Fungal Pathogens of Secondary article
Nonhuman Animals . Introduction
John MB Smith, University of Otago, Dunedin, New Zealand . Fungal Diseases of Domestic Companion Animals
. Fungal Diseases of Domestic Farm Animals
Fungal infections of nonhuman animals, including domestic companion and farm animals, . Fungal Diseases of Fish and other Aquatic Vertebrates
fish and other aquatic vertebrates are common and involve an increasing variety of . Control of Fungal Diseases in Veterinary Practice
environmental and occasionally endogenous fungi. In most cases, the causal fungi are of
low virulence and require that the host be immunologically compromised in order to
initiate active disease. Methods of control and possible treatment of these diseases are
Introduction ton). These appear to have evolved from soil Ascomycetes
Fungal diseases of animals other than humans are common (genus Arthroderma), with the elaboration of enzymes
and, like their human counterparts, are increasing both in capable of digesting keratin (keratinases) contributing to
range and numbers, with an ever-increasing number of their ability to colonize and attack the stratum corneum of
supposedly harmless fungi being recovered from serious the skin, hair and nails. The disease is invariably conﬁned
disease. Most infections are seen in debilitated and to these dead keratin structures, with invasion into the
compromised animals, i.e. they are opportunistic (oppor- deeper living cellular layers a rarity (Smith, 1975). Ring-
tunistic mycoses), and are caused by environmental fungi worm is common in a wide variety of nonhuman animals
of low virulence. Successful treatment of such infections (Table 1).
often requires correction of any underlying compromisa- Surveys in cats have demonstrated a fur Microsporum
tion or pathology, including surgical removal of involved canis carriage rate of up to 40%, with only around 10% of
tissues, as well as appropriate antifungal agents. The latter these exhibiting obvious cutaneous lesions (Baxter, 1973).
alone are seldom successful. More virulent dimorphic Infection and/or colonization rates are greatest around the
fungi, such as Histoplasma capsulatum, continue to be time kittens are born (e.g. December/January and again
signiﬁcant in endemic geographical areas, e.g. the USA. March/April in the southern hemisphere), and in animals
Not surprisingly, opportunistic mycoses are encoun- in poor health or conﬁned together in close proximity, e.g.
tered most frequently in captive and/or stressed animals, catteries. Cats may be infected with or without evident
including avian species. Fungal diseases in companion and clinical lesions, or be asymptomatic transient carriers of
domestic animals, including farm animals, tend to be of fungus spores (Mignon and Losson, 1997). Following
lesser signiﬁcance, although diseases such as ringworm can overt infection, animals may remain carriers of the fungus
involve high percentages of animals and constitute an for several weeks. Lesions are usually most obvious around
important reservoir of fungi capable of causing human the face and ear regions, and some evidence exists that the
disease, i.e. ringworm in animals is an important zoonosis. disease, or at least colonization, is more prevalent in
The following short account will attempt to summarize animals infected with Feline immunodeﬁciency virus (FIV).
present information concerning important mycoses (fun- Other, more signiﬁcant dermatophytes that have been
gal infections) of nonhuman animals, and suggest possible recorded from cats include Microsporum canis var.
therapeutic considerations. distortum, the zoophilic Trichophyton mentagrophytes
var. mentagrophytes (granular variety), and the geophilic
Microsporum gypseum (Smith, 1975).
Ringworm caused by Microsporum canis is not as
common in dogs as it is in cats; inapparent colonization
Fungal Diseases of Domestic and/or disease rates seem to be only around one-tenth of
Companion Animals that seen in cats. As in cats, lesions are most conspicuous
around the head region. A wide variety of other
Ringworm dematophytes seem relatively frequent in dogs (Smith,
1975). These include the zoophilic Trichophyton menta-
By far the most prevalent fungal disease of cats and dogs is grophytes var. mentagrophytes (normally a pathogen of
ringworm – a cutaneous disease caused by a group of fungi rodents) and Trichophyton mentagrophytes var. erinacei
known collectively as dermatophytes, and containing three (the hedgehog fungus) and the soil dwelling Microsporum
genera (Microsporum, Trichophyton, and Epidermophy-
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Fungal Pathogens of Nonhuman Animals
Table 1 Dermatophytes more common in nonhuman animals
Animal More common dermatophytes/comment
Cat Microsporum canis
Cow Trichophyton verrucosum
Dog Microsporum canis, Microsporum gypseum,
Trichophyton mentagrophytes var. mentagrophytes
Hedgehog Trichophyton mentagrophytes var. erinacei
Horse Trichophyton equinum, Microsporum canis (as M. equinum)
Pig Microsporum nanum
Poultry Microsporum gallinae (apparently now rare)
Rodent/laboratory animals Trichophyton mentagrophytes var. mentagrophytes
Sheep Trichophyton verrucosum (unusual variety)
gypseum. Isolation of the anthropophilic Trichophyton sites of infection for the causal yeast Cryptococcus neofor-
rubrum from dogs presumably reﬂects contagion from the mans (Smith, 1989; Malik et al., 1997a). This fungus now
feet of the owner. has three named varieties: var. neoformans (serotype D),
var. gattii (serotypes B,C) and var. grubii (serotype A).
