CHAPTER 6

Update on Fungal Infections

in Reptiles
Jean A. Paré

Fungi are ubiquitous on the skin of reptiles1; thus the mere The CANV might not be a truly emerging reptile pathogen but
isolation of a fungus from a lesion is clinically irrelevant if rather one that has gone undiagnosed, misdiagnosed, or unrec-
unsupported by compatible histopathologic findings. Morpho- ognized for decades. Nevertheless, this fungus is the single
logic characteristics of fungal elements in tissue sections are most important fungal pathogen of reptiles, and research has
critical in assigning causality to isolates or dismissing them demonstrated it may act as a primary pathogen.4 More than
as contaminants. The literature is replete with cases of reptile 30 CANV isolates collected from various sources over the last
mycoses in which various fungi were incriminated but for which 25 years have been catalogued, and all but one were retrieved
causality was never established or even substantiated. Fungal from reptile lesions. Most of these were initially misidentified,
identification was subjectively ventured based on hyphal or often as Trichophyton, Geotrichum, Malbranchea, or as a distinct
yeast morphologic features in histologic sections when mate- Chrysosporium species. Repeated attempts at mating isolates
rial was unavailable for culture. Only when we possess a sound to yield a teleomorph have been unsuccessful, and although
understanding of which fungi have in the past posed a threat all reptile CANV isolates are morphologically indistinguish-
to reptiles can we assign the “emerging” epithet to a fungal able from the true anamorphic stage of Nannizziopsis vriesii,
agent. For this to happen, we need to strictly consider cases in they do differ slightly when examined at the molecular level
which identification and causality of an isolate were firmly or (Hambleton S, Sigler L, and Paré JA: unpublished data). They
reasonably ascertained. When the existing literature pertain- are now known to represent an assembly of closely related fungi,
ing to fungal disease in reptiles is objectively reviewed, only a many of which remain to be named (Hambleton S, Sigler L
few fungi have emerged as genuine repeat offenders. Common and Paré JA: unpublished data). Chrysosporium ophiodiicola
environmental organisms such as Purpureocillium lilacinum and Chrysosporium guarroi, recently described agents of derma-
(formerly Paecilomyces lilacinus), Fusarium solani and other tomycosis in a Black Ratsnake (Elaphe obsoleta)5 and a Green
fusaria, Metarhizium anisopliae, Beauveria bassiana, various Iguana (Iguana iguana),6 respectively, are renamed fungi that
aspergilla, and yeast such as Candida or Cryptococcus can and would have previously fallen under the CANV group umbrella.
will cause disease in reptiles under the right circumstances.2,3 CANV infection is contagious and typically occurs in captive
Pigmented fungi very rarely cause disease in squamates but, in reptiles as outbreaks of severe, progressive necrogranuloma-
contrast, are well-represented among agents of fungal disease tous dermatitis that eventually disseminates. This fungus con-
in chelonians, especially tortoises and box turtles (Terrapene sistently expands its list of susceptible hosts. Recent additions
spp.). Infection with these opportunistic fungi is usually a include Broad-headed Snakes (Hoplocephalus bungaroides),7
result of overwhelming exposure, immune compromise, and Brown Anoles (Anolis sagrei),8 coastal Bearded Dragons (Pogona
stress from inadequate or substandard captive conditions, or barbata),9 Leopard Geckos (Eublepharius macularius),10 and
any combination thereof. In wild chelonians and crocodilians, even Tuataras (Sphenodon punctatus).11 Of substantial concern
stressful climatic events such as cold spells or cold-stunning is the recent identification of the CANV as a cause of severe
in sea turtles often precede systemic or pulmonary mycoses disease in wild snakes, which carries significant conservation
with otherwise fairly innocuous fungi. Similarly, in captive implications. The CANV, more precisely C. ophiodiicola, was
specimens, thermal extremes from mechanical breakdowns or strongly incriminated as the cause of disfiguring facial lesions
other causes of environmental failure can subsequently lead in free-ranging Eastern Massasauga Rattlesnakes (Sistrurus
to mycosis. Antifungal prophylaxis is routine in sea turtles catenatus catenatus)12,13 in Illinois. Four snakes collected from
recovering from cold spells, and it may be wise to do the same the wild in southern Illinois over a period of 3 years as part
for other captive reptiles that have experienced accidental of a health survey were compromised by deep, severe, very
cooling events. aggressive granulomatous infection resulting in effacement
Of course, fungi other than those already listed can infect of normal facial and cranial anatomic structures.12 The head
reptiles, and none among those is more of a threat than the of affected snakes becomes distorted from the infection, and
fungus currently referred to as the “Chrysosporium anamorph the disease was dubbed facial disfiguration syndrome (FDS).
of Nannizziopsis vriesii” (CANV), which we now know is an The clinicopathologic picture was peculiarly yet strikingly
established cause of contagious, deep, and often fatal dermato- consistent among affected snakes but was also identical to
mycosis in a variety of lizards and snakes and in crocodiles.2,3 that of a Western Massasauga Rattlesnake (Sistrurus catenatus

