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Bilateral seminoma with hepatic metastasis in a cockatiel (Nymphicus hollandicus).

Abstract: An 18-year-old, intact male cockatiel (Nymphicus hollandicus) presented with a clinical history of dyspnea, lethargy, and reluctance to perch. Coelomic ultrasonographic examination revealed hypoechoic nodules in the proximity of, and within, the liver. The bird did not respond to supportive care and was euthanatized. At necropsy, the testes were bilaterally enlarged, whitish-tan, firm, and multilobulated. The right hepatic lobe contained a mass that had a similar color and consistency to those in the testes. On histologic and ultrastructural examinations, the diagnosis was bilateral testicular seminoma with hepatic metastasis. To our knowledge, this is the first case of a metastatic bilateral testicular seminoma reported in a cockatiel.

Key words: seminoma, metastasis, germinal cell, electron microscopy, avian, cockatiel, Nymphicus hollandicus

Clinical Report

A 105-g, 18-year-old, intact male pied cockatiel (Nymphicus hollandicus) presented at the Louisiana State University, Veterinary Teaching Hospital and Clinics (Baton Rouge, LA, USA) for dyspnea. The bird was fed a seed-based diet with occasional table food. It had a 1-week history of sneezing and head-shaking, and 2 days before presentation, the bird became lethargic and dyspneic and was reluctant to perch. At presentation, the cockatiel was moderately to severely dyspneic and exhibited tail-bobbing. It was in good body condition (body condition score, 4 of 5) on physical examination, and the abdominal skin was diffusely yellow, suggestive of subcutaneous fat deposition. Palpation revealed abdominal distension and caudal displacement of the ventriculus, and increased respiratory noises were present on auscultation.

The initial treatment protocol consisted of supportive care that included subcutaneous fluids (50 mL/kg per day, lactated Ringer's solution), doxycycline (50 mg/kg IM; Vibramycin, Pfizer, Capelle a/d IJssel, The Netherlands), and vitamin A (10 000 IU/kg IM, Injacom ADE, Northwest Pharmacy Compounding Center, Houston, TX, USA) and placement in an oxygen cage with supplemental heat. Results of a complete blood cell count revealed a mild heterophilic leukocytosis (14.8 x [10.sup.3] cells/[micro]L; reference range, 2.3-7.9 x [10.sup.3] cells/[micro]L) and a moderate lymphopenia (0.3 x [10.sup.3] cells/[micro]L; reference range, 1.3-6.6 x [10.sup.3] cells/[micro]L), indicative of a possible stress response. (1) Results of a plasma biochemical profile showed a mild increase in concentrations of aspartate aminotransferase (659 IU/L; reference range, 128-396 IU/L), creatine kinase (1137 IU/L; reference range, 160-420 IU/L), and cholesterol (6.1 mmol/L; reference range, 2.33-5.17 mmol/L), suggestive of muscle or liver damage. (1)

The next day, the cockatiel was anesthetized with isoflurane and whole-body radiographs were taken. The radiographic images revealed a diffuse increase in radiodensity of the body cavities with a loss of contrast and compression of the air sacs (Fig 1A and B). The bird recovered uneventfully from anesthesia. Additionally, transcoelomic echocardiography and coelomic ultrasound examination were performed without sedation. No abnormalities were noted during the echocardiographic examination. However, upon coelomic ultrasonographic examination, a hypoechoic mass measuring 1.63 x 1.57 cm was visualized in the coelom close to the liver, with additional small, hypoechoic nodules within the hepatic parenchyma (Fig 2). These results suggested an intracoelomic neoplasm with metastatic involvement of the liver. Dexamethasone (0.25 mg/kg IM ql2h) and butorphanol (2 mg/kg IM q8h; Torbugesic, Fort Dodge Animal Health, Fort Dodge, IA, USA) were added to the bird's treatment regimen. After 2 days of treatment, the bird did not show any clinical improvement, at which time the owner elected euthanasia.

