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Bilateral malignant seminomas in two unrelated, aged trumpeter hornbills (Bycanistes buccinator).

Abstract: Seminomas occur infrequently in birds. Two cases of bilateral malignant seminomas in unrelated trumpeter hornbills (Bycanistes buccinator) are described. Case 1 was a 22-year-old trumpeter hornbill submitted for necropsy because of sudden death at a zoo in California. Postmortem examination revealed multiple masses within the body cavity, 2 of which replaced both testes. Case 2 was a 19-year-old trumpeter hornbill at a zoo in North Carolina that underwent exploratory surgery for a suspected gastrointestinal obstruction. Both testes were diffusely enlarged, compressing and replacing the adjacent kidneys. In both birds, the masses were composed of discrete, round to polyhedral cells, typical of seminomas. Examination of the ancestry of the hornbills showed they were unrelated to each other, suggesting a potential predisposition for these birds to develop seminomas.

Key words: seminoma, metastasis, testes, avian, trumpeter hornbill, Bycanistes buccinator

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Clinical report

A 22-year-old, male trumpeter hornbill (Bycanistes buccinator) (case 1) was presented to the California Animal Health and Food Safety Laboratory at the University of California, Tulare, for necropsy due to sudden death. The bird was bright and alert before death with no physical abnormalities except for moderate emaciation (700 g). Gross examination identified that both testes had been replaced by 2 large masses. The left mass (5.5 x 3 x 2.5 cm) was white with a firm, necrotic focus (1 x 1 cm) on the cut surface (Fig 1A). The right mass (3.5 x 2.5 x 2 cm) was similar in appearance and consistency. A similar third mass (2 x 3 x 2 cm) was in the posterior aspect of the abdomen between the dark red and variably atrophic kidneys and firmly attached to the synsacrum (Fig 1A). Near the pancreas, a fourth pale, firm, flat mass (2 x 1 x 1 cm) was attached to the duodenal serosa (Fig 1B). Both lungs demonstrated patchy congestion and edema. The major vessels of the heart appeared thickened. Esophagus and crop were empty, and the gizzard contained only a small amount of food. The intestinal tract was diffusely distended and contained little ingesta. The liver was enlarged and congested and showed red, pale foci on its surface. Both thyroid glands were mildly enlarged.

Another 19-year-old, male trumpeter hornbill (case 2) with a 2/5 keel score (weight, 600 g) underwent exploratory coeliotomy at the North Carolina Zoological Park Hanes Veterinary Medical Center for a suspected gastrointestinal obstruction after an intermittent history of lethargy, anorexia, and polyuria. The testes were diffusely enlarged (4.5 x 2.5 cm), oval to irregular, and white. They compressed the adjacent renal poles, and approximately 60%-70% of the renal mass appeared similarly white. The hornbill was euthanatized.

Sections of representative tissues from both hornbills collected at necropsy were routinely processed for microscopic examination and stained with hematoxylin and eosin. In both cases, masses were histologically composed of densely cellular sheets of atypical round cells with indistinct stroma. Neoplastic cells had indistinct cell borders with a moderate amount of wispy, pale, eosinophilic cytoplasm surrounding a round to oval, vesicular nucleus with 1-2 prominent nucleoli (Fig 2A). Anisocytosis and anisokaryosis were moderate. with 2 (case 1) and 10 (case 2) mitotic figures in 10 high-power fields, including bizarre mitotic figures and occasional multinucleation. Multifocal intravascular invasion was observed. A frequent "starry sky" appearance was present within the neoplasm (Fig 2A) and was admixed with rare, small, lymphoid aggregates (case 2) or few heterophils and macrophages (case 1). The tubular structure of both testes was completely replaced by the neoplastic growth, except for a few seminiferous tubules randomly scattered throughout the mass. In case 1, the neoplasms compressed both kidneys (Fig 2B) and pancreas (Fig 2C), and part of the right testicular neoplasm infiltrated the right kidney. In case 2, the infiltrative mass replaced approximately 50% of the renal parenchyma (Fig 2D) with multifocal necrosis and atrophy of entrapped tubules. Additional findings were severe periportal hepatitis consisting of variable numbers of lymphocytes admixed with fewer heterophils and plasma cells; peribronchiolar aggregations of macrophages containing intracytoplasmic silica; accumulation of amorphous, basophilic material admixed with colloid within the thyroid follicles (case 1); and mild interstitial lymphoplasmacytic nephritis (case 2).

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Discussion

The current report describes bilateral seminomas with metastases in 2 unrelated trumpeter hornbills. The parents of case 2 were wild caught and imported at a later date than the studbook entry for case 1 (D. Zombeck, written communication, February 2013). Finding similar, bilateral, malignant seminomas in 2 aged hornbills suggests these birds may have a predilection for developing seminomas, and the tumor should be suspected in clinically ill, older, male hornbills.