53
54 SECTION I   •  ADVANCES IN REPTILE MEDICINE

FIGURE 6-2  Wild adult Timber Rattlesnake (Crotalus hor­ridus)

with suspected Chrysosporium ophiodiicola infection. The
FIGURE 6-1 Wild juvenile Timber Rattlesnake (Crotalus hor- whole side of the face is swollen and distorted. The eye is
ridus) with early Chrysosporium ophiodiicola infection, con- shrunken, and the spectacle is opaque. The supraocular and
firmed at the National Wildlife Health Center, Madison, Wisc. preocular scutes are necrotic and coalesced. The rostrum
The rostrum is swollen, especially on the left side. Nasal, inter- is rounded and swollen and covered with abnormal scales.
nasal, and loreal scutes are hyperkeratotic and necrotic, and (Photo courtesy of J. Condon.)
the nares are effaced. (Photo courtesy of J. Condon.)

tergeminus) with extensive and invasive granulomatous fungal

infection reported in 1979.14 In the latter case, the description
of the hyphae in tissue sections was not consistent with the
presumptive diagnosis of phycomycosis, an obsolete term for
zygomycosis, and this snake may well have been a misidenti-
fied case of C. ophiodiicola facial mycosis or FDS. Extensive
dermatomycosis, very suggestive of FDS, has recently been
observed in wild Timber Rattlesnakes (Crotalus horridus) in
New England13,15 (Figure 6-1). Necrogranulomatous lesions
may not be limited to the face and may extend to the rest of the
body. Snakes are typically found with lesions as they emerge
from hibernacula in the spring, but some sick snakes are
also seen basking outside dens in winter months (Condon J:
Pers. com.,) (Figure 6-2). Infection progressively hinders
feeding, and snakes become emaciated before they succumb.
This disease might have substantially impacted northeastern
Timber Rattlesnake populations. Investigations as to the caus-
ative agent are being conducted, but available data are also FIGURE 6-3 Wild adult Northern Watersnake (Nerodia sipe-
pointing to C. ophiodiicola. A wild Black Ratsnake and one of don) with Chrysosporium ophiodiicola infection, confirmed
several Copperheads (Agkistrodon contortrix) with severe and at the National Wildlife Health Center, Madison, Wisc. The
ultimately fatal granulomatous skin disease in New Jersey were rostral, nasal, internasal, and prefrontal scutes are necrotic
confirmed with C. ophiodiicola (Schantz K: unpublished data,) and thickened. The nares are effaced. The snout is distorted
in the last 2 years. This spreading epidemic of fungal disease and shortened. (Photo courtesy of J. Condon.)
chiefly affects wild crotalid snakes but might have spilled over
to sympatric Ring-necked Snakes (Diadophis punctatus), Black grow or grows very poorly at 35°C, and this limited thermotol-
Racers (Coluber constrictor), Gartersnakes (Thamnophis sp.), erance may partially account for some affected snakes with less
and Watersnakes (Nerodia sp.) (Figure 6-3), all of which were severe lesions healing after emergence from the hibernaculum.
seen with facial lesions consistent with CANV dermatitis. Simple exposure to sunlight and warmer days would impede
C. ophiodiicola is known from Europe and Australia and proba- fungal growth and therefore disease progression, allowing ani-
bly occurs worldwide (Sigler L and Paré JA: unpublished data), mals to progressively improve with each shedding thereafter
yet much remains to be known about this fungus and its impact (Figure 6-4). In cases in which lesions are too extensive or
on free-ranging animals. The ecologic niche of C. ophiodiicola deep, surgical debridement with topical care and long-term
and other CANV isolates remains unclear, but it has been antifungal therapy are needed. Adjunct fluid therapy, as well
implicated in the past as causing disease mostly in recently as nutritional and thermal support, is usually initially indi-
caught or newly imported terrestrial and aquatic reptiles. cated to stabilize the patient beforehand or concurrently with
Treatment may be protracted, as lesions are often advanced by systemic medications and assist in recovery. Voriconazole,
the time sick snakes are first observed. C. ophiodiicola does not terbinafine, and itraconazole are all valid drug options, on the
 CHAPTER 6   •  Update on Fungal Infections in Reptiles 55