Until recently, var. neoformans accommodated both
Endemic primary mycoses serotypes A and D. Lesions most commonly involve the
It is not surprising that diseases such as histoplasmosis nasal cavity and adjacent or contiguous structures,
(Histoplasma capsulatum), blastomycosis (Blastomyces including the nasopharynx. This suggests that infectious
dermatitidis) and coccidioidomycosis (Coccidioides immi- propagules from the environment (e.g. decaying gum and
tis), are very common in nonhuman animals in geographi- other trees, pigeon excreta) lodge in and penetrate some
cal areas of the world (e.g. the USA) where the causative breach in the integrity of the mucosae of the nasal or sinus
fungi are endemic (Jungerman and Schwartzman, 1972; regions, or somehow evade local host defences at this site, a
Ainsworth and Austwick, 1973). Dogs, by virtue of their hypothesis supported by the fact that the yeast has been
sniﬃng habit, are regularly exposed to these soil fungi and recovered in signiﬁcant numbers from the nasal cavity of
are commonly infected by all three fungi. around 10% of apparently normal dogs (Malik et al.,
With histoplasmosis, dogs seem particularly susceptible 1997b). Both Cryptococcus neoformans var. neoformans
with lesions varying from small calciﬁed nodules (e.g. in and Cryptococcus neoformans var. gattii have been
lungs) to acute disseminated rapidly fatal disease. The recovered from cryptococcosis in dogs and cats, with var.
disease has also been recorded in cats. Blastomycosis is also gattii seemingly disproportionately common (around 25%
common in dogs in endemic areas (e.g. eastern North cases) in some surveys (Malik et al., 1997a). The ability of
America, and parts of India and Africa), with lesions Cryptococcus neoformans to colonize the nasal cavity of
involving the pulmonary, osseous and cutaneous tissues. normal animals has signiﬁcant clinical implications for
Yeast-phase cells of Blastomyces dermatitidis have been veterinarians, who may often make a diagnosis of
recovered from the stools of a dog with pulmonary disease, cryptococcal rhinosinusitis based on culture alone.
and raise the potential of cross infection! Disease in cats is Clearly, other criteria must be utilized in order to make
less common. Severe, disseminated coccidioidomycosis an unambiguous diagnosis of nasal disease; for example,
has frequently been reported in dogs, especially boxers and positive serum latex agglutination test, presence of yeasts
Dobermann pinschers, in areas of the USA (e.g. San in tissue sections. Nasal discharge and sneezing are
Joaquin Valley) where the causative fungus is endemic. common with cryptococcal rhinitis.
Extension of cryptococcal infection from the nasal
cavity through the cribriform plate or via the blood or
Cryptococcosis lymphatics to involve other tissues (e.g. brain, skin, lung,
Cryptococcosis is an uncommon but increasingly impor- kidney, lymph nodes) can occur. Solitary lung nodules are
tant life-threatening opportunistic fungal infection of a recorded, but rare, event. Although FIV infection does
humans and other animals throughout the world. In cats not appear to impart an unfavourable prognosis, aﬀected
and dogs (as well as horses, goats and koala bears), the cats tend to have more advanced and/or disseminated
nasal cavity and paranasal sinuses appear to be the primary disease. Some evidence is available that Cryptococcus
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Fungal Pathogens of Nonhuman Animals
neoformans may survive in dogs for several years following Chromomycosis
apparently successful therapy.
