Granulocytic Sarcoma in a Budgerigar (Melopsittacus undulatus)

AnaPatricia García, Kenneth S. Latimer, W. L. Steffens, and Branson W. Ritchie

College of Veterinary Medicine, The University of Georgia, Athens, Georgia 30602.

Abstract. An adult female Budgerigar was presented with dyspnea and abdominal distention. After a few days of supportive treatment the bird died and a necropsy was performed. A large, cystic, perihepatic mass was present. Microscopically, this mass was composed of multifocal to coalescing aggregates of proliferating heterophils. The neoplastic cell population showed maturation from the blast stage to differentiated granulocytes. Electron microscopy demonstrated that the granulocytic cells belonged to the heterophilic lineage. The final diagnosis was granulocytic sarcoma.

Key Words: Avian, Budgerigar, Melopsittacus undulatus, Chloroma, Granulocytic sarcoma, Heterophil, Myelocytoma, Myeloblastoma

Introduction

Granulocytic leukemia is the neoplastic proliferation of granulocytes originating in the bone marrow. Infrequently, granulocytic leukemia in mammals is associated with the formation of sarcomatous tissue masses called chloromas. ¹ These neoplastic tissue masses usually arise in visceral organs. They are characterized by a green color that is imparted by myeloperoxidase in the specific (azurophilic) granules of neutrophils. Similar hematopoietic neoplasms in birds are known by the synonyms granulocytic sarcoma, myelocytoma, or myeloblastoma. These neoplasms are associated with the proliferation of heterophils and their precursors, which lack myeloperoxidase. Granulocytic sarcoma is relatively common in domestic fowls but is rare in exotic birds. ^1-3 The purpose of this case report is to describe a granulocytic sarcoma in a Budgerigar.

Case Report

An adult female Budgerigar (Melopsittacus undulatus) was presented to the University of Georgia Veterinary Medical Teaching Hospital with abdominal distention and dyspnea. The bird died a few days after admission despite supportive treatment. Necropsy examination of the animal revealed a large, cystic, perihepatic mass.

Microscopically, the mass was composed of multifocal to coalescing aggregates of proliferating granulocytes (Fig. 1). This cell population showed maturation from myeloblasts to more differentiated granulocytes (Fig. 2). Cytoplasmic granules appeared red and slightly elongate, suggesting heterophilc cell lineage. The neoplasm also contained numerous variably sized and shaped vascular spaces. More normal sections of liver contained scattered foci of extramedullary heterophil production, often centered around blood vessels beneath the hepatic capsule.

Fig. 1. Budgerigar, granulocytic sarcoma, H&E stain. Perihepatic mass appears hypercellular.	Fig. 2. Budgerigar, granulocytic sarcoma, H&E stain. More differentiated cells contain red cytoplasmic granules.

Electron microscopy of ultrathin sections of the mass revealed two types of neoplastic cells. The first cell type consisted of large, round blasts with a thin rim of cytoplasm containing occasional granules. The second cell type appeared smaller, round , and more differentiated. These cells had more aggregated chromatin within cell nuclei and more abundant cytoplasm containing membrane-bound granules (Fig. 3). The cytoplasmic granules were round in cross section and elongated in longitudinal section. Some of the granules were more electron dense than others and occasionally appeared to have a lighter central core (Fig. 4). These ultrastructural characteristics were typical of heterophilic lineage. The definitive diagnosis in this Budgerigar was perihepatic granulocytic sarcoma.

Fig. 3. Budgerigar, granulocytic sarcoma, electron micrograph. Heterophil granules are round in cross section and elongate in oblique or longitudinal section. Notice variation in granule radiodensity.	Fig. 4. Budgerigar, granulocytic sarcoma, electron micrograph. More radiodense heterophil granules occasionally have a lighter central core. Radiolucent granules also are present.