[FIGURE 1 OMITTED]

The gross necropsy examination revealed bilaterally enlarged and slightly firm testes, approximately 2 x 1.5 x 1.5 cm each (Fig 3A, top). The cut surface was white tan with a multilobulated appearance (Fig 3A, middle). The liver had an approximately 3 x 2 x 2 cm right lobe and a 2 x 1.5 x 1.5 cm left lobe (Fig 3B). The cranial two-thirds of the right hepatic lobe was white tan (Fig 3A, bottom; Fig 3B). The coelomic cavities contained approximately 3 mL of yellow, clear fluid. Sections of formalin-fixed tissues were submitted for histologic and ultrastructural examinations.

Microscopically, the parenchyma of the testes was diffusely effaced and was replaced by a well-circumscribed and partially encapsulated, multilobular, highly cellular neoplasm composed of large, polyhedral to round cells, consistent with germ cells, arranged in solid sheets and separated by a fibrovascular stroma. Neoplastic cells had indistinct cell borders; a moderate amount of eosinophilic to amphophilic cytoplasm; large, round, and often eccentric nuclei, with finely stippled chromatin; and 1 to 2 prominent nucleoli (Fig 3C). The mitotic index was 22 per 10 high-power fields. Moderate anisocytosis and anisokaryosis were observed, and multifocal areas of necrosis were noted in the neoplasm. The cranial two-thirds of the right hepatic lobe were effaced by neoplastic germ cells that were similar to those described in the testes (Fig 3D). In addition to the neoplastic lesions, the bird had severe atherosclerosis with calcification, ossifying and cartilaginous metaplasia in the wall of the major arteries, and moderate pulmonary edema.

[FIGURE 2 OMITTED]

To further characterize the neoplastic cells, transmission electron microscopic examination was performed with formalin-fixed sections of the testicular neoplasm. Ultrastructurally, the neoplastic cells contained a single, large nuclei and abundant cytoplasm, with evenly dispersed organelles, including mitochondria, abundant particulate glycogen, and rough endoplasmic reticulum (Fig 4A). The nuclei were roughly round and contained one or multiple prominent nucleoli. Neoplastic cells were occasionally connected by desmosome-like formations (Fig 4B). The histologic and ultrastructural characteristics of the neoplastic cells were compatible with germ cells, and the final diagnosis was bilateral testicular seminoma with hepatic metastatic involvement.

Discussion

In this report, we describe a case of bilateral testicular seminoma with hepatic metastasis. To our knowledge, this is the first such case to be reported in a cockatiel. The main clinical signs for the bird was moderate to severe dyspnea, and ultrasonographic examination revealed hypoechoic coelomic and hepatic nodules. The postmortem examination revealed bilaterally enlarged testicles and the liver contained a firm, white-tan focus. The testicle of a healthy bird can increase substantially in size by 300-fold to 500-fold during the breeding season. (2) Therefore, bilateral testicular hyperplasia could not be excluded from the differential diagnoses based on the gross finding. The size of liver varies among species, and the right lobe is generally larger in Psittaciformes, (3) which was noticed in this case. The testicular and hepatic masses were histologically diagnosed as malignant seminoma, and the neoplastic cells were further characterized by transmission electron microscopy.

Seminoma is a primary neoplasm of the testis, arising from germinal epithelium of seminiferous tubules. (4) The neoplasm is grossly gray to white in appearance. Histologically, seminomas consist of polyhedral germ cells either within seminiferous tubules or arranged in extratubular solid sheets, (4) and the latter type was seen in this case. The ultrastructural appearance of the seminoma cells in this bird was similar to that described in dogs (5) and humans, (6) such as frequent mitochondria, abundant glycogen deposition, and occasional desmosome-like formations. Seminoma is most commonly seen in dogs but has also often been reported in the stallion, especially in cryptorchid testicles. (4) In addition, seminomas have been reported in rams, bulls, goats, and cats, (4) as well as in birds, (7-11) although the occurrence is rare. Other primary testicular neoplasms in domestic animals are Sertoli cell tumors, interstitial cell tumors, and teratomas. (4)