A number of fungi are capable of producing melanin-like
pigments in their hyphae and spores – the so-called black
Infection by Malassezia species moulds. These pigmented or phaeoid fungi (often incor-
rectly called dematiaceous) are found naturally in the soil,
The genus Malassezia contains at least seven species of water and organic debris; some are plant pathogens.
lipophilic yeasts found as members of the normal Taxonomic aspects of the causal fungi have caused
cutaneous ﬂora in humans and other animals. Of the seven considerable confusion, as has the nomenclature of the
species, Malassezia pachydermatis (which is not dependent disease. While all disease caused by these fungi can be
on lipid supplementation for in vitro growth), earlier condensed under the term chromomycosis, cutaneous and
referred to as ‘Pityrosporum canis’, appears to play an systemic infections in which the phaeoid moulds have a
important role in chronic dermatitis and otitis externa, septate tissue morphology have been referred to as
especially in carnivores. It is the most common yeast that phaeohyphomycosis, while in situations where the tissue
contributes to otitis externa as a perpetuating factor in forms are predominantly large, thick-walled dark-brown
dogs, and to a lesser extent in cats. Malassezia sympodialis septate cells (‘sclerotic bodies’ or muriform cells), the term
has also been recovered from otitis externa in cats, and chromoblastomycosis is often used (Smith, 1989); how-
seems to be the most common of the four lipid-dependent ever, a distinction, based on fungal tissue morphology,
Malassezia species that have been isolated from healthy between these two forms of chromomycosis is often not
cats (Crespo et al., 2000). possible. Lesions appear to develop following some form
of cutaneous trauma.
A number of phaeoid fungi have been recovered from
Other opportunistic mycoses disease, mainly cutaneous but occasionally systemic, in
cats and dogs, e.g. Alternaria species (possibly Alternaria
Of the other numerous fungal disease that have been alternata), Bipolaris spicifera (syn. Drechslera spicifera),
recorded in cats and dogs, three are worthy of special Phialemonium obovatum (osteomyelitis), and Pseudomi-
mention: aspergillosis, pythiosis and chromomycosis. crodochium suttonii from dogs; and Exophiala jeanselmei
(syn. Phialophora jeanselmei), Phialophora verrucosa,
Xylohypha batiana (previously Cladosporium species,
Aspergillosis systemic disease) and Xylohypha emmonsii in cats (Smith,
Aspergillosis has been recorded in a wide variety of
domestic and wild animals, including avian species, and a
tremendous volume of early literature exists on veterinary
aspects of this primarily respiratory disease (Smith, 1989). Fungal Diseases of Domestic
Since the mid-1970s, numerous reports concerning asper-
gillosis involving the nasal cavity of dogs (with Aspergillus Farm Animals
fumigatus the usual causal fungus) have appeared in
journals, while disseminated disease (attributable to Fungal diseases in farm animals such as cattle, sheep,
Aspergillus terreus and Aspergillus deﬂectus) with minimal horses, pigs and poultry received a good deal of attention in
to absent respiratory involvement has been increasingly the 1950s–1970s. Since then, reports appearing in the
recorded in dogs, especially German shepherds. world’s literature have diminished; reasons for this decline
are unknown, but possibly reﬂect the general worldwide
diminishing interest in veterinary mycology.
A more recently recognized aquatic/soil fungus, Pythium
insidiosum (syn. ‘Hyphomyces destruens’), has been recov- Ringworm continues to be a problem in farm animals
ered from cutaneous and gastrointestinal disease in dogs, despite the advent of vaccines apparently eﬀective against
and less commonly cats. In the case of dogs, a high cattle ringworm (Trichophyton verrucosum), and at least
proportion of infected animals have a history of swimming experimentally against ringworm in horses (Trichophyton
or exposure to swampy or wet grass areas (Dykstra et al., equinum) and companion animals (Microsporum canis in
1999). As in horses, in which the disease is more common cats). Some idea of the important causal agents is shown in
(‘swamp cancer’), exposure of dogs to water, soil or plants Table 1. Outbreaks of ovine ringworm in the USA have
seems a risk factor for pythiosis. It also seems that some been associated with an unusual dermatophyte resembling
sort of trauma is a necessary predisposing event. Surgical Trichophyton verrucosum, while infection by Trichophyton
intervention is the mainstay of treatment. mentagrophytes var. mentagrophytes may reach epizootic
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Fungal Pathogens of Nonhuman Animals
proportions in farmed fur-bearing animals (Smith, 1975). worldwide distribution and has been reported in almost all
Apart from damaging the hides and coats of animals, domestic animals and birds, as well as many wild species.
ringworm in farmed animals is a potentially serious public Aspergillosis was apparently ﬁrst recorded in 1813 (in a
health problem (zoonosis). Scaup duck, Aythya marila).
