observed in young colonies.
A similar case of laboratory misidentification based on culture-morphological identification was described by Kizerwetter-Świda et al. (2024) [29], in which Chrysosporium spp. were isolated from a cat with dermatological lesions typical of dermatophytosis caused by Trichophyton spp. The authors noted that the dermatological lesions in the cat were clinically consistent with dermatophytosis usually caused by Trichophyton spp., including alopecia on the back of the neck, ventral abdomen, and hind limbs. Initial identification of the pathogen, based on phenotypic properties, indicated Trichophyton spp., but this was excluded by MALDI-ToF MS. Ultimately, the correct identification of the strain as C. articulatum was confirmed through ribosomal gene sequencing [9].
In our study of the keratinophilic properties of pathogens during cultivation on a modified Sabouraud medium enriched with animal keratin, we found that both strains of Chrysosporium spp., isolated from the biomaterial of a racehorse and a farm horse from central and northern Kazakhstan, exhibited keratinophilic properties. This was evidenced by the more rapid colony formation and biomass accumulation on Sabouraud media containing keratin. Previous studies have reported the isolation of keratinophilic fungi of the genus Chrysosporium from soil, animal hair, and bird feathers [42,44,45]. For instance, fifteen keratinophilic fungi, including eight species of Chrysosporium, predominantly C. zonatum, were isolated from the hair of cows and buffaloes, soil from fields, and animal cages [44]. In India, representatives of the genus Chrysosporium were isolated from feather samples of 117 birds representing 11 species examined for keratinophilic fungi: C. indicum (26.4%), C. tropicum (11.1%), C. aphanoascus spp. (2.5%), and C. arthroderma tuberculatum (3.4%) [45].
As is well known, the pathogenic properties of skin mycosis pathogens are primarily attributed to the activity of the keratinase enzyme and their ability to degrade keratin [106]. In pure cultures, a positive hair perforation test was observed, demonstrating pronounced keratinolytic properties. This included abundant mycelium growth on the hair surface, damage to the hair cuticle, corrosion of the hair surface, loosening and thinning of the hair, and the appearance of noticeable “pegs”, although not characteristic of T. mentagrophytes.
It is important to note that strain A. alternata No. 15.23.7.1H, isolated from horse biomaterial in association with C. kreiselii 15.23.7H, did not display pronounced keratinolytic properties. A. alternata No. 15.23.7.1H is a keratinophilic fungus, as it grew abundantly on the hair surface in vitro, without forming characteristic “pegs” and causing minimal damage to the cuticle, manifesting as longitudinal cracks on its surface. Based on this observation, the diagnosis was initially dermatophytosis caused by T. mentagrophytes. However, molecular genetics identification of the strains revealed 98.9% identity with the C. kreiselii sequence and 98.9% identity with the C. zonatum sequence, allowing us to exclude the diagnosis of T. mentagrophytes.
Furthermore, it is important to note that several geophilic Chrysosporium spp., including Anixiopsis stercoraria, C. keratinophilum, C. tropicum, C. pannorum, C. curreyi, A. multifidum, and A. tuberculatum, were reported by Chabasse D. et al. (1989) [107] to not exhibit actual hair contamination during pathogenicity assessments. While the authors did not confirm the pathogenic role of these keratinophilic fungi, they noted that their ability to remain viable for several weeks in skin and abdominal tissue suggested that they could become pathogenic under certain conditions [46].
The determination of the susceptibility of Chrysosporium strains isolated from horses to antifungal drugs revealed that both strains are resistant to fluconazole. Specifically, the C. kreiselii strain 15.23.7H, isolated from a racehorse in the Karaganda region, is resistant to nearly all the studied antifungals, while the C. zonatum strain 9.23.6H is susceptible to all drugs except fluconazole. Our findings are consistent with those of authors who have discussed the global issue of dermatophyte and mold fungi resistance to antifungal drugs [108].
It is also important to note that no information exists regarding the successful treatment of cutaneous forms of equine mycoses caused by Chrysosporium spp. using antifungal drugs. We hypothesize that this may be linked to the morphological similarity of Chrysosporium spp. to dermatophytes of the Trichophyton genus, especially T. mentagrophytes, as reported earlier [1,10,24]. This similarity may have led to misdiagnosis and inappropriate treatment strategies.
We argue that the presence of keratinophilic and keratinolytic properties, combined with resistance to antimycotics, are significant factors supporting the pathogenicity of Chrysosporium strains. This suggests that these strains did not merely colonize the horse’s coat accidentally but actually caused skin pathology in the horses. A similar case of Chrysosporium spp. isolation from horses was described by Khalaf et al. (2024) [50]. Our data on the identification of Chrysosporium strains align with the viewpoint of specialists [103], who believe that the low frequency of reported primary skin infections caused by Chrysosporium may reflect either an underestimation of this diagnosis in the literature or a misidentification of this fungus as a more commonly encountered species with similar morphology.
We conclude that detecting Chrysosporium skin infections in horses in Kazakhstan requires a thorough retrospective analysis of the spectrum of newly identified pathogens, with a comprehensive characterization of the pathogenicity of the strains. Accurate identification of the pathogen, along with an assessment of pathogenicity factors and sensitivity to antimycotics, will help develop effective treatment and prevention strategies, minimizing the risk of medical errors in the management of equine skin mycoses associated with Chrysosporium spp.

5. Conclusions

Chrysosporium spp. were isolated from lesions on the skin of horses in Kazakhstan for the first time. Molecular genetics identification of the strain revealed a 98.9% identity with the sequences of C. kreiselii and C. zonatum in each case. The C. kreiselii strain was isolated from horse biomaterial in association with the opportunistic pathogen strain A. alternata No. 15.23.7.1H, while the C. zonatum strain was isolated in monoculture. The C. kreiselii and C. zonatum strains were distinguished by their pronounced pathogenicity, keratinophilic properties, and resistance to antifungal drugs. Both strains are resistant to Fluconazole. The C. kreiselii 15.23.7H strain is also resistant to Nystatin and Amphotericin, and is weakly susceptible to Clotrimazole and Ketoconazole. The C. zonatum 9.23.6.H strain is weakly susceptible to Amphotericin and is resistant to Clotrimazole and Fluconazole.

