Survey on the fungal flora of the cloaca of
healthy pet reptiles
S. NARDONI, R. PAPINI, G.M. MARCUCCI, F. MANCIANTI
Dipartimento di Patologia Animale, Profilassi ed Igiene degli Alimenti, Università di Pisa, Viale delle Piagge 2, 56124 Pisa, ITALY.
*Corresponding author: E-mail: [email protected]
SUMMARY
RÉSUMÉ
The aim of this survey was to identify the fungal flora colonizing the
cloaca of healthy reptiles kept in a pet shop to be sold as pets. The examined reptiles were belonging to the sub-orders Sauria (n=140) and Ophidia
(n=17) or to the order Testudines (n=61). Following culture, the samples
showed the presence of fungi in 75.2% of them. Fourteen genera of filamentous fungi, including 8 Aspergillus species, were identified as well as 6
genera of yeasts, including 13 species of Candida, 1 of Cryptococcus, and
1 of Pichia. A great number of the fungi isolated were known to be opportunistic agents of mycosis both in reptiles and humans. Therefore, the possible role of pet reptiles as carriers of opportunistic fungi into the human
environment should be carefully evaluated.
Enquête sur la flore fongique du cloaque de reptiles sains de
compagnie
Keywords: Pet reptiles, fungal flora, opportunistic fungi,
zoonosis.
Le but de ce travail était d’identifier la flore fongique du cloaque de
reptiles sains, présents dans une animalerie pour être vendus comme des
animaux de compagnie. Les reptiles examinés appartenaient aux sous-ordres
Sauria (n=140) et Ophidia (n=17) ou à l’ordre Testudines (n=61). Après culture,
les échantillons ont montré la présence de champignons chez 75,2% d’entre
eux. Quatorze genres de champignons filamenteux, dont 8 espèces
d’Aspergillus, ont été identifiés ainsi que 6 genres de levures, dont 13 espèces
de Candida, 1 de Cryptococcus et 1 de Pichia. Un grand nombre des champignons isolés est connu pour être des agents opportunistes de mycose chez
les reptiles et chez l’homme. Le possible rôle des reptiles de compagnie en
tant que porteurs de champignons potentiellement pathogènes dans l’environnement humain doit donc être attentivement évalué.
Mots-clés : Reptiles de compagnie, flore fongique,
champignons opportunistes, zoonose
Introduction
The number of reptiles kept as exotic pets in households
was dramatically increased during the last years.
Consequently, the risk of acquiring infections transmitted by
these animals is also progressively increased. Although
Salmonella species represent with no doubt the most important pathogenic agents transmissible from infected reptiles to
man, it is also known that reptilian species can carry other
potential zoonotic agents, including opportunistic fungi [8].
As pets, reptiles can live in close vicinity of man and, thus,
they are likely to play an important role in spreading potential fungal pathogens in households and in their transmission
to humans. Indeed, spores of pathogenic fungi excreted from
reptiles via faeces and urine could increase their prevalence
in the environment shared with humans. This could raise the
risk of exposure to these fungi, leading to opportunistic fungal infections [3]. Opportunistic fungal infections have become increasingly common and, concomitantly, there has been
a gradual rise in the number of rare fungal infections both in
immunocompromised and normal patients [12]. A case of
mycotic brain abscess caused by a Chrysosporium anamorph
of Nanniziopsis wriesii, a known fungal pathogen in reptiles,
Revue Méd. Vét., 2008, 159, 3, 159-165
has been reported in a HIV-seropositive man [19].
Consequently, the epidemiological role that reptiles, living in
close vicinity of man, may play as carriers of opportunistic
fungi needs to be accurately assessed.
Many studies have been carried out on the presence of
fungi in internal organs of free living lizards (Agama
agama), wall geckos (Hemidactylus sp.) and turtles
(Chelonia mydas) [5], the gut of caught garden lizards (A.
agama) [3], various body sites of captive Chelonia and
Squamata with a variety of unspecified clinical signs [11],
cloacae of free ranging sea turtles [16], shell lesions of captive soil turtles (Testudo graeca, Testudo hermanni and
Testudo horsfieldii) [4], skin samples of captive healthy
Squamata [15], and faecal samples of wild eastern box turtles (Terrapene carolina carolina) [9]. However, reports of
fungi isolated from the cloacal tract of pet reptiles are scant.
