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Metastatic thymoma in a scarlet macaw (Ara macao).

Abstract: A 49-year-old female scarlet macaw (Ara macao) was presented with a mass in the cervical region. The bird showed no evidence of pain or discomfort, it swallowed food normally, and its breathing pattern was unremarkable. Results of contrast radiographic imaging revealed a well-demarcated mass in the right cervical region not related to the crop. After surgical resection and histopathologic evaluation, a malignant nodular stage of an epithelioid cortical-type thymoma was diagnosed. One year later, metastasis of the thymoma to the lung was diagnosed and confirmed at postmortem examination. The final diagnosis was corrected to malignant nodular stage of an epithelioid cortical-type thymoma with metastasis to the lung. This is the first report in an avian species of a malignant thymoma with metastasis to the lung after complete resection of the initial cervical thymoma and a survival time of 1 year.

Key words: thymoma, neoplasia, soft tissue mass, contrast radiographic imaging, surgery, cervical region, avian, scarlet macaw, Ara macao

Clinical Report

An approximately 49-year-old female (DNA-sexed) scarlet macaw (Ara macao) was presented to the veterinary clinic at Karlsruhe Zoo because of a mild elevation of feathers in the right cervical region. The bird came to the zoo in 1975 and was estimated to be about 10 years of age at that time. For the next 39 years, it had been housed together with a male scarlet macaw in an indoor enclosure with access to an outdoor aviary in the summer. The bird had laid eggs only 2 times, in 2010 and 2011, but eggs were not fertile. The diet consisted of a seed mixture and fruits supplemented with a vitamin and mineral powder. Annual examination of feces (parasitologic and microbiologic) as well as weight monitoring showed no abnormalities in the past. The bird had never shown signs of illness, and no further clinical history of either scarlet macaws was available. The patient showed no evidence of pain or discomfort, and the intake and swallowing of food was normal. On physical examination, the macaw weighed 800 g, and the breathing pattern was unremarkable. A well-defined, solid, moveable mass, about 5 cm in diameter, was palpated in the right cervical region near the thoracic inlet. No other abnormalities were observed.

For contrast imaging, barium sulfate (15 mL/kg) was administered orally a short time before full-body radiographs were taken. Results of digital radiographs showed 2 soft-tissue dense masses of different sizes that did not involve the crop (Fig 1). The larger mass displaced the crop; however, it did not prevent passage of contrast medium into the stomach. No other abnormalities were visible on the radiographs. Differential diagnoses for the masses were fungal granuloma, foreign body reaction, bacterial granuloma, hypovitaminosis A-induced abscess or granuloma, branchial cysts, and neoplasia.

Because of the size, location, and extent of the masses, surgical treatment was elected. The bird was premedicated with meloxicam (0.2 mg/kg IM) and subcutaneous fluids (25 mL SC, 0.9% NaCl) 15 minutes before the beginning of surgery. For anesthesia, the bird was induced with isoflurane administered by face mask, intubated with an uncuffed, 3.0-mm endotracheal tube, and maintained with isoflurane administered at 1.5%-3.0% for the duration of the surgery. The bird was positioned on a heating pad and monitored by electrocardiogram during the procedure. The feathers were plucked over the cervical mass, and the area was prepared aseptically for surgery. The bird was stable throughout surgery, which took 50 minutes. A 5-cm skin incision was made over the mass, and the mass was dissected from the surrounding cervical muscles and vascular structures by a combination of sharp and blunt dissection. The mass appeared to be several combined structures that looked botryoid (Fig 2). The crop, the right carotid artery, and the right jugular vein were identified and spared during the dissection. Because of the pronounced vascularity of the mass, several ligatures were necessary, and hemorrhage was controlled with bipolar cautery. The entire mass was removed successfully without complications. The skin was closed with absorbable suture (4-0 Vicryl; Ethicon, Johnson & Johnson Intl, St-Stevens-Woluwe, Belgium).