While respiratory tract disease and birds (e.g. ‘brooder
pneumonia’ in poultry) are, respectively, the common form
Endemic primary mycoses of aspergillosis and main type of animal aﬀected, aspergilli
Where the causative fungi are endemic in soil, histoplas- (usually Aspergillus fumigatus) have been associated with
mosis, blastomycosis and coccidioidomycosis are rela- lung lesions and abortion in cattle, keratomycosis and
tively frequent in farm animals (Jungerman and guttural pouch lesions in horses, and pulmonary lesions in
Schwartzman, 1972; Ainsworth and Austwick, 1973). lambs (Smith, 1989). Some reports suggest that Aspergillus
Histoplasmosis has been recorded in pigs, cattle and nidulans (teleomorph Emericella nidulans) is the most
horses. Blastomycosis is common in horses in endemic signiﬁcant cause of equine guttural pouch lesions. Fungal
regions, with cutaneous lesions involving the lower legs the contaminated (mouldy) straw/hay, food or bedding is
most common presenting sign; lung lesions are invariably often implicated in the pathogenesis of such infections. In
present. Although numerous farm animals (e.g. horses, cattle, it seems that the gastrointestinal tract may be an
cattle, pigs, sheep) can be shown skin test-positive for unappreciated portal of entry of the fungus. As in humans,
coccidioidomycosis in endemic areas, disseminated disease allergic pulmonary disease may be seen in farm animals,
is rare. At autopsy, aﬀected animals may display a few e.g. horses.
lesions in pulmonary lymph nodes and the lung.
Candidosis Although one of the early (1901) isolations of Cryptococcus
Candidosis has been recognized in lower animals since at neoformans from any sort of animal was from pulmonary
least 1858, and it seems that, apart from Candida albicans, lesions in a pig, this basidiomycete yeast (teleomorph
other Candida species (e.g. Candida tropicalis) have Filobasidiella neoformans) is an uncommon cause of
considerable pathogenic potential for such animals (Smith, disease in farm animals. Cerebral, nasopharyngeal and
1989). This classical endogenous opportunistic mycosis pulmonary lesions in horses; mastitis in cattle; mastitis,
occurs in association with well-deﬁned predisposing pulmonary and central nervous system disease in goats
factors; for example, antibacterial therapy or food (including disease by Cryptococcus neoformans var. gattii);
fortiﬁcation, excessive skin hydration, immaturity, the and pulmonary, central nervous system and nasophar-
stress of captivity/overcrowding, malnutrition. yngeal disease in sheep have all been recorded, albeit
While poultry pathologists are in some debate concern- ´
infrequently (Smith, 1989; Baro et al., 1998). In most cases,
ing the present-day signiﬁcance of candidosis in poultry it is assumed that the causal fungus was Cryptococcus
(e.g. chicken, turkeys), large scale epizootics would now neoformans var. neoformans or var. grubii.
seem rare. In other animals, the alimentary tract of young
animals appears the most common site of infection. Of the
common farm animals, candidosis has most often been Mucormycosis (zygomycosis)
seen in pigs (oral, oesophageal, gastric, skin lesions), while Infection by mucoraceous fungi, i.e. fungi belonging to the
in cattle over 20 Candida species have been recovered from order Mucorales (phylum Zygomycota, class Zygomy-
mycotic mastitis (Smith, 1989). The exact taxonomic cetes), has been recorded in a number of farm animals:
position of the yeast ‘Candida slooﬃae’, responsible for cattle, pigs, horses, sheep, goats, poultry (Smith, 1989).
lesions involving the pars oesophagea of piglets fed diets Disease appears to follow ingestion of food containing
high in fermentable sugar, is unknown, although it has fungal hyphae, and be precipitated by some sort of local
been suggested that this possibly represents a variety of gastrointestinal erosion or ulceration. As with many other
Candida (Torulopsis) pintolopesii. opportunistic mycoses, mucormycosis is most common in
young, immature and/or stressed animals. Pregnancy may
Aspergillosis favour involvement of the unborn fetus and lead to
abortion. There is evidence that, after infection of the
A tremendous volume of literature had appeared by the pregnant bovine uterus, fungal elements can be dissemi-
early 1900s concerning veterinary aspects of aspergillosis nated to vital organs, such as the lungs. In some countries
(Smith, 1989). Relatively few reports have appeared since (e.g. New Zealand), bovine abortion has been associated
these times, and mainly involve unusual cases and/or new with dry weather and the feeding of rotting plant material
hosts. As in humans, aspergillosis in other animals, (silage) in which the fungus (Mortierella wolﬁi) is growing.
