Pathology in Practice

Morena Bernadette Wernick Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, CH-8057 Zurich, Switzerland.

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Monika Hilbe Institute of Veterinary Pathology, Vetsuisse Faculty, University of Zurich, CH-8057 Zurich, Switzerland.

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Madeleine Kaufmann-Bart Zyto-Histo Diagnostics, Im Wingert 4, 8427 Rorbas-Freienstein, Switzerland.

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Sarah Albini Department of Poultry and Rabbit Diseases, Institute of Veterinary Bacteriology, Vetsuisse Faculty, University of Zurich, CH-8057 Zurich, Switzerland.

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Richard K. Hoop Department of Poultry and Rabbit Diseases, Institute of Veterinary Bacteriology, Vetsuisse Faculty, University of Zurich, CH-8057 Zurich, Switzerland.

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Jean-Michel Hatt Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, CH-8057 Zurich, Switzerland.

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History

An 18-year-old female Senegal parrot (Poicephalus senegalus), weighing 160 g (0.35 lb), was evaluated because of a rapidly growing mass in the region of the left side of the neck. The mass was first detected 3 months prior to the examination. The parrot had been obtained from an animal shelter at the age of 8 years and had since been otherwise clinically normal. Husbandry was considered adequate, although the parrot had lived alone without a partner bird for several years. The parrot's diet consisted of a seed mix and fruits, and water was offered ad libitum.

Clinical and Gross Findings

On physical examination, a large (3 × 2 × 2-cm) subcutaneous mass was identified in the left region of the neck. On palpation, the mass was firm but mobile. Analysis of a blood sample revealed mildly low hemoglobin concentration (12.0 g/dL; reference range, 14 to 20.3 g/dL) and moderately high creatine kinase activity (2,305 U/L; reference range, 312 to 1,002 U/L). The WBC count was within reference limits. Radiography revealed a round, soft tissue opaque mass in the left region of the neck without apparent connection to the crop. Apart from the mass, the skeletal structures and internal organs were unremarkable. Because of financial constraints, the owner declined surgery and the parrot was initially treated orally with enrofloxacin,a itraconazole,b and meloxicamc at home. Cytologic examination of fine-needle aspirate samples of the mass obtained 2 days later revealed a large number of round cells with a small cytoplasmic rim, round to oval nuclei with dense chromatin, and visible nucleoli.

The mass decreased markedly in size after 1 week of treatment; a CT scan revealed a homogenous soft tissue mass in the left region of the neck without connection to the trachea, esophagus, or crop. Skeletal structures and internal organs were considered normal, and no other masses in any other organs were detected. The bird remained in a good clinical condition for 3 more months but was euthanized because of sudden onset of signs of depression and ulcer formation with severe inflammation at the distal portion of the mass. The parrot was submitted for a complete necropsy and ancillary testing.

On gross examination, the parrot was in a good body condition. Directly overlying the neck muscles in the cervical region, a large mass (2 × 3 × 4 cm) and a smaller mass (0.5 × 0.7 × 1 cm) were detected (Figure 1). The larger mass could be easily detached from the skin. It was smooth on the outside and contained approximately 1 mL of yellowish fluid with dark-green sediment. On drainage of the fluid, the tissue was off-white and pale red in color and composed of several lumps connected by a thin wall. The smaller solid red mass was positioned over the neck muscles, without any connection to the larger mass or the underlying tissue. Both thyroid glands appeared normal.

Figure 1—
Figure 1—

Photographs of the cervical region of an 18-year-old Senegal parrot (Poicephalus senegalus) that was euthanized 13 weeks after initial evaluation because of a rapidly growing mass in the region of the left side of the neck. A—A large fluid-filled mass and a smaller solid mass (asterisk) directly overlie the neck muscles. Bar = 2 cm. B—The larger mass was cut open and drained of its fluid, which revealed that it was cavitated with a smooth surface. The lining consisted of uneven walls composed of multiple nodules. Bar = 2 cm.

