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Mixed Thymoma in an American Robin (Turdus migratorius).

Abstract: A mixed thymoma was diagnosed in a 15-year-old female American robin (Turdus migratorius) that exhibited poor body condition, dysphagia, hyporexia, and depression. A 1.5-cm subcutaneous nodule was present in the cranio-ventral cervical region, which had been noticed by the owner 15 days before presentation. On cytologic evaluation of a fine-needle aspirate, well-differentiated lymphocytes were observed. Surgical excision was elected; however, the mass was firmly attached to the esophagus and the jugular vein, and the attempt at excision resulted in fatal hemorrhage. On histologic examination of the mass, small, well-differentiated lymphocytes were observed mixed with neoplastic reticular cells and Hassall's corpuscles. On immunohistochemical analysis, the cytoplasm of 80% of the reticular cells showed abundant detectable brown antigen binding with pancytokeratin staining, and most lymphoid cells showed detectable antigen in the cytoplasm by using CD3 antibodies. The cytologic, histopathologic, and immunohistochemical features of the neoplasm in this robin were consistent with a mixed thymoma.

Key words: neoplasm, cervical region, immunohistochemistry, thymoma, mixed thymoma, avian, American robin, Turdus migratorius

Clinical Report

A 15-year-old American robin (Turdus migratorius) was presented to the Faculty of Veterinary Medicine and Zootechincs of the National Autonomous University of Mexico Avian Hospital for examination. The owner had noted an acute swelling of the neck of approximately 15 days duration and hyporexia and depression of 2 days duration. The bird had been housed alone since a juvenile as a companion bird in a private indoor enclosure and was fed a diet composed of plantain bananas and poultry grower ration (70:30).

On physical examination, a firm, nonmovable, 1.5-cm subcutaneous mass was found on the cranioventral aspect of the neck (Fig 1A). The bird was in poor body condition (weight, 68 g) and appeared depressed, dehydrated, and dysphagic. Respiratory distress was not observed.

The bird was hospitalized for diagnostic testing and supportive care. A complete cell blood count and plasma biochemical profile could not be performed because of unavailability of collection tubes for small-volume samples ([less than or equal to]100 [micro]L), and collecting a volume greater than 0.3 mL was considered life threatening in this bird. Radiographs were not performed because of the owner's financial constraints. The bird received anti-inflammatory and analgesic therapy with meloxicam (0.2 mg/kg IM q12h), subcutaneous crystalloid fluids (50 mL/kg per day, Hartmann solution), and antibiotic therapy with enrofloxacin (15 mg/kg PO q12h) for 2 days, during which time it showed significant clinical improvement.

A fine-needle aspirate of the mass was obtained for cytologic examination. The aspirate sample was stained with Papanicolaou stain, and results showed groups of small to medium lymphoid cells with a background of erythrocytes. The cells showed scant cytoplasm, well-defined borders, round to oval nuclei with thick granular chromatin, moderate anisokaryosis, and 1-2 prominent nucleoli. Because a definitive diagnosis could not be made based on these results, surgical excision and biopsy was elected. (1-3)

For anesthesia the, bird was induced with isoflurane administered by face mask, intubated with a 14-gauge intravenous catheter with the stylet removed, and maintained with 1.5% isoflurane. The bird was positioned in dorsal recumbency, the feathers were plucked from the surgical site, and the skin was prepared aseptically with 1% povidone-iodine solution. A 1-cm skin incision was made on the ventral surface of the mass, and blunt dissection was performed to separate the subcutaneous plane from the mass, which showed multiple petechial hemorrhagic foci on its surface. The right jugular vein and the esophagus were firmly attached to the mass, resulting in inadvertent laceration of the jugular vein during dissection. Hemorrhage could not be controlled, and the patient died during the procedure. The owner did not authorize necropsy; however, the mass was submitted for histologic examination.

Grossly, the mass was 1.5 cm in diameter, firm, well delineated, encapsulated, and white to gray, mixed with multiple areas of hemorrhage. On cut sections, the surface was smooth and white, mixed with multifocal zones of hemorrhage. The excisional biopsy was fixed for 24 hours in neutralbuffered formalin solution (10%) and processed by routine histologic technique. Tissues were cut in 3[micro]m-thick sections and stained with hematoxylin and eosin.