The available data are limited to yeasts in diseased and
necropsied animals [11] or to what can be extrapolated from
wild animals [3, 5, 9, 16] and from other body sites of sampling [4, 15]. In contrast to previous investigations therefore
the present study surveyed the presence of fungi in the cloacal content of healthy reptiles kept in a pet shop to be sold as
companion animals.
NARDONI (S.) AND COLLABORATORS
160
Materials and methods
ANIMALS AND SPECIMEN COLLECTION
From December 2005 to July 2006, 21 species of apparently
healthy reptiles belonging to the sub-orders Sauria (n=140)
and Ophidia (n=17) or to the Order Testudines (n=61) were
investigated. Details are given in Table I. All the animals (n
= 218) were captive-bred. At the time of sampling, they were
living in terrariums or aquariums reproducing different types
of ecosystems and were housed in a pet shop located in the
city of Florence (Italy), where they were kept for sale. In
order to document the isolation of fungi and their prevalence,
cloacal samples were collected by gently inserting one sterile
cotton swab into the cloaca of each animal and rotating the
swab against the inner cloacal wall until faecal material was
obtained. Immediately after collection, cotton swabs were
dipped in 0.5 ml of sterile saline solution with added 5%
gentamicin to avoid bacterial contamination, and kept at
+4°C prior to analysis. Within 12 hours, the samples were
transported to the laboratory to be processed as soon as possible.
CULTURE OF SAMPLES
Samples were seeded on Petri dishes containing Malt
Extract Agar (MEA, Difco Laboratories, Detroit, USA) as
solid culture medium to allow isolation of moulds, and on
MEA with added 10% biphenyl to encourage selective
growth of yeasts. After seeding, all the plates were incubated
at 25°C. Following seeding, from day 4 to day 7, the agar
plates were inspected daily for fungal growth. When fungal
colonies were detectable, subcultures were carried out to
obtain pure cultures suitable for identification.
IDENTIFICATION OF ISOLATED FUNGI
Filamentous fungi were identified on the basis of macroscopic and microscopic morphological characteristics.
Typing was achieved to the genus level except for fungi
belonging to the genus Aspergillus, where the identification
was conducted to species level according to the keys of
RAPER and FENNEL [17]. Yeasts were identified on the
basis of morphological, physiological, and biochemical characteristics, including “germ tube test”, urease production,
and carbohydrate assimilation using the API ID 32C® system (BioMérieux, Roma, Italia). Identifications were achieved to the genus level except for yeasts belonging to the
genus Candida, Cryptococcus, and Pichia where the identification was conducted to species level. The final classification was made according to BARNETT et al. [1].
STATISTICAL ANALYSIS
Animals were categorised according to habitat (aquatic or
terrestrial), feeding (carnivorous, omnivorous or vegetarian),
and zoological classification (Testudines, Sauria or Ophidia).
Positivity rates and prevalence of fungi were determined as
the number of positive samples/total number of samples x
100. The corresponding 95% confidence intervals (95% CI)
were also calculated. Differences between groups were compared by the Chi-square test, where a P value ≤ 0.05 was
considered significant. Descriptive statistics and comparison
of results were performed with Excel 6.0 for Windows 95.
Results
Overall, fungi were found in 164 out of 218 (75.2±5.7%)
cloacal samples. More specifically, fungi were isolated from
50 out of 61 (81.9±9.9%) Testudines, 103 out of 140
(73.5±5.6%) Sauria, and 11 out of 17 (64.7±22.8%) Ophidia.
