REPTILE MYCOTIC INFECTIONS FROM THE LITERATURE AND 55 CASES

REPTILE MYCOTIC INFECTIONS FROM THE LITERATURE AND 55 CASES Drury R. Reavill, DVM, Dipl ABVP (Avian), Dipl ACVP, 1 Mike Melloy, DVM, 2 * and Robert E. Schmidt, DVM, PhD, Dipl ACVP 1 1 Zoo/Exotic Pathology Service, 2825 KOVR Drive, West Sacramento, CA 95605 USA; 2 Petroglyph Animal Hospital, 6633 Caminito Coors NM, Albuquerque, NM 87120 USA ABSTRACT As with other animals, mycotic disease is usually secondary to other infections (bacteria, parasitic, viral), or to predisposing factors such as poor husbandry, suboptimal temperatures, prolonged antibiotic use, and poor nutrition. In reptiles, fungal infections of the skin, shell, and subcutis are more common than those of other organ systems. Many fungal infections are caused by saprophytes that have invaded the tissue. In this review, we briefly cover the literature reports on fungal disease in the three reptile groups; chelonians, lizards, and snakes. Tables 1, 2, and 3 are summaries of the cases from our service. Our cases are presented after the literature review. The majority of our cases have no information pertaining to treatment or of culture reports that identify the fungal organisms. Histologically, the microbes are divided into yeast forms (generally with pseudohyphae formation indicating tissue invasion) and fungal hyphae. It is difficult to make an accurate identification of fungal organisms based on fungal hyphae in hematoxylin and eosin sections. 10,11 It is assumed that most of these microbes are environmental contaminants, such as Fusarium, Absidia, Mucor, Aspergillus, and Rhizopus. and Shell The fungal dermatoses of reptiles mimic bacterial dermatitis and mixed infections are common. The skin/shell lesions may appear as brown to greenish yellow discolorations and develop into blisters, ulcers, nodules, crusts, soft spots in the shell, granulomas, or swollen limbs. Most reports of skin infection in chelonians, lizards, and snakes are attributed to a wide variety of soil fungi. 17 Fungal shell infections have been reported in desert tortoises (Gopherus agassizii) 6 and Florida softshell turtles (Trionyx ferox). 9 In the tortoises lesions included necrotic shells with multiple foci of cell debris and heterophilic inflammation within the epidermal horn layer that were subtended by necrotic dermal bone colonized by both bacteria and fungi. Mucor sp. caused ulcerative epidermitis in the softshell turtles. The turtles presented with circular grey skin lesions on the body including the carapace and plastron. Most died within 2 wk. Fungal hyphae and bacteria were confined to the epidermis. Death in these turtles was suspected to be due to osmotic imbalance due to loss of the epidermal barrier. 62

lesions in chelonians can become extensive granulomatous lesions and even progress to systemic disease. Cutaneous and renal geotrichosis in a giant tortoise (Geochelone elephantopus) 18 presented with ulcerative skin lesion on all legs and on lower and lateral surfaces of the neck and head. Fungal hyphae and spores were seen in the skin and kidney. Culture of these tissues yielded Geotrichum candidum, a common environmental contaminant. Scoleocobasidium humicola, a soil fungus and etiologic agent of phaeoyphomycesis in fish (a systemic infection) was the cause of cutaneous lesions in Eastern box turtles (Terrapine carolina var. carolina). 23 These turtles developed both granulomatous and ulcerated papules on the feet and tail. Mycotic granulomata with many yeast-like organisms and pseudohyphae, resulted in ulcerated forefeet in a musk turtle (Sternotherus odoratus). The granulomas extended into the muscle. 