Pathology in Practice

Lara M. Cusack Georgia Aquarium, 225 Baker St NW, Atlanta, GA 30313.

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Tonya M. Clauss Georgia Aquarium, 225 Baker St NW, Atlanta, GA 30313.

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Cara L. Field Georgia Aquarium, 225 Baker St NW, Atlanta, GA 30313.

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Gregory D. Bossart Georgia Aquarium, 225 Baker St NW, Atlanta, GA 30313.

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 VMD, PhD
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Alvin C. Camus College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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History

The carcass of a 19-year-old 2.7-kg (5.9-lb) sexually intact male African penguin (Spheniscus demersus) was submitted for necropsy at the College of Veterinary Medicine, University of Georgia. The bird was from an aquarium-housed population at the Georgia Aquarium. Approximately 6 months prior to death, the bird was evaluated at the aquarium's veterinary department because of intermittent lethargy and anorexia. Coelomic distension developed over a 6-month period during which time radiographic, ultrasonographic, and CT findings confirmed the presence of free coelomic fluid. A diagnosis of right-sided heart failure was made on the basis of echocardiographic findings of moderate to severe right atrial and ventricular enlargement, tricuspid valve regurgitation, pulmonary hypertension, and dilation of hepatic veins. Medical treatment with furosemide, enalapril, pimobendan, and sildenafil was initiated. Despite medical treatment as well as coelomic aspirations to remove accumulating fluid, the penguin's condition continued to decline and it died 124 days following the start of treatment.

Gross Findings

At necropsy, the penguin was in good body condition. There was severe bilateral jugular engorgement, enlargement of the right side of the heart, and approximately 10 mL of clear pericardial fluid. The right atrioventricular valve was thickened and had rare 2-mm-diameter opaque nodules along its margin. Arising from the mesenteric border of the proximal jejunal serosa adjacent to the pancreas was an irregular 1.0 × 0.9 × 0.7-cm, firm, pale, tan nodule. On cut surface, the mass extended to, but did not compromise, the intestinal lumen (Figure 1).

Figure 1—
Figure 1—

Photographs of an intestinal mass in a 19-year-old African penguin (Spheniscus demersus) that was treated for right-sided heart disease. Despite medical treatment, the bird's condition continued to decline and it died 124 days following initiation of treatment. A—Grossly, an irregular, 1.0 × 0.9 × 0.7-cm, firm, pale tan nodule arising from the proximal jejunal serosa along its mesenteric attachment is visible. Bar = 1 cm. B—On cut surface, the mass appears glistening white (arrows) and extends to but does not compromise the intestinal lumen located immediately ventral to it. The paired tan structures located dorsal to the mass are portions of the pancreas. Bar = 0.5 cm.

Citation: Journal of the American Veterinary Medical Association 250, 7; 10.2460/javma.250.7.755

Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page→

Histopathologic Findings

Histologic examination of sections of the affected portion of the jejunum revealed that the intestinal muscularis was markedly thickened by an expansile, well-circumscribed, unencapsulated mass of neoplastic cells that were haphazardly arranged in broad interlacing bundles. Individual 5- to 10-μm-wide tumor cells were fusiform with abundant, fibrillar, pale eosinophilic cytoplasm. Centrally located nuclei were mildly anisokaryotic, ovoid to elongated with rounded to blunted ends, stippled chromatin, and an occasional single small nucleolus. Rare binucleated cells were also present (Figure 2). Mitoses were not observed. The overlying mucosa was unaffected. Immunohistochemical staining revealed that the tumor cells were strongly positive for desmin and negative for smooth muscle actin (SMA), KIT (CD117), and S-100. The avian tissue failed to react with mammalian (mouse) vimentin-specific antibody. Interestingly, there was SMA-specific staining of the muscularis mucosae and vascular smooth muscle in other areas of the jejunal section, but normal smooth muscle of the muscularis externa also failed to stain for SMA.

Figure 2—
Figure 2—

Photomicrographs of the jejunal nodule from the penguin in Figure 1. A—The nodule originates from the muscularis (arrows) and is composed of an expansile, well-circumscribed neoplasm formed by a relatively homogeneous population of broad, fusiform cells with abundant eosinophilic cytoplasm and mildly anisokaryotic, ovoid to elongate nuclei. Neoplastic cells form long haphazardly arranged interlacing fascicles. H&E stain; bar = 100 μm. B—The neoplasm was predominated by cells with characteristic elongate nuclei with blunt ends. H&E stain; bar = 20 μm. C—Among the neoplastic cells, rare binucleated forms were identified. H&E stain; bar = 20 μm.

