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Pericardial mesothelioma in a yellow-naped amazon parrot (Amazona auvopalliata).

Abstract: A 37-year-old female yellow-naped Amazon parrot (Amazona auropalliata) was presented with a history of lethargy, inappetence, and decreased vocalizations. On examination, the coelom was moderately distended and palpated fluctuant, and the heart was muffled on auscultation. Coelomic ultrasound, coelomocentesis, and radiographs were performed and revealed an enlarged cardiac silhouette and marked coelomic effusion. Pericardial effusion was confirmed by echocardiography. A well-circumscribed, hyperechoic soft tissue density was observed at the level of the right atrium on initial echocardiography; however, a cardiac mass was not identified by computed tomography scan or repeat echocardiograms. Ultrasound-guided pericardiocentesis was performed under anesthesia, and cytology results were consistent with hemorrhage; no neoplastic cells were identified. A repeat echocardiogram 4 days after pericardiocentesis revealed recurrence of the pericardial effusion. Due to the grave prognosis, the owners declined endoscopic pericardiectomy, and the patient died the following day. On postmortem examination, the pericardial surface of the heart was covered in a white to yellow, multinodular mass layer. Histologic analysis revealed a multinodular mass extending from the atria, running along the epicardium distally, and often extending into the myocardium. Neoplastic cells present in the heart mass and pericardium did not stain with a Churukian-Schenk stain, and thyroglobulin immunohistochemistry was negative. Cytokeratin and vimentin stains showed positive expression in the neoplastic cells within the mass. These results are consistent with a diagnosis of mesothelioma. This is the first report of mesothelioma in a psittacine bird.

Key words: mesothelioma, neoplasia, avian, yellow-naped Amazon parrot, Amazona auropalliata

Clinical Report

A 37-year-old female yellow-naped Amazon parrot (Amazona auropalliata) was examined because of a 1-week history of lethargy, inappetence, and decreased vocalization. The parrot had been examined for suspected heavy metal toxicosis 2 years before. At that time, the parrot was diagnosed with degenerative joint disease of both stifles, bilateral corneal opacities of unknown etiology, and posttraumatic remodeling of previous left humeral and distal radial fractures. The parrot had been acquired from a private breeder at a young age, and the diet consisted of seeds, nuts, dried fruit, and fresh vegetables.

On examination, the parrot was bright, alert, and responsive. The bird weighed 450 g and was thin, with a body condition score of 3/9. The coelom was moderately distended and palpably fluctuant. The heart rate was 280 beats/min, and heart sounds were muffled on auscultation; however, no obvious murmurs or arrhythmias were detected. The respiratory rate was 40 breaths/min, and moderate crackles were auscultated over the air sacs and lungs. Irregular, 2-3 mm diameter white corneal plaques were present bilaterally. The parrot's respiratory effort increased mildly during examination, but recovery time appeared normal.

[FIGURE 1 OMITTED]

The patient was admitted to the hospital for diagnostic testing and supportive care and was placed in an oxygen cage with heat support (29.4[degrees]C [85[degrees]F]). A blood sample collected from the right jugular vein was submitted for a complete blood cell count (CBC) and plasma biochemical profile. Results of the CBC revealed hemoconcentration (packed cell volume 53% with 1+ polychromasia; reference interval, 44%-49%) and a moderate leukopenia (4.5 x [10.sup.3] cells/[micro]L; reference interval, 6-11 x 103 cells/pL) characterized by a marked lymphopenia (6%; reference interval, 20% 45%) and severe relative heterophilia (92%; reference interval, 55%-80%). (1) Plasma biochemical analysis results showed a decreased albumin : globulin ratio (0.5; reference interval, 1.9-5.0), marked hypoalbuminemia (0.8 g/dL; reference interval, 1.9-3.52 g/dL), increased aspartate aminotransferase (501 U/L; reference interval, 130-350 U/L) and creatine kinase activities (2340 U/L; reference interval, 55345 U/L), and decreased lactate dehydrogenase activity (45 U/L; reference interval 155-425 U/L). (1)

