Disseminated pancreatic adenocarcinoma in an eclectus parrot (Eclectus roratus)

Alexandre B. Le Roux 1Department of Diagnostic Imaging, Animal Medical Center, New York, NY 10065.

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Katherine Quesenberry 2Department of Avian and Exotic Medicine, Animal Medical Center, New York, NY 10065.

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Kyle A. Donnelly 2Department of Avian and Exotic Medicine, Animal Medical Center, New York, NY 10065.

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Taryn A. Donovan 3Department of Anatomic Pathology, Animal Medical Center, New York, NY 10065.

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Abstract

CASE DESCRIPTION

A 15-year-old 0.412-kg (0.906-lb) sexually intact male eclectus parrot (Eclectus roratus) was evaluated because its owners found it lethargic and dyspneic at the bottom of its cage.

CLINICAL FINDINGS

The parrot was thin and had generalized muscle wasting, diffuse feather loss, pale mucous membranes, and melena. The coelomic cavity was distended and soft on palpation, with coelomic effusion suspected. Results of a CBC indicated leukocytosis with left shift heterophilia, including toxic heterophils, lymphopenia, and anemia. Plasma biochemical analyses revealed severe hyperamylasemia.

TREATMENT AND OUTCOME

Radiography revealed no evidence of a metallic foreign body but severe loss of coelomic detail, suggestive of a coelomic mass, coelomic effusion with coelomitis, or both. Ultrasonography and CT revealed severe accumulation of coelomic fluid; a large, heterogeneous, irregularly marginated, and moderately vascularized mass in the caudal aspect of the coelomic cavity; and multiple hepatic, coelomic, and pulmonary nodules. On the basis of a poor prognosis, the parrot was euthanized. Necropsy results confirmed exocrine pancreatic adenocarcinoma, with disseminated metastases in the liver, gastrointestinal tract, coelomic cavity, and lungs.

CLINICAL RELEVANCE

In birds, pancreatic adenocarcinoma is rarely reported but should be considered a differential diagnosis for hyperamylasemia, coelomic mass, coelomic effusion, or abnormal gastrointestinal signs, alone or in combination. Ultrasonography and CT can be useful in further evaluating such patients and should be considered in the diagnostic plan.

Abstract

CASE DESCRIPTION

A 15-year-old 0.412-kg (0.906-lb) sexually intact male eclectus parrot (Eclectus roratus) was evaluated because its owners found it lethargic and dyspneic at the bottom of its cage.

CLINICAL FINDINGS

The parrot was thin and had generalized muscle wasting, diffuse feather loss, pale mucous membranes, and melena. The coelomic cavity was distended and soft on palpation, with coelomic effusion suspected. Results of a CBC indicated leukocytosis with left shift heterophilia, including toxic heterophils, lymphopenia, and anemia. Plasma biochemical analyses revealed severe hyperamylasemia.

TREATMENT AND OUTCOME

Radiography revealed no evidence of a metallic foreign body but severe loss of coelomic detail, suggestive of a coelomic mass, coelomic effusion with coelomitis, or both. Ultrasonography and CT revealed severe accumulation of coelomic fluid; a large, heterogeneous, irregularly marginated, and moderately vascularized mass in the caudal aspect of the coelomic cavity; and multiple hepatic, coelomic, and pulmonary nodules. On the basis of a poor prognosis, the parrot was euthanized. Necropsy results confirmed exocrine pancreatic adenocarcinoma, with disseminated metastases in the liver, gastrointestinal tract, coelomic cavity, and lungs.

CLINICAL RELEVANCE

In birds, pancreatic adenocarcinoma is rarely reported but should be considered a differential diagnosis for hyperamylasemia, coelomic mass, coelomic effusion, or abnormal gastrointestinal signs, alone or in combination. Ultrasonography and CT can be useful in further evaluating such patients and should be considered in the diagnostic plan.