Seminomas are primary testicular germ cell tumors that arise from the germinal epithelium of the seminiferous tubules. (1) Benign seminomas restricted to the testes are most common in birds, but malignant tumors that spread to adjacent tissues or metastasize to other organs (kidney, spleen, liver, pancreas, lungs, heart, peritoneum) have been reported. (2-5) Usually seminomas in birds are unilateral, but bilateral tumors have been described in a cockatiel (Nymphicus hollandicus), (4) black swan (Cygnus atratus), (6) duck (Anas platyrhynchos), (7) and 7 of 11 aged pigeons (Columba livia). (5) Affected testes are usually diffusely enlarged and often displace or compress other visceral organs, especially air sacs. Weight loss and ascites may accompany the tumors. The contralateral testis is usually within reference intervals but can be atrophied. (5,8)

Microscopically, seminomas are classified as typical, atypical, or spermatocyte. (9) Typical seminomas in birds are further subdivided into intratubular or diffuse types. Occasionally, both patterns occur within the same tumor. Foci of lymphocytes, like those observed in case 2 and characteristic of mammalian seminomas, occur rarely or not at all in avian seminomas. The cytologic features observed in both cases parallel those reported in mammalian seminomas: large, polyhedral cells with sharp borders, vesicular nuclei, prominent nucleoli, and scant basophilic or amphophilic cytoplasm. (1) Necrosis of individual cells and vacuolated histiocytes scattered in the parenchyma produce a starry sky effect within the neoplasm. (1,2) Other testicular tumors have been described in birds, (10) although their histologic features are quite distinctive. Teratomas are tumors containing multiple cell types arising from more than one embryonic layer. They can be composed of bone, cartilage, smooth muscle, nerves, fat, melanocytes, squamous epithelium, and/or feathers. Sertoli cell tumors are characterized by elongate cells with basal nuclei and moderate to abundant basophilic cytoplasm, arranged in a palisading manner around the central lumina of tubules. Leydig cell tumors contain large, polygonal cells with abundant, occasionally vacuolated cytoplasm, and they are arranged in irregular acini. Based on the described histologic features--all absent on our cases--teratoma, Sertoli cell tumor, and Leydig cell tumors can be ruled out.

Although uncommon, seminomas have occurred in several avian species in the orders Galliformes (chickens, guinea fowl, turkey, quail), Columbiformes (pigeons, doves), Anseriformes (ducks, swans), Psittaciformes (parrots, cockatiels, budgerigars [Melopsittacus undulatus]), and Passeriformes (arrow-marked babbler [Turdoides jardineii]). (2,3,5-22) These tumors are found more commonly in pet birds older than 5 years (16) because of their longer life span compared with commercial chickens and turkeys. In a 7-year survey of postmortem cases, 21 seminoma cases were identified in 54 companion birds. (21) In a 10-year survey of neoplasia in pet birds, more than 88% of the seminomas were described in budgerigars. (18) Few tumors have been described in species within the order Bucerotiformes (hornbills), such as a hepatocellular adenoma in a Luzon hornbill (Penelopides manillae) (23) and a squamous cell carcinoma in a great hornbill (Buceros bicornis), (24) but to our knowledge, this is the first report of seminoma in hornbills.

In domestic animals seminomas often develop in cryptorchid testes (1); however, because avian testes are normally intra-abdominal, this does not appear to increase the risk of testicular tumors in birds.

In birds, clinical findings of testicular neoplasia are coelomic distension, anorexia, lethargy, and dyspnea (25,26) or occasional signs of feminization such as partial change of cere color from blue to brown in budgerigars. (8,27) Tumors can enlarge considerably before clinical signs are recognized. Radiographs, ultrasound, and cytologic examination of a fine-needle biopsy can be performed to establish an antemortem diagnosis. Cytologic evaluation of fine-needle aspirates from a seminoma has been reported in a rock dove (11); however, cytologic differentiation of seminomas from other testicular tumors may be a diagnostic challenge (28) and histologic evaluation is necessary. Testicular tumors should always be included as a differential diagnosis for a space-occupying mass causing organ displacement within the coelomic cavity in a male bird. Other differentials are renal or adrenal neoplasia, orchitis, and normal increased testicular size during active breeding.

Different treatment strategies have been attempted, including surgical removal, chemotherapy, radiation therapy by orthovoltage or strontium-90, and hormonal therapy, with variable results depending on the affected species. (21) Moreover, surgical resection can be problematic in birds because of the short vascular supply to the testes. (29) Therefore, early detection by physical examination and diagnostic imaging are critical for successful treatment and prognosis.

Acknowledgments: We thank Dr Lewis Wright (Fresno Chaffee Zoo) and Dr Ryan DeVoe (North Carolina Zoological Park Hanes Veterinary Medical Center) for submitting cases 1 and 2, respectively, and Debbie Zombeck for checking the studbook for trumpeter hornbills in North America and determining that these 2 birds were unrelated.

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Morena B. Wernick, DVM, Dipl ECZV (Avian), Jeremy R. Tobias, DVM, Robert B. Moeller, DVM, Dipl ACVP, John Barnes, BS, DVM, PhD, Dipl ACVP, Dipl ACPV, Chiara Palmieri, DVM, PhD, Dipl ECVP, and H. L. Shivaprasad, BVSc, MS, PhD, Dipl ACPV

From the California Animal Health and Food Safety Laboratory System, Tulare Branch. University of California, Davis, 18830 Road 112, Tulare, CA 93274, USA (Wernick, Moeller, Shivaprasad); the Department of Population Health & Pathobiology, College of Veterinary Medicine, North Carolina State University, 1060 William Moore Drive, Raleigh, NC 27607, USA (Tobias, Barnes); and the School of Veterinary Science, the University of Queensland, Gatton Campus, 4343 Gatton, QLD, Australia (Palmieri). Present address (Wernick): Tierklinik TS AG, Burgerstrasse 11, CH-3600 Thun, Switzerland.
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Title Annotation:Clinical Report
Author:Wernick, Morena B.; Tobias, Jeremy R.; Moeller, Robert B.; Barnes, John; Palmieri, Chiara; Shivapras
Publication:Journal of Avian Medicine and Surgery
Article Type:Clinical report
Date:Jun 1, 2015
Words:2374
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