Microscopically, the mass was composed of hypercellular areas of reticular cells arranged in nests and separated by connective tissue. These cells had abundant eosinophilic cytoplasm and poorly defined borders. Nuclei were vesicular and round to oval, with 1-2 prominent nucleoli and moderate anisokaryosis in more than 50% of reticular cells (Fig 1B). In some areas, the reticular cells resembled epithelioid cells forming concentric lamellae of keratin similar to Hassall's corpuscles (Fig 1C), and 1-2 multiple mitotic figures were observed per field of x400. Multifocal aggregates of round lymphoid cells arranged in solid sheets were also observed; these cells had scant eosinophilic cytoplasm, small nuclei with thick granular chromatin, 1-2 prominent nucleoli, and moderate anisokaryosis in 35% of lymphoid cells; no mitotic figures were observed (Fig ID). In another field, hemorrhage and necrosis were evident. The neoplastic tissue had encapsulated, well-defined borders, and no invasion into blood vessels or the capsule was observed.

Tissue samples were sent to the Pathology Unit of the General Hospital in Mexico City, Mexico. Immunohistochemistry was performed by labeled streptavidin biotin peroxidase. A panel of primary polyclonal murine antibodies against pancytokeratin AE1/AE3 (keratin) and CD3 (T-cells) were used (Dako North America, Carpentaria, CA, USA). Pancytokeratin and CD3 antibody dilutions were 1:50 and 1:250, respectively; goat anti-mouse biotinylated secondary antibodies (Dako North America) were applied, and diaminobenzidine tetrahydrochloride was used as chromogen. Antigen retrieval for all antibodies was performed with citrate buffer, pH 9, in a pressure cooker. Results of pancytokeratin staining revealed abundant brown antigen binding in 80% of the cytoplasm of the reticular cells; most lymphoid cells showed detectable antigen in the cytoplasm by using CD3 antibodies (Figs IE and F). Considering the anatomic location of the neoplasm described above, and the histologic features (histomorphologic and immunohistochemical), a mixed thymoma was diagnosed in this American robin.


In this report we describe an unusual case of a mixed thymoma in a 15-year-old American robin. The thymus is a primary lymphoid organ where T lymphocytes differentiate and mature. It is derived from the third and fourth pharyngeal pouches and formed by 2 chains of 3 to 8 lobes each, which are located along the neck near the jugular vein. The thymus is composed of epithelial and lymphoid cells. The epithelial component, also called reticular cells, serves as support for lymphoid cells. In some areas, the epithelial reticular cells are arranged concentrically in a structure known as a Hassall's corpuscle. In domestic fowl, the thymus involutes at 4 months of age at the onset of sexual maturity. The thymus also contains a small number of B lymphocytes that migrate to the thymus after hatching. Unlike in mammals, the thymus in birds can function as a secondary lymphoid organ. (4)

Thymomas are tumors derived from epithelial components of the thymus that contain variable degrees of nonneoplastic lymphocytes. (5-7) They are rare in domestic animals, slow growing, encapsulated, and, in general, display a benign behavior. The biological behavior of thymomas is similar in animals and humans, in which 65% of thymomas are encapsulated and noninvasive, while 35% are invasive (3) and may metastasize. (2,8-12) In animals, malignant thymomas have been reported, in which the thymomas invade locally, metastasize, or both (thymic carcinomas). (8-10,13,14) The invasive capabilities of malignant tumors are associated with enhanced tumor cell motility, increased production of proteases, and altered tumor cell adhesion characteristics. (15) In birds, only 2 cases of malignant thymoma have been reported, the first one in a burrowing owl (Athene cunicularia) (16) and the second in a scarlet macaw (Ara macao). (12) The thymoma in the American robin we describe showed no invasion into the surrounding capsule or the blood vessels; therefore, it was considered benign (Table 1).

In veterinary pathology, thymomas are classified based on histologic components as epithelial, lymphocytic, or mixed. (5,6,17) These tumors are considered rare in domestic animals, except in Saanen breed dairy goats, (5,18,19) and African soft-furred rats (Mastomys natalensis). (18,20) Less frequently, thymomas have been described in dogs, (14,21) cats, (8) rabbits, (22) cows, sheep, (23-25) and horses. (10) In avian species, thymomas are rarely reported. They have been documented in domestic chickens, (7,26,27) 3 budgerigars (Melopsittacus undulatus), (11,28) a Java sparrow (Lonchura oryzivora), (29) a common mynah bird (Acridotheres tristis), (1) a finch, (30) a burrowing owl (Athene cunicularia), (16) a canary (Serinus canarius), (31) and a scarlet macaw (Ara macao) (12) (Table 1). These neoplasms are rare in domestic animals with no apparent sex predisposition. (5) In birds, there are too few reports to evaluate if a sex predisposition exists for thymoma development. Although thymomas have been diagnosed more commonly in adult birds, this neoplasia can occur in immature birds (Table 1), such as described in chickens from 8 weeks of age (7) and in a 1-year-old canary. (31)