FIGURE 6-4  Wild adult Timber Rattlesnake (Crotalus hor­ridus) FIGURE 6-5  Cadaver of an adult Veiled Chameleon (Chamaeleo
with suspected Chrysosporium ophiodiicola infection. The calyptratus) with Chamaeleomyces granulomatis infection. A
subocular and upper labial scales have necrosed and sloughed, myriad of smooth, spherical, cream-colored abscesses cover
exposing the dermis. The rostrum is rounded and slightly dis- the entire length of the tongue. (Photo courtesy Dr. Mads F.
torted, possibly scarred from prior or deep infection. Lesions in Bertelsen, Copenhagen Zoo, Copenhagen, Denmark.)
this snake might be resolving. (Photo courtesy of J. Condon.)

basis of prior CANV in vitro susceptibility studies.16,17 Secondary

bacterial infection may also need to be addressed.
C. guarroi causes a contagious, deep dermatitis in Green
Iguanas that seems to be spreading in Europe and Asia through
the pet trade. First reported in Spain,6 it has also been docu-
mented in South Korea18 and is likely more widespread in pet
Green Iguanas than recognized. Trichophyton mentagrophytes
var. interdigitale, the most common cause of human ringworm
worldwide, was isolated from several farmed Green Iguanas
in Iran19 that were seen with crusting gray dermatitis, clini-
cally very similar to that caused by C. guarroi. This report is
unique in that it is the first unequivocally documented account
of dermatophytosis in a reptile because all previous reports
implicating any dermatophyte in reptile skin disease were
questionable and likely misdiagnosed CANV infections. Green FIGURE 6-6 Liver of the same adult Veiled Chameleon
Iguanas with fungal dermatitis therefore might pose a zoonotic (Chamaeleo calyptratus) in Figure 6-5 with Chamaeleomyces
granulomatis infection. Note the miliary abscesses scattered
threat; thus fungal isolation appears mandatory to distinguish
across the hepatic parenchyma. (Photo courtesy Dr. Mads F.
between disease caused by C. guarroi and T. mentagrophytes Bertelsen, Copenhagen Zoo, Copenhagen, Denmark.)
var. interdigitale. The corollary is that Green Iguanas may contract
dermatophytosis from owners and handlers with tinea.
Another fungus, Chamaeleomyces granulomatis,20 may qual- in liver and other tissue, leading to some confusion when a
ify as an emergent agent of infectious disease in reptiles. This mold is isolated. Some antibiotics may promote induction of
novel fungus has just recently been identified as the cause of the yeast phase of C. granulomatis in tissue.24 Terbinafine may
disseminated infection in seven Veiled Chameleons (Chamae- be the antifungal of choice, if the disease is caught early.21 The
leo calyptratus) in a Danish zoologic institution. Infection was source of the fungus and means of dissemination across ani-
characterized by conspicuous clusters of spherical, yellowish mals within a collection remain unknown.
to cream, sometimes coalescing abscesses on the tongue, skin, Undoubtedly, new fungal agents of infection in reptiles
and multiple viscera20 (Figures 6-5 and 6-6). Eighteen Veiled remain to be discovered. This will only happen if diligent care
Chameleons also were seen with this disease at a veterinary is taken by clinicians and pathologists to isolate and properly
hospital over a period of 2 years.21 The fatality rate was high identify fungi that are truly causing lesions in reptiles, as con-
because disease was often advanced at the time of presentation. firmed histologically. Fungal isolates should be preserved in
A very similar disease was first reported more than 4 decades microfungus depositories so that they are available for eventual
ago in 4 of 50 Jewelled Chameleons (Furcifer lateralis) import- further examination.
ed to France from Madagascar.22 The lizards were dying with
identical lesions from Paecilomyces viridis, a fungus now syn-
onymized with C. granulomatis.20 This condition also resulted REFERENCES
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