History
A 6-year-old 61-cm 1.2-kg (2.6-lb) female savannah monitor (Varanus exanthematicus) in a zoological collection became anorexic. The monitor had no previous history of illness. On physical examination, the coelom was considered distended and a large semiflocculent mass was palpated in the left side of the coelomic cavity. The lizard did not appear to be in pain while being examined. The monitor was referred for evaluation, and radiographs of the coelomic cavity were obtained (Figure 1).
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Diagnostic Imaging Findings and Interpretation
A moderate to severe increase in soft tissue opacity is evident throughout the mid and caudal portion of the coelom. There is marked attenuation of gas within the lungs with cranial and dorsal displacement of the caudal margins of the lung lobes, resulting from a mid-coelomic mass effect. Multiple ovoid well-mineralized structures are seen within the mid and caudoventral aspect of the coelom (Figure 2).
To better define the mass, an ultrasonographic examination of the coelomic cavity was performed by use of an 8- to 5-MHz microconvex array transducer and a 15- to 7-MHz linear transducer. A large volume of echogenic effusion is present throughout the mid to caudal aspect of the coelom (Figure 3). Associated with the cranial aspect of the left ovary, there is a complex, well-vascularized mass measuring 5.6 × 5.6 × 5.6 cm. Within the cranial aspect of the mass, there is an irregularly shaped anechoic region, which has distal acoustic enhancement. Well-defined oval to fusiform hyperechoic structures, with strong distal acoustic shadowing, are seen along the periphery of the mass. The right ovary has a normal ultrasonographic appearance. The liver has a coarse echotexture and contains multiple hyperechoic nodules measuring up to 8 mm in diameter. In addition, a well-defined 5-mm-diameter anechoic structure with distal acoustic enhancement is present within the right aspect of the liver; this structure is separate from the gallbladder, and may represent a cyst.
Primary differential diagnoses for the ovarian mass included abscess, granuloma, or neoplasia. The possible causes of the hyperechoic hepatic nodules included granulomas, metastatic neoplasia, nodular regeneration, or abscesses.
Treatment and Outcome
The monitor was anesthetized, and an exploratory coeliotomy was performed. A mass was found closely associated with the left ovary, and the ovary and mass were removed. A lesion associated with the coelomic wall was identified and removed. A wedge biopsy specimen of the liver was obtained. After surgery, the monitor was treated with ceftazidime (20 mg/kg [9.1 mg/lb], IM, q 72 h for 27 days) and meloxicam (0.5 mg/kg [0.23 mg/lb], PO, q 48 h for 12 days).
Findings on cytologic examination of a coelomic wall lesion included a predominant population of inflammatory cells, primarily mature heterophils and vacuolated macrophages that occasionally contained phagocytized erythrocytes and leukocytes. No infectious agents or neoplastic cells were identified. These findings were indicative of marked, chronic, active pyogranulomatous coelomitis. On histologic examination, the mass associated with the left ovary contained a large multilobular structure. The mass consisted of variably sized polygonal cells arranged in sheets and packets supported by fine fibrovascular stroma and divided into lobules by thick, dense fibrous septa arising from the collagenous capsule. A presumptive diagnosis of granulosa cell tumor was made. No histologic evidence of neoplasia was found in the liver biopsy specimen. Aerobic culture of a swab specimen of the interior of the neoplasm resulted in scant growth of a Bacillus sp. By use of anaerobic culture methods, a second unidentified gram-positive rod was cultured.
The monitor was found dead in its cage 7 months later and was submitted for necropsy. It was determined that the granulosa cell tumor had regrown with an associated fibrinous peritonitis and visceral metastases.
Comments
Initial survey radiographs documented a mass effect that could not be further characterized without additional imaging in a noninvasive manner. The easiest examination to undergo that would provide parenchymal information was an ultrasonographic examination. With the use of ultrasonography, coelomic fluid and a mass associated with the left ovary were identified. The mineralized structures identified on the radiographs were confirmed to be associated with the left ovarian mass. Although there are multiple possible differential diagnostic considerations for the hepatic nodules, it was possible to assess an abnormality within the liver.
Although the route of entry of bacteria into the neoplastic mass in the monitor of the present report was uncertain, possibly this followed a period of bacteremia. Considering that Clostridium difficile, Clostridium innocuum, Clostridium perfringens, and Clostridium sordelli have been frequently identified in cultures of blood samples obtained from healthy-appearing captive lizards, particularly monitors,1 these lizards may be predisposed to become clinically ill following trauma or immunosuppression.
For the monitor of the present report, a histopathologic diagnosis of granulosa cell tumor was made. Samples of the tumor were also examined by means of transmission electron microscopy; neoplastic cells were strongly supportive of a granulosa cell tumor on the basis of previous suggested criteria.2 Granulosa cell tumors have been reported in a water monitor (Varanus salvator),a garter snake (Thamnophis sirtalis),3 and 2 other snake species.4 In the monitor of the present report, histologic evidence of neoplastic cells was not observed at the margins of the liver where the biopsy specimen was obtained. If metastatic lesions were present, they were missed. A more thorough examination of the liver at the time of surgery should have been performed to identify and obtain a biopsy sample from a nodule seen on ultrasonography.
Given the paucity of reports of such tumors in monitor lizards or other reptiles, we do not know whether granulosa cell tumors in these species typically metastasize.
Garner MM, Northwest ZooPath, Monroe, Wash: Personal communication, 2011.
1. Hanel R, Heard DJ & Ellis GA, et al. Isolation of Clostridium spp. from the blood of captive lizards: real or pseudobacteremia. Bull Assoc Reptil Amphib Vet 1999; 9: 4–8.
2. Drachenberg CB, Mendenhall S, Papadimitriou JC. Adult type granulosa cell tumor, presenting as extra-ovarian metastases: ultrastructural diagnosis. Ultrastruct Pathol 1996; 20: 231–239.
3. Onderka DK, Zwart P. Granulosa cell tumor in a garter snake (Thamnophis sirtalis). J Wildl Dis 1978; 14: 218–221.
4. Mader D. Reptile medicine and surgery. 2nd ed. St Louis: Saunders, 2006.