Citation: Journal of the American Veterinary Medical Association 250, 7; 10.2460/javma.250.7.755

Morphologic Diagnosis and Case Summary

Morphologic diagnosis and case summary: intestinal leiomyoma in an African penguin.

Comments

In the case described in the present report, microscopic findings were consistent with leiomyoma. Leiomyomas are benign tumors of smooth muscle that develop throughout the gastrointestinal, genitourinary, and hepatobiliary systems; within organ capsules and trabeculae; and in the skin of domestic animals. Leiomyomas must be differentiated from other spindle cell neoplasms; in particular, those located in the intestine must be differentiated from members of a heterogeneous group of gastrointestinal stromal tumors (GISTs) and GIST-like tumors with similar light microscopic features.1,2 Results of immunohistochemical staining have indicated that a small percentage of leiomyomas in dogs are negative for SMA.3,4 Leiomyomas typically express either desmin, SMA, or both, with or without vimentin, but are negative for KIT and S-100.4 Leiomyomas are discrete, expansile, nonencapsulated masses that can be overlooked as normal smooth muscle. They are composed of relatively uniform, tightly packed spindle cells arranged in wide interlacing fascicles. The neoplastic cells have indistinct borders and eosinophilic, occasionally vacuolated cytoplasm. Nuclei are elongated with blunted ends. Binucleated or multinucleated cells and moderate anisokaryosis may be present. Mitoses are uncommon. Although well-differentiated leiomyosarcomas may have few features of malignancy, they are invasive, have mitotic rates higher than that of normal smooth muscle, and often have areas of necrosis. Poorly differentiated leiomyosarcomas appear as short, narrow fascicles formed by cells with closely apposed nuclei and reduced cytoplasmic volume, compared with normal myocytes. They can also have an increased frequency of binucleate, multinucleate, and bizarre cells as well as edema and necrosis.1,2

Neoplastic disease is common among avian species, and there exists a solid resource of published information on the incidence and the gross and microscopic appearance of neoplasms of domesticated birds.5–8 More frequent clinical evaluation, in combination with longer life spans and a potential genetic predisposition associated with inbreeding, has resulted in more frequent reports of neoplasia in captive and companion birds, compared with reports of neoplasia in their free-ranging counterparts. However, detailed knowledge pertaining to the cause, development, clinical effects, and treatments of neoplasia in these avian patients remains limited.5,6

Intestinal neoplasia in birds is rare, although primary intestinal leiomyosarcomas without evidence of metastasis in budgerigars have been reported.5,7,9,10 Other reports include diffuse intestinal lymphosarcoma in an Amazon parrot, gastrointestinal adenocarcinoma in a conure, and metastatic intestinal carcinoma in multiple avian species.11–15 Leiomyomas in domestic avian species are most commonly associated with the urogenital system.7 The pathogenesis of leiomyomas is unknown, but they are typically slow growing. Associated clinical signs are dependent on the location and size of the tumor and include dysphagia, abdominal distention, organ displacement, and gastrointestinal or reproductive tract obstruction.5 Complete surgical excision is typically curative.1 Cytologic examination of tumor aspirate specimens usually reveals sparse cellularity, with scattered free nuclei or few spindle cells with elongated nuclei.5

Reports of neoplasia in penguins are limited, despite these species being commonly displayed in zoos and aquaria. Among penguins, 4 cases of melanoma; 2 cases each of cholangiocarcinoma, ventricular adenocarcinoma, and lymphoma; and 1 case each of choanal squamous cell carcinoma and intestinal lymphosarcoma have been described.11,16–26 This is the first reported case of a leiomyoma in a penguin, to our knowledge.

The cause of death in the penguin of the present report was right-sided heart failure of unknown etiology. The intestinal leiomyoma was considered an incidental finding on postmortem examination, but the bird did have intermittent clinical signs consistent with discomfort following ingestion of food. Although this was attributed to the space-occupying effects of accumulated coelomic fluid, the neoplasm may have been a contributing factor. Immunohistochemical findings in this case were confounding. The tumor cells failed to stain for SMA, as did intestinal smooth muscle of the muscularis externa. Vascular smooth muscle and the muscularis mucosae were positive for SMA, suggesting differences in the antigenic reactivity of actin from these sites. The possibility of a GIST-like tumor cannot be entirely ruled out given the facts that the tumor cells were negative for KIT and mammalian (mouse) vimentin antibody failed to react with the avian tissue.4

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