Author Contributions

Conceptualization, Y.K. and V.K.; methodology, Y.K., R.U. and V.K.; software, A.S. and R.U.; validation, Y.K., A.S. and G.B.; formal analysis, G.B., R.U. and A.S.; investigation, Y.K.; resources, Y.K. and V.K.; data curation, Y.K. and V.K.; writing—original draft preparation, Y.K., V.K. and A.S.; writing—review and editing, Y.K. and V.K.; visualization, G.B., A.S. and R.U.; supervision, Y.K. and V.K.; project administration, Y.K.; funding acquisition, Y.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the Ministry of Science and Higher Education of the Republic of Kazakhstan under project # AP19678812 for 2023–2025.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of Seifullin Kazakh Agrotechnical Research University (decision #2, dated 03 November 2022).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The original contributions presented in the study are included in the article; further inquiries can be directed to the corresponding author.

Acknowledgments

The authors express their sincere gratitude to the veterinarians at agricultural enterprises for their assistance in collecting biological material from sick animals on-site.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Young, A. Ringworm in Horses (Dermatophytosis); UC Davis Veterinary Medicine Center for Equine Health: Davis, CA, USA, 2022. [Google Scholar]
  2. Cafarchia, C.; Figueredo, L.A.; Otranto, D. Fungal Diseases of Horses. Vet. Microbiol. 2013, 167, 215–234. [Google Scholar] [CrossRef] [PubMed]
  3. Fadok, V.A. An overview of equine dermatoses characterized by scaling and crusting. Vet. Clin. N. Am. Equine Pract. 1995, 11, 43–51. [Google Scholar] [CrossRef] [PubMed]
  4. Berdybaev, U.B. Fungal Diseases in Kazakhstan. Kazgosizdat: Almaty, Kazakhstan, 1959; pp. 3–65. [Google Scholar]
  5. 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 Maced. J. Med. Sci. 2017, 5, 409–413. [Google Scholar] [CrossRef] [PubMed]
  6. Kukhar, Y.; Kiyan, V.; Smagulova, A.; Nikulina, A. Identification of dermatomycetes isolated from people and animals with dermatophytoses on the territory of Kazakhstan. Adv. Anim. Vet. Sci. 2019, 7, 21–27. [Google Scholar]
  7. White, S.D. Equine Bacterial and Fungal Diseases: A Diagnostic and Therapeutic Update. Clin. Tech. Equine Pract. 2005, 4, 302–310. [Google Scholar] [CrossRef]
  8. Kane, J.; Padhye, A.A.; Ajello, L. Microsporum equinum in North America. J. Clin. Microbiol. 1982, 16, 943–947. [Google Scholar] [CrossRef]
  9. Romano, C.; Massai, L.; Gianni, C.; Crosti, C. Case Reports: Six Cases of Infection Due to Trichophyton verrucosum. Mycoses 2001, 44, 334–337. [Google Scholar] [CrossRef]
  10. Scott, D.W. Marked Acantholysis Associated with Dermatophytosis Due to Trichophyton equinum in Two Horses. Vet. Dermatol. 1994, 5, 105–110. [Google Scholar] [CrossRef]
  11. Scott, D.W.; Miller, W.H. Equine Dermatology; WB Saunders: St. Louis, MO, USA, 2003; p. 96. [Google Scholar]
  12. Pier, A.C.; Zancanella, P.J. Immunization of horses against dermatophytosis caused by Trichophyton equinum. Equine Pract. 1993, 15, 23–27. [Google Scholar]
  13. Keller, M.; Krehon, S.; Stanek, C.; Rosengarten, R. Keratinopathogenic mould fungi and dermatophytes in healthy and diseased hooves of horses. Vet. Rec. 2000, 147, 619–622. [Google Scholar] [CrossRef]
  14. Kaleybar, M.T.; Inalou, A.H.; Katiraee, F. Clinical and mycological evaluations of horses affected with cutaneous lesions in Ardabil, Iran. J. Zoonotic Dis. 2021, 5, 42–49. [Google Scholar] [CrossRef]
  15. Blackford, J. Superficial and Deep Mycoses in Horses. Vet. Clin. N. Am. Large Anim. Pract. 1984, 6, 47–58. [Google Scholar] [CrossRef] [PubMed]
  16. Gnat, S.; Łagowski, D. Fungal infections in horses. Part I. Dermatomycoses and keratomycoses. Vet. Life A Socio-Prof. Sci. J. Natl. Vet. Med. Chamb. 2021, 96, 260–267. [Google Scholar]
  17. Padalino, B.; Sandy, J.R.; Barrasso, R.; Trotta, A.; Bozzo, G.; Cafarchia, C. Rare generalized form of fungal dermatitis in a horse: Case report. Animals 2020, 10, 871. [Google Scholar] [CrossRef]
  18. Figueredo, L.A.; Cafarchia, C.; Otranto, D. Geotrichum candidum as etiological agent of horse dermatomycosis. Vet. Microbiol. 2011, 148, 368–371. [Google Scholar] [CrossRef]
  19. Kuwano, A.; Tanaka, K.; Kawabata, M.; Ooi, Y.; Takahashi, R.; Reilly, J.D. A survey of white line disease in Japanese racehorses. Equine Vet. J. 1999, 31, 515–518. [Google Scholar] [CrossRef]
  20. Ovchinnikov, R.S.; Manoyan, M.G.; Panin, A.N. Emergent fungal infections of animals: New species of pathogens. Vet. Pharm. 2014, 2, 48–51. [Google Scholar]
  21. Bennett, A.; Ponder, M.M.; Garcia-Diaz, J. Phoma infections: Classification, potential food sources, and its clinical impact. Microorganisms 2018, 6, 58. [Google Scholar] [CrossRef]