A 15-year-old 0.412-kg (0.906-lb; reference range, 0.347 to 0.512 kg [0.763 to 1.126 lb]1) sexually intact male eclectus parrot (Eclectus roratus) was evaluated because its owners found it acutely lethargic and dyspneic at the bottom of its cage. The husbandry and diet of the parrot were considered adequate. On physical examination, the parrot was thin, with pectoral muscle atrophy (keel score2 of 2 on a scale of 1 [emaciated] to 5 [obese]) and general muscle wasting, and the parrot had diffuse absence of covert and downy feathers over the sternum, back, legs, and inner wings, consistent with feather destructive behavior. At rest, the parrot had a respiratory rate of approximately 30 breaths/minute (reference range, 24 to 45 breaths/min1) and a heart rate of approximately 200 beats/minute (reference range, 150 to 300 beats/min3). The coelomic cavity was distended and soft on palpation, and coelomic effusion was suspected. In addition, the parrot had pale mucous membranes, and melena was observed in its feces. Our initial differential diagnosis list was broad, with consideration given to neoplasia and infectious disease (eg, bacterial, mycobacterial, Chlamydia psittaci, fungal, or protozoal infection). Heavy metal toxicosis could not be completely ruled out, and bacterial enteritis or ventricular or intestinal foreign body were also considered given the presence of melena.

Results of a CBC indicated lymphopenia (955 lymphocytes/μL; reference range, 2,870 to 7,120 lymphocytes/μL4) and leukocytosis (19,100 leukocytes/μL; reference range, 9,000 to 15,000 leukocytes/μL4), characterized with a left shift heterophilia, with toxic heterophils (15,471 heterophils/μL; reference range, 5,750 to 8,750 heterophils/μL4), mild eosinophilia (573 eosinophils/μL; reference range, 0 to 120 eosinophils/μL4), and mild basophilia (382 basophils/μL; reference range, 0 to 120 basophils/μL4). In addition, the parrot was anemic (Hct, 22%; reference range, 45% to 55%4), likely with nonregenerative anemia because polychromasia was not reported. Results of plasma biochemical analyses indicated high activities of creatine kinase (968 U/L; reference range, 118 to 345 U/L4) and amylase (> 36,000 U/L; reference range, 200 to 645 U/L4) and a high concentration of uric acid (25.6 mg/dL; reference range, 2.5 to 8.7 mg/dL4). The parrot had low plasma concentrations of albumin (0.50 g/dL; reference range, 1.23 to 2.26 g/dL4), total protein (1.4 g/dL; reference range, 3.0 to 5.0 g/dL4), cholesterol (79 mg/dL; reference range, 130 to 350 mg/dL4), and bile acids (21.4 μmol/L; reference range, 30.0 to 110.0 μmol/L4). Results were within reference limits for all other plasma analytes, including concentrations of lead (< 3.30 μg/dL; reference limit, < 6 μg/dL) and zinc (0.8 ppm; reference range, 0.8 to 2.5 ppm).

Whole-body, standing dorsoventral (box shot) radiography was performed without sedation to assess whether metallic foreign material was in the gastrointestinal tract and whether a large amount of fluid, a mass, or both was in the coelomic cavity. Findings included no evidence of metallic opaque foreign material but severe loss of coelomic detail, suggestive of a coelomic mass, coelomic effusion with coelomitis, or both in the caudal aspect of the coelomic cavity (Figure 1). Radiographic assessment of the coelomic organs was limited because of loss of coelomic detail and the standing box positioning used.

Figure 1—
Figure 1—

Whole-body, standing dorsoventral (box shot) radiographic image of a 15-year-old 0.412-kg (0.906-lb) sexually intact male eclectus parrot (Eclectus roratus) evaluated for a sudden onset of lethargy and dyspnea. There is severe loss of coelomic detail in the caudal aspect of the coelomic cavity (arrow), suggestive of coelomic effusion, a coelomic mass, or both.

Citation: Journal of the American Veterinary Medical Association 257, 6; 10.2460/javma.257.6.635

Because of suspected coelomic effusion, coelomic ultrasonography was performed for further assessment (Figure 2). A large (approx 3-cm-diameter), heterogeneously iso- to hypoechoic mass with irregular margins was observed centrally in the caudal aspect of the coelomic cavity. This mass was closely associated with the liver and loops of small intestines, which were distended with hypoechoic fluid and had segmental areas of irregular mural thickening. These abnormal findings for the small intestines could have explained the parrot's melena. A large amount of hypoechoic fluid was present in the coelomic cavity, and multiple small, broad-based homogeneously isoechoic nodules were observed disseminated along the coelomic wall. The primary origin of the large coelomic mass was difficult to determine ultrasonographically because of its close relation with several coelomic organs; however, considering the ultrasonographic features combined with the abnormalities detected on blood work, a pancreatic origin was highly suspected, with other organs of origin (eg, liver, intestine, or mesentery) also considered. Regarding the type of mass, a malignant neoplasm (eg, carcinoma or round cell neoplasia) with metastases was primarily considered; however, disseminated pyogranulomatous inflammation had not been ruled out.