Coelomic ultrasonography was performed with the bird under manual restraint and revealed marked coelomic effusion. Free fluid was noted predominantly surrounding the liver; however, a focal accumulation of fluid was present adjacent to the liver, suggesting a cystic structure. A portion of the coelomic effusion (14 mL) was removed via ultrasound-guided fine needle aspiration; it was clear with a green-brown coloration. Because of financial constraints of the owners, cytology of the fluid was not pursued. To minimize respiratory distress associated with positioning in dorsal recumbency, radiographs were not performed until after the ultrasound-guided coelomocentesis. Anesthesia was induced and maintained with isoflurane in 100% oxygen for whole-body right lateral and ventrodorsal radiographs (Fig 1). There was marked soft tissue enlargement of the caudal coelomic cavity with left lateral displacement of the ventriculus and intestines. A rounded soft tissue margin was present caudodorsal to the heart, compatible with a markedly enlarged liver or effusion. The cardiac silhouette appeared globoid, and the cardiac silhouette width: thorax width ratio was increased compared to published normal values for medium-sized psittacine birds (66%; reference interval, 51%-61%). (2) The abdominal air sacs were not observed, and the thoracic air sacs were diminished in size. The patient recovered from anesthesia with minimal complications.

The next day, echocardiography revealed a moderate volume of pericardial effusion that did not appear to be causing significant tamponade (Fig 2). All cardiac chambers appeared normal in size, and systolic function was subjectively normal. A well-circumscribed hyperechoic soft tissue density was observed at the level of the right atrium. Differential diagnoses included a mass, fibrin, or a normal structure highlighted by the effusion.

[FIGURE 2 OMITTED]

The patient was anesthetized as before, and coelomocentesis was performed with a 20-gauge intravenous catheter before positioning the parrot in dorsal recumbency. Coelomocentesis yielded 12 mL of fluid with a similar appearance to the previously collected coelomic effusion. A whole-body computed tomography scan was performed with a 40-slice scanner with a standard algorithm. Ioversol (0.5 mL/kg; Optiray 350, Mallinckrodt, Hazelwood, MO, USA) contrast solution was administered through a 24-gauge intravenous catheter placed in the right basilic vein. Moderate pericardial effusion with a Hounsfield unit of 12 was observed, suggesting protein or cellular content. No mass associated with the heart was observed on pre- or postcontrast images. Left caudolateral displacement of the ventriculus and intestines was confirmed due to coelomic effusion, and there was evidence of encapsulation of the fluid in some areas. The liver was normal size; however, the portal vein appeared equivocally enlarged. The thoracic air sacs were decreased in size with normal walls and contents, and the abdominal air sacs were completely collapsed.

While the patient was anesthetized, pericardiocentesis was performed by sonographic guidance, and 4 mL serosanguineous fluid was removed. Echocardiography after the pericardiocentesis did not show evidence of a mass, and the fluid was gone from the pericardial sac. Cytologic evaluation of the pericardial effusion revealed a very low cellularity and finely stippled pink background containing high numbers of erythrocytes admixed with small numbers of macrophages and rare reactive mesothelial cells. Erythrophagocytic and hemosiderin-laden subsets of macrophages were also seen. These findings were indicative of chronic and active hemorrhage (ie, hemopericardium). The parrot recovered uneventfully from anesthesia.

Echocardiography was repeated the following day without anesthesia, and trace pericardial effusion was seen. The heart was properly positioned and did not appear enlarged. Echocardiography of an apparently healthy 10-month-old female yellow-naped Amazon parrot was performed the same day for comparison. No obvious cardiac masses were observed in the patient when compared with the healthy parrot. Based on the results of the diagnostic tests, idiopathic pericardial effusion was suspected, although neoplasia could not be completely ruled out. Monitoring for clinical signs of cardiac insufficiency and frequent repeat echocardiograms were recommended.

Per recommendation of the cardiologist, echocardiography was performed 4 days after the pericardiocentesis and revealed recurrence of the pericardial effusion. The pericardial effusion was hyperechoic compared with the original effusion, possibly because of clotted blood or fibrin deposits within the pericardial cavity. Repeat pericardiocentesis was not performed because of the small amount of fluid present and the presence of structures between the pericardial sac and the body wall.

Endoscopic pericardiectomy was offered to the owner as the treatment of choice for recurrent idiopathic pericardial effusion or neoplastic pericardial effusion. The prognosis was considered grave because of the rapid recurrence of the pericardial effusion. The owner declined treatment options and elected to monitor quality of life at home with eventual euthanasia as deemed necessary. The parrot died at home the next day.