Omnivores had the highest prevalence rate (39/48,
81.2±11.1%), vegetarians had an intermediate rate (102/135,
75.5±7.3%), and carnivores had the lowest one (23/35,
65.7±15.8%). Thirty-six out of 43 (83.7±11.2%) aquatic reptiles
and 128 out of 175 (73.1±6.6%) terrestrial reptiles tested
positive. Despite these trends, no statistically significant
difference was detected. With the exception of the black tailed
rattlesnake (Crotalus molossus), cloacal isolated fungi were
detected in representatives of all the other reptiles sampled,
as shown in Table I. Different distributions of fungal occurrence
were found in positive animals: moulds with one (n=46), two
(n=27), three (n=11), or four (n=2) types of isolated agents,
yeasts with one (n=31) or two (n=4) types, and various
combinations of them (n=38). The occurrence of multiple
(from 2 to 6) types of isolated fungi within a single host was
common, being present in 82 of the positive samples
(50±10.8%). On the other hand, many isolated fungi could
be obtained from different hosts. Altogether, 14 genera of
moulds, including 8 Aspergillus species, were identified as
well as 6 genera of yeasts, including 13 species of Candida,
1 of Cryptococcus, and 1 of Pichia. The occurrence of
moulds and yeasts in the sampled reptiles are shown in Table
II and III, respectively. Penicillium sp. (39.9±6.5%) was the
most commonly occurring isolated organism followed by
Acremonium sp. (18.3±5.1%). Cladosporium sp. and
Aspergillus niger were found in 8.2±3.6% and 6.4±3.1% of
samples respectively, while Candida tropicalis, Geotrichum
sp. and Trichosporon sp. were recovered from 5.5±2.9% of
samples. Aspergillus versicolor and Mucor sp. occurred in
3.2±2.2% of samples. Candida krusei and Candida pelliculosa
were isolated from 2.7±1.8% and 2.3±1.8% of samples
respectively, while Paecylomyces sp. and Cryptococcus albidus
were recovered from 1.8±1.3% of samples. Other isolated
organisms, including Candida catenulata, Candida glabrata,
Rhizopus sp. and Scopulariopsis sp. (1.4±1.3% each) as well
as Alternaria sp., Aspergillus flavus, Aspergillus fumigatus,
Aspergillus nidulans, Aspergillus ochraceous, Candida albicans, Candida famata, Candida guilliermondii, Candida
norvegica, Fusarium sp., and Trichoderma sp. (0.9±1.2%
each) were infrequently detected. The less common isolated
organisms were Aspergillus oryzae, Aspergillus wentii,
Candida lusitaniae, Candida membranaefaciens, Candida
parapsilosis, Candida rugosa, Exophiala sp., Pichia etchelsii,
Syncephalastrum sp., Verticillium sp. and Saccharomyces sp.
(0.4±0.8% each). Due to heavy bacterial contamination, 9
(4.1%) of the isolated yeasts were lost in culture before they
could be identified.
Revue Méd. Vét., 2008, 159, 3, 159-165
FUNGI IN PET REPTILES
Reptile taxonomy L a t i n n a m e
Order Testudines
Order Squamata
Suborder Sauria
Suborder Ophidia
161
Common name
Habitat
Regimen
Examined
count
Positive
count
Pseudemys scripta elegans
Red-Eared Turtle
Aquatic
Omnivorous
43
36
Geochelona carbonaria
Redfoot Tortoise
Terrestrial
Omnivorous
1
1
Testudo graeca
Greek Tortoise
Terrestrial
Vegetarian
1
1
Testudo hermanni
Hermann's Tortoise
Terrestrial
Vegetarian
13
9
Testudo marginata
Marginated Tortoise
Terrestrial
Vegetarian
2
2
Testudo pardalis
Leopard Tortoise
Terrestrial
Vegetarian
1
1
Chamaleo calyptratus
Veiled Chameleon
Terrestrial
Vegetarian
10
7
Eublepharis macularius
Leopard gecko
Terrestrial
Carnivorous
1
1
Gerrhosaurus validus
Giant African Plated Lizard
Terrestrial
Vegetarian
1
1
Iguana iguana
Green iguana
Terrestrial
Vegetarian
110
83
Paroedura pictus
Madagascar Ground Gecko
Terrestrial
Carnivorous
4
1
Physignathus cocincinus
Chinese Water Dragon
Terrestrial
Carnivorous
5
4
Pogona vitticeps
Bearded Dragon
Terrestrial
Carnivorous
5
4
Tiliqua scincoides
Eastern Blue-tongued Lizard Terrestrial
Omnivorous
2
1
Tupinambis merianae
Argentine Black and White Tegus
Terrestrial
Omnivorous
2
Boa costriptor
Boa Constrictor
Terrestrial
Carnivorous
1
1
Crotalus molossus
Black Tailed Rattlesnake
Terrestrial
Carnivorous
1
0
Elaphe guttata
Corn Snake
Terrestrial
Carnivorous
4
2
Lampropeltis triangulum
Milk Snake
Terrestrial
Carnivorous
1
1
Python molurus
Indian Python
Terrestrial
Carnivorous
3
2
Python regius
Royal Python
Terrestrial
Carnivorous
7
5
TABLE 1: Zoological taxonomy, habitat, regimen, number of reptiles examined and number of reptiles positive for fungi in their cloacal content.
Revue Méd. Vét., 2008, 159, 3, 159-165
1
NARDONI (S.) AND COLLABORATORS
162
Moulds isolated
Acremonium
E x a m i n e d reptiles (n=218)
Testudines (n=61)
Sauria (n=140)
Red-Eared Turtle (25)
Chinese Water Dragon (1)
Positive
p e rc e n t a g e
Ophidia (n=17)
18.3%
Green iguana (14)
Alternaria
Green iguana (2)
0.9%
A. flavus
Green iguana (1)
0.9%
Veiled Chameleon (1)
A. fumigatus
Red-Eared Turtle (2)
A. niger
Red-Eared Turtle (1)
Chinese Water Dragon (1)
Boa Constrictor (1)
Hermann's Tortoise (3)
Giant African Plated Lizard (1)
Corn Snake (1)
Green iguana (4)
Indian Python (1)
0.9%
6.4
Veiled Chameleon (1)
A. nidulans
Red-Eared Turtle (1)
Madagascar Ground Gecko (1)
0.9%
A. ochraceous
Leopard Tortoise (1)
Green iguana (1)
0.9%
A. oryzae
Marginated Tortoise (1)
A. versicolor
Marginated Tortoise (1)
Bearded Dragon (1)
Red-Eared Turtle (2)
Green iguana (3)
A. wentii
0.4%
3.2%
Green iguana (1)
0.4%
Green iguana (5)
8.2%
Exophiala
Green iguana (1)
0.4%
Fusarium
Green iguana (2)
0.9%
Green iguana (1)
3.2%
Cladosporium
Leopard Tortoise (1)
Red-Eared Turtle (12)
Mucor
Greek Tortoise (1)
Hermann's Tortoise (2)
Marginated Tortoise (1)
Red-Eared Turtle (2)
Rhizopus
Bearded Dragon (1)
Boa Constrictor (1)
1.4%
Corn Snake (1)
Paecylomyces
Leopard gecko (1)
Veiled Chameleon (3)
Penicillium
1.8%
Red-Eared Turtle (25)
Bearded Dragon (3)
Corn Snake (1)
Redfoot Tortoise (1)
Chinese Water Dragon (3)
Real Python (4)
Greek Tortoise (1)
Green iguana (36)
Hermann's Tortoise (6)
Leopard gecko (1)
Marginated Tortoise (1)
Veiled Chameleon (5)
39.9%
Green iguana (3)
Scopulariopsis
Green iguana (3)
Syncephalastrum
1.4%
Indian Python (1)
Trichoderma
Red-Eared Turtle (1)
Verticillium
Red-Eared Turtle (1)
Green iguana (1)
0.4%
0.9%
0.4%
TABLE 2: List of moulds isolated from the cloacal content of reptiles, animal species in which they were found (number of positive individuals per species in brackets), and percent of positive animals per mould isolated (/total number of examined reptiles).