  22. Konkel Neabore, L. Wake-up Call: Rapid Increase in Human Fungal Diseases under Climate Change. Environ. Health Perspect. 2024, 132, 42001. [Google Scholar] [CrossRef]
  23. Gurung, S.K.; Adhikari, M.; Kim, S.W.; Bazie, S.; Kim, H.S.; Lee, H.G.; Kosol, S.; Lee, H.B.; Lee, Y.S. Discovery of two Chrysosporium species with keratinolytic activity from field soil in Korea. Mycobiology 2018, 46, 260–268. [Google Scholar] [CrossRef]
  24. Mitola, G.; Escalona, F.; Salas, R.; García, E.; Ledesma, A. Morphological characterization of in-vitro human hair keratinolysis, produced by identified wild strains of Chrysosporium species. Mycopathologia 2002, 156, 163–169. [Google Scholar] [CrossRef] [PubMed]
  25. Grahn, B.; Wolfer, J.; Keller, C.; Wilcock, B. Equine keratomycosis: Clinical and laboratory findings in 23 cases. Prog. Vet. Comp. Ophthalmol. 1993, 3, 2–7. [Google Scholar]
  26. Pin, D.; Vidémont, E.; Derian-Autier, D.; Guillot, J.; Plouzeau, E. First description of onychomycosis caused by Chrysosporium keratinophilum in captive Bennett’s wallabies (Macropus rufogriseus rufogriseus). J. Zoo Wildl. Med. 2011, 42, 156–159. [Google Scholar] [CrossRef] [PubMed]
  27. Al-Musallam, A.; Tan, C.S. Chrysosporium zonatum, a new keratinophilic fungus. Persoonia 1989, 14, 69–71. [Google Scholar]
  28. Ovchinnikov, R.S.; Vasyliev, D.B. Pathogenic Chrysosporium-Related Fungi in Reptiles and Other Animals. In Recent Trends in Human and Animal Mycology; Springer: Singapore, 2019. [Google Scholar] [CrossRef]
  29. Kizerwetter-Świda, M.; Bąk, I.; Biegańska, M.J.; Dembele, K.; Chrobak-Chmiel, D. Chrysosporium articulatum mimicking Trichophyton spp. infection in a cat: A case presentation and literature review. BMC Vet. Res. 2024, 20, 359. [Google Scholar] [CrossRef]
  30. Labuda, R.; Bernreiter, A.; Hochenauer, D.; Kubátová, A.; Kandemir, H.; Schüller, C. Molecular systematics of Keratinophyton: The inclusion of species formerly referred to Chrysosporium and description of four new species. IMA Fungus 2021, 12, 17. [Google Scholar] [CrossRef]
  31. Boehm, T.M.; Mueller, R.S. Dermatophytosis in dogs and cats—An update. Tierarztl. Prax. Ausg. K Kleintiere Heimtiere 2019, 47, 257–268. [Google Scholar] [CrossRef]
  32. Ajello, L. Soil as a natural reservoir for human pathogenic fungi. Science 1956, 123, 876–879. [Google Scholar] [CrossRef]
  33. Kidd, S.E.; Weldhagen, G.F. Diagnosis of Dermatophytes: From Microscopy to Direct PCR. Microbiology 2022, 43, 9–13. [Google Scholar] [CrossRef]
  34. Ogórek, R.; Suchodolski, J.; Piecuch, A.; Przywara, K.; Višňovská, Z. Keratinophilic and keratinolytic fungi in cave ecosystems: A culture-based study of Brestovská Cave and Demänovská Ľadová and Slobody Caves (Slovakia). Appl. Sci. 2022, 12, 1455. [Google Scholar] [CrossRef]
  35. Jain, N.; Sharma, M. Influence of temperature and culture conditions on the survival of keratinophilic and dermatophytic fungi. Braz. Arch. Biol. Technol. 2022, 65, e22210337. [Google Scholar] [CrossRef]
  36. Lott, M.J.; Moore, R.L.; Milic, N.L.; Power, M.; Shilton, C.M.; Isberg, S.R. Dermatological conditions of farmed crocodilians: A review of pathogenic agents and their proposed impact on skin quality. Vet. Microbiol. 2018, 225, 89–100. [Google Scholar] [CrossRef] [PubMed]
  37. Saidi, S.A.; Bhatt, S.; Richard, J.L.; Sikdar, A.; Ghosh, G.R. Chrysosporium tropicum as a probable cause of mycosis of poultry in India. Mycopathologia 1994, 125, 143–147. [Google Scholar] [CrossRef] [PubMed]
  38. Yamaguchi, S.; Sano, A.; Hiruma, M.; Murata, M.; Kaneshima, T.; Murata, Y.; Takahashi, H.; Takahashi, S.; Takahashi, Y.; Chibana, H.; et al. Isolation of dermatophytes and related species from domestic fowl (Gallus gallus Domesticus). Mycopathologia 2014, 178, 135–143. [Google Scholar] [CrossRef]
  39. Watt, P.R.; Robins, G.M.; Galloway, A.M.; O’Boyle, D.A. Disseminated opportunistic fungal disease in dogs: 10 cases (1982–1990). J. Am. Vet. Med. Assoc. 1995, 207, 67–70. [Google Scholar] [CrossRef]
  40. Hajsig, M.; de Vries, G.A.; Sertic, V.; Naglic, T. Chrysosporium evolceanui from pathologically changed dog skin. Vet. Arh. 1974, 44, 209–211. [Google Scholar]
  41. Scott, E.M.; Carter, R.T. Canine keratomycosis in 11 dogs: A case series (2000–2011). J. Am. Anim. Hosp. Assoc. 2014, 50, 112–118. [Google Scholar] [CrossRef]
  42. Cook, E.; Meler, E.; Garrett, K.; Long, H.; Mak, K.; Stephens, C.; Thompson, A. Disseminated Chrysosporium infection in a German shepherd dog. Med. Mycol. Case Rep. 2016, 10, 29–33. [Google Scholar] [CrossRef]
  43. Dokuzeylul, B.; Basaran Kahraman, B.; Sigirci, B.D.; Gulluoglu, E.; Metiner, K.; Or, M.E. Dermatophytosis caused by a Chrysosporium species in two cats in Turkey: A case report. Vet. Med. 2013, 5, 633–646. [Google Scholar] [CrossRef]