Necropsy revealed a strongly adherent, thickened pericardial sac containing serosanguineous fluid and clotted blood. The pericardial surface of the heart was covered in a white to yellow, multinodular tissue layer that circumferentially surrounded the atria and extended distally along the pericardium to the ventricles (Fig 3A). The abnormal tissue appeared to extend into the myocardium on cut section. Cytologic examination of an impression smear of the pericardial mass revealed cohesive polygonal cells with a low nuclear: cytoplasm ratio and extracellular amorphous eosinophilic material. Gross examination also revealed a prominent lymphatic vessel running along the trachea (lymphangiectasia). There was 5 mL serosanguineous fluid in the coelom and fibrinous adhesions between the intestines and body wall, indicating moderate multifocal active coelomitis. The liver was strongly adhered to the pericardial sac by a white, fibrous adhesion, suggestive of chronic coelomitis. Severe, regionally extensive pulmonary congestion and atelectasis were present. The right thyroid gland appeared diffusely mottled, tan to white, and enlarged, measuring 1 x 0.5 x 0.5 cm. On cut section, it had a green center with 1-2 mm of compressed tissue. The left thyroid gland was pink and measured 4X3X3 mm. Incidental gross findings were minimal multifocal ulcerative ventriculitis and bilateral focal chronic lipid keratopathy. Affected and routine tissues were collected and fixed in 10% neutral buffered formalin. Tissue sections were routinely processed, embedded in paraffin, sectioned, and stained with hematoxylin and eosin.

[FIGURE 3 OMITTED]

Histologic analysis revealed a multinodular mass extending from the atria, running along the epicardium distally, and often extending into the myocardium (Fig 3B). The mass was composed of cuboidal cells separated by fibrous trabeculae and arranged in anastomosing trabeculae, labyrinthine patterns, papillary projections, and follicular-like outlines. Neoplastic cells had variably distinct cell borders and contained round to oval nuclei, clumped chromatin, and a moderate amount of eosinophilic cytoplasm. Variable moderate anisokaryosis and anisocytosis were observed, with a mitotic index of 33 per 10 x 400 fields. Areas of necrosis were present throughout the mass, and aggregates of scattered lymphocytes and heterophils were present within and around the mass. Multiple foci of neoplastic cells similar to those described in the heart were seen on the visceral surface of the pericardium, extending into the pericardial wall (Fig 3C). Excessive fibrosis between the pericardium and liver suggested a desmoplastic response. Evaluation of the liver revealed hepatitis, bile duct proliferation, and congestion. There was degeneration and necrosis of much of the hepatic tissue. Severe thyroid glandular atrophy was present bilaterally. However, a large cyst-like region of central necrosis in the right thyroid gland made it appear enlarged compared to the left thyroid gland, which was comprised of low numbers of colloid-containing follicles. Examination of the lungs revealed pulmonary atelectasis, likely secondary to the coelontic effusion. Differentials for the heart and pericardial mass included ectopic thyroid carcinoma and mesothelioma.

Neoplastic cells did not stain with a Churukian-Schenk stain, making a tumor of neuroendocrine origin unlikely (Fig 3D). A portion of the formalin-fixed, paraffin-embedded mass and the left thyroid gland (control) were sent to the University of Pennsylvania Ryan Veterinary Hospital Diagnostic Laboratories for additional immunohistochemical analysis. Thyroglobulin immunohistochemistry showed positive expression in the normal thyroid follicular cells, but the neoplastic cells in the heart mass were negative. Vimentin and cytokeratin stains (AE1/AE3) were positively expressed in the control tissues and both were expressed within the mass (Fig 3E and F). These results are consistent with a diagnosis of mesothelioma. (3,4)

Additional environmental and occupational questioning of the owners was performed due to the postmortem diagnosis of mesothelioma. Questions were based on reported sources of human asbestos exposure and asbestos-containing products. (5-6) No risk factors for mesothelioma development were identified.

Discussion

This report describes the clinical signs and diagnosis of a pericardial mesothelioma in a yellow-naped Amazon parrot. To our knowledge, this is the first description of a mesothelioma in a psittacine bird.

Mesotheliomas are rare tumors of mesodermal origin that arise from the serosal lining of the pleural, peritoneal, and/or pericardial cavities, as well as the vaginal and testicular tunics. (7,8) Tumor spread is typically through invasion of contiguous tissue, and distant metastasis is rare. (9)

Asbestos exposure has been linked to the development of mesothelioma in both humans and dogs. (8,10) Other recognized risk factors for mesotheliomas in humans are nonasbestiform environmental exposures, ionizing radiation, viruses, and genetic susceptibility. (11) The etiology of mesothelioma in other species is unknown and considered spontaneous. (12) Spontaneous, or idiopathic. mesotheliomas have been documented in many species. (12,13) Spontaneous mesotheliomas are rarely reported in birds but have been diagnosed in chickens, a pheasant, a pigeon (Columba livid), and a ferruginous hawk (Buteo regalis). (13-15) Additionally, mesotheliomas have been induced in chickens by several viruses, most notably a strain of avian leukosis virus. (9,13)