On gross examination, the mass was firm, weighed 56 g, and consisted of 1 large section, measuring 5 cm in diameter, and 3 smaller sections, each measuring 2 cm in diameter. On transverse cut section, the surface was fatty and of mixed color, including white, yellow, grey, and black, inside a thin capsule (Fig 3). The mass was fixed in neutral buffered formalin solution (10%) and submitted for histopathologic examination.

Microscopically, the mass consisted of densely cellular nests separated by connective tissue. The nests of cells were pleomorphic and consisted mainly of large, heterogeneous reticular cells. Small lymphocytes and lymphoblasts were multifocal, but low in number, and heterophils were rare (Fig 4). Epithelioid reticular cells were arranged concentrically and interpreted as Hassall corpuscles. Squamous differentiation was occasionally seen. Epithelioid reticular cells had indistinct cell margins and abundant, fine, pale eosinophilic cytoplasm, as well as amphophilic vacuoles of different size. Nuclei were vesicular and round to oval, with marked anisokaryosis and prominent, often multiple, nucleoli (Fig 5). Mitotic count was low, and no invasion into blood vessels or surrounding capsule and tissues were noted. In accordance with these findings, a benign, solid epithelioid thymoma was diagnosed.

The bird recovered rapidly and uneventfully from anesthesia, and on the evening after surgery it was eating and showed no signs of pain or discomfort. The bird was treated with meloxicam (0.9 mg/kg PO q24h for 3 days) and was fed supportively with fruit puree and softened rusk for the next 5 days. After 5 days in the hospital, the bird was discharged and returned to its partner in the aviary.

One year later, the macaw presented with respiratory signs, fluffed feathers, and poor general body condition. Diagnostic imaging was performed again, with the result showing a soft-tissue mass visible on the vertebral column and expanding into the lung. A biopsy sample of the mass obtained by endoscopy was firm and appeared white and fatty. Histopathologic examination of the biopsy sample revealed lung tissue with diffuse, large, densely cellular nests separated by connective tissue (Fig 6). The cells were pleomorphic and consisted mainly of large heterogeneous reticular cells. Small lymphocytes and lymphoblasts were multifocal but in low numbers. Epithelioid reticular cells had indistinct cell margins and abundant, finely pale eosinophilic cytoplasm, as well as amphophilic vacuoles of different sizes. Nuclei were vesicular, round to oval, with marked anisokaryosis and prominent, often multiple, nucleoli. Mitotic figures were detected in low numbers, with evident invasion into the blood vessels and surrounding lung tissue. Because of the same histopathologic morphology as the solid epithelioid thymoma initially diagnosed, the diagnosis was metastasis of the initial neoplasm.

The macaw was euthanized and a postmortem examination was performed. Body weight of the bird was 782 g with a body condition score of 3/5. Multifocal, white, fatty, firm tubercles that were 0.5 cm in diameter were present in the lung tissue. The aorta was firm with diffuse yellow plaques on the intima. On histopathologic examination, the lung tubercles consisted of the same cells that were described in the biopsy sample of the lung. Plaques inside the aorta consisted of fibrous connective tissue with severe deposition of cholesterol clefts and fat cells, as well as minimal diffuse mineralization, indicating advanced atherosclerosis. Other histopathologic changes identified were hyperplasia of connective fibrous tissue in the kidney glomerula, golden brown pigment in the neurons of the brain, and vacuolar degeneration of the adrenal interrenal cells. Final diagnoses were lung metastasis of a cortical-type thymoma, atherosclerosis stage IV, lipofuscinosis of brain neurons, and adrenal interrenal cell degeneration.

Discussion

This report describes the first case of a malignant nodular stage of an epithelioid cortical-type thymoma in a parrot. One year after successful surgical removal of the primary neoplasia, which was characterized as a benign epithelioid cortical-type thymoma, metastasis of the thymoma was identified in the lung. The final diagnosis therefore was corrected to malignant nodular stage of an epithelioid cortical-type thymoma with metastasis to the lungs.