  44. Otcenasek, M.; Dvorak, J. The isolation of Chrysosporium keratinophilum (Frey) Carmichael 1962 and similar fungi from Czechoslovakian soil. Mycopathologia 1964, 23, 121–124. [Google Scholar]
  45. Abdel-Razik, M.; Zaki, S.M. Experimental pathogenicity and molecular characterization of an environmental isolate of Chrysosporium zonatum Al-Musallam and Tan (Family: Onygenaceae, Order: Onygenales). Int. J. Agric. Biol. 2008, 10, 273–277. [Google Scholar]
  46. Sur, B.; Ghosh, G.R. Keratinophilic fungi from Orissa, India, II: Isolations from feathers of wild birds and domestic fowls. Sabouraudia 1980, 18, 275–280. [Google Scholar] [CrossRef] [PubMed]
  47. Gründer, S.; Mayser, P.; Redmann, T.; Kaleta, E.F. Mycological examinations on the fungal flora of the chicken comb. Mycoses 2005, 48, 114–119. [Google Scholar] [CrossRef]
  48. Rippon, J.W. Adiaspiromycosis. In Medical Mycology; Rippon, J.W., Ed.; W.B. Saunders: Philadelphia, PA, USA, 1982; pp. 645–648. [Google Scholar]
  49. Hughes, K.; Borman, A.M. Adiaspiromycosis in a wild European rabbit, and a review of the literature. J. Vet. Diagn. Investig. 2018, 30, 614–618. [Google Scholar] [CrossRef]
  50. Khalaf, D.D.; Abouelhag, H.A.; Elnomrosy, S.M.; Ela, N.H.A.; AbdAllah, M.I.; Farahat, E. Molecular identification and phylogenetic classification of fungal pathogens isolated from Egyptian Arabian horses. Int. J. Vet. Sci. 2025, 14, 165–170. [Google Scholar] [CrossRef]
  51. Wijayawardene, N.N.; Hyde, K.D.; Al-Ani, L.K.T.; Tedersoo, L.; Haelewaters, D.; Rajeshkumar, K.C.; Zhao, R.L.; Aptroot, A.; Leontyev, D.V.; Saxena, R.K.; et al. Outline of Fungi and fungus-like taxa. Mycosphere 2020, 11, 1060–1456. [Google Scholar] [CrossRef]
  52. Kidd, S.; Halliday, C.; Alexiou, H.; Ellis, D. Description of Medical Fungi, 3rd ed.; Newstyle Printing; The National Library of Australia Cataloguing: Adelaide, Australia, 2016; 264p. [Google Scholar]
  53. Kukhar, E.V.; Kurmanov, B.A.; Kiyan, V.S.; Egorcheva, E.V.; Muranets, A.P.; Sharipova, A.M.; Panchenko, N.A.; Nikulina, A.I. Changes in the traditional spectrum of pathogens of trichophytosis of cattle in Kazakhstan. In Proceedings of the Role of Veterinary Science and Practice in the Effective Development of Animal Husbandry: Materials of Int. Scientific-Practical. Conf., LLP “Kazakh Research Institute of Veterinary Medicine”, Almaty, Kazakhstan, 25–26 October 2012; pp. 333–340, ISBN 978-601-7344-85-6. (In Russian). [Google Scholar]
  54. Umitzhanov, M.; Bizhanov, B.R.; Boranbayeva, R.S.; Arisbekova, A.T.; Tokeyev, S.O. Vaccinal compounds and vaccines used in the Republic of Kazakhstan against dermatomycosis of agricultural animals and carnivores. In Proceedings of the International Scientific and Practical Conference “Research Progress—2009”, Sofia, Bulgaria, 17–25 February 2009; pp. 53–54, ISBN 978-966-8736-05-6. (In Russian). [Google Scholar]
  55. Kemaykin, V.; Tabinbaev, N.; Khudaibergenova, M.; Olifirovich, A.; Abdrakhmanova, L.; Denning, D.; Klimko, N. An estimate of severe and chronic fungal diseases in the Republic of Kazakhstan. J. Fungi 2018, 4, 34. [Google Scholar] [CrossRef]
  56. Aimoldina, A.; Smagulova, A.; Batpenova, G.; Konnikov, N.; Algazina, T.; Jetpisbayeva, Z.; Azanbayeva, D.; Amantayev, D.; Kiyan, V. Mycological Profile and Associated Factors Among Patients with Dermatophytosis in Astana, Kazakhstan. J. Fungi 2025, 11, 65. [Google Scholar] [CrossRef]
  57. Ivanushkina, N.E. Genus Aspergillus: Nomenclature, classification, distribution. In New in Taxonomy and Nomenclature of Fungi; Dyakov, Y.T., Sergeev, Y.V., Eds.; National Academy of Mycology: Moscow, Russia, 2003; pp. 136–165. (In Russian) [Google Scholar]
  58. Kukhar, Y.; Kiyan, V. Biological properties of anamorphe and teleomorphe of the causing agent of human interdigital trichophythy. Exp. Biol. 2022, 1, 113–125. [Google Scholar] [CrossRef]
  59. Elinov, N.P.; Vasilyeva, N.V.; Raznatovsky, K.I. Dermatomycoses, or superficial mycoses of the skin and its appendages—Hair and nails. Laboratory diagnostics. Probl. Med. Mycol. 2008, 10, 27–34. (In Russian) [Google Scholar]
  60. Umitzhanov, M.; Abdiramanova, B.; Abutalip, A.; Bakirov, N.; Sarimbekova, S. Comparative assessment of regulated methods and PCR in the diagnosis of trichophytosis in veterinary mycology. Open Vet. J. 2023, 13, 1614–1622. [Google Scholar] [CrossRef] [PubMed]
  61. National Research Council (US) Institute for Laboratory Animal Research. The Development of Science-Based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop; National Academies Press (US): Washington, DC, USA, 2004. Available online: https://www.ncbi.nlm.nih.gov/books/NBK25438/ (accessed on 2 April 2025).