As evidenced by this case report, the clinical diagnosis of pericardial mesothelioma is considered difficult. In human patients, it is estimated that 1 mesothelioma is undiagnosed for every 4-5 reported cases. (16) Difficulty of diagnosis of mesothelioma in dogs is attributed to clinical signs related to cavitary effusions rather than development of a discrete mass. (7)

The presenting clinical signs, physical examination findings, and results of noninvasive diagnostic testing in the Amazon parrot reported here were consistent with those of birds and dogs with both neoplastic and nonneoplastic pericardial effusion. Clinical signs are usually vague and may include lethargy, inappetence, weight loss, weakness, and exercise intolerance. (17,18) Physical examination findings are often related to hemodynamic impairment due to pericardial effusion and can include muffled heart sounds, ascites, dyspnea, tachycardia, and jugular vein distension. (4,18) The crackles auscultated over the lungs and air sacs of the Amazon parrot in this report were most likely referred noises due to the coelomic effusion. Furthermore, results from blood tests are often nonspecific in dogs with pericardial effusion, and the parrot's hematologic and biochemical values were suggestive of mild dehydration, muscle damage, stress, and inflammation and/or infection. (18) The cause of the leukopenia and hypoalbuminemia was uncertain, and acute or chronic inflammation or infection was a major differential diagnosis. On radiographs, a globoid heart may be appreciated in animals with pericardial effusion. (17-19) Additionally, birds with concurrent coelomic effusion may exhibit collapsed air sacs and decreased serosal detail on radiographs. (17) An electrocardiogram was not performed in this case; however, small complexes and electrical alternans are the most common changes found in dogs. (19)

Echocardiography is essential for the definitive diagnosis of pericardial effusion in birds and other species. (17,20) Because of its close relationship to the heart wall, the pericardial sac can usually be seen sonographically only in the presence of disease. (17) Reports of echocardiographic sensitivity for detecting canine cardiac masses are variable, ranging from 17% to 80% during the first exam and up to 88% for repeat exams. (20) Serial echocardiograms are recommended in all cases of pericardial disease, especially for detection of more diffuse tumor types, such as mesothelioma. Echocardiography can help determine the size, location, and point of attachment of cardiac mass lesions and may help suggest a tentative diagnosis of the tumor type. (18) Echocardiography was unsuccessful in identifying the tumor mass around the heart in the Amazon parrot we describe. This may have been due to the diffuse nature of the mass, the limited window for imaging in an avian patient, the high avian heart rate, or paucity of published normal images for reference.

Advanced imaging was pursued in this case to further investigate the presence of a heart-associated mass. A definitive mass was not observed on pre- or postcontrast computed tomography images, despite being identified postmortem. It is possible that motion artifact due to the rapid heartbeat of the avian patient obscured the mass.

Pericardiocentesis is often indicated in dogs with pericardial effusion for analysis of the effusion and to resolve hemodynamic impairment. (7) Pericardiocentesis has been reported as a diagnostic and treatment option for pericardial effusion in a Fischer's lovebird (Agapornis fischeri) and an orange-winged Amazon parrot (Amazona amazonica). (21,22) Cytologic analysis of the pericardial fluid in the case reported here was consistent with hemorrhage, and no neoplastic cells were seen in the fluid sample. Several studies in dogs with pericardial neoplasia have shown that cytologic examination of pericardial effusion is an unreliable method for distinguishing between neoplastic and nonneoplastic pericardial diseases. (18) Difficulty in differentiation is most common for diagnosis of idiopathic pericarditis and mesothelioma. (20) Mesothelial cells may undergo hypertrophy and alteration in chronic effusions. (7) Reactive mesothelial cells are commonly found in canine pericardial effusions and often cytologically closely resemble neoplastic cells. (18)

In dogs, the most common causes of pericardial effusion are hemangiosarcoma, idiopathic pericarditis, mesothelioma, chemodectoma, thyroid gland adenocarcinoma, and infective pericarditis. (20) Differential diagnoses for pericardial effusion in the Amazon parrot reported here initially included neoplasia, idiopathic pericarditis, primary cardiac disease, trauma, and infection. Based on antemortem findings, idiopathic hemopericardium or an unidentified pericardial neoplasm was suspected.