including birds, is primarily a respiratory disease. It has a Apart from bovine abortion/placentitis caused by Mor-
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tierella wolﬁi, more signiﬁcant diseases and causal fungi are subcutaneous granulomas containing sinus tracts
alimentary tract lesions, often involving regional lymph (although primary gastrointestinal lesions also occur in
nodes, and systemic disease in cattle (Absidia corymbifera, dogs). Animals apparently become infected after pro-
Mortierella wolﬁi, Rhizomucor pusillus, Rhizopus micro- longed contact with infectious zoospores in swamp water.
sporus); alimentary tract lesions and systemic disease in
pigs (Absidia corymbifera, Rhizopus microsporus); placen-
titis and systemic disease in horses; placentitis and
alimentary tract lesions, and systemic disease in sheep Over 60 species of fungi have been identiﬁed as the causal
(Rhizomucor pusillus); alimentary tract lesions in goats; agents of keratomycosis, with disease in horses seemingly
and alimentary and respiratory tract lesions in chickens, common. More signiﬁcant fungal genera incriminated in
ostriches and other birds. Unlike humans, involvement of horses include Aspergillus, Fusarium, Cladosporium and
the craniofacial structures has not been a feature of Alternaria. The list of pathogens will undoubtedly increase:
zygomycosis in other animals (Smith, 1989). Mucoraceous for example, the recent isolation of Cladorrhinum bulbillo-
fungi appear to have an aﬃnity for growth within blood sum from keratomycosis in a Percheron horse. Trauma to
vessels, which may help explain many pathological features the eye is possibly a signiﬁcant predisposing event. The
seen with the disease. pathological role of some fungal isolates is open to debate.
Entomophthoramycosis (zygomycosis) Infection by Pneumocystis carinii
Entomophthoramycosis has also been recorded in lower It seems that Pneumocystis carinii is a fungus, rather than a
animals, especially horses (Smith, 1989). Causal fungi protozoan as originally suggested; it is now included under
include Basidiobolus species (often as Basidiobolus ranar- the Ascomycetes (order Pneumocystidales). This fungus,
um), and Conidiobolus coronatus (syn. Entomophthora which is an extremely common and important pathogen in
coronata) which are members of the class Zygomycetes, humans (e.g. human immunodeﬁciency virus (HIV)-
order Entomophthorales. With Basidiobolus, lesions in- infected patients), has never been grown in the laboratory.
volve the nasal skin and associated structures (equine nasal However, it appears that antigenic diﬀerences occur
granuloma), as well as cutaneous regions of the head, neck, between ‘isolates’ from diﬀerent animal species, and that
abdomen and upper leg regions. Involvement of these distinct species speciﬁc strains exist (Durand-Joly et al.,
‘upper body regions’, by slow spreading granulomatous 2000). Apart from humans, many other nonhuman
lesions containing necrotic cores (‘kunkers’), helps distin- animals can be parasitized by this fungus, including the
guish this disease from pythiosis. The causative Basidio- lungs of piglets and horses. It has been documented as the
bolus species appear to favour hotter, more tropical regions cause of spontaneous pneumonia in several pig herds in
of the world (e.g. northern Australia), and seem ubiquitous Denmark.
in decaying vegetation and the gastrointestinal tract of
amphibians, reptiles, bats and macropods (e.g. wallabies).
Minor skin trauma apparently predisposes to infection.
Infection by the related fungus, Conidiobolus coronatus, Fungal Diseases of Fish and other
has also been recorded in horses in more tropical regions.
Lesions, consisting of polyps and granulomas, which may Aquatic Vertebrates
spread locally, have been demonstrated on the nostrils,
nasal mucosa and lips of infected animals. It does not Infection by oomycetes
appear to be as common as infection with Basidiobolus.
A number of fungi belonging to the phylum Oomycota,
particularly members of the Saprolegniaceae, are impor-
Pythiosis tant pathogens of aquatic animals (Smith, 1989; Noga,
2000). While infections are occasionally recorded in ‘wild’
As already mentioned, cutaneous infection with the ﬁsh, aquarium- and hatchery-reared species are in the main
aquatic oomycete Pythium insidiosum is a well-recognized involved. Intensive ﬁsh farming and water temperatures
problem with horses (‘swamp cancer’). In addition, lesions above 108C seem predisposing factors. Although Sapro-
attributed to this fungus have been found in the lungs, legnia species have been found infecting ﬁsh in the absence
lymph nodes and bones of infected horses (possibly of obvious physical epidermal damage and/or concomitant
dissemination from the cutaneous lesions). This disease microbial infection (i.e. apparently acting as primary
(pythiosis) has now been recorded from numerous tropical pathogens), most infections are probably best regarded
and subtropical countries and is commonest in horses, but as secondary to some form of cutaneous trauma. Attach-
sheep are suspected hosts, based on histopathology (Smith, ment and germination of zoospores on cutaneous surfaces
1989). In all species, the disease presents as large, ulcerated, is possibly a signiﬁcant factor associated with trauma.