Figure 2—
Figure 2—

Transverse ultrasonographic images of the coelomic cavity of the parrot in Figure 1 obtained at the cranial (A) and caudal (B) aspects of the coelomic cavity. A large (approx 3-cm-diameter) heterogeneously iso- to hypoechoic mass (arrowheads; A and B) with irregular margins is present in the coelomic cavity. This mass is closely associated with loops of hypoechoic fluid-filled and distended small intestines (asterisks; A and B) that have segmental areas of irregular mural thickening (double-headed arrow; B). A small, broad-based nodule (single-headed arrow; B) is evident on the coelomic wall, and a moderate accumulation of hypoechoic coelomic fluid is present.

Citation: Journal of the American Veterinary Medical Association 257, 6; 10.2460/javma.257.6.635

Fine-needle aspirate samples of the coelomic fluid and the large coelomic mass were obtained with ultrasonographic guidance. After preparation including cytocentrifugation and staining with H&E stain, cytologic examination revealed cells that were round to slightly polygonal, were loosely to tightly aggregated, had small to moderate amounts of medium blue cytoplasm, and had oval nuclei with fine to coarsely stippled chromatin and often multiple prominent nucleoli. These cells displayed mild to moderate anisocytosis and anisokaryosis with occasional karyomegaly and multinucleation. Up to 10-fold nuclear pleomorphism was identified in the neoplasm. Scattered heterophils and vacuolated macrophages were found in the background. On the basis of the presence of cellular and nuclear pleomorphism, karyomegaly, and multinucleation, malignant neoplasia was suspected. The cytologic interpretation for the coelomic mass was a neoplasm of epithelial origin, because of the cohesive nature of the cells; however, the definitive cell of origin was unknown, and gonadal origin was not ruled out. Carcinoma was considered most likely, and atypical sarcoma was considered less likely.

The parrot underwent general anesthesia for whole-body CT.a Anesthesia was induced with isoflurane in oxygen, delivered by face mask. Intubation was achieved with a 3.5-mm-internal-diameter noncuffed endotracheal tube, and anesthesia was maintained with isoflurane (vaporizer setting, 1.5%) in oxygen (3 L/min) with intermittent positive-pressure ventilation. A 24-gauge, 0.75-inch catheter was placed in the basilic vein of the left wing, and the parrot was positioned in dorsal recumbency, with its wings extended and taped laterally. On CT, images were acquired in soft tissue window (window width, 250 HU; window level, 60 HU) and lung window (window width, 2,500 HU; window level, −200 HU) before and after administration of a nonionic iodinated contrast medium (iohexolb [300 mg iodine/mL]; 2.2 mL/kg [1.0 mL/lb], IV). Computed tomography revealed a soft tissue–attenuating (precontrast attenuation, 45 to 50 HU; postcontrast attenuation, 90 to 95 HU), moderately vascularized mass that had heterogeneous contrast enhancement (Figure 3). Central areas of the mass that lacked contrast enhancement (25 to 30 HU) were evident and could have represented intralesional cysts or necrosis. The mass occupied much of the caudal aspect of the coelomic cavity, was primarily on midline to slightly right of midline, and closely associated with loops of small intestine, which were abnormally distended with gas and fluid. This mass displaced most of the small intestine cranially and extended along the portal system to the level of the right caudal margin of the liver. The parrot's hepatic parenchyma had heterogeneous contrast-medium enhancement, with multiple hypoattenuating intraparenchymal nodules (postcontrast attenuation, 60 to 65 HU) of various sizes. Numerous soft tissue–attenuating, homogeneously contrast-enhancing, broad-based nodules (precontrast attenuation, 40 to 45 HU; postcontrast attenuation, 80 to 85 HU) were evident along the parietal and visceral coelomic surfaces, and there was a large amount of coelomic fluid (10 to 15 HU). Throughout the pulmonary parenchyma, several round, soft tissue–attenuating nodules (precontrast attenuation, 55 to 60 HU) were observed and ranged in size from 3 to 5 mm in diameter. The proventriculus was moderately distended with ingesta and gas. For the large mass, a malignant neoplasm of pancreatic origin was considered most likely, and carcinoma, with carcinomatosis and pulmonary and hepatic metastases, was suspected. A poor prognosis was given, and the owners elected euthanasia for the parrot.