  62. Ajello, L.; Georg, L.K.; Kaplan, W.; Kaulman, L. Laboratory Manual for Medical Mycology; US Department of Health Education and Welfare, Public Health Service, Communicable Disease Centre: Atlanta, GA, USA, 1966. [Google Scholar]
  63. Robert, R.; Pihet, M. Conventional Methods for the Diagnosis of Dermatophytosis. Mycopathologia 2008, 166, 295–306. [Google Scholar] [CrossRef] [PubMed]
  64. Tamura, T.; Sato, T.; Matsumoto, M.; Hara, H.; Yamaguchi, M.; Imai, S.; Yoshida, M.; Kobayashi, T.; Kobayashi, H.; Kobayashi, Y.; et al. Evaluation of sugar fermentation and assimilation by fungal isolates from farm animals. J. Appl. Microbiol. 2015, 118, 1567–1575. [Google Scholar] [CrossRef]
  65. Lerm, B.; Kenyon, C.; Schwartz, I.S.; Kroukamp, H.; de Witt, R.; Govender, N.P.; de Hoog, G.S.; Botha, A. First report of urease activity in the novel systemic fungal pathogen Emergomyces africanus: A comparison with the neurotrope Cryptococcus neoformans. FEMS Yeast Res. 2017, 17, fox069. [Google Scholar] [CrossRef]
  66. Saleem, S. Proteolytic Activity and Health Impact of Fungi Isolated from Chickens Feathers in House Breeding Cages. Int. J. Agric. Biol. 2023, 29, 154–160. [Google Scholar]
  67. Kirtsideli, I.U.; Kachalkin, A.V.; Sokolova, D.S. Diversity and enzymatic activity of soil micromycetes. Mycol. Phytopathol. 2010, 44, 375–384. [Google Scholar]
  68. Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antimicrobial Susceptibility Testing of Filamentous Fungi, 2nd ed.; M38-A2; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2008. [Google Scholar]
  69. Wayne, P. Method for Antifungal Disk Diffusion Susceptibility Testing of Yeast. In Approved Guideline CLSI Document M44-A2, 2nd ed.; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2009. [Google Scholar]
  70. Kukhar, E.V.; Sharipova, A.M.; Shevtsov, A.B. Selection of a method for isolating DNA from dermatophytes and other micromycetes. Probl. Med. Mycol. 2013, 15, 95. [Google Scholar]
  71. Psifidi, A.; Dovas, C.I.; Bramis, G.; Lazou, T.; Russel, C.L.; Arsenos, G.; Banos, G. Comparison of Eleven Methods for Genomic DNA Extraction Suitable for Large-Scale Whole-Genome Genotyping and Long-Term DNA Banking Using Blood Samples. PLoS ONE 2015, 10, e0115960. [Google Scholar] [CrossRef]
  72. White, T.J.; Bruns, T.; Lee, S.; Taylor, J. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In PCR Protocols: A Guide to Methods and Applications; Academic Press: Cambridge, MA, USA, 1990; Volume 38, pp. 315–322. [Google Scholar]
  73. Tamura, K.; Stecher, G.; Kumar, S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 2021, 38, 3022–3027. [Google Scholar] [CrossRef]
  74. Steininger, C.; van Lunzen, J.; Sobottka, I.; Rohde, H.; Horstkotte, M.A.; Stellbrink, H.J. Mycotic Brain Abscess Caused by Opportunistic Reptile Pathogen. Emerg. Infect. Dis. 2005, 11, 349–350. [Google Scholar] [CrossRef]
  75. Han, J.I.; Lee, S.J.; Na, K.J. Necrotizing Dermatomycosis Caused by Chrysosporium spp. in Three Captive Green Iguanas (Iguana iguana) in South Korea. J. Exot. Pet Med. 2010, 19, 240–244. [Google Scholar] [CrossRef]
  76. Cabañes, F.J.; Sutton, D.A.; Guarro, J. Chrysosporium-Related Fungi and Reptiles: A Fatal Attraction. PLoS Pathog. 2014, 10, e1004367. [Google Scholar] [CrossRef] [PubMed]
  77. Abarca, M.L.; Martorell, J.; Castellá, G.; Ramis, A.; Cabañes, F.J. Dermatomycosis in a Pet Inland Bearded Dragon (Pogona vitticeps) Caused by a Chrysosporium Species Related to Nannizziopsis vriesii. Vet. Dermatol. 2009, 20, 295–299. [Google Scholar] [CrossRef] [PubMed]
  78. Bertelsen, M.F.; Crawshaw, G.J.; Sigler, L.; Smith, D.A. Fatal Cutaneous Mycosis in Tentacled Snakes (Erpeton tentaculatum) Caused by the Chrysosporium Anamorph of Nannizziopsis vriesii. J. Zoo Wildl. Med. 2005, 36, 82–87. [Google Scholar] [CrossRef]
  79. Bowman, M.R.; Paré, J.A.; Sigler, L.; Naeser, J.P.; Sladky, K.K.; Hanley, C.S.; Helmer, P.; Phillips, L.A.; Brower, A.; Porter, R. Deep Fungal Dermatitis in Three Inland Bearded Dragons (Pogona vitticeps) Caused by Chrysosporium Anamorph of Nannizziopsis vriesii. Med. Mycol. 2007, 45, 371–376. [Google Scholar] [CrossRef]
  80. Hedley, J.; Eatwell, K.; Hume, L. Necrotising Fungal Dermatitis in a Group of Bearded Dragons (Pogona vitticeps). Vet. Rec. 2010, 166, 464–465. [Google Scholar] [CrossRef]
  81. Hellebuyck, T.; Baert, K.; Pasmans, F.; Van Waeyenberghe, L.; Beernaert, L.; Chiers, K.; De Backer, P.; Haesebrouck, F.; Martel, A. Cutaneous Hyalohyphomycosis in a Girdled Lizard (Cordylus giganteus) Caused by the Chrysosporium Anamorph of Nannizziopsis vriesii and Successful Treatment with Voriconazole. Vet. Dermatol. 2010, 21, 429–433. [Google Scholar] [CrossRef]