The avian thymus gland is a bilateral, palepinkish, multilobular structure situated on each side of the neck close to the jugular vein. (1) It extends from the angle of jaw to the thoracic inlet and consists of lobules of epithelial and lymphocytic cells, each confined by a connective tissue capsule. The gland is at its largest in a sexually immature bird and normally regresses as the bird gets older. The thymus together with the bursa of Fabricius are primary lymphoid organs. The thymus serves as the source of T lymphocytes, which are the circulating cells responsible for cell-mediated immune response." (2,3)

In birds, a thymoma can develop under the skin anywhere from the jaw to the thoracic inlet and can be solid, cystic, or hemorrhagic. (2) Contrary to the thymoma described here, neoplasms from the lymphocytes are more common in birds and called thymic lymphomas. Neoplasms from the epithelial cells of the thymus are termed thymomas. (4) The first documentation of a thymoma in an avian species was in 1934 in a domestic duck (Anas platyrhynchos). (5) Two years later, a malignant thymoma with suspected metastasis in the lung was described in a chicken. (6) The first description of a malignant thymoma in a psittacine bird was from a budgerigar (Mellopsittacus undulatus). (7) Overall, however, thymomas in birds are rare. Single bird case reports are mainly of benign thymomas without metastasis, as described in a Java sparrow (Padda oryzivora), (8) an African grey parrot (Psittacus erithacus), (9) a burrowing owl (Athene cunicularia), (10) a Senegal parrot (Poicephalus senegalus), (11) and a common myna (Acridotheres tristis). (12) Malignant metastatic thymoma in a macaw has not been described previously.

In human medicine, thymomas are classified into 3 types: type A if the epithelial cells have an oval or fusiform shape (lower lymphocyte count); type B if cells have an epithelioid shape; and type AB if the tumor contains a combination of both cell types. (4) Type B thymomas are of 3 subtypes: B1 (lymphocyte-rich), B2 (cortical), and B3 (epithelial). Thymic cortical epithelial cells have abundant cytoplasm, vesicular nuclei with finely divided chromatin and small nucleoli, and cytoplasmic filaments that contact adjacent cells. In contrast, thymic medullary epithelial cells are spindle shaped with oval dense nuclei and scant cytoplasm. If the thymoma features more cortical cells, it is thought to be less benign. (4)

Various diseases, as mentioned above, can cause a subcutaneous mass on the right or left side of the neck. Although thymomas are more common in older birds, this neoplasm cannot be excluded in immature birds. (9) Therefore, a complete diagnostic workup, including hematologic testing and plasma biochemical analysis, as well as diagnostic imaging, is needed before specific diagnostic procedures like fine-needle aspiration or surgical excision and biopsy are recommended. However, diagnostic imaging like radiography and computed tomography, both without and with contrast enhancement, are helpful to diagnose a mass of soft density, usually not invading the esophagus, crop, trachea, or cervical spine. (10-12) Furthermore, whole-body computed tomography scans are useful to exclude metastasis, especially in the lung. (11) Use of ultra-sonography, which is common in cases of thymomas in human and small mammal medicine, are not yet described in birds. Cytologic examination of fine-needle aspirates in birds can show pleomorphic cells with anisonucleosis and irregular nuclear membranes, dense chromatin, and visible nucleoli as well as mitotic figures." (11-12) Final diagnosis is possible with histopathologic examination of the mass. Immunhistochemical testing can be helpful to differentiate between thymoma and thymic lymphoma by labeling cytokeratins CK14 and CK18, as well as showing positive results for proliferating cell nuclear antigen in cases of thymomas. (8-12,13) The World Health Organization nomenclature for human neoplasms seems to be applicable to characterization of thymomas in avian medicine. (12)

According to the above-described World Health Organization classification in human medicine, the thymoma in the macaw described here could be classified as cortical type (B2). (4) The thymoma was completely encapsulated without microscopic or macroscopic invasion of the surrounding capsule, tissue, or vessels, so that according to the Masaoka staging system, which is used widely in human medicine, a benign stage was diagnosed.14 However, 1 year later, metastasis of the thymoma to the lung was identified; therefore, the initial diagnosis of a benign stage was corrected to a malignant nodular stage of an epithelioid cortical-type thymoma, according to the recently proposed classification. (15)

A report published in 1936 described a domestic chicken with a thymoma with similar morphology and metastatic behavior as in this macaw. (6) In this report, similar metastasis into the lung was evident, without capsular involvement or invasion into the surrounding tissue or the vessels. (6) In a report in a Senegal parrot, which included histopathology of the lung, no metastases were detected in lung tissue. (11) In the Senegal parrot, a benign, lymphocyte-rich thymoma (B1) was diagnosed. (11) In only one other avian case was malignancy suspected, that of a budgerigar with a thymoma that showed capsular involvement and infiltration of the mediastinal fat. (7) According to the Masaoka system, this is a typical feature of malignancy during staging; unfortunately, histopathologic examination of the lung was not performed in this case, so metastatic behavior was not confirmed. However, in review of these 2 cases compared with the case we describe, staging and metastatic behavior of thymomas in birds appears comparable to the classification used in human medicine, as was suggested in a report describing cervical type AB thymoma in a common myna. (4,12,14,15)

There are no reports of specific treatment of thymoma in psittacine species. Currently, surgical removal is the only described treatment option for noninvasive thymomas in avian species. Surgical excision was described in a Java sparrow that survived at least 4 months after removal of the neoplasia. (8) Depending on the size and location of the tumor, however, surgical intervention may indicate a poor prognosis. In a report of thymoma in a burrowing owl, the size of the thymoma, the proximity to the right jugular vein, and the adherence to the esophagus likely contributed to a poor postsurgical outcome. (10) In an African grey parrot, the age of the patient (2 months) and the infiltrative nature, location, and malignancy of the thymoma resulted in death during surgery. (9) In the macaw we describe, extensive vascularity of the mass and potential adhesion to major vessels and the crop wall could not be fully excluded in advance of surgery. However, despite the mass being highly vascular, excessive bleeding was prevented. Apart from its advanced age, this macaw was in good physical condition, and the mass was clearly demarcated and suspected as benign at the time of the initial excision. Therefore, the prognosis was good for complete resection without metastasis and recrudescence. However, because of the occurrence of lung metastasis identified 1 year later, this case demonstrates that staging and grading of neoplasms in birds are important, and further work is needed to standardize tumor descriptions in avian medicine.

References

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(2.) Doneley B. Avian Medicine and Surgery in Practice. Boca Raton, FL: CRC Press; 2010.

(3.) Harcourt-Brown NH. Anatomy and physiology. In: Harcourt-Brown NH, Chitty J, ed. BSA VA Manual of Psittacine Birds. 2nd ed. Gloucester, UK: British Small Animal Veterinary Association; 2005:7-21.

(4.) Dadmanesh F, Sekihara T, Rosai J. Histologic typing of thymoma according to the new World Health Organization classification. Chest Surg Clin N Am. 2001; 11(2):407-420.

(5.) Worms G, Klotz HP. Contribution a l'etude des tumeurs thymiques chez und Canard. Bull Assoc France Cancer. 1934;23:420-432.

(6.) Feldmann WH. Thymoma in a chicken (Gallus domesticus). Am J Cancer. 1936;26(3):576-580.

(7.) Zubaidy AJ. An epithelial thymoma in a budgerigar (Melopsittacus undulatus). Avian Pcithol. 1980;9(4): 575-581.

(8.) Maeda H, Ozaki K, Fukui S, Narama I. Thymoma in a Java sparrow (Pacida oryzivora). Avian Pathol. 1994;23(2):353-357.

(9.) Diaz-Figueroa O, Garner MM, Tully TN Jr. What is your diagnosis? J Avian Med Surg. 2004; 18(1):51-53.

(10.) Kinney ME, Hanley CS, Trupkiewicz JG. Surgical removal of a thymoma in a burrowing owl (Athene cunicularia). J Avian Med Surg. 2012;26(2):85-90.

(11.) Wernick MB, Hilbe M, Kaufmann-Bart M, et al. Pathology in practice. Thymoma in a parrot. J Am Vet Med Assoc. 2013;243(8): 1117-1119.

(12.) Khaki F, Javanbakht J, Sasani F, et al. Cervical type AB thymoma (mixed) tumour diagnosis in a mynah as a model to study human: clinicohistological, immunohistochemical and cytohistopathological study. Diagn Pathol. 2013;8:98.

(13.) Balaguer L, Romano J, Mora A. A poorly-differentiated squamous cell thymoma in a chicken with lymphoma. Avian Pathol. 1995;24(4):737-741.

(14.) Masaoka A, Monden Y, Nakahara K, Tanioka T. Follow-up study of thymomas with special reference to their clinical stages. Cancer. 1981;48(11):2485-2492.

(15.) Fukui T, Fukumoto K, Okasaka T, et al. Clinical evaluation of a new tumour-node-metastasis staging system for thymic malignancies proposed by the International Association for the Study of Lung Cancer Staging and Prognostic Factors Committee and the International Thymic Malignancy Interest Group. Eur J Cardiothorac Surg. 2016;49(2):574-579.

Barbara Lang, Dr Med Vet, Susanne Vorbruggen, Dr Med Vet, Ruth Kothe, Dr Med Vet, Gerd Britsch, Dr Med Vet, and Volker Schmidt, Dr Med Vet, Dipl ECZM (Avian, Herp)

From Zoo Karlsruhe, Ettlinger Str. 6, 76137 Karlsruhe, Germany (Lang); the Clinic for Birds and Reptiles Dr. Britsch, Am Storrenacker lb, 76139 Karlsruhe, Germany (Vorbruggen, Kothe, Britsch); and the Clinic for Birds and Reptiles, University of Leipzig, An den Tierkliniken 17, 04103 Leipzig, Germany (Schmidt).

Caption: Figure 1. Lateral and ventrodorsal radiographs of a scarlet macaw after orally administered barium sulfate. Two soft tissue masses (arrow) are visible in the cervical region. The crop is distinctly displaced by the bigger mass, and the contrast medium has passed into the stomach.

Caption: Figure 2. Intraoperative photograph of a thymoma resection in the scarlet macaw described in Figure 1. The mass has a botryoid appearance of several combining structures.

Caption: Figure 3. Gross appearance of the thymoma after surgical resection in the scarlet macaw described in Figure 1. The mass was completely excised without complications. Transverse section revealed a fatty cut surface of mixed color, including white, yellow, grey, and black, inside a thin capsule.

Caption: Figure 4. Photomicrograph of the thymoma described in Figure 3 showing densely cellular nests (*) separated by connective tissue (+). The cells are pleomorphic and consist mainly of large heterogeneous reticular cells (black arrow). Small lymphocytes and lymphoblasts are multifocal (white arrow), but on a low grade, and heterophils are rare (hematoxylin and eosin, X200).

Caption: Figure 5. Photomicrograph of the thymoma described in Figure 3. Reticular cells have indistinct cell margins and abundant, finely pale eosinophilic cytoplasm, as well as amphophilic vacuoles of different sizes (black arrow). Nuclei are vesicular, round to oval, with marked anisokaryosis, and prominent, often multiple nucleoli (hematoxylin and eosin, X400).

Caption: Figure 6. Photomicrograph of lung metastasis of an epithelial cortical-type thymoma in the macaw described in Figure 1. Lung tissue (*) with diffuse, large, densely cellular nests of pleomorphic and mainly large heterogeneous reticular cells (+). Small lymphocytes and lymphoblasts are multifocal, but in low numbers. Mitotic figures are present in a low grade (black arrow), and invasion to the blood vessels (white arrow) and surrounding lung tissue is evident (hematoxylin and eosin, X200).
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Author:Lang, Barbara; Vorbruggen, Susanne; Kothe, Ruth; Britsch, Gerd; Schmidt, Volker
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Mar 1, 2017
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