Revue Méd. Vét., 2008, 159, 3, 159-165
FUNGI IN PET REPTILES
Moulds isolated
C. albicans
C. catenulata
163
E x a m i n e d reptiles (n=218)
Testudines (n=61)
Hermann's Tortoise (2)
Sauria (n=140)
C. guilliermondii
C. krusei
C. lusitaniae
C. membranaefaciens
C. norvegica
C. parapsilosis
C. pelliculosa
C. rugosa
C. tropicalis
Cr. albidus
Geotrichum
Pichia etchelsii
Trichosp.oron
Saccharomyces
Unindentified
Ophidia (n=17)
0.9%
Chinese Water Dragon (1)
Green iguana (1)
Veiled Chameleon (1)
C. famata
C. glabrata
Positive
p e rc e n t a g e
1.4%
Milk Snake (1)
Royal Python (1)
Red-Eared Turtle (1)
Hermann's Tortoise (2)
Chinese Water Dragon (1)
Green iguana (1)
Green iguana (2)
Argentine Black and White Tegus (1)
Green iguana (3)
Green iguana (1)
0.9%
2.7%
0.4%
0.4%
0.9%
Red-Eared Turtle (1)
Marginated Tortoise (2)
Hermann's Tortoise (1)
Hermann's Tortoise (1)
Marginated Tortoise (1)
Red-Eared Turtle (4)
Greek Tortoise (1)
Hermann's Tortoise (1)
Red-Eared Turtle (1)
Red-Eared Turtle (1)
Marginated Tortoise (1)
Madagascar Ground Gecko (1)
Green iguana (1)
Eastern Blue-tongued Lizard (1)
Green iguana (3)
Green iguana (1)
Green iguana (11)
Green iguana (2)
Green iguana (12)
Green iguana (1)
Chinese Water Dragon (1)
Green iguana (4)
Green iguana (6)
0.9%
1.4%
0.4%
2.3%
0.4%
5.5%
Royal Python (1)
Indian Python (1)
1.8%
5.5%
0.4%
5.5%
5.5%
0.4%
4.1%
TABLE 3: List of yeasts isolated from the cloacal content of reptiles, animal species in which they were found (number of positive individuals per species in brackets), and percent of positive animals per yeast isolated (/total number of examined reptiles).
Discussion
All the isolated organisms found in the present survey are
known to be widespread environmental contaminants with
worldwide distribution. In addition, many of the yeast isolates
have previously been reported as saprophytic commensals of
reptiles [11]. Overall, despite some differences in prevalence
rates, the range of isolated organisms obtained from the cloacae
of pet reptiles in this survey is in agreement with findings of
other investigations where the external or internal mycoflora
of reptiles was examined [4, 11, 15]. According to FLAMANT
et al. [4], since reptiles are poykilothermic animals, body
temperature doesn’t play an important role in determining
internal or external fungal flora. Differences in prevalence
rates can probably be attributed to different sampling
methods, study design, variety of animal species, number of
animals examined, geographical location, and so on.
It is not known when and how during captivity the positive
reptiles acquired fungal contaminants in their cloacae. It is
possible that reptiles were contaminated before they were
Revue Méd. Vét., 2008, 159, 3, 159-165
carried into the shop. They probably acquired fungal contaminants
in the cloacal content by ingestion of contaminated food
(preys, vegetables) or water, by contact with faeces of other
contaminated animals, or during defecation by contact with
contaminated substrate which accumulated on the exterior of
the cloaca. Many reptilian species shared the same types of
isolated fungi. The basis of this sharing is uncertain but
might be related to common exogenous sources of contamination. On the other hand, in many cases, different fungal
isolates (up to six) could be obtained from a single positive
swab. The distribution of the same fungal isolates in different
hosts and the presence of many fungal isolates in a single
host suggest that reptiles may act as facultative animal carriers
for moulds and yeasts in their cloacae.
All the animals sampled in this survey were symptom free,
although 75.2% of them were harbouring fungi. This agrees
with the results of other studies [3, 5, 15] and emphasizes the
importance of histopathology in the diagnosis of fungal diseases
in reptiles [7, 15]. It is known that many mycotic agents
remain harmless in healthy individuals while they can become
opportunistic in immunocompromised hosts. The opportu-
164
nistic pathogenic role of most of the present fungal isolates
has been well documented in reptiles and humans.
With regard to the isolated moulds, the most prevalent
genus was Penicillium sp. followed by Acremonium sp. and
Cladosporium sp.. A Penicillium species has been reported
as a cause of systemic mycosis in a Seychelles giant tortoise
(Geochelone gigantea) and has been detected in association
with A. niger and Curvularia lunata varaeria from superficial
lesions on the skin and gingiva of saltwater crocodiles
(Crocodylus porosus) and freshwater crocodiles (Crocodylus
johnstoni) [7]. The genus includes thousands of species.