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Fungal Pathogens of Nonhuman Animals
Major pathogens are Saprolegnia parasitica, Saproleg- In addition to the above, it has been known for at least 30
nia diclina, Achlya prolifera, various Pythium species and years that ulcerative skin lesions, which could spread to
Aphanomyces astaci (magnusii), the common agent of involve deeper tissues, were relatively common in captive,
‘crayﬁsh plague’. Continuing investigations by the Srivas- for example zoological, toads (e.g. Bufo marinus) and
tavas in India have demonstrated the potential pathogeni- ‘frogs’. Lesions reveal phaeoid hyphae; in most publica-
city of almost all species of Achlya and Saprolegnia for a tions the disease has been listed simply as ‘chromomycosis’
variety of freshwater ﬁsh. Over 60 species of lower fungi with the taxonomic position of the causative fungus (or
have been recorded as pathogens or potential pathogens of fungi) undetermined (Smith, 1989).
aquatic animals. Infection by darkly pigmented fungi also seems to be
common in ﬁsh (Smith, 1989). Cutaneous and systemic
(e.g. central nervous system) infections by various species
Chytridiomycosis of Exophiala (e.g. Exophiala pisciphila, Exophiala salmo-
nis) have been recorded in a wide range of ﬁsh (e.g. various
Global declines in amphibian populations are perhaps one catﬁsh, blue gills, smooth dogﬁsh, killiﬁsh, sturgeon,
of the most pressing and enigmatic environmental Atlantic salmon, trout, scup, Atlantic cod, sea horse,
problems of the late 1990s. Recent studies in the rainforests Sargassium triggerﬁsh, clownﬁsh, ﬂounder). In addition,
of Australia, South and Central America and North Phoma herbarum has been recovered from systemic disease
America have found chytridiomycosis to be a major cause in coho salmon, Atlantic salmon, chinook salmon and
of mass deaths in amphibians (Daszak et al., 1999). This rainbow trout; ‘Scolecobasidium humicola’ from rainbow
fungal disease, ﬁrst described in 1998, appears to be caused trout and cho salmon; and ‘Scolecobasidium tshawytschae’
by a new genus of chytrid fungus (phylum Chytridiomy- in chinook salmon. With the last two fungi, the taxonomy
cota), in which sporangia containing zoospores are remains unclear and they possibly represent members of
prominent in infected keratinized tissues (e.g. epidermis, the genus Dactylaria or Ochroconis.
keratinized mouth parts). Diagnosis is by identiﬁcation of Paecilomyces species are common soil fungi and
characteristic intracellular ﬂask-shaped sporangia within frequently contaminate water supplies. Various species
the keratinized tissues. Chytrids are ubiquitous, primitive have been incriminated in invasive and disseminated
fungi that develop without hyphae and are found in infections in nonhuman animals, especially those with
aquatic habitats and moist soil, where they degrade lowered body temperatures. Infection in reptiles and
cellulose, chitin and keratin. They are well known as amphibians is probably fairly common. Apart from
parasites of plants, algae, protists and invertebrates; the septate aspergillus-like hyphae and conidia, histopatholo-
amphibian pathogen is the ﬁrst example of a chytrid gical preparations may reveal only budding yeast-like
parasitizing vertebrates. Identiﬁcation of the pathogen as a forms closely resembling the intracellular forms of
member of the order Chytridiales was originally conﬁrmed Histoplasma capsulatum and Penicillium marneﬀei. Disease
by zoospore ultrastructure and 18S ribosomal deoxyribo- has been recorded in Aldabra tortoises (pulmonary,
nucleic acid (rDNA) sequence data; the fungus has since Paecilomyces fumosoroseus; systemic, Paecilomyces lilaci-
been described as a new genus and species, Batrachochy- nus) and the green sea turtle (pulmonary, Paecilomyces
trium dendrobatidis. Amphibian species found infected lilacinus) (Smith, 1989).
include Taudactylus acutirostris, Rheobatrachus species Other more notable fungal parasites of aquatic animals
(gastric brooding frog), Litoria moorei (western green or include Fusarium solani (from cutaneous lesions in
‘motorbike’ frog), Bufo periglenes (golden toad), Bufo lobsters), and other Fusarium species from cutaneous and
boreas (boreal toad), Bufo canorus (Yosemite toad), more deep-seated lesions in crayﬁsh, alligators, turtles,
Atelopus species, Telmatobius niger, Gastrothecus pseustes, crocodiles and lobsters (Smith, 1989); however, as the
Rana yavapiensis, Rana pipiens and Rana chiricahuensis potential of fungi to colonize and invade cutaneous areas
(leopard frogs) and dendrobatid frogs. of aquatic animals is obviously high, it seems likely that the
list of causal fungi will continue to increase.