  82. Johnson, R.S.P.; Sangster, C.R.; Sigler, L.; Hambleton, S.; Paré, J.A. Deep Fungal Dermatitis Caused by the Chrysosporium Anamorph of Nannizziopsis vriesii in Captive Coastal Bearded Dragons (Pogona barbata). Aust. Vet. J. 2011, 89, 515–519. [Google Scholar] [CrossRef]
  83. Nichols, D.K.; Weyant, R.S.; Lamirande, E.W.; Sigler, L.; Mason, R.T. Fatal Mycotic Dermatitis in Captive Brown Tree Snakes (Boiga irregularis). J. Zoo Wildl. Med. 1999, 30, 111–118. [Google Scholar]
  84. Paré, J.A.; Sigler, L.; Hunter, D.B.; Summerbell, R.C.; Smith, D.A.; Machin, K.L. Cutaneous Mycoses in Chameleons Caused by the Chrysosporium Anamorph of Nannizziopsis vriesii (Apinis) Currah. J. Zoo Wildl. Med. 1997, 28, 443–453. [Google Scholar]
  85. Thomas, A.D.; Sigler, L.; Peucker, S.; Norton, J.H.; Nielan, A. Chrysosporium Anamorph of Nannizziopsis vriesii Associated with Fatal Cutaneous Mycoses in the Salt-Water Crocodile (Crocodylus porosus). Med. Mycol. 2002, 40, 143–151. [Google Scholar] [CrossRef] [PubMed]
  86. Abarca, M.L.; Martorell, J.; Castella, G.; Ramis, A.; Cabanes, F.J. Cutaneous Hyalohyphomycosis Caused by a Chrysosporium Species Related to Nannizziopsis vriesii in Two Green Iguanas (Iguana iguana). Med. Mycol. 2008, 46, 349–354. [Google Scholar] [CrossRef] [PubMed]
  87. Van Waeyenberghe, L.; Baert, K.; Pasmans, F.; van Rooij, P.; Hellebuyck, T.; Beernaert, L.; de Backer, P.; Haesebrouck, F.; Martel, A. Voriconazole, a Safe Alternative for Treating Infections Caused by the Chrysosporium anamorph of Nannizziopsis vriesii in Bearded Dragons (Pogona vitticeps). Med. Mycol. 2010, 48, 880–885. [Google Scholar] [CrossRef] [PubMed]
  88. Paré, J.A.; Sigler, L.; Rypien, K.L.; Gibas, C.F.C. Cutaneous Mycobiota of Captive Squamate Reptiles with Notes on the Scarcity of Chrysosporium anamorph of Nannizziopsis vriesii. J. Herpetol. Med. Surg. 2003, 13, 10–15. [Google Scholar] [CrossRef]
  89. Paré, J.A.; Sigler, L.; Rosenthal, K.L.; Mader, D.R. Microbiology: Fungal and Bacterial Diseases of Reptiles. In Reptile Medicine and Surgery, 2nd ed.; Mader, D.R., Ed.; Saunders Elsevier: St. Louis, MO, USA, 2006; pp. 217–238. [Google Scholar]
  90. Paré, J.A.; Coyle, K.A.; Sigler, L.; Maas, A.K.; Mitchell, R.L. Pathogenicity of the Chrysosporium Anamorph of Nannizziopsis vriesii for Veiled Chameleons (Chamaeleo calyptratus). Med. Mycol. 2006, 44, 25–31. [Google Scholar] [CrossRef]
  91. Allender, M.C.; Dreslik, M.; Wylie, S.; Phillips, C.; Wylie, D.B.; Maddox, C.; Delaney, M.A.; Kinsel, M.J. Chrysosporium sp. Infection in Eastern Massasauga Rattlesnakes. Emerg. Infect. Dis. 2011, 17, 2383–2384. [Google Scholar] [CrossRef]
  92. Schmidt-Ukaj, S.; Loncaric, I.; Klang, A.; Spergser, J.; Häbich, A.-C.; Knotek, Z. Infection with Devriesea agamarum and Chrysosporium guarroi in an inland bearded dragon (Pogona vitticeps). Vet. Dermatol. 2014, 25, 555-e97. [Google Scholar] [CrossRef]
  93. Prabhakar, A.L.M.S.; Siddiqui, A.S.U.; Wani, A.H.; Mehta, N.K.; O’Neill, C.W.J. Case Report. A disseminated infection due to Chrysosporium queenslandicum in a garter snake (Thamnophis). Mycoses 1999, 42, 107–110. [Google Scholar] [CrossRef]
  94. Abarca, M.L.; Martorell, J.; Castella, G.; Cabanes, F.J. Chrysosporium guarroi sp. nov. a New Emerging Pathogen of Pet Green Iguanas (Iguana iguana). Med. Mycol. 2010, 48, 365–372. [Google Scholar] [CrossRef]
  95. Rajeev, S.; Sutton, D.A.; Wickes, B.L.; Miller, D.L.; Giri, D.; Van Meter, M.; Thompson, E.H.; Rinaldi, M.G.; Romanelli, A.M.; Cano, J.F.; et al. Isolation and characterization of a new fungal species, Chrysosporium ophiodiicola from a mycotic granuloma of a black rat snake (Elaphe obsolete obsolete). J. Clin. Microbiol. 2009, 47, 1264–1268. [Google Scholar] [CrossRef]
  96. Elad, D. Disseminated canine mold infections. Vet. J. 2019, 243, 82–90. [Google Scholar] [CrossRef] [PubMed]
  97. Smagulova, A.M.; Glotova, T.I.; Kukhar, E.V. Spectrum of pathogens causing skin mycoses in domestic and wild animals in Kazakhstan and the West Siberian region of Russia. Adv. Med. Mycol. 2023, 15, 37–41. [Google Scholar]
  98. Kukhar, E.V.; Kiyan, V.S.; Leontyev, S.V.; Smagulova, A.M. Spread of pathogens causing mycoses of the skin of wild game animals in some regions of the Republic of Kazakhstan. In Proceedings of the Fundamental Science and Priorities of the 21st Century: Proceedings International Scientific and Practical Conference, Astana, Kazakhstan, 29 November 2024; 2025; pp. 325–335, ISBN 978-601-08-4845-0. (In Russian). [Google Scholar]
  99. Warwick, A.; Ferrieri, P.; Burke, B.; Blazar, B.R. Presumptive Invasive Chrysosporium Infection in a Bone Marrow Transplant Recipient. Bone Marrow Transplant. 1991, 8, 319–322. [Google Scholar] [PubMed]
  100. Dincy, P.C.; Meera, T.; Susanne, P.A.; Promila, R.M. Disseminated Cutaneous Chrysosporium Infection. Trop. Dr. 2019, 49, 306–308. [Google Scholar] [CrossRef]
  101. Stebbins, W.G.; Krishtul, A.; Bottone, E.J.; Phelps, R.; Cohen, S. Cutaneous Adiaspiromycosis: A Distinct Dermatologic Entity Associated with Chrysosporium Species. J. Am. Acad. Dermatol. 2004, 51, S185–S189. [Google Scholar] [CrossRef]
  102. Suchonwanit, P.; Chaiyabutr, C.; Vachiramon, V. Primary Cutaneous Chrysosporium Infection Following Ear Piercing: A Case Report. Case Rep. Dermatol. 2015, 7, 136–140. [Google Scholar] [CrossRef]
  103. Pare, J.A.; Jacobson, E.R. Mycotic diseases of reptiles. In Infectious Diseases and Pathology of Reptiles: Color Atlas and Text; Jacobson, E.R., Ed.; CRC Press: Boca Raton, FL, USA; Taylor and Francis: Abingdon, UK, 2007; pp. 527–570. [Google Scholar]
  104. Lorch, J.M.; Knowles, S.; Lankton, J.S.; Michell, K.; Edwards, J.L.; Kapfer, J.M.; Staffen, R.A.; Wild, E.R.; Schmidt, K.Z.; Ballmann, A.E.; et al. Snake fungal disease: An emerging threat to wild snakes. Philos. Trans. R. Soc. B Biol. Sci. 2016, 371, 20150457. [Google Scholar] [CrossRef]
  105. Bailina, G.E.; Kuchar, E.V.; Kiyan, V.S.; Smagulova, A.M. Spectrum of opportunistic mycosis pathogens in domestic and farm animals in Kazakhstan. P.N. Kashkin Res. Inst. Med. Mycol. Probl. Med. Mycol. 2023, 25, 84. Available online: https://mycology.szgmu.ru/images/2-2023.pdf (accessed on 2 April 2025). (In Russian).
  106. Borovkova, K.E.; Makarova, M.N.; Nikiforova, L.R.; Salmova, Y.V. Animal models of fungal infections. Lab. Anim. Sci. Res. 2021, 3, 25–48. [Google Scholar] [CrossRef]
  107. Chabasse, D.; De Gentile, L.; Bouchara, J.P. Pathogenicity of some Chrysosporium species isolated in France. Mycopathologia 1989, 106, 171–177. [Google Scholar] [CrossRef]
  108. Langfeldt, A.; Gold, J.A.W.; Chiller, T. Emerging Fungal Infections: From the Fields to the Clinic, Resistant Aspergillus fumigatus and Dermatophyte Species: A One Health Perspective on an Urgent Public Health Problem. Curr. Clin. Microbiol. Rep. 2022, 9, 46–51. [Google Scholar] [CrossRef]
Jof 11 00297 g001
Figure 1. Taxonomic composition and percentage of fungi isolated from affected areas of horse skin in the northern and central regions of Kazakhstan (2023–2024).
Figure 1. Taxonomic composition and percentage of fungi isolated from affected areas of horse skin in the northern and central regions of Kazakhstan (2023–2024).
Jof 11 00297 g001
Jof 11 00297 g002
Figure 2. Appearance of skin lesions in horses with mycosis caused by Chrysosporium spp.: (A) lesions on the horse’s head, (B) scaling lesions.
Figure 2. Appearance of skin lesions in horses with mycosis caused by Chrysosporium spp.: (A) lesions on the horse’s head, (B) scaling lesions.
Jof 11 00297 g002
Jof 11 00297 g003
Figure 3. External appearance of colonies from pure cultures isolated from horse biomaterial on the 15th day of cultivation: (A)—front view and (B)—rear view of the colony; (С)—microscopic analysis of strain 15.23.7H; (D)—features of the microscopic structure of strain 15.23.7.1H; (E)—features of the mycelium structure of strain 9.23.6H; smooth mycelium (1), cluster-shaped microconidia (2), septate mycelium (3), macroconidia (4), microconidia (5).
Figure 3. External appearance of colonies from pure cultures isolated from horse biomaterial on the 15th day of cultivation: (A)—front view and (B)—rear view of the colony; (С)—microscopic analysis of strain 15.23.7H; (D)—features of the microscopic structure of strain 15.23.7.1H; (E)—features of the mycelium structure of strain 9.23.6H; smooth mycelium (1), cluster-shaped microconidia (2), septate mycelium (3), macroconidia (4), microconidia (5).
Jof 11 00297 g003
Jof 11 00297 g004
Figure 4. Maximum likelihood phylogenetic tree (divergence = 0.10).
Figure 4. Maximum likelihood phylogenetic tree (divergence = 0.10).
Jof 11 00297 g004
Jof 11 00297 g005
Figure 5. Results of the biochemical test for the enzymatic activity of C. kreiselii No. 15.23.7H and C. zonatum No. 9.23.6H, isolated from horse biomaterial.
Figure 5. Results of the biochemical test for the enzymatic activity of C. kreiselii No. 15.23.7H and C. zonatum No. 9.23.6H, isolated from horse biomaterial.
Jof 11 00297 g005
Jof 11 00297 g006
Figure 6. Keratinophilic properties of C. kreiselii and C. zonatum strains.
Figure 6. Keratinophilic properties of C. kreiselii and C. zonatum strains.
