Abstract
In December 2003, an adult male eastern box turtle (Terrapene carolina carolina) was presented to The Wildlife Center of Virginia (WCV) after approximately 2 mo in a rehabilitation facility for marked swelling of the right hindlimb. In September 2003, a mass from the area of the right proximal tibia was removed and histopathologically diagnosed as chromomycosis. On presentation, the turtle was 450 g, well hydrated, and in good body condition. Swelling with localized edema was visible around and distal to the right stifle, and a circumferential mass was palpable around the right proximal tibia. The lateral two digits were missing from the right hind foot. Radiographs revealed marked soft tissue swelling of the entire right hindlimb, particularly the caudal and plantar aspects. No additional abnormalities were noted. The turtle was euthanatized due to the severity of the soft tissue involvement.
On gross necropsy, the liver was diffusely pale, and a black branching line was visible on the surface of the right lobe. Multifocal darkened areas of the lungs were also noted. There was an adhesion between the skin and underlying tissue on the caudolateral aspect of the right hindlimb at the level of mid-tibia, and a remnant of suture material remained cranially. Subcutaneously, an approximately 3 cm x 1 cm encapsulated mass ran the entire caudal aspect of the lower right hindlimb. The capsule was filled with a dark brown-black, friable necrotic material. On histopathology, there were pale and clear hepatocytes in the liver. There was no microscopic evidence in any of the submitted tissues (lung, heart, esophagus, stomach, spleen, pancreas, liver, kidney, testicle, intestine, cloaca, and right hindlimb integument) of a systemic fungal infection. Histopathology of the subcutaneous soft tissue of the right hindlimb showed a mass-like granulomatous inflammatory process including a mix of lymphoid cells, eosinophils and histiocytes. Included were numerous multinucleated histiocytic giant cells, often arranged in ringed groups around necrotic debris. Numerous fungal elements were seen within the necrotic centers and associated with multinucleated cells. The fungi were phaeoid (brown) hyphae and yeast-like cells. With Gomori methenamine silver stains, they appeared as chains of ovoid yeast-like bodies (conidia) as well as short rectangular hyphae with occasional right-angle budding. In addition, Torulopsis (Candida) glabrata and Exophiala (Phialophora) jeanselmei were isolated from fungal culture of the empty lesion capsule and a section of necrotic tissue. The final diagnosis was phaeohyphomycosis of soft tissues.
Torulopsis glabrata is a yeast that is normal flora of the mouth, gut, or urinary tract (in humans) but, in weak or immunocompromised patients, can cause opportunistic infection.6 We suspect that T. glabrata was a contaminant, as none of the yeast were identified in the histopathology of any of the submitted tissues. Exophiala jeanselmei is a saprophytic dematiaceous (pigmented) fungus that is most commonly found in decaying wood and soil that is enriched with organic waste, as well as polluted water and sewerage.3,5,8,9 It is also considered opportunistic, but phaeohyphomycosis caused by Exophiala species has been reported in both immunosuppressed and immunocompetent patients.10
Chromomycosis is a general term for a group of clinicopathologic syndromes including superficial chromomycosis, chromoblastomycosis, and chromohyphomycosis (used interchangeably with phaeohyphomycosis).1,8,9 The distinction lies in tissue location (cutaneous vs. extracutaneous)7,8 and fungal form (hyphal vs. muriform cells)1,3,8,9. It is most often associated with traumatic inoculation2,5,8,10 and/or immunocompromised hosts1,7. The condition has been described in mammals, reptiles, amphibians, crustaceans, fish, and birds.1,2 Infection can be diagnosed cytologically or histologically, but the causative agent must be isolated by culture.1,7 Many different courses of chemotherapy are described, but many agree that efficacy is questionable.10 Excision or debulking is recommended before chemotherapy begins and is potentially curative.3,5,7,8,10 Some consider itraconazole to be the drug of choice3,5,7,10 while others report it to be ineffective8. Ancillary flucytosine,3,7,10 terbinafine,5 or ketoconazole4,5 are also sometimes used. Fluconazole and amphotericin B appear to be subject to resistance1 or simply ineffective7.
When dissected, there was a small opening in the caudodistal portion of the subcutaneous capsule and although the integument showed no obvious evidence of trauma, the absent digits of the right hindlimb suggested such; however, we were unable to determine definitively whether this infection was the result of direct inoculation, immunosuppression, or both.
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