Other mycoses in aquatic animals
A fungus identiﬁed (possibly incorrectly) as Basidiobolus Control of Fungal Diseases
ranarum has been described in wild captive dwarf toads in Veterinary Practice
(Bufo hemiophrys baxteri) and captive dwarf African
clawed frogs (Hymenochirus curtipes). This fungus has General
already been mentioned (see above) as an important
mucocutaneous pathogen of horses grazing in swampy Apart from endogenous mycoses, such as candidosis
areas in some topical areas of the world, e.g. northern caused by Candida albicans, most fungal infections
Australia. encountered in veterinary practice are exogenous, with
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Fungal Pathogens of Nonhuman Animals
the causal fungi being saprobic in the environment, e.g. compromising situations, including impairment of white
soil, decaying vegetation. Ringworm is really the only blood cell function. Investigation of aﬀected animals for
signiﬁcant contagious mycosis, although some evidence is such abnormalities would now seem an important facet of
available that some yeasts, such as Candida albicans, can be veterinary medicine.
passed between individual animals. With aspergillosis, preventing exposure of animals to
mouldy bedding and food is obviously a major control
factor (Smith, 1989); however, in many cases predisposing
Control measures factors associated with infection are less clear-cut, and may
involve the stress of captivity and transport, and medica-
Control measures are thus based on reducing exposure of tions given to control other problems (e.g. antiinﬂamma-
susceptible animals to environmental contagion, minimiz- tory agents). Avoidance of such procedures is a logical
ing the chances of cutaneous trauma, and on reducing the control measure.
physiological stress placed on malnourished, captive and
intensively reared animals (Smith, 1989). Many of these
measures are common sense; for example, reduction of Antifungal chemotherapy
overcrowding, removal of wet and/or mouldy bedding and
food. Once diseases, such as ringworm, become endemic in Both fungal and mammalian cells are typically eukaryotic.
laboratory animal colonies or catteries, airborne spread of The formulation of antifungals free from human and other
fungal spores from infected animals, and the ability of such animal toxicity has therefore been a problem. Fungi do,
spores to remain viable in dust and the environment for however, possess a cell wall composed of a polysaccharide
many weeks, makes elimination of the disease diﬃcult matrix in which glucans appear structurally important;
(Smith, 1975). Often wholesale slaughter followed by however, most of the current systemic antifungal agents act
decontamination and/or sterilization of cages and the by interfering with the synthesis and function of the
environment is the only viable alternative. In such cytoplasmic membrane and in particular the membrane
situations, useful antifungal agents include 70% alcohol, sterol, egosterol (Table 2). Ergosterol is the primary sterol in
hypochlorite (bleach) solutions and the more toxic the fungal cell, as opposed to cholesterol in the mammalian
aldehydes (e.g. formaldehyde, glutaraldehyde). cell membrane. Alterations in membrane porosity and
The successful treatment and control of nonhuman permeability, and impairment of cytochrome P-450-
animal infections by Candida species requires both dependent enzyme activities seem important. Some poten-
appropriate chemotherapy (see below) and the removal tial considerations for the treatment of more common
or lowering of obvious compromising conditions (Smith, animal mycoses are shown in Table 3.
1989). Apparent recovery has been initiated by supportive Of the antifungals currently available, the azoles would
procedures such as the removal of antibacterial residues appear of most beneﬁt to veterinary surgeons. While
from food and water (considered responsible for disease in topical ointments or creams can be considered (e.g.