Citation: Journal of the American Veterinary Medical Association 243, 8; 10.2460/javma.243.8.1117

Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page

Histopathologic Findings

Samples of the lungs, liver, kidneys, proventriculus, ventriculus, skin, brain, and parts of the 2 masses were examined histologically. Tissues of the lungs, liver, kidneys, proventriculus, and ventriculus were apparently normal. Both the larger and the smaller mass appeared to be of thymic origin. In both masses, no clear distinction of the corticomedullary areas was possible. The larger mass contained mostly small mature lymphocytes and a few lymphoblasts at the edge that was interpreted as being the cortex. In the medullary region, clusters of large polygonal cells with abundant eosinophilic homogenous cytoplasm and a round, slightly vesiculated nucleus with inconspicuous nucleolus were interpreted as epithelial cells. Concentric clusters of epithelial cells, arranged multifocally and with a highly eosinophilic cytoplasm, were interpreted as Hassall's corpuscles (Figure 2). In the smaller mass, many small, mature lymphocytes and fewer lymphoblasts were present mainly in the region of the cortex. In the medullary area, Hassall's corpuscles were observed multifocally Both masses were enclosed and divided by moderate to large amounts of fibrovascular tissue. The skin above the 2 masses had a hyperplastic epidermis with a large number of fat cells in the dermis with foamy cytoplasm between collagen fibers of the connective tissue, which was interpreted as a local, fatty degeneration.

Figure 2—
Figure 2—

Photomicrograph of a section of the large mass from the Senegal parrot in Figure 1. Epithelial cells are arranged concentrically and interpreted as Hassall's corpuscles (arrowheads). Around the epithelial cells, a large number of mature lymphocytes and fewer lymphoblasts can be seen (asterisk). In between the lymphatic cells, there are a few large polygonal cells with abundant eosinophilic homogeneous cytoplasm, which are considered epithelial cells (arrows). H&E stain; bar = 100 μm.

Citation: Journal of the American Veterinary Medical Association 243, 8; 10.2460/javma.243.8.1117

Immunohistochemical staining with antibodies directed against CD3 (mouse anti-CD3 [T cells] antibodyd), CD20 (rabbit anti-CD20 [B cells] antibodye), and vimentinf (mouse anti-vimentin antibody) was performed. Briefly, slides were pretreated by microwave for CD3 staining (buffer pH, 9) and vimentin staining (buffer pH, 6), but were not pretreated for CD20 staining. Antibodies against CD3, CD20, and vimentin were diluted 1:50, 1:100, and 1:100, respectively, and incubated at room temperature (approx 25°C). A mouse antibody–labeled streptavidin-biotin kitg or rabbit antibody biotin-independent peroxidase-based kith was used as the secondary antibody, and 3-amino-9-ethylcarbazolei was applied as chromogen. Control sections of thymus and bursa obtained from healthy broiler chicks were positive for CD3, vimentin, or CD20. The mature lymphocytes in the cortical area of both masses were positive for CD3, confirming the T-cell origin (Figure 3). Results of immunohistochemical staining with antibodies directed against cytokeratinj were negative, but epithelial cells may stain variably with commonly used anti–cytokeratin antibodies.1 These epithelial cells were negative for vimentin; thus, mesenchymal origin was excluded (Figure 4). The combined histologic and immunohistochemical findings were suggestive of thymoma.

Figure 3—
Figure 3—

Photomicrograph of a section of the large mass from the Senegal parrot in Figure 1 following immunohistochemical staining for CD3. Notice that the lymphocytes are positive. CD3 (T-cell) immunohistochemical stain (mouse anti-CD3 antibody); bar = 100 μm.

Citation: Journal of the American Veterinary Medical Association 243, 8; 10.2460/javma.243.8.1117

Figure 4—
Figure 4—

Photomicrograph of a section of the large mass from the Senegal parrot in Figure 1 following immunohistochemical staining for vimentin. The stroma and vessel wall are strongly positive for vimentin. In between the mesenchymal cells, there are round cells with large amounts of cytoplasm that are negative for vimentin (arrows). Vimentin immunohistochemical stain (mouse anti-vimentin antibody); bar = 100 μm.

Citation: Journal of the American Veterinary Medical Association 243, 8; 10.2460/javma.243.8.1117

Morphologic Diagnosis and Case Summary

Morphologic diagnosis and case summary: lymphocyte-rich thymoma in a Senegal parrot.

Comments

The gross and histopathologic findings for the parrot of this report were consistent with lymphocyte-rich thymoma. Thymomas are localized, usually benign neoplasms that originate from epithelial cells of the thymus. In companion birds, thymomas have only rarely been described.1–3 Depending on the cells undergoing neoplastic transformation, they can either be classified as epithelial or lymphocytic thymomas.2 In birds, these tumors may develop anywhere in the subcutis of the neck, from the mandibular region to the thoracic inlet.1,2 On gross examination, tumors can appear cystic and hemorrhagic.1,2 Most often, the only clinical sign is an enlarging mass in the region of the neck, but signs related to the space-occupying effect of the mass, such as dysphagia, dysphonia, regurgitation, cough, or dyspnea, can also be observed.2,4,5 In domestic animals, thymomas may be associated with paraneoplastic complications, such as myasthenia gravis, or accompanied by megaesophagus or polymyositis,5,6 but these findings have never been reported for avian patients, to our knowledge.

In the case described in this report, differential diagnoses for the mass at the time of the initial examination included abscess, persistent hematoma, branchial cyst, and neoplasia of a cervical structure. The diagnosis of thymoma relies on cytologic examination of fine-needle aspiration samples or histologic examination of biopsy specimens. Histologically, thymomas have pleomorphic cell populations of small to moderately sized lymphocytes, lymphoblasts, and large reticular cells. Reticular cells are arranged in sheets with large, round to oval vesicular nuclei and a strongly eosinophilic cytoplasm. Mitotic figures are common. Reticular cells may stain for cytokeratin and proliferating cell nuclear antigen.1 Thymomas can easily be mistaken for thymic lymphoma because of their variable degree of lymphocytic infiltration; thus, several sections from different locations should be examined to identify evident epithelial stuctures.6 In the parrot of the present report, a mixed cell population was identified, as previously identified in studies7,8 of thymomas in dogs and cats. The histologic findings supported the suggested diagnosis of lymphocyte-rich thymoma.

Reports of thymoma in pet birds include cases of 4 budgerigars (Melopsittacus undulatus),5,9 2 of which were not further described but were mentioned in a survey of 168 neoplasms in budgerigars.9 In addition, thymomas in an adult finch of unspecified species,4 2 Java sparrows (Padda oryzivora),5,6 a peach-faced lovebird (Agapornis roseicollis),5 and a cockatiel (Nymphicus hollandicus)5 have been described. The masses in all cases were located in the neck region, mostly on the left side4,5 but also on the right side9 and in the submandibular space.5 The outcome was variable, with descriptions of either successful surgical removal6 or unsuccessful surgery in which the birds died as a result of excessive intraoperative hemorrhage.5 In addition, 1 bird was treated with prednisolone sodium phosphate orally but died 5 months after initial evaluation.5

Excision of thymomas is generally curative, given that they rarely metastasize.2,4 In comparison to mammals, thymomas in birds are located subcutaneously in the lateral aspect of the neck and therefore should be easy to remove, although invasion or attachment to vascular and other structures may complicate excision.4 Chemotherapy with prednisolone administered orally has been performed in 1 case, but the bird had little improvement.5 Given that excision of thymomas in dogs is facilitated by reducing tumor size with precedent radiation therapy, this may as well be beneficial in avian patients.5 The case described in the present report has contributed to the scarce reports of thymoma in psittacine birds. Although rare in older psittacine patients, lymphocyte-rich thymoma should nonetheless be included among the differential diagnoses of lateral neck masses.

a.

Baytril 2.5%, Bayer Health Care, Provet AG, Lyssach, Switzerland.

b.

Sporanox, Janssen-Cilag AG, Baar, Switzerland.

c.

Metacam, Boehringer Ingelheim (Schweiz) GmbH, Basel, Switzerland.

d.

DAKO M725401, DAKO Denmark A/S, Glostrup, Denmark.

e.

RB-9013-P, NeoMarkers Inc, Fremont, Calif.

f.

DAKO M7020, DAKO Denmark A/S, Glostrup, Denmark.

g.

LSAB, DAKO K0690, DAKO Denmark A/S, Glostrup, Denmark.

h.

EnVision, DAKO K5007, DAKO Denmark A/S, Glostrup, Denmark.

i.

AEC, DAKO K3464, DAKO Denmark A/S, Glostrup, Denmark.

j.

DAKO M082101, DAKO Denmark A/S, Glostrup, Denmark.

References

  • 1. Schmidt RE, Reavill DR, Phalen DN. Lymphatic and hematopoietic system. In: Pathology of pet and aviary birds. Ames, Iowa: Blackwell Publishing Co, 2003; 131147.

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  • 2. Reavill DR. Tumors of pet birds. Vet Clin North Am Exot Anim Pract 2004; 7: 537560.

  • 3. Coleman C. Lymphoid neoplasia in pet birds: a review. J Avian Med Surg 1995; 9: 37.

  • 4. Latimer KS, Rakich PM, Weiss R. Thymoma in a finch. J Avian Med Surg 2001; 15: 3739.

  • 5. Rae MA, Shafar D. Thymoma in caged birds, in Proceedings. Annu Conf Expo Assoc Avian Vet 1996; 101108.

  • 6. Maeda H, Ozaki K, Fukui S, et al. Thymoma in a Java sparrow (Padda oryzivora). Avian Pathol 1994; 23: 353357.

  • 7. Zitz JC, Birchard SJ, Couto GC, et al. Results of excision of thymoma in cats and dogs: 20 cases (1984–2005). J Am Vet Med Assoc 2008; 232: 11861192.

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  • 8. Rae CA, Jacobs RM, Couto CG. A comparison between the cytological and histological characteristics in thirteen canine and feline thymomas. Can Vet J 1989; 30: 497500.

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    • Export Citation
  • 9. Blackmore DK. The clinical approach to tumours in cage birds. I. The pathology and incidence of neoplasia in pet birds. J Small Anim Pract 1966; 7: 217223.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Figure 1—

    Photographs of the cervical region of an 18-year-old Senegal parrot (Poicephalus senegalus) that was euthanized 13 weeks after initial evaluation because of a rapidly growing mass in the region of the left side of the neck. A—A large fluid-filled mass and a smaller solid mass (asterisk) directly overlie the neck muscles. Bar = 2 cm. B—The larger mass was cut open and drained of its fluid, which revealed that it was cavitated with a smooth surface. The lining consisted of uneven walls composed of multiple nodules. Bar = 2 cm.

  • Figure 2—

    Photomicrograph of a section of the large mass from the Senegal parrot in Figure 1. Epithelial cells are arranged concentrically and interpreted as Hassall's corpuscles (arrowheads). Around the epithelial cells, a large number of mature lymphocytes and fewer lymphoblasts can be seen (asterisk). In between the lymphatic cells, there are a few large polygonal cells with abundant eosinophilic homogeneous cytoplasm, which are considered epithelial cells (arrows). H&E stain; bar = 100 μm.

  • Figure 3—

    Photomicrograph of a section of the large mass from the Senegal parrot in Figure 1 following immunohistochemical staining for CD3. Notice that the lymphocytes are positive. CD3 (T-cell) immunohistochemical stain (mouse anti-CD3 antibody); bar = 100 μm.

  • Figure 4—

    Photomicrograph of a section of the large mass from the Senegal parrot in Figure 1 following immunohistochemical staining for vimentin. The stroma and vessel wall are strongly positive for vimentin. In between the mesenchymal cells, there are round cells with large amounts of cytoplasm that are negative for vimentin (arrows). Vimentin immunohistochemical stain (mouse anti-vimentin antibody); bar = 100 μm.

  • 1. Schmidt RE, Reavill DR, Phalen DN. Lymphatic and hematopoietic system. In: Pathology of pet and aviary birds. Ames, Iowa: Blackwell Publishing Co, 2003; 131147.

    • Search Google Scholar
    • Export Citation
  • 2. Reavill DR. Tumors of pet birds. Vet Clin North Am Exot Anim Pract 2004; 7: 537560.

  • 3. Coleman C. Lymphoid neoplasia in pet birds: a review. J Avian Med Surg 1995; 9: 37.

  • 4. Latimer KS, Rakich PM, Weiss R. Thymoma in a finch. J Avian Med Surg 2001; 15: 3739.

  • 5. Rae MA, Shafar D. Thymoma in caged birds, in Proceedings. Annu Conf Expo Assoc Avian Vet 1996; 101108.

  • 6. Maeda H, Ozaki K, Fukui S, et al. Thymoma in a Java sparrow (Padda oryzivora). Avian Pathol 1994; 23: 353357.

  • 7. Zitz JC, Birchard SJ, Couto GC, et al. Results of excision of thymoma in cats and dogs: 20 cases (1984–2005). J Am Vet Med Assoc 2008; 232: 11861192.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Rae CA, Jacobs RM, Couto CG. A comparison between the cytological and histological characteristics in thirteen canine and feline thymomas. Can Vet J 1989; 30: 497500.

    • Search Google Scholar
    • Export Citation
  • 9. Blackmore DK. The clinical approach to tumours in cage birds. I. The pathology and incidence of neoplasia in pet birds. J Small Anim Pract 1966; 7: 217223.

    • Crossref
    • Search Google Scholar
    • Export Citation

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