3 The service has six cases of primary skin lesions in chelonians. We have two water turtles, a red ear slider (Trachemys scripta elegans) and a softshell turtle, with shell lesions of ulcerative dermatitis, progressing to osteomyelitis. Both bacteria and fungal hyphae were present in the lesions. A gopher tortoise (Gopherus polyphemus) developed a skin lesion and severe osteoarthritis due to a fungal organism. One box turtle (Terrapene carolina) had an acute dermatitis of the shell with intralesional bacteria and pigmented fungus (chromomycosis). Chromomycosis is primarily a systemic fungal infection caused by pigmented fungi of the family Dematiaceae. These fungi are saprophytes that live in soil and decaying vegetable matter, predominantly in warmer climates of tropical and subtropical countries. Some identified members include Cladosporium herbarum, Scolecobasidium humicola, Fonsecaea spp., Phialophora spp., Rhinocladiella spp., Hormodendrum spp., Curvularia spp., and Drechslera spp. 16 The fungal organisms produce a characteristic amber-brown, thickwalled, septate structures known as sclerotic bodies. Another box turtle had extensive granulomatous lesions of one front foot due to these pigmented fungi. A batagur turtle (genus species unknown) also developed a severe necrotizing dermatitis, cellulitis, and myositis of one leg in which both bacteria and fungal hyphae were noted. Culture results are not recorded for any of these cases and the fungal organisms remain unidentified. Chrysosporium anamorph of Nannizziopsis vriesii, a dermatophyte-like fungus was isolated from skin biopsies of three different species of captive adult chameleons. 15 A Parson s chameleon (Chamaeleo parsonii) presented with vesicles that became crusty brown lesions on the limbs and body in which fungal elements had been observed by histologic examination. One adult jewel chameleon (Chamaeleo lateralis) in this collection developed black skin lesions and died with a pulmonary fungal granuloma. A third isolate was obtained from a skin biopsy of a Jackson s chameleon (Chamaeleo jacksoni) with deep ulcerative cutaneous lesions located at the base of the tail. Cryptococcosis has produced skin lesions in a variety of lizards, although we have seen no cases. An Eastern water skink (Eulamprus quoyii) 7 presented for a small, discrete, painless mass over the 63

lower thoracic spine. Numerous vacuoles of various sizes separated by fibrovascular stroma contained yeast structures. Aspergillosis produced chronic extensive dermal granulomas in two San Esteban chuckwallas (Sauromalus varius). 21 These lesions progressed through the body wall and into the cerebrum and the lung. We identified 14 cases of mixed bacterial and fungal chronic ulcerative dermatitis with either a cellulitis or dermal granulomas. The lizard species include; bearded dragon (Pogona vitticeps), chameleon, panther chameleon (Furcifer pardalis), New Caledonia giant gecko (Rhacodactylus leachianus), standing s gecko (Phelsuma standingi), fat tail gecko (Hemitheconyx caudicinctus), leaf gecko (Phyllodactylus sp.), and four iguanas (Iguana iguana). Three of these cases progressed to develop a fungal osteomyelitis. Superficial fungal and yeast epidermitis and dermatitis were recognized in three cases, two iguanas and a lacerta lizard. The fungal organisms were forming hyphae and penetrating across the epithelium. These were also mixed infections with bacteria. Given the cases in which skin lesions progressed to granulomas and systemic infection, these organisms should be addressed during therapy in lizards. Fatal mycotic dermatitis occurred in captive brown tree snakes (Boiga irregularis). 14 All snakes died within 14 days after clinical signs were first noted. The first lesions developed on the ventral scales and began as areas of erythema and edema with vesicle formation, followed by development of caseous brown plaques. The fungus was identified as the Chrysosporium anamorph of Nannizziopsis vriesii, described previously in chameleons. 