Clinical signs caused by thymomas are frequently secondary to the increasing size of the tumor acting as a space-occupying mass. (6) In birds, because of the location of the thymus along the neck, thymomas can develop anywhere from the mandible to the thoracic inlet (Table 1). Therefore, thymoma should be considered as one of the differential diagnoses for cervical swelling, which also include fungal or bacterial granuloma, foreign body reaction, granuloma induced by hypovitaminosis A, branchial cyst, and neoplasia. (12,16) Depending on the location, various related sequelae can develop, such as compression and stasis of the crop, dyspnea due to displacement of the trachea, and dysphagia associated with esophageal dilation. (11,32) Signs of dysphagia and poor body condition were observed in the robin we describe. In the reports of the scarlet macaw (12) and the budgerigar, (11) respiratory signs were described, as well as dysphagia in the latter case, whereas in the mynah bird (1) and the burrowing owl (16) only weight loss was noticed. In the finch, (30) Java sparrow, (29) and canary (31) no clinical signs were reported other than cervical swelling.

In goats, there have been reports of congestive heart failure due to the space occupied by a large intrathoracic mass, which compromised cardiac fuction. (33) Congestive heart failure has not been documented in birds, probably because of the location of the avian thymus. Reports in dogs, cats, and people describe paraneoplastic syndromes associated with thymoma, such as myasthenia gravis, hypercalcemia, polymyositis, cytopenia, and dermatitis. (2,13,29,34) In avian thymomas, myasthenia gravis or other paraneoplasic syndromes have not been described, including in this case in the American robin. (1,11,12,16,29-31) Diagnostic evaluation of these neoplasms can be done by radiography, ultrasonography, computed tomography, (35) and biopsy with histologic evaluation. (16) In this case, results of histopathologic examination established the diagnosis of a mixed thymoma.

The treatment of choice for thymomas in people and in domestic animals (including birds) is complete surgical removal. (2,3,16,30,36) In birds, surgical resection is the only described procedure for noninvasive thymomas (12,16); however, surgical removal of these tumors is complicated because of the close proximity of the thymic tissue to the great vessels, such as the jugular vein. (16,30) In this robin and in the case of the burrowing owl, (16) the mass was firmly adhered to the jugular vein, and in the robin, it was also attached to the esophagus, which complicated the surgery, resulting in fatal hemorrhage. In people, other supplementary treatments are available in addition to surgery, such as radiation therapy, chemotherapy, and corticosteroid treatment. (37) In dogs and cats, radiation therapy has been reported as a successful treatment for invasive thymomas. (4,38) In avian species, no alternative treatment modalities such as radiation therapy or chemotherapy have been reported, although chemotherapy or radiation therapy should be considered with invasive thymoma. (16) In birds, however, more research is required to fully understand the biologic behavior of this neoplasm and which innovative therapies can be used for treatment. (36)

Acknowledgments: We thank Fernando Garcia Lacy, MVZ, Msc, for editorial assistance in the preparation of this manuscript.

Vanessa Hernandez Urraca, MMVZ, Elizabeth Morales Salinas, MZV, Dr, Ernesto Carrera Gonzalez, Dr, and Felix Domingo Sanchez Godoy, MVZ, MC

From the Department of Avian Medicine and Zootechnics (Hernandez Urraca. Sanchez Godoy) and the Pathology Department (Morales Salinas), Faculty of Veterinary Medicine and Zootechnics, National Autonomous University of Mexico (UNAM), Av. Universidad 3000, Ciudad Universitaria 04510, Ciudad de Mexico, Mexico; and the Pathology Unit, General Hospital of Mexico, Calle Dr. Balmis 148, Colonia Doctores, Delegacion Cuauhtemoc, 06726, Ciudad de Mexico. Mexico (Carrera Gonzalez).


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Caption: Figure 1. (A) American robin that was presented for evaluation with clinical signs of hyporexia and depression. At the ventral aspect of the neck, a firm, nonmovable, well-defined, subcutaneous mass (arrow) measuring 1.5 cm was present. (B) Reticular cells in a thymoma of an American robin. Neoplastic reticular cells (arrow) with oval, round, euchromatic nuclei, 1 prominent nucleoli and a moderate amount of cytoplasm with poorly defined edges are visible (hematoxylin and eosin, bar = 50 [micro]m). (C) Section of neoplastic tissue where numerous lymphocytes and epithelial cells forming Hassall's corpuscle (asterisks) are noted (hematoxylin and eosin, bar = 200 [micro]m). (D) Lymphoid cells (arrows) with small, round, hyperchromatic nuclei with scant cytoplasm and moderate anisokaryosis are present (hematoxylin and eosin, bar = 50 [micro]m). (E) Immunohistochemistry for cytokeratin in thymoma described above. The cytoplasm of 80% of the reticular cells shows abundant detectable antigen that stains brown (asterisks), indicating antibody for ancytokeratin (AE1/AE3) (bar = 50 [micro]m). (F) Immunohistochemistry for T cells in thymoma described above. The cytoplasm of most lymphocytes has abundant detectable antigen that stains brown (arrowheads), indicating antibody for CD3 (bar = 50 [micro]m).
Table 1. Thymomas described in birds.