Discussion

Neoplasia is a frequent cause of death in pet Budgerigars (Melopsittacus undulatus), affecting more than 15% of birds that are examined at necropsy. ¹ The most common neoplasms in Budgerigars are carcinomas of the kidney, ovary, and testis. In contrast, hematopoietic neoplasms are rare in Budgerigars. Carcinomas of the genitourinary tract and fibrosarcomas in chickens are part of a spectrum of neoplasms that may be caused by infectious type C retroviruses (avian leukosis/sarcoma viruses). In addition, two similar forms of hematopoietic neoplasia (designated myelocytomatosis and myeloblastosis) have been observed in chickens. These neoplastic diseases are associated with avian myeloblastosis virus and often result in hepatomegaly and splenomegaly from neoplastic cell infiltration. ¹ Furthermore, myelocytomatosis is associated with the formation of neoplasms on the surface of bones with intimate contact to the periosteum. These neoplasms consist of compact masses of uniform myelocytes. In contrast, myeloblastosis affects most parenchymatous organs and is characterized by massive intravascular and extravascular accumulations of myeloblasts with a variable proportion of more differentiated myelocytes. ²

The avian leukosis/sarcoma viruses are closely related and, depending on their genetic makeup, cause a variety of neoplasms with short to long latencies. Some viral strains such as avian myeloblastosis virus, avian erythroblastosis virus, and the sarcoma viruses contain specific viral oncogenes that cause rapid neoplastic transformation of target cells with subsequent tumor development within a few days or weeks. These avian leukosis/sarcoma viruses of chickens have been divided into six subgroups (A, B, C, D, E and J) on the basis of their host range in chicken embryo fibroblasts of different genetic types, interference patterns with members of the same and different viral groups, and type of viral envelope antigens. Viruses of subgroup A and B occur as common exogenous viruses in the field. In contrast, viruses of subgroups C and D rarely have been associated with field disease in chickens. The subgroup E viruses include the ubiquitous endogenous leukosis viruses of low pathogenicity. ² Subgroup J viruses have been isolated from meat-type chickens and are associated with an increased incidence of myelocytomatosis. ^2,3

In chickens and other animals harboring infectious retroviruses, the virus particles can be detected readily by electron microscopic examination of normal or neoplastic tissues. However, electron microscopic search for retroviral particles
in budgerigar neoplasms has been unrewarding. ⁴ Using immunodiagnostic techniques, avian leukosis viral antigens have been detected in sera from tumor-bearing Budgerigars using an enzyme-linked immunosorbant (ELISA) assay. ⁵ In addition, renal tumor tissues from Budgerigars were positive for the RAV -2 strain of avian leukosis virus using dot-blot analysis and Southern blot hybridization. These data suggest that avian retroviruses may be implicated as etiologic agents of certain neoplasms in Budgerigars. In the Budgerigar of this report, we did not observed viral particles in granulocytic sarcoma tissue prepared for electron microscopic examination. Further analysis of neoplastic tissue will be required to confirm or refute the presence of retroviruses in this neoplasm.

Granulocytic sarcoma (chloroma, myelocytomatosis, myeloblastic sarcoma, myelocytic sarcoma) has been reported in four Budgerigars and a White-tailed Black Cockatoo (Calyptorhynchus funereus latirostris). ⁶ The histologic differential diagnosis for these lesions also includes osseous metaplasia, extramedullary hematopoiesis, myelolipoma, and hemangiolipoma. ⁷ Osseous metaplasia is recognized by the presence of osteoid and spicules of mineralized bone associated with the hematopoietic cells. Extramedullary hematopoiesis occurs with some frequency in birds and may be observed in diverse locations including the spleen, liver, kidney, adrenal gland, gastrointestinal tract, heart, and dura mater. Histologically, extramedullary hematopoiesis is associated with the production of mature leukocytes, erythrocytes, and/or thrombocytes in any combination. Hematopoietic cell proliferation is unaccompanied by sarcomatous tissue masses. Myelolipoma consists of the coproduction of hematopoietic cells and lipocytes. These masses are observed most commonly in the subcutis and liver, but also may be observed within the thoracoabdominal cavity. ^7,8 Hemangiolipoma consists of adipose tissue and a vasoformative component similar to hemangioma. The diagnosis of granulocytic sarcoma is based upon the presence of a sarcomatous tissue mass composed of proliferating myeloblasts that show little differentiation to mature granulocytes.

References

1. Latimer KS: Oncology. In: Ritchie BW, Harrison GJ, and Harrison LR. (eds): Avian Medicine: Principles and Applications. Wingers Publishing, Inc. , Lake Worth, Florida, pp. 667-669, 1994.

2. Payne LN, Fadly AM: Leukosis/Sarcoma group. In: Calnek BW, Barnes HJ, Beