Mammalia, Perissodactyla: Equidae
Mammalia, Perissodactyla: Equidae
Fungal infections in Equidae
Amir Seyedmousavi1, Jacques Guillot2
1Department of Laboratory Medicine, Clinical Center, National Institutes of Health, Bethesda, U.S.A.
2Department of Dermatology, Parasitology, Mycology, Oniris Veterinary College, Nantes, France
Equidae (from Latin, equus, “horse”) is a family of perissodactyl ungulate mammals which includes the modern horses, zebras, and asses. All seven current members of this family are in the single genus Equus.The species Equus caballus includes a lot of domestic strains of horses. American Mustang or the Australian brumby are feral horses descended from domesticated animals. Equus przewalskii, also called the takhi or Mongolian wild horse, is a rare and endangered horse originally native to the steppes of Central Asia. Three species (E. zebra, E. burchelli, and E. grevyi) are called zebras and two (E. asinus and E. hemionus) are called asses. The term equid refers to any member of the family.
The genus Equus first appeared during the Pliocene Age and was once widespread in grassland and desert habitats through North America, Asia, Africa, and Europe. The current distribution is over open habitats of eastern and southern Africa and regions of Asia. Modern equids tend to live in harsh, dry lands, and many occupy grasslands shared by nomadic peoples. Wild equids generally are polygynous and highly social.
Major superficial mycoses
Dermatophytosis
Dermatophytes are frequently responsible for superficial skin diseases in equids. The main causative agents are Trichophyton equinum in young and adult animals, and Microsporum canis (syn. M. equinum) more often in young horses (Chermette et al. 2008). Other dermatophytes such as T. mentagrophytes or Nannizzia gypsea are also isolated from lesions. Hairs are slightly erected at the beginning of the infection with subsequent small alopecic lesions that give a shabby appearance to the hair coat. Lesions are usually found under the saddle and the girth areas. The infection, which is not pruriginous, is rapidly spreading between horses in the same stable. Kerion and miliary dermatitis may also occur, showing a marked inflammation with exsudative lesions. Kerion is usually described on the head and is due to T. mentagrophytes, T. verrucosum, or N. gypsea.
Transmission of T. equinum to humans is possible but extremely rare (Shwayder et al., 1994; Huovinen et al., 1998; Takatori & Ichijo, 1985; Maslen & Thompson, 2007). Brasch et al. (2009) reported a case of tinea capitis. Chollet et al. (2015) described an outbreak of dermatophytosis in 21 patients following the contact with a single horse infected by T. mentagrophytes.
The dermatophyte species T. bullosum may be detected in the fur of horses and donkeys (Lyskova et al., 2015; Watanabe et al., 2021, Peano et al. 2022). Occasionally, transmission to humans has been reported (Sitterle et al., 2012).
Major subcutaneous and deep mycoses
Aspergillosis
Aspergillosis in equids covers a wide range of diseases from localized conditions to fatal disseminated infections, as well as allergic reactions caused by fungi belonging to the genus Aspergillus. The most common forms of aspergillosis include guttural pouch infection, keratomycosis and pneumonia.
Guttural pouch mycosis is a rare but potentially life-threatening condition affecting adult horses. Lesions associated with this mycosis are typically found on the internal carotid artery, along the dorsal roof of the medial compartment of the guttural pouches, outpouchings of the Eustachian tubes in the parotid region of equids (Lepage et al. 2004). It is still unclear why this anatomical area is infected by a variety of fungal organisms, most frequently Aspergillus nidulans (Guillot et al. 1997). The erosion of the internal carotid leads to the sudden development of profuse epistaxis. Within a few days, fatal hemorrhage occurs in 50% of cases. Inflammation of the cranial nerves leads to the development of dysphagia (with nasal discharge), laryngeal hemiplegia, facial paresis or Horner’s syndrome (Seyedmousavi et al. 2015).
Keratomycosis is a relatively common vision-threatening disease in equids. Clinical presentations include microerosions, ulceration with or without corneal melting, fungal plaque, and stromal abscess. Aspergillus and Fusarium spp. are the most commonly identified fungal pathogens (Sherman et al. 2017).
Pulmonary aspergillosis in horses may present mild respiratory signs, tachypnea associated with adventitious lung or pleural sounds and fever (Sweeney et al. 1999). Severe pulmonary forms and dissemination in horses were reported by Headley et al. (2014).
Histoplasmosis
Histoplasma capsulatum is a dimorphic fungus widely distributed in the tropical or subtropical areas of the world and infects numerous mammalian hosts. Histoplasma capsulatum include three distinct subspecies from which H. capsulatum var. farciminosum mainly affects the skin and the subcutaneous lymphatic system in horses, donkeys, and mules (Scantelbury et al. 2015). The fungus is transmitted through contact of infected material with traumatized skin, by biting flies and ticks, or inhalation of spores. The disease, called equine epizootic lymphangitis, is highly prevalent in Ethiopia (Barrandeguy 2018). Clinical signs include unilateral nodules on head, neck and occasionally trunk. Nodules initially are firm but rupture and exude blood-tinged exudate. Large ulcer may form and lesions may spread on the body. Lacrimation, conjunctivitis, and respiratory signs sometimes occur. Infected horses become restless because of the nuisance due to numerous flies attracted by cutaneous lesions. The outcome is variable and depends on the immune status of the host, inoculum size, and the virulence of the isolate.
Equids may also be infected by H. capsulatum var. capsulatum. A few cases have been described with localized infection of lungs, bone marrow, placenta, digestive tract or lymph nodes (Rezabek et al 1993, Nunes et al 2006). A single case of disseminated equine histoplasmosis that involved lung, pleura, spleen, kidney, liver, small intestine, and colon has been reported (Johnston et al. 1995). Richter et al. (2003) described a case of keratitis due to Histoplasma sp. in a horse.
Less common mycoses
Candidiasis
Mucosal oral or gastrointestinal infection due to Candida albicans has been described in horses. The condition, characterized by white-grayish lesions, often accompanied by hyperkeratosis, is usually associated with young age, long term antibiotic use, or immunosuppression (Gross 1983). Environmental yeast species, such as C. parapsilosis, C. tropicalis, and Meyerozyma guilliermondii, can also cause abortion in horses (Stout et al. 2008). Disseminated candidiasis has been also reported in horses. Clinical signs are often unspecific, and may lead to myocarditis, endocarditis or endophthalmitis. Candida keratitis has been reported in horses in the absence of disseminated disease (Brooks et al. 2013).
Cryptococcosis
The pathogenic agents of cryptococcosis are classified into two species, Cryptococcus neoformans and C. gattii. Studies on animals in Vancouver Island revealed C. gattii in the nasal passage of Horses (Duncan et al., 2011). Isolation of C. neoformans and C. gattii and cases of naturally occurring cryptococcosis have been documented in horses in several veterinary studies from Papua New Guinea, Australia, New Zealand, and the Hawaiian Islands. In horses, lesions of cryptococcosis have been described in the respiratory tract (with cases of rhinitis, sinusitis or pneumonia) as well as in reproductive and digestive systems (Allano et al. 2019, Begg et al. 2004, Cruz et al. 2009, McGill et al. 2009). Disseminated infections leading to meningitis have also been reported (McGill et al. 2009).
Mucormycosis and entomophthoromycosis
The opportunistic pathogenic members of the Mucorales are ubiquitous within the environment of domestic animals and in indoor habitats, but infection almost invariably is established only when the normal balance between animal and the fungus is disturbed. In horses, mucormycotic lesions have been reported in different organs, especially in the respiratory system and gastrointestinal tract, and may lead to systemic spread to multiple organs (Guillot et al. 2000). Moreover, cases of localized skin infection have also been described. Mixed fungal (Carrasco et al. 1997, Thirion-Delalande et al. 2005) or bacterial (Astorga et al. 2004) infections have been reported in horses.
Entomophthoromycosis is a group of rare subcutaneous and mucocutaneous fungal infections predominant in tropical and subtropical areas. Infections due to Basidiobolus and Conidiobolus members have been described in the nasopharyngeal mucosa and subcutaneous tissue (Owens et al. 1984, Zamos et al. 1996)
Phaeohyphomycosis
Phaeohyphomycosis is an umbrella term covering subcutaneous and systemic infections caused by pigmented fungi, where the agents develop in host tissue with brownish to olivaceous hyphal elements. Among melanized fungi, Alternaria alternata has been reported sporadically as causative agent of equine skin disease that may take the form of a cutaneous nodular phaeohyphomycosis (Genovese et al. 2001). In reported case studies, a sharply delimited, firm, brown-black dermal nodule was observed at the right tuber ischium in a horse. Microscopically, the dermis of the excised specimen had multiple pyogranulomas, from which many contained thick-walled, dark brown fungal elements, some with internal septation compatible with muriform cells.
Bipolaris spicifera (Schauffer, 1972; Kaplan et al., 1975) and Curvularia lunata (Boomker et al. 1977) have been implicated in similar cases in horses.
The first description of Exophiala equina concerned a subcutaneous infection in a horse (Pollacci, 1923).
Bipolaris hawaiiensis was isolated from a case of rhinitis (Legere et al. 2019) and Curvularia sp. from a case of keratitis (Conrado et al. 2023).
Plumlee et al. (2017) detected DNA from members of Chaetomiaceae family in the brain of horses with fungal encephalitis. Rantala et al. (2015) described an unusual case of endometritis case associated with Cladophialophora bantiana in a horse.
A case of mycetoma due to Phialophora oxyspora in a horse was published by Lopez et al. (2007).
Infections due to dimorphic fungi (other than Histoplasma capsulatum)
In comparison with other mammals, horses have low susceptibility to coccidioidomycosis.However, some equids, such as Przewalski and Arabian horses, as well as immunocompromised horses of any breed, seem to be more susceptible (James et al. 2019, Macías-Rioseco et al. 2022). When horses develop clinical disease, severity and outcome are quite variable (Ziemer 1992). Clinical signs in horses with coccidioidomycosis usually include chronic weight loss and cough. Cases of rhinitis, dermatitis, and osteomyelitis have also been reported. Pregnant mares may develop coccidioidomycosis leading to abortion or mastitis.
Blastomycosis is a serious dimorphic fungal disease caused by geographically restricted, thermally dimorphic fungi of the genus Blastomyces. Some cases of blastomycosis have been described in horses living in endemic areas. The clinical signs generally include pneumonia sometimes associated with cutaneous and subcutaneous lesions (Toribio et al., 1999, Dolente et al., 2003, Wilson et al., 2006). Méndez-Angulo et al. (2011) described an unusual case of osteomyelitis without involvement of the lungs.
Paracoccidioidomycosis is the most important systemic mycosis in Latin American countries. In horses, asymptomatic Paracoccidioides brasiliensis and/or P. lutzii infection has been detected by intradermal tests and serological surveys (da Costa et al. 1978, Mendez et al. 2017).
Sporotrichosis has also been reported in equids (Barros et al. 2011). From propagules in the environment, Sporothrix schenckii can cause disease in humans and other animals including donkeys, and horses (Crothers et al. 2009). Lesions of sporotrichosis are subcutaneous nodules. The species Sporothrix brasiliensis can also be acquired through animal bites or scratches, especially from cats.
Pneumocystosis
Pneumocystis species infect a very wide range of mammals, including horses. All species are host-specific and there is no transmission from a horse to humans or to animals other than horses. Equine pneumocystosis occurs mostly in foals within 6 months after birth (Ainsworth et al. 1993). Several cases have been reported in Arabian foals with combined immunodeficiency. In these animals, clinical signs include marked respiratory signs leading to death. In 2021, Pneumocystis fungi have been associated with acute interstitial pneumonia in foals, a severe, multifactorial syndrome with lung tissue recovery in surviving animals (Punsmann et al. 2021).
Miscellaneous fungal infections
Out of the 18 species currently described within the genus Malassezia, several ones (M. furfur, M. slooffiae, M. obtusa, M. globosa, M. restricta, M. equina and M. pachydermatis) have been isolated from the skin of horses (Cabañes et al., 2007). Colonization is usually asymptomatic but perineal and ventral abdominal exudates associated with pruritus, alopecia or crusts have been described (White et al., 2006).
Skin lesions due to Geotrichum candidum have been described in horses (Figueredo et al. 2011, Padalino et al. 2020).
Giorgi et al. (1986) described an uterus infection due to Diutina rugosa in a mare.
Shadomy & Dixon (1989) reported a case of ocular infection due to Papulaspora equi and Pusterla et al. (2002) reported a case of adiaspiromycosis due to Emmonsia crescens in a horse.
Pseudofungal infections
Pythiosis
Pythium insidiosum is an aquatic oomycete responsible for subcutaneous or digestive infections in several mammalian species, but most frequently in equids. Pythiosis typically occurs in swampy areas in tropical and subtropical countries. The majority of the equine cases have been described in the USA, Brazil, Australia and Egypt (Yolanda & Krajaejun 2022). Cutaneous pythiosis is the most prevalent form, generally presenting as single lesions in the appendicular region (Pereira et al. 2024). In horses, lesions of pythiosis contain yellowish gritty coral-like bodies called “kunkers”. Pruritic is usually marked. Intestinal forms have also been described in horses (Gaastra et al. 2010). Souto et al. (2016) and Tonpitak et al. (2018) described cases of nasal pythiosis.
Rhinosporidiosis
This is an infection by Rhinosporidium seeberi. The infection leads to the development of polyps in the nasal cavity. The condition is usually asymptomatic but sometimes the presence of polyps is associated with epistaxis, nasal discharge or sneezing. A few cases have been reported in horses (Niño & Freire, 1964, Allison & Ramachandran 2015, Tizzano et al. 2022). Sometimes polyps are detected in the larynx (Nolley et al. 2008, Burgess et al. 2012).
Protothecosis
Protothecosis is caused by achlorophyllous algae of various Prototheca species. Schöniger et al. (2016) described two equine cases of pyogranulomatous rhinitis associated with P. zopfii.