Histopathologic examination is considered the gold standard for diagnosis of mesothelioma. Samples can be acquired as biopsies during subtotal pericardiectomy or on postmortem examination. (4) Human mesotheliomas are classified into 3 major histologic subtypes: epithelial, sarcomatous, and mixed (i.e., biphasic). (11) In humans and dogs, the epithelial type is the most common and consists of large, spheroidal, or cuboidal cells. (10,11) Alternatively, sarcomatous-type mesotheliomas are composed of ovoid to spindle-shaped cells. (11) Although histopathology is the gold standard for mesothelioma diagnosis, results can be inconclusive because mesotheliomas can histologically resemble other tumors. (4,11)

Immunohistochemistry can be performed to confirm the histogenic origin of a mass with inconclusive histopathologic results. The surface mesothelium of normal serosa is derived from multipotent subserosal cells in the underlying layer of connective tissue. Resting multipotent subserosal cells express vimentin only, whereas proliferating cells coexpress vimentin and low-molecularweight cytokeratins. As the cells differentiate into surface mesothelium, vimentin expression ceases, and expression of high-molecular-weight cytokeratins begins. (4) Although somewhat variable, mesothelial tumors often coexpress vimentin and cytokeratins. These markers can be used to distinguish mesotheliomas from adenocarcinomas, which do not express vimentin, and chemodectomas, which do not express vimentin or cytokeratins. (4) A negative Churukian-Schenk stain helped to rule out a neoplasm of neuroendocrine origin. In this Amazon parrot, concomitant expression of cytokeratin and vimentin strongly supported the diagnosis of a neoplasm of mesothelial origin.

An ectopic thyroid follicular carcinoma was considered a differential in this case because of the morphology and location of neoplastic cells and the accompanying changes in the thyroid glands. Additionally, thyroid gland carcinomas are a reported cause of pericardial effusion in dogs. (20) The cause of the thyroid changes in this Amazon parrot is unknown. The parrot also had degeneration and necrosis of the liver, likely caused by inflammation from the extensive coelomitis.

Mesothelioma is a rapidly fatal disease in humans and companion animals. (16) Despite the discovery of many risk factors and possible molecular and genetic targets in humans, no effective therapy exists. (11) The treatment of choice for human and small animal pericardial mesothelioma is pericardiectomy with adjunct chemotherapy. (7) Intracavitary chemotherapy with cisplatin, carboplatin, or mitoxantrone has been used for the palliative treatment of canine mesothelioma, with or without intravenous doxorubicin administration, and has prolonged survival times. (7,23) Intrathoracic chemotherapy allows for higher drug concentrations at the tumor site with a reduced risk of toxicity. (7) Prognosis for mesothelioma is poor to grave in all species, and the median survival time for dogs with mesothelioma-related pericardial effusion is 2-6.5 months. (19,20) In dogs, death is usually attributed to pleural effusion associated with tumor spread into the pleural space after repeated pericardiocentesis or pericardiectomy. (7)

Although no exposure to asbestos was identified in this case, the role of companion animals in identifying epidemiological agents and risk factors for human cancer has been proposed. Positive links have been found between canines diagnosed with mesothelioma and exposure of the owners to asbestos. (24) A detailed history, including questions about occupational and nonoccupational asbestos exposure, is warranted in cases of avian mesothelioma because of the associated human health risk. Mesothelioma has a long latent period in humans, and tumors may not be diagnosed until several decades after asbestos exposure. (8,16) It is possible that mesothelioma due to environmental exposure may be diagnosed earlier in companion avian patients compared with their owners.

Acknowledgments: We thank Misty Bailey for her technical writing support and Anik Vasington and Thomas Vigliotta for assistance with images.

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(23.) Charney SC, Bergman PJ, McKnight JA, et al. Evaluation of intracavitary mitoxantrone and carboplatin for treatment of carcinomatosis, sarcomatosis and mesothelioma, with or without malignant effusions: a retrospective analysis of 12 cases (1997-2002). Vet Comp Oncol. 2005;3(4): 171-181.

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Brynn McCleery, DVM, Michael P. Jones, DVM, Dipl ABVP (Avian), Jorden Manasse, BVMS, Sara Johns, DVM, Rebecca E. Gompf, DVM, MS, Dipl ACVIM (Cardiology), and Shelley Newman, DVM, DVSc, Dipl ACVP

From the Departments of Small Animal Clinical Sciences (McCleery, Jones, Johns, Gompf) and Biomedical and Diagnostic Sciences (Manasse, Newman), College of Veterinary Medicine, University of Tennessee, 2407 River Dr, Knoxville, TN 37996, USA. Present address (Manasse): Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2015 Linden Dr, Madison, WI 53706, USA.
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Author:McCleery, Brynn; Jones, Michael P.; Manasse, Jorden; Johns, Sara; Gompf, Rebecca E.; Newman, Shelley
Publication:Journal of Avian Medicine and Surgery
Article Type:Clinical report
Date:Mar 1, 2015
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