Figure 3—
Figure 3—

Dorsal (A and E), sagittal (B), and transverse (C and D) multiplanar reconstruction CT images of the parrot in Figures 1 and 2 before (E) and after (A through D) administration of contrast medium, with the plane of each CT image depicted by the dotted line in the panel's inset image. In the caudal aspect of the coelomic cavity is a large, soft tissue–attenuating, moderately vascularized mass (asterisks; A through C) that has heterogeneous contrast-medium enhancement and numerous soft tissue–attenuating, broad-based nodules (arrowheads; A through C). The hepatic parenchyma has heterogeneous contrast-medium enhancement and multiple hypoattenuating intraparenchymal nodules (black arrows; A, B, and D) of various sizes. A large amount of coelomic fluid (pound sign) is present, and the proventriculus is moderately distended with ingesta and gas (double-headed arrows; A, B, and D). In the lungs, there are several round (approx 3 to 5 mm in diameter) soft tissue–attenuating nodules (white arrows; E). A through D—Images displayed in a soft tissue window (window width, 250 HU; window level, 60 HU; slice thickness, 1 mm). E—Image displayed in a lung window (window width, 2,500 HU; window level, −200 HU; slice thickness, 1 mm).

Citation: Journal of the American Veterinary Medical Association 257, 6; 10.2460/javma.257.6.635

Postmortem examination of the parrot confirmed the presence of multifocal to coalescing nodules in the region of the pancreas, with local dissemination throughout the coelom, body wall, air sacs, and intestinal serosa and distant metastases to other organs, including the liver and lungs (Figure 4). The coelomic cavity contained approximately 75 mL of amber-colored effusion. The proventriculus and duodenum were severely distended, whereas the remainder of the small intestines were less distended. The parrot's oral cavity and cloaca macroscopically appeared clinically normal. Results of histologic examination of the mass were consistent with adenocarcinoma of the exocrine pancreas. The mass had intralesional hemorrhage, necrosis, and desmoplasia. Neoplastic cells contained bright pink zymogen granules in the cytoplasm, had frequent mitotic figures (> 100 in 10 hpf [40 × magnification or 2.37 mm2]), and had substantial cellular and nuclear pleomorphism, indicative of a more aggressive biological behavior. In some regions of the neoplasm, there were transitions from exocrine to ductular morphology, in which tubuloacinar structures were observed. There was a predominant acinar morphology of the pancreatic adenocarcinoma; however, a small section of the pancreas contained neoplastic cells that exhibited both exocrine and ductular morphologies. There was evidence of intravascular invasion, with distant metastases confirmed in the liver, lungs, and regional air sacs. Local coelomic dissemination was also observed, with metastatic neoplasia over the serosa of the ventriculus, small intestines, intestinal mesentery, and abdominal air sacs. Mild, scattered inflammatory infiltrates were observed at the periphery of the pancreatic nodules, comprised predominantly of lymphocytes and plasma cells, with rare foci of heterophilic, histiocytic inflammation and accumulation of hemosiderin. Regions of tumor necrosis were present and accompanied with fibrinous exudate, cysts, fat necrosis, hemorrhage, and fibrosis. No evidence of pancreatitis was present. In addition, results were negative for a PsHV PCR assay performed at the Zoological Medicine and Wildlife Disease Laboratory, University of Florida College of Veterinary Medicine on FFPE sections of the pancreas as previously described.5