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

Reported testicular tumors in birds include seminoma, Sertoli cell tumor, interstitial cell tumor, lymphosarcoma, undifferentiated sarcoma, and teratoma. (12,13) resticular tumors occur with high incidence in budgerigars (Melopsittacus undulatus). (12,14 17) Although relatively rare, seminomas have been reported multiple times in psittacine species. (14-18) In a 10-year survey (14) of neoplasia in pet birds, 43 seminomas were reported, and budgerigars were markedly over-represented (more than 88% of the seminomas were reported in budgerigars). In another survey, (18) seminomas were reported in 22 budgerigars and an Amazon parrot (Amazona species). More recently, in a 7-year retrospective postmortem survey, 21 seminoma cases in a population of 54 companion birds (39%) were identified, and 4 of those 21 cases (19%) were found in cockatiels without metastasis. Sertoli cell tumors have been reported in cockatiels with metastasis to the liver in 2 cases. (15) Metastatic seminomas are not common, but metastasis to kidney and spleen has been reported in companion birds. (15,18) In nonpsittacine species, seminomas have been reported in domestic fowl, mallard duck (Anas platyrhynchos), guinea fowl (Numida meleagris), dove (Streptopelia turtur), pigeon (Columba livia), swan (Cygnus species), Jardine's babbler (Turdoides bicolor), turkey, and quail (Coturnix species). (7-12,19-22) Multiple visceral metastases of unilateral seminomas were recently reported (9) in a mallard duck (11) and in a guinea fowl. A seminoma in a monorchid guinea fowl without metastasis has been described. (19) In birds, seminomas are usually unilateral (7,11). however, bilateral seminomas have been described in a black swan (Cygnus atratus) (10) and a duck. (8)

The most common clinical presentations reported with testicular neoplasia are coelomic distension, (17) anorexia, lethargy, and dyspnea. (12,13,15,16) Signs of feminization, such as brown hypertrophy of the cere, are frequently encountered in older budgerigars with gonadal neoplasms, most commonly functional Sertoli cell tumors and infrequently seminomas, (13) with an unknown pathophysiologic process. This cockatiel was presented with lethargy and dyspnea. The described clinical signs can be attributed to the mass effect of the tumor displacing and compressing the coelomic organs and the caudal air sacs. In addition, atherosclerosis along with pulmonary edema may have exacerbated the clinical signs. Radiographs and ultrasound were important diagnostic tools in this case. Coelios-copy was not performed because of the limited air space present in the coelom in this particular case. Cytologic examination of a fine-needle biopsy sample, which has been reported as a reliable antemortem diagnostic technique for diagnosis of seminoma in dogs (23) and humans, (24) could be performed. Cytologic evaluation of fine-needle aspirates from a seminoma has been reported in a rock dove (Columba livia). (7) Renal neoplasia, orchitis, adrenal neoplasia, and natural variations in testicular size concurrent with the breeding season, in addition to testicular neoplasia, are important differentials for a coelomic mass in this location in male birds. (20) Various treatment modalities have been attempted, including surgical removal, chemotherapy, radiation therapy, and hormonal therapy, with mixed results dependent on the species affected. (15) Surgical removal is the treatment of choice; however, because of the short length of vessels supplying blood to the testes, surgical resection of a testicular mass in birds is difficult. (20) Attempts at surgical removal in 3 cockatiels with seminomas have been reported; one died during recovery from surgery. (15) A cockatiel with complete removal was still alive at 39 months. One cockatiel with incomplete removal of a seminoma was treated with transcoelomic orthovoltage radiation, which resulted in complete resolution with an 18-month follow-up. (15) Minimally invasive endoscopic orchiectomy may provide a better alternative for safely removing a neoplastic testis in an avian patient diagnosed with a seminoma. (25)

References

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Ahmad Saied, DVM, Hugues Beaufrere, Dr Med Vet, Thomas N. Tully Jr, DVM, MSc, Dipl ABVP (Avian), Dipl ECZM (Avian), and Nobuko Wakamatsu, DVM, PhD, Dipl ACVP

From the Departments of Pathobiological Sciences (Saied, Wakamatsu) and Veterinary Clinical Sciences (Beaufrere, Tully), School of Veterinary Medicine, Louisiana State University, Skip Bertman Dr, Baton Rouge, LA 70803, USA.
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Author:Saied, Ahmad; Tully, Thomas N., Jr.; Wakamatsu, Nobuko
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Geographic Code:1USA
Date:Jun 1, 2011
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