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Fungal Pathogens of Nonhuman Ani

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					Fungal Pathogens of                                                                                             Secondary article

Nonhuman Animals                                                                                     . Introduction
                                                                                                                      Article Contents


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
poorly understood.


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,
                                                                       1989).
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.
Pythiosis
                                                                       Ringworm
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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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.
                                                                        Cryptococcosis
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-
                                                                         Keratomycosis
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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   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

6                              ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net
                                                                                             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
                                   Antifungals
 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
                                     unproven benefit
 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
  (Basidiobolus, Conidiobolus)
 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
  Saprolegnia)                                                        water
 Paecilomyces species              Possibly itraconazole
 Pneumocystis carinii              Co-trimoxazole
                                    (antibacterial agent)
 Pythiosis                         Unknown                           Surgery; possibly immunotherapy; membrane active drugs likely
                                                                      to be ineffective
 Ringworm (dermatophytosis)        Itraconazole, fluconazole         Griseofulvin, ketoconazole shampoo, topical terbinat azole for
                                                                      discrete lesions
 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


and also excised. Parenteral long-acting anaesthesia is                      Dykstra MJ, Sharp NJH, Olivry T et al. (1999) A description of
preferred for large lesions so that time can be taken with the                 cutaneous–subcutaneous pythiosis in fifteen dogs. Medical Mycology
surgery. Regular postoperative irrigation of the wound                         37: 427–433.
                                                                             Jungerman PF and Schwartzman RM (1972) Veterinary Medical
until the ‘crater’ has completely granulated has been
                                                                               Mycology. Philadelphia: Lea and Febiger.
suggested, followed by dressings whenever time permits.                      Malik R, Craig AJ, Wigney DI, Martin P and Love DN (1996)
Healing may take 2–3 months with large wounds.                                 Combination chemotherapy of canine and feline cryptococcosis using
   While topical ointments and creams are useful for the                       subcutaneously administered amphotericin B. Australian Veterinary
treatment of discrete ringworm lesions in companion                            Journal 73: 124–128.
animals, it would seem more logical to combine this with                     Malik R, Martin P, Wigney DI et al. (1997a) Nasopharyngeal
oral fluconazole or itraconazole wherever possible. Gently                      cryptococcosis. Australian Veterinary Journal 75: 483–488.
                                                                             Malik R, Wigney DI, Muir DB and Love DN (1997b) Asymptomatic
shampooing animals with ketoconazole is an additional
                                                                               carriage of Cryptococcus neoformans in the nasal cavity of dogs and
possibility in animals without obvious lesions; however,                       cats. Journal of Medical and Veterinary Mycology 35: 27–31.
brushing and grooming should be kept to a minimum as                         Mignon BR and Losson BJ (1997) Prevalence and characterization of
these may result in minor skin trauma and induce overt                         Microsporum canis carriage in cats. Journal of Medical and Veterinary
disease (Smith, 1975).                                                         Mycology 35: 249–256.
   Apart from the treatment of individual animals, ‘mass                     Noga EJ (2000) Fish Disease – Diagnosis and Treatment. Ames, IA: Iowa
therapy’ using supplemented food or water has been                             State University Press.
                                                                             Smith JMB (1975) Superficial and cutaneous mycoses. In: Hubbert WT,
attempted (with reasonable success) for avian candidosis.
                                                                               McCulloch WF and Schnurrenberger PR (eds) Diseases Transmitted
Additives that have been used successfully are nystatin                        from Animals to Man, 6th edn, pp. 469–487. Springfield, IL: Thomas.
(2 500 000 iu kg 2 1 food), copper sulphate (1:2000 in                       Smith JMB (1989) Opportunistic Mycoses of Man and Other Animals.
drinking water) and garlic (2–4% concentration in food).                       Wallingford: CAB International.
It has been suggested that blockage of lipid synthesis is an
important component of the anticandidal activity of garlic
(Smith, 1989).
                                                                             Further Reading
References
                                                                             Ainsworth GC and Austwick PKC (1973) Fungal Diseases of Animals,
Ainsworth GC and Austwick PKC (1973) Fungal Diseases of Animals,               2nd edn. Farnham Royal: Commonwealth Agricultural Bureaux.
  2nd edn. Farnham Royal: Commonwealth Agricultural Bureaux.                     ´
                                                                             Gueho E, Midgley G and Guillot J (1996) The genus Malassezia with
    ´
Baro T, Torres-Rodriguez JM, de Mendoza MH, Morera Y and Alia C                description of four new species. Antonie van Leeuwenhoek 69: 337–355.
  (1998) First identification of autochthonous Cryptococcus neoformans        Jungerman PF and Schwartzman RM (1972) Veterinary Medical
  var. gattii isolated from goats with predominantly severe pulmonary          Mycology. Philadelphia: Lea and Febinger.
  disease in Spain. Journal of Clinical Microbiology 36: 458–461.            Noga EJ (2000) Fish Disease – Diagnosis and Treatment. Ames, IA: Iowa
Baxter M (1973) Ringworm due to Microsporum canis in cats and dogs in          State University Press.
  New Zealand. New Zealand Veterinary Journal 21: 33–37.                     Rippon JW (1988) Medical Mycology, 3rd edn. Philadelphia: Saunders.
Crespo MJ, Abarca ML and Cabanes FJ (2000) Otitis externa associated
                                   ˜                                         Smith JMB (1975) Superficial and cutaneous mycoses. In: Hubbert WT,
  with Malassezia sympodialis in two cats. Journal of Clinical Micro-          McCulloch WF and Schnurrenberger PR (eds) Diseases Transmitted
  biology 38: 1263–1266.                                                       from Animals to Man, 6th edn, pp. 469–487. Springfield, IL: Charles C
Daszak P, Berger L, Cunningham AA et al. (1999) Emerging infectious            Thomas.
  diseases and amphibian population declines. Emerging Infectious            Smith JMB (1989) Opportunistic Mycoses of Man and Other Animals.
  Diseases 5: 735–748.                                                         Wallingford: CAB International.
Durand-Joly I, Wakefield AE, Palmer RJ et al. (2000) Ultrastructural          Smith JMB and Austwick PKC (1967) Fungal diseases of rats and mice.
  and molecular characterization of Pneumocystis carinii isolated from a       In: Cotchin E and Roe FJC (eds) Pathology of Laboratory Rats and
  rhesus monkey (Macaca mulatta). Medical Mycology 38: 61–72.                  Mice, pp. 681–732. Oxford: Blackwell.




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