Species                       Sex      Age

American robin                Female   15 years
  (Turdus migratorius)

Budgerigar (11)               Female   --
  (Melopsittacus undulatus)

Burrowing owl (16)            Male     12 years
  (Athene cunicularia)

Canary (31)                   Female   1 year
  (Serinus eanarius)

Chicken (7)                   Female   8 weeks

Finch (30)                    --       Adult
  (unspecified species)

Java sparrow (29)             Female   3 years
  (Lonehura oryzivora)

Mynah (1)                     Male     13 years
  (Acridotheres tristis)

Scarlet macaw (12)            Female   49 years
  (Ara macao)

Species                       Tumor location

American robin                Ventral region of the neck
  (Turdus migratorius)

Budgerigar (11)               Right side of the base of the neck
  (Melopsittacus undulatus)

Burrowing owl (16)            Right cervical region
  (Athene cunicularia)

Canary (31)                   Submandibular
  (Serinus eanarius)

Chicken (7)                   --

Finch (30)                    Left side of the neck
  (unspecified species)

Java sparrow (29)             Left side in the caudal region
  (Lonehura oryzivora)          of the neck

Mynah (1)                     Left ventrolateral side of the neck.
  (Acridotheres tristis)        near the thoracic inlet

Scarlet macaw (12)            Right cervical region near the
  (Ara macad)                   thoracic inlet; after 1 year.
                                second mass on the vertebral
                                column expanding into
                                the lung

Species                       Signs

American robin                Poor body condition.
  (Turdus migratorius)          hyporexia, dysphagia.

Budgerigar (11)               Respiratory distress.
  (Melopsittacus undulatus)     malaise, dysphagia

Burrowing owl (16)            Weight loss
  (Athene cunicularia)

Canary (31)                   None reported
  (Serinus eanarius)

Chicken (7)                   None reported

Finch (30)                    None reported
  (unspecified species)

Java sparrow (29)             None reported
  (Lonehura oryzivora)

Mynah (1)                     Weight loss
  (Acridotheres tristis)

Scarlet macaw (12)            After 1 year presented
  (Ara macad)                   respiratory signs,
                                fluffed feathers, poor
                                body condition

Table 1. Extended.

Diagnostic method                     Treatment   Classification

Histopathology                        Surgery     Mixed thymoma
(surgical resection)
Died during surgery

Histopathology (necropsy)             --          Epithelial thymoma

Histopathology                        Surgery     Thymoma
(surgical resection)
Died 6 days after surgery

Histopathology (necropsy)             Surgery     Mixed thymoma
Died during anesthesia
before surgery

Histopathology (necropsy)             --          Thymoma
                                                  (Marek's disease)

Histopathology (necropsy)             --          Lymphocytic
Died during examination                           thymoma

Histopathology (Surgical resection)   Surgery     Thymoma
Reported healthy 4 months after

Histopathology (necropsy)             --          Mixed thymoma

Histopathology (surgical resection    Surgery     Epithelioid
and incisional biopsy)                            cortical-type
Euthanatized 1 year after surgery                 thymoma
because of metastasis to the
vertebral column and lung

Diagnostic method                     Biologic       Paraneoplasic
                                      behavior       syndrome

Histopathology                        Benign         None reported
(surgical resection)
Died during surgery

Histopathology (necropsy)             Possibly       None reported

Histopathology                        Locally        None reported
(surgical resection)
Died 6 days after surgery             invasive

Histopathology (necropsy)             Benign         None reported
Died during anesthesia
before surgery

Histopathology (necropsy)             --             None reported

Histopathology (necropsy)             Benign         None reported
Died during examination

Histopathology (Surgical resection)   Benign         None reported
Reported healthy 4 months after

Histopathology (necropsy)             Benign         None reported

Histopathology (surgical resection    Malignant      None reported
and incisional biopsy)
Euthanatized 1 year after surgery
because of metastasis to the
vertebral column and lung
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Title Annotation:Clinical Report
Author:Urraca, Vanessa Hernandez; Salinas, Elizabeth Morales; Gonzalez, Ernesto Carrera; Godoy, Felix Domin
Publication:Journal of Avian Medicine and Surgery
Date:Sep 1, 2018
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