Figure 4—
Figure 4—

Necropsy images of the coelomic cavity and viscera, with the duodenal loop and coelomic mass exteriorized (A), isolated cranial aspect of the liver (D), and isolated right lung lobe (E) and photomicrographs of the pancreas and duodenum (B), coelomic mass (C), and pulmonary nodule (F) of the parrot in Figure 1. A—Visible are a large (approx 4.5 × 2.8 × 3.5-cm), tan and mottled pink to red, firm mass (arrowheads) and the duodenal loop with similar appearing nodules (arrow). Bar = 5 mm. B—Between 2 sections of duodenum (asterisks) is a section of pancreas (arrow) with multifocal to coalescing neoplastic nodules. H&E stain; bar = 500 μm. C—This high magnification photomicrograph of the large coelomic mass, which was diagnosed as pancreatic adenocarcinoma, shows neoplastic cells with pink zymogen granules (thin horizontal arrows) in the cytoplasm and resembling exocrine pancreatic epithelial cells. Mitotic figures (thick vertical arrow) are frequent, and there is up to 5-fold nuclear pleomorphism (thick horizontal arrow). H&E stain; bar = 20 μm. D—Superficially and throughout the hepatic parenchyma are multifocal to coalescing, firm, tan to light red nodules (≤ 9 mm in diameter) of pancreatic adenocarcinoma (arrow). Bar = 5 mm. Inset—Photomicrograph of hepatic parenchyma (asterisk) between 2 metastatic nodules of pancreatic adenocarcinoma (pound signs). H&E stain; bar = 200 μm. E—A focal, 5-mm-diameter nodule (arrow) is observed protruding from lung parenchyma. Bar = 5 mm. F—Photomicrograph of a margin of a pulmonary nodule (most of the image) adjacent to lung parenchyma (far right of the image). The nodule is comprised of epithelial cells forming acinar structures (vertical arrows) with features of the exocrine pancreas, including pink zymogen granules (horizontal arrows) in the cytoplasm. H&E stain; bar = 20 μm.

Citation: Journal of the American Veterinary Medical Association 257, 6; 10.2460/javma.257.6.635

Discussion

Anatomically, the pancreas in birds is enclosed by the duodenum, which is arranged in a narrow, U-shaped loop, with the ascending and descending duodenal segments tightly held together by the mesentery. In most avian species, the pancreas has 3 ducts and lobes, with 2 main lobes (a dorsal and a ventral lobe) in the U-shaped duodenal loop and a third lobe (a splenic lobe) that extends from the dorsal lobe to beyond the duodenum.6–8 Clinically normal pancreas cannot be routinely identified with ultrasonography or CT because of the small size of the pancreas in birds,9 and to our knowledge, there is no reported description for diagnostic imaging of clinically normal pancreatic anatomy in birds.

Although CT findings for a yellow-naped Amazon parrot (Amazona auropalliata) with acute pancreatitis has been reported,10 to our knowledge, the present report is the first to describe ultrasonographic and CT findings for a bird with pancreatic adenocarcinoma. Pancreatic carcinoma is uncommon in birds, with, to our knowledge, only 8 instances reported, including in a yellow-naped Amazon parrot,11 chicken,12 mynah bird,13 parakeet,14 guinea fowl,15 cockatiels,16,17 and macaw.18 In 611–15,18 of these 8 affected birds, pancreatic carcinoma was diagnosed postmortem. An infiltrative, poorly marginated pancreatic mass was commonly observed macroscopically, with associated loss of the clinically normal pancreatic architecture, frequent infiltration of the adjacent small intestine, and the presence of coelomic effusion. In the most severely affected patients,17 numerous adhesions bunched the intestines and other organs into nearly a solid mass. Only 2 reports16,17 describe findings for diagnostic imaging in birds with pancreatic carcinoma. In 1 of the affected birds, an oval mass with soft tissue opacity that had a rim with mineral opacity was observed dorsal to the ventriculus, and radiographic images obtained had decreased coelomic serosal detail,16 similar to the parrot of the present report. For the second bird, gastrointestinal barium contrast radiography revealed a soft tissue opaque mass that was in the central aspect of the coelomic cavity and that caused centripetal displacement of the small intestine and caudal displacement of the cloaca, consistent with a centrally located coelomic mass.17

Of 8 reported11–18 birds with pancreatic carcinoma, 411,15,17,18 were confirmed to have had exocrine pancreatic differentiation. Pancreatic carcinoma displays aggressive biological behavior in people, cats, and dogs, and may arise from the ductular cells or acinar cells.19 In a study19 of 34 cats, 5 of 34 (15%) cats with exocrine pancreatic carcinoma were diabetic, and in people, diabetes is a predisposing factor to developing pancreatic carcinoma.20,21 Diabetes mellitus has been reported14,22,23 in birds, including a parakeet with islet cell carcinoma and a blue and gold macaw with pancreatic adenocarcinoma. In contrast, the parrot of the present report was euglycemic, excluding diabetes mellitus.