turkeys), replacement of mouldy nonnutritious food with ketoconazole for otitis externa in dogs, terbinatine for
food rich in vitamins, and the removal of rotting and damp discrete ringworm lesions, natamycin for ulcerative
bedding (considered responsible for skin disease in pigs). In keratomycosis), the use of oral azole agents (e.g. ketoco-
addition, veterinarians seem slow to realize that opportu- nazole, ﬂuconazole, itraconazole, voriconazole) would
nistic mycoses, especially those that spread systemically, appear to hold most appeal. Of these, voriconazole appears
are invariably associated with a series of well-deﬁned to have the widest antifungal spectrum, being active
Table 2 Site of action of more readily available antifungals
Fungal target site Examples
Cell wall synthesis/function Echinocandins, Pneumocandins, Nikomycins, Pradimicins
(e.g. glucans, chitin, mannoproteins)
Membrane permeability/function Polyenes (e.g. amphotericin B, natamycin, nystatin)
(e.g. ergosterol synthesis) Azoles (e.g. miconazole, clotrimazole, ketoconazole,
fluconazole, itraconazole, voriconazole)
Terbinafine (an allylamine)
Protein synthesis Sordarins
(e.g. elongation factor 2)
DNA/RNA synthesis/function Flucytosine (5-fluorocytosine)
(e.g. blocking of mitosis) Griseofulvin
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net 7
Fungal Pathogens of Nonhuman Animals
Table 3 Potential antifungal considerations for selected mycoses in nonhuman animals
Disease/fungus First choice Alternatives/comment
Aspergillosis Largely unknown/ Voriconazole, itraconazole and amphotericin B possible
unproven benefit considerations; surgery
Blastomycosis Itraconazole Voriconazole; amphotericin B; ketoconazole
Candidosis Fluconazole Possibly drugs (e.g. amphotericin B) in drinking water for
gastrointestinal disease; topical azoles for cutaneous lesions
Chromomycosis Largely unknown/ Possibly itraconazole; surgery
Chytridiomycosis Unknown Polyenes and azoles likely to be ineffective
Coccidioidomycosis Itraconazole Voriconazole, amphotericin B, ketoconazole, fluconazole
Cryptococcosis Fluconazole Amphotericin B, itraconazole, ketoconazole, flucytosine
Entomophthoramycosis Possibly itraconazole Surgery important; ketoconazole
Fusarium species Possibly voriconazole Highly resistant fungi
Histoplasmosis Itraconazole Voriconazole, amphotericin B, ketoconazole; fluconazole
Malassezia pachydermatis Ketoconazole (topical) Topical azoles
Oomycosis (Achlya, Unproven Drugs (e.g. formaldehyde, malachite green, sodium chloride) in
Paecilomyces species Possibly itraconazole
Pneumocystis carinii Co-trimoxazole
Pythiosis Unknown Surgery; possibly immunotherapy; membrane active drugs likely
to be ineffective
Ringworm (dermatophytosis) Itraconazole, fluconazole Griseofulvin, ketoconazole shampoo, topical terbinat azole for
Zygomycosis (mucormycosis) Largely unknown Surgery; amphotericin B
against a variety of important fungal pathogens (e.g. nasopharyngeal), followed by systemic antifungal therapy
Histoplasma capsulatum, and related dimorphic fungi, (e.g. ﬂuconazole, itraconazole, ketoconazole, amphoter-
Candida species, cryptococci and aspergilli). It can icin B) (Malik et al., 1997a, 1997b).
obviously be considered for nonhuman animal infections The prognosis of extensive cutaneous pythiosis in horses
by such fungi. Invasive cryptococcosis and candidosis in and dogs is poor. Primitive fungi, such as Pythium
lower animals (e.g. cats, dogs, ferrets) have been success- insidiosum and related oomycetes, do not utilize ergosterol
fully treated with ﬂuconazole, itraconazole or ketocona- as the main sterol in the cell membranes, and hence are
zole (Malik et al., 1997a). Such oral treatment would relatively unaﬀected by the membrane-active polyenes (e.g.
appear to be more convenient and tolerable than intrave- amphotericin B) and azoles (e.g. itraconazole). Potential
nous amphotericin B, with or without concurrent oral treatments for such diseases include immunotherapy and
ﬂucytosine. Cats and dogs have also apparently been radical excision of the infected tissues (Dykstra et al.,
successfully cured of cryptococcosis using subcutaneous 1999). Whether or not chemotherapy with antifungals that
amphotericin 2–3 times a week over several months (Malik target sites other than the cell membrane will prove useful
et al., 1996). As with human disease, the duration for which remains unknown. As with an increasing number of
treatment should be continued remains uncertain – opportunistic human mycoses, surgical removal of in-
probably at least 12 weeks. volved tissues must be a serious consideration with
In addition to chemotherapy, surgery is an important nonhuman infections. Surgery must be extensive, with a
adjunct with many opportunistic mycoses. With crypto- reasonable amount of surrounding normal tissue being
coccosis, considerable success has been achieved with removed as well. Any local discrete foci of infection that
physical dislodgement or debulking of lesions (e.g. may have arisen by lymphatic spread must be looked for
8 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net
Fungal Pathogens of Nonhuman Animals
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