15 The fungal organism causing a mycotic dermatitis in a black ratsnake (Elaphe obsoleta) was identified as Monilia sitophila, an organism previously considered to be nonpathogenic, and a troublesome laboratory contaminant. 2 The lesions were of dull and roughened scales that expanded and coalesced to involve extensive areas. In a series of six snakes with mycotic dermatitis, four had concurrent Pseudomonas bacteria isolated from the skin lesions. 8 The fungal organisms were suspected to be environmental contaminates and suboptimal environmental temperature a contributing factor in the development of disease. Death of snakes due to skin lesions is believed to be related to disruption of normal cutaneous barrier, allowing body fluid and electrolyte loss through damaged skin. Fungal or bacterial toxemia may also be a factor. A corn snake (Elaphe guttata), two timber rattlesnakes (Crotalus horridus), and bull snake (Pituophis catenifer sayi) developed disseminated and fatal infections of a zygomycete fungus. 12 All snakes had granulomas in the subcutis and visceral tissues. Although the portal of entry was not discussed, three snakes had skin or oral lesions and one has disseminated disease that was prominent in the gastrointestinal tract. 64

Of the twelve mycotic skin lesions in snakes we have identified, four were superficial infections of the epidermis [Southern copperhead (Agkistrodon contortrix contortrix), anaconda (Eunectes murinus), ball python (Python regius), and Andean milk snake (Lampropeltis triangulum)]. All but the copperhead had combined bacterial and yeast proliferations. Five snakes had varying degrees of ulcerative or pustular dermatitis. Two presented with masses in the subcutis [black rat snake (Elaphe obsoleta) and Western hognose (Heterodon nasicus)] that were identified as fungal granulomas. The Eastern Massasauga rattlesnake (Sistrurus catenatus catenatus) has extensive necrosis and inflammation of the hemipene due to both bacteria and fungal organisms. Digestive Gastrointestinal tract mycotic infections are reported as part of systemic disease in chelonians. We have two cases of combined fungal and bacterial ulcerative stomatitis and glossitis in a box turtle and radiated tortoise (Geochelone radiata). The glossitis lesion supported yeast and pseudohyphae. A fungal and yeast enteritis/cloacitis were recognized in a radiated and Mediterranian tortoise (Testudo graeca). The animals all died. Mycotic digestive tract infections are uncommon in lizards. One report describes a fatal mycotic enteritis (phycomycoses) in a Jackson s chameleon (Chameleo jacksoni). 19 The chameleon presented with a rectal prolapse. Fungal hyphae were seen in the mucosa, submuscosa, tunica muscularis, and serosa of an intussusception of the terminal colon. One fungal oral lesion is described in a lizard. This fungal mandibular periodontal osteomyelitis was successfully treated in a panther chameleon (Furcifer pardalis). 4 The service has eight lizards with mycotic infections of the digestive tract. The majority of cases involved yeast. Two cases [bearded dragon (Pogona vitticeps) and iguana (Iguana iguana)] of oral lesions with mixed bacteria and yeast were found in our records. The iguana lesion progressed to a cellulitis and osteomyelitis. Yeast gastroenteritis was found in two chameleons and two iguanas. One of the chameleons also had fungal granuloma in the liver. Fungal hyphae were present in a serositis associated with an intestinal intussusception in an iguana. A bearded dragon had a fungal cholecystitis. Reports of digestive tract mycotic infections in snakes are not found in our literature search. Our two cases involve the oral cavity in a garter snake (Thamnophis species) and ratsnake. Both animals had extensive granulomas and in the garter snake, the face and orbit were distorted. Respiratory In chelonians, fungal pneumonia can be seen as a sequelae to prolonged antibiotic use and chronically low environmental temperatures. 65

Chronic fungal pneumonia was diagnosed in one desert tortoise (Gopherus agassizii) presenting with a condition of cutaneous dyskeratosis. 6 Severe unilateral pulmonary candidiasis was caused by Candida albicans in a Greek tortoise (Testudo graeca). Treatment with intrapulmonary amphotericin B (0.1 mg/kg every 24 hr for 34 days) was successful. 5 We have one case of a severe fungal pyogranulomatous pleuralpneumonia in a radiated tortoise. Literature cases of respiratory disease in lizards are not found. We have one case of acute pleuritis and pneumonia with intralesional bacteria and yeast in a Cunningham s skink (Egernia cunninghami). A fungal septicemia with lesions and fungal hyphae in the heart and lung was seen in a bearded dragon. Coccidioidomycosis pneumonia is described in a Sonoran gopher snake (Pituophis melanoleucus affinis) and in a common anaconda (Eunectes murinus). 13,22 We have no cases of ophidian mycotic pneumonia. Special Senses Otitis media in box turtles have been attributed to dietary imbalances and possible underlying organochlorine pesticides. 20 A mixture of bacteria and rarely yeast have been isolated from these inflammatory lesions. We found no cases of otic mycotic infections. An unidentified fungus was isolated from a granulomatous keratitis and panophthalmitis in a reticulated python (Python reticulatus). 1 The lesion developed after use of antibiotics and corticosteroid on an inflamed eye. Among the cases of the service, there are three animals with a mycotic keratitis. A California desert tortoise had a mixed bacterial and yeast infection. Two geckos (fat tail and Bibron s) had a fungal keratitis and in the Bibron s (Pachydactylus bibronii), it had progressed to a panophthalmitis. LITERATURE CITED 1. Collette, B.E., and O.H. Curry. 1978. Mycotic keratitis in a reticulated python. J. Am. Vet. Med. Assoc. 173(9):1117-1118. 2. Dillberger, J., and M. Abou-Gabal. 1979. Mycotic dermatitis in a black ratsnake. Mykosen. 22(6):187-190 3. Frye, F.L., and F.R. Dutra. 1974. Mycotic granulomata involving the forefeet of a turtle. Vet. Med./Sm. Ani. Clin. 12:1554-1556. 4. Heatley, J.J., M.A. Mitchell, J. Williams, J.A. Smith, and T.N. Tully, Jr. 2001. Fungal Periodontal Osteomyelitis in a Chameleon, Furcifer pardalis. J. Herpe. Med. Surg. 11(4):7-12. 5. Hernandez-Divers, S.J. 2001. Pulmonary candidiasis caused by Candida albicans in a Greek 66

tortoise (Testudo graeca) and treatment with intrapulmonary amphotericin B. J. Zoo. Wildl. Med. 32(3):352-359. 6. Homer, BL. K.H. Berry, M.B. Brown, G. Ellis, et al. 1998. Pathology of diseases in wild desert tortoises from California. J. Wildl. Dis. 34(3):508-523. 7. Hough, I. 1998. Cryptococcosis in an eastern water skink. Aust. Vet. J. 76(7):471-472. 8. Jacobson, E.R. 1980. Necrotizing mycotic dermatitis in snakes: clinical and pathologic features. J. Am. Vet. Med. Assoc. 177(9):838-841. 9. Jacobson, E.R., M.B. Calderwood, and S.L. Clubb. 1980. Mucormycosis in hatchling Florida softshell turtles. J. Am. Vet. Med. Assoc. 177(9):835-837. 10. Jensen, H.E., B. Aalbaek, P. Lind, and H.V. Krogh. 1996. Immunohistochemical diagnosis of systemic bovine zygomycosis by murine monoclonal antibodies. Vet. Pathol. 33(2):176-183. 11. Jensen, H.E., S.N. Olsen, and B. Aalbaek. 1994. Gastrointestinal aspergillosis and zygomycosis of cattle. Vet. Pathol. 31(1):28-36. 12. Kaplan, W., F.W. Chandler, A.A. Padhye, and T.E. Hamm. 1983. A zygomycotic infection in captive snakes. Sabouraudia. 21:85-91. 13. McNamara, T.S., R.A. Cook, J.L. Behler, L. Ajello, and A.A. Padhye. 1994. Cryptococcosis in a common anaconda (Eunectes murinus). J. Zoo. Wildl. Med. 25(1);128-132. 14. Nichols, D.K., R.S. Weyant, E.W. Lamirande, L. Sigler, and R.T. Mason. 1999. Fatal mycotic dermatitis in captive brown tree snakes. J. Zoo. Wildl. Med. 30(1):111-118. 15. Pare, J.A., L. Sigler, D.B. Hunter, R.C. Summerbell, D.A. Smith, and K.L. Machin. 1997. Cutaneous mycoses in chameleons caused by the Chrysosporium anamorph of Nannizziopsis vriesii (Apinis) currah. J. Zoo. Wildl. Med. 28(4):443-453. 16. Reavill, D.R. 2001. Amphibian skin diseases. Vet. Clin. North. Am. Exot. Anim. Pract. 4(2):413-440. 17. Rossi, J.V. Dermatology. In: Reptile Medicine and Surgery. Mader DR (ed) W.B. Saunders Co., Philadelphia 1996, p112. 18. Ruiz, J.M., E. Arteaga, J. Martinez, E.M. Rubio, and J.M. Torres. 1980. Cutaneous and renal geotrichosis in a giant tortoise (Geochelone elephantopus). Sabouraudia. 18(1):51-59. 19. Shalev, M., J.C. Murphy, and J.G. Fox. 1977. Mycotic enteritis in a chameleon and a brief review of phycomycoses of animals. J. Am. Vet. Med. Assoc. 171(9): 872-875. 20. Tangredi, B.P., and R.H. Evans. 1997. Organochlorine pesticides associated with ocular, nasal, or otic infection in the eastern box turtle (Terrapene carolina carolina). J. Zoo. Wildl. Med. 28(1): 97-100. 21. Tappe, J.P., F.W. Chandler, S. Liu, and E.P. Dolensek. 1984. Aspergillosis in two San Esteban chuckwallas. J. Am. Vet. Med. Assoc. 185(11):1425-1428. 22. Timm, K.I., R.J. Sonn, and B.D. Hultgren. 1988. Coccidioidomycosis in a Sonoran gopher snake, Pituophis melanoleucus affinis. J. Med. Vet. Mycology 26:101-104. 23. Weitzman, I., S.A. Rosenthal, and J.L. Shupack. 1985. A comparison between Dactylaria gallopava and Scoleocobasidium humicola: first report of an infection in a tortoise caused by S. humicola. J. Med. Vet. Mycol. 23:287-293. 67

Table 1. Fungal lesions in chelonians. Primary Site Species Bacteria Present Digestive Digestive Tortoise, Mediterranean Tortoise, Radiated Fungus Diagnosis Morphology Yes Yeast Intestine: acute erosive, ulcerative, and transmural fibrinonecrotic enteritis with bacteria and yeast Yes Yeast Tongue: severe ulcerative and necrotizing glossitis with intralesional fungus and bacteria Digestive Tortoise, Radiated Yes Cloaca: necrosis and acute inflammation with intralesional fungal hyphae and bacteria Digestive Turtle, Box Yes Oral cavity: acute ulcerative stomatitis Respiratory Tortoise, Radiated Tortoise, Gopher with intralesional bacteria and fungus Lung: pneumonia and pleural pyogranulomas with fungus : necrotizing fibrinous dermatitis and osteoarthritis with intralesional fungus Batagur Turtle Yes Leg: severe necrotizing dermatitis, cellulitis, and myositis (leg abscess) with bacteria and fungi Turtle, Box Yes Pigmented Fungus Turtle, Box Pigmented Fungus Turtle, Red Ear Slider Special senses Turtle, Soft Shell Tortoise, Calif. Desert Shell biopsy: intracorneal pustule formation and acute dermatitis with intralesional bacteria and pigmented fungus Feet: granulomatous chromomycosis cellulitis and dermatitis Yes Shell lesions: ulcerative and erosive dermatitis with osteomyelitis and intralesional bacteria and fungus Yes and shell: erosive and ulcerative fungal and bacterial dermatitis Yes Yeast Eye: ulcerative blepharitis and acute conjunctivitis with limbal and corneal suppurative inflammation and intralesional bacteria and yeast 68

Table 2. Fungal lesions in lizards. Primary site Species Bacteria Present Digestive Bearded Dragon Bearded Dragon Fungus Morphology Diagnosis Liver: fungal cholecystitis Digestive Yes Yeast Oral biopsy: superficial glossitis with inflammatory exudate and intralesional bacteria and yeast Digestive Chameleon Yeast Intestine: severe enteropathy Digestive Chameleon, Veiled Yeast Large intestine: colitis with mucosal yeast proliferation and intraluminal nematodes Liver: fungal granulomas Digestive Iguana Yes Yeast Stomach: ulcerative gastritis with intralesional bacteria and fungus Digestive Iguana Yes Yeast Choana: pyogranulomatous osteomyelitis and cellulitis with intralesional bacteria and yeast Digestive Iguana Yeast Intestine: acute enteritis with intraluminal yeast Stomach: gastritis with intraluminal yeast Digestive Iguana Intestine: intestinal intussusception and serositis with intralesional fungus Disseminated Bearded Dragon Septicemia disseminated mycotic infection Respiratory Cunningham k Yes Yeast Lung: pleuritis and pneumonia with intralesional bacteria and yeast Bearded : necrotizing dermatitis Dragon Chameleon Yes Yeast : ulcerative dermatitis with intralesional bacteria and yeast Chameleon Yes Yeast : erosive dermatitis with intralesional yeast and bacteria Chameleon, Panther Chameleon, Veiled Bearded Dragon Tail: severe diffuse fungal granulomas and granulomatous inflammation with cellulitis, rhabdomyositis and osteomyelitis Yes Tail: acute to subacute ulcerative dermatitis, cellulitis, myositis, and myelitis with intralesional fungus and bacteria biopsy: subacute to chronic ulcerative dermatitis with dermal fungal granulomas 69

Table 2. Fungal lesions in lizards (continued). Primary site Species Bacteria Fungus Diagnosis Present Morphology Gecko, Fat Tail Yes Yeast Foot: pyogranulomatous dermatitis, cellulitis, and osteomyelitis with Gecko, Leaf Tail intralesional bacteria and yeast Yes Toe: superficial epithelial bacterial and fungal keratin granuloma with subacute to chronic dermatitis, cellulitis, and osteomyelitis Iguana Yes lesion on nose: dermatitis with keratin fungal and bacterial proliferation Iguana Yes Yeast : dermal necrosis focal extensive transepidermal fungal proliferation Iguana Yes Tail: coagulative necrosis with ulcerative dermatitis and intralesional bacteria and fungi Iguana Yes Pigmented Fungus biopsy from tail: dermatitis and cellulitis with intralesional pigmented fungus and bacteria Iguana Yes : ulcerative dermatitis with intralesional fungus and bacteria Iguana : ulcerative and necrotic dermatitis with intralesional fungus and fungal vasculitis Lacerta lizard Cutaneous papilloma with superficial epidermitis and intralesional fungus Special senses Special senses Gecko, New Caledonia Giant Legs: ulcerative necrotizing dermatitis and cellulitis with intralesional fungal hyphae Gecko, : ulcerative fungal dermatitis, Standing cellulitis and myositis Gecko Eye: severe chronic inflammation Gecko, Bibrons Yes Eye: necrotizing panophthalmitis with intralesional bacteria and fungus 70

Table 3. Fungal infections in snakes. Primary Site Species Bacteria Fungus Diagnosis Present Morphology Digestive Garter Snake Yeast Oral mass: fungal granulomas Digestive Rat Snake Oral mass: fungal granulomas Southern Scale biopsy: fungal epidermitis Copperhead Anaconda Yes Yeast : multifocal intracorneal exudate with intralesional bacteria and yeast Anaconda : multifocal pustular dermatitis : hyperkeratosis and fungal colonization Anaconda Yes Yeast : acute dermatitis with intracorneal inflammatory exudate and intralesional bacterial and fungus Hognose, Western Biopsy masses: subacute to granulomatous dermatitis and cellulitis with vasculitis and intralesional fungi Python, Ball Yeast : erosive and ulcerative nonsuppurative dermatitis with yeast Python, Ball Yes Yeast : fungal and bacterial epidermitis with parakeratosis and hyperkeratosis Python, Burmese Black Rat Snake Eastern Massasauga Rattlesnake Sea Snake Yes, Pseudomo nas sp. Andean Milksnake : ulcerative subacute dermatitis Subcutaneous mass: multifocal to coalescing chronic fungal granulomas Yes Hemipene: extensive acute inflammation and necrosis with intralesional bacteria and fungus Fusarium sp. : ulcerative and erosive dermatitis and cellulitis with intralesional fungus and bacteria Yeast : fungal keratin proliferation and acute dermatitis with epidermal and dermal edema 71