Although Penicillium marneffei is by far the most important
one, a number of diseases caused by other species have been
reported in humans [12]. The genus Acremonium has been
recovered from cases of mycetoma, onychomycoses, mycotic
keratitis and as a colonizer of soft contact lens in man [18].
Cladosporium sp. has been reported along with Paecylomyces
sp. from pulmonary nodules of maricultured green sea turtles (C. mydas) with mycotic pneumonia and in an adult anaconda (Eunectes murinus) with granulomatous lesions of the
mandible [7]. It is one of the commonly reported agents of
cutaneous phaeohyphomycosis in man [18].
Altogether, species of the genus Aspergillus were isolated
with consistency. Aspergillus species have been identified in a
St. Hilaire’s terrapin (Hydrastis hilarii) who died of generalized
aspergillosis, from mycotic granulomas of the forefeet in a
female musk turtle (Sternotherus odoratus), from pneumonic
lesions of American alligators (Alligator mississippiensis), in
association with Mucor sp. and Rhizopus sp. from cutaneous
lesions of a 100-year-old American crocodile (Crocodylus
acutus) with necrotizing dermatitis, in two San Esteban
chuckwallas (Sauromalus varius) with edematous and necrotic
lesions, in a black pointed teguixin (Tupinambis nigropunctatus)
died for generalized mycosis, in a puff adder (Bitis arietans)
with peritonitis [7], and from pulmonary lesions of two dead
green anacondas (E. murinus) [13]. A. flavus, A. fumigatus,
A. nidulans, A. niger, A. ochraceus, A. oryzae, and A. versicolor
can cause allergic states, toxicosis, and opportunistic invasive
infections in humans, though with different frequency. These
fungi affect the respiratory tract in most of the cases but any
organ can be involved [18].
Mucor sp., Paecylomyces sp., Rhizopus sp. and Scopulariopsis
sp. were infrequently found in this survey. Mucor sp. and
Rhizopus sp. have been reported in juvenile Florida softshell
turtles (Apalone ferox) with necrotizing shell and skin
lesions [7]. Mucor sp. has also been isolated from infected
skin of wood turtles (Clemmys insculpta), pulmonary lesions
of three species of crocodiles with fatal respiratory infections,
and cutaneous lesions of a bearded dragon (Pogona barbata)
[7]. In humans, Mucor sp. and Rhizopus sp. are amongst the
aetiological agents of zygomycosis causing rhinofacial,
rhinocerebral, cutaneous or subcutaneous forms and pulmonary, systemic, abdominal-pelvic or gastric disease [18]. A
Paecylomyces species has been found to be associated with
C. albicans in oral, gastric and hepathic nodular lesions in an
Aldabra tortoise (G. gigantea) [7]. Paecylomyces species are
uncommon human pathogens but have been documented in
cases of mycotic keratitis, endocarditis and endophtalmitis
[18]. A Scopulariopsis species has been recovered from shell
NARDONI (S.) AND COLLABORATORS
lesions of a captive soil turtle (T. graeca) [4]. In humans,
Scopulariopsis sp. has been mostly associated with cutaneous and pulmonary pathologies [18].
The remaining isolated moulds, including Alternaria sp.,
Exophiala sp., Fusarium sp., Syncephalastrum sp.,
Trichoderma sp. and Verticillium sp. were only occasionally
found. Alternaria sp. and Verticillium sp. have been identified in dermal lesions of two dead captive green anacondas
(E. murinus) [13]. In humans, Alternaria sp. is frequently
involved in cases of asthma and can colonize previously
injured skin [18]. An Exophiala species has been reported as
a cause of phaeohyphomycosis in a free living eastern box
turtle (T. carolina carolina) [10]. Species of this genus are
also amongst the aetiological agents of human phaeohyphomycosis [18]. Fusarium species have been identified as the
cause of cutaneous mycosis in loggerhead sea turtles
(Caretta caretta), as well as pathogens on crocodile farms,
and as the cause of deep tissues mycosis in saltwater crocodiles
(C. porosus) and freshwater crocodiles (C. johnstoni) [7].
Fusarium species are important agents of mycotic keratitis,
onychomycosis and burned skin colonization in man [18].
Syncephalastrum sp. has been associated with mycotic
dermatitis in two crocodiles [2] and can be an agent of
human zygomycosis [18]. Trichoderma sp. has been involved
in cases of necrotizing mycotic dermatitis in snakes [6] and
can be a serious cause of peritonitis in human patients undergoing dialysis [18].
As far as yeasts are concerned, several Candida species
were isolated in this survey. C. albicans has been identified
as the causative agent of pneumonia in crocodiles and caimans,
as well as recovered from multiple necrotic areas of the liver
of a two-banded chameleon (Chamaeleo bitaeniatus), and
from necrotic esophageal lesions in a crocodile tegu
(Crocodilus lacertinus) [7]. Although Candida species are
found in the normal flora of skin and digestive tract in man,
C. albicans, C. glabrata, C. guilliermondii, C. krusei, C.
lusitaniae, C. parapsilosis, and C. tropicalis are well known
opportunistic human pathogens. Diseases caused by
Candida species cover a range of pathologic effects, including oral, bronchial, pulmonary, alimentary, mucocutaneous
and systemic candidiasis as well as vaginitis, balanopostitis,
endocarditis and meningitis [18].
Geotrichum sp. and Trichosporon sp. were recovered less
frequently. Geotrichosis has been documented in a group of
captive carpet pythons (Morelia spilotes variegata) with
mycotic dermatitis and in a northern water snake (Nerodia
sipedon) with caseous subcutaneous nodules [7]. A
Trichosporon species has been isolated from the liver and
kidney of several captive banded rock rattlesnakes (Crotalus
lepidus klauberi) [18]. In humans, lesions caused by
Geothricum sp. are bronchopulmonary, bronchial, oral, vaginal,
cutaneous, and very rarely alimentary, while Trichosporon
sp. has been involved in a variety of opportunistic infections
[18].
Finally, Cr. albidus, P. etchelsii and Saccharomyces sp.
were only sporadically detected. Though Cryptococcus neoformans is the main aetiological agent of cryptococcosis in
humans, Cr. albidus and a few other species have been isolated on rare occasions in severely immunocompromised
Revue Méd. Vét., 2008, 159, 3, 159-165
FUNGI IN PET REPTILES
165
patients. Saccharomyces sp. has been implicated in several
cases of pulmonary disease and mycosis of the stomach [18].
D., BOUCHARA J.P: Flore fongique des lésions de la carapace des
tortues terrestres de compagnie dans l’ouest de la France. J. Mycol.
Med., 2003, 13, 67-72.
Pet shops are common sources of new companion animals
such as pet reptiles. Pet ownership is an important risk factor
for the occurrence of many zoonoses, including mycoses.
Living in close vicinity to man, reptiles could play an important
role in the transmission of fungal agents to human beings [3].
The high isolation rate of fungi from cloacae of pet reptiles
and the identification of opportunistic agents in the present
survey suggest a potential human risk of opportunistic fungal
infection from these pets. Extremely high dispersal of fungal
spores has been found in faecal samples of reptiles [9]. Other
authors have shown that reptiles from pet shops may harbour
zoonotic infectious agents [14]. A case of mycotic brain
abscess caused by a fungal pathogen of reptiles has been
reported in a 38 year old, HIV-seropositive Nigerian man
[19]. Therefore, our findings and those of other authors
indicate that reptiles sold at pet shops in Italy may be considered
as a potential source of human opportunistic mycoses. In
addition, our results provide some insight about the normal
cloacal mycoflora of healthy pet reptiles. At present, it is not
known whether pet reptiles may be more active carriers of
fungal agents in their cloacae, when compared to free living
reptiles, or not. Such a difference might be related to
environmental factors varying between free living and pet
reptiles. For instance, the latter may be exposed to poor
husbandry such as overcrowding, poor hygienic measures,
high humidity, poor water and diet quality, and so on that
might enhance the possibility of acquiring fungal contaminants.
Since only one pet shop specialised in reptiles could be
surveyed in the present study, further investigations are needed
to clarify the true extent and public health implications of pet
reptiles as carriers of opportunistic fungi.
5. - GUGNANI H.C., OKAFOR J.I.: Mycotic flora of the intestine and
other internal organs of certain reptiles and amphibians with special
reference to characterization of Basidiobolus isolates. Mykosen,
1979, 23, 260-268.
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