Exocrine pancreatic insufficiency secondary to exocrine pancreatic parenchymal effacement by neoplastic tissue has been reported11 in a yellow-naped Amazon parrot with a pancreatic exocrine adenocarcinoma. Exocrine pancreatic insufficiency was diagnosed with specific pancreatic function assessments (ie, triglyceride tolerance test and fecal evaluations for trypsin and neutral and split fats) not performed for the eclectus parrot of the present report; however, severe hyperamylasemia was detected in the eclectus parrot, and measurement of serum amylase activity is recommended for the diagnosis of pancreatic disease in avian species.17,24 Particularly, serum amylase activity > 1,500 U/L should lead clinicians to consider acute pancreatitis in birds with signs of abdominal pain or gastrointestinal abnormalities.24 The lack of pancreatitis in the parrot of the present report, however, suggested that the finding of severe hyperamylasemia in birds (> 36,000 U/L) is not a specific marker of pancreatitis and could also be associated with noninflammatory causes, as reported in dogs and cats.25 In addition, the parrot of the present report had a high plasma concentration of uric acid, a common indicator of renal disease in birds; however, the parrot's kidneys were macroscopically and histologically normal on postmortem examination. Other causes of high plasma concentration of uric acid in birds includes severe tissue necrosis, severe dehydration, or starvation,26 a combination of which could have explained hyperuricemia in our patient.

Results of studies27–29 suggest that viral infection could be associated with pancreatic oncogenesis in birds, in that guinea fowl inoculated with avian osteopetrosis retroviruses strains Pts-56 and MAV-2(0) later had a high incidence of multifocal pancreatic neoplasms of various differentiation and malignancy. Development of pancreatic adenocarcinoma in chickens inoculated with myelocytomatosis virus strain MC29 has also been reported.28 Those findings suggest that life-long viremia that induces repeated injuries to pancreatic cells could be associated with pancreatic tumorigenesis in birds. Similarly, biliary and pancreatic duct carcinoma has been reported in birds with internal papillomatosis and PsHV 1, genotype 3.18,30–33 However, the pancreatic carcinomas in those birds were ductular in origin, whereas, to our knowledge, acinar pancreatic carcinoma has not yet been reported in association with PsHV. Similarly, the parrot of the present report had predominantly acinar morphology of its pancreatic carcinoma and no cloacal or oral cavity papillomas, which suggested that chronic infection with PsHV was unlikely. This was supported with negative postmortem results for the PsHV PCR assay performed on FFPE sections of the parrot's pancreas. Although fresh tissue is recommended for the PsHV PCR assay,34 the test can detect PsHV DNA in FFPE tissue sections.35 Nonetheless, negative results of a PsHV PCR assay on FFPE tissue sections should be interpreted with caution because multiple factors (eg, duration of formalin fixation, differences in formalin permeability in tissues, and tissue sample thickness) could affect the DNA integrity of the sample and the ability for the assay to detect PsHV DNA in FFPE tissues,34,35 and a false-negative result for the parrot of the present report could not be completely excluded.

The present report, to our knowledge, was the first to describe ultrasonographic and CT findings for a bird with pancreatic adenocarcinoma and highlighted the need to include pancreatic adenocarcinoma as a differential diagnosis for severe hyperamylasemia in birds, instead of limiting the potential diagnosis to acute pancreatitis. Furthermore, in birds with accumulation of coelomic fluid, advanced diagnostic imaging (eg, ultrasonography and CT) coupled with coelomic fluid evaluation should be considered, and pancreatic neoplasia should be included in the list of differential diagnoses, especially in the presence of a coelomic mass.

Acknowledgments

The authors declare that there were no conflicts of interest. The authors thank Dr. Jamie L. Haddad for help with the cytologic interpretations.

ABBREVIATIONS

FFPE

Formalin-fixed paraffin-embedded

PsHV

Psittacid herpesvirus

Footnotes

a.

Aquilion 64, Canon Medical Systems USA Inc, Tustin, Calif.

b.

Omnipaque 300, GE Healthcare, Princeton, NJ.

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