Jof 11 00297 g006
Jof 11 00297 g007
Figure 7. Hair deformation under the influence of Chrysosporium spp. strains: (A)—control, (B)—mycelial growth on the hair surface, (C)—hair cuticle damage, (D)—hair keratinolysis.
Figure 7. Hair deformation under the influence of Chrysosporium spp. strains: (A)—control, (B)—mycelial growth on the hair surface, (C)—hair cuticle damage, (D)—hair keratinolysis.
Jof 11 00297 g007
Jof 11 00297 g008
Figure 8. Comparative sensitivity of fungal strains isolated from horses to antifungal drugs: (A)—C. kreiselii strain No. 15.23.7H; (B)—C. zonatum strain No. 9.23.6H; (C)—A. alternata strain No. 15.23.7H.
Figure 8. Comparative sensitivity of fungal strains isolated from horses to antifungal drugs: (A)—C. kreiselii strain No. 15.23.7H; (B)—C. zonatum strain No. 9.23.6H; (C)—A. alternata strain No. 15.23.7H.
Jof 11 00297 g008
Table 1. Pathogens of Chrysosporium spp. and the pathologies they cause.
Table 1. Pathogens of Chrysosporium spp. and the pathologies they cause.
Isolated FungusObjectSourceImmunosuppressionTreatmentReference
Chrysosporium infection of reptiles
Chrysosporium spp.Reptiles, green iguanas (Iguana iguana), eastern horned rattlesnakes (Sistrurus catenatus)fungal brain abscess, necrotizing dermatomycosis, deep ulcers, necrosisconditions of detentionitraconazole[74,75]
Chrysosporium spp., Nannizziopsis vriesiibearded dragons (Pogona vitticeps), green iguanas (Iguana iguana), snakes (various species), inland dragon (Pogona vitticeps), tentacled snakes (Erpeton tentaculatum), tree snakes (Boiga irregularis), saltwater crocodiles (Crocodylus porosus)vesicular lesions and bullae, necrosis, scaling, and ulceration, progressing to involve muscles and bones
deep mycosis, necrotizing fungal dermatitis, cutaneous hyalohyphomycosis		poor living conditions and stressitraconazole, ketoconazole, voridazole[76,77,78,79,80,81,82,83,84,85,86,87,88,89]
N. vriesii, C. guarroi, C. queenslandicum,
C. ophiodiicola		chameleons, reptiles, tentacle snakes (Erpeton tentaculatum), dragon (Pogona vitticeps), bearded dragon (Pogona vitticeps), Thamnophis snakes, green iguanas (Iguana iguana)systemic lesions, necrosis and soft tissue lesions, ulcers and infiltration in the skin, widespread infection, including both skin lesions and lesions of internal organsgeneral weakness and anorexia, progressive emaciation, necrosis, and death of the animal, the infection may spread to deep tissues and become systemicketoconazole, itraconazole, voriconazole, itraconazole[82,90,91,92,93,94,95]
Chrysosporium infection of warm-blooded animals and birds
C. tropicumchickensdermatomycosis, mycosis of the comb of chickensphysical inactivity, crowded conditionsnot indicated[37]
Chrysosporium spp.dogfungal infection, signs of multiple foci of discospondylitisbreed predispositionitraconazole[39]
C. evolceanui9-year-old miniature pinscher dogchrysosporiasis of the skinlocalized exudative epidermitis on the neck and both sides of the croup, skin hyperpigmentation, hormonal disorderscetavlon[39]
Chrysosporium spp.dogs—11 piecesfungal keratitisgenetic predispositionantifungal drugs, euthanasia[41]
Chrysosporium spp.German shepherdDisseminated Chrysosporium infectionlesions of the iliac lymph nodes and spleenposaconazole[43,96]
C. articulatum, Chrysosporium spp.cat
cats—2 pieces		trichophytosis, dermatophytosis, superficial skin lesionsfood allergy, host-borne infectiondiet[29,43]
C. keratinophilumkangaroo, Bennett’s wallabyonychomycosis of the clawsonychodystrophy, onychomadesis, severe digital tumorketoconazole[26]
Chrysosporium-related fungihorseskeratomycosis in horsescorneal ulcer, stromal abscess, or severe diffuse nonulcerative keratitisantifungal agents locally[25]
C. zonatumhorsehaircolonizing horsehair, association with M. gypseumskin lesionnone/lost to follow up[27]
C. zonatumEgyptian Arabian Horsesnot publishednot publishednot published[50]
Table 2. Isolation of pathogens from horse biomaterial in Kazakhstan.
Table 2. Isolation of pathogens from horse biomaterial in Kazakhstan.
Region of KazakhstanNumber of SamplesMicromycetes Identified
TotalPositiveNo GrowthTotalDermatophytesMoldYeast
North Kazakhstan region21129111100
Akmola region33321438314
Kostanay region23716201190
Karaganda region13112163103
Total9062289013707
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Kukhar, Y.; Bailina, G.; Smagulova, A.; Uakhit, R.; Kiyan, V. Characteristics of Chrysosporium spp. Pathogens Causing Skin Mycoses in Horses. J. Fungi 2025, 11, 297. https://doi.org/10.3390/jof11040297

AMA Style

Kukhar Y, Bailina G, Smagulova A, Uakhit R, Kiyan V. Characteristics of Chrysosporium spp. Pathogens Causing Skin Mycoses in Horses. Journal of Fungi. 2025; 11(4):297. https://doi.org/10.3390/jof11040297

Chicago/Turabian Style

Kukhar, Yelena, Gulshat Bailina, Ainura Smagulova, Rabiga Uakhit, and Vladimir Kiyan. 2025. "Characteristics of Chrysosporium spp. Pathogens Causing Skin Mycoses in Horses" Journal of Fungi 11, no. 4: 297. https://doi.org/10.3390/jof11040297

APA Style

Kukhar, Y., Bailina, G., Smagulova, A., Uakhit, R., & Kiyan, V. (2025). Characteristics of Chrysosporium spp. Pathogens Causing Skin Mycoses in Horses. Journal of Fungi, 11(4), 297. https://doi.org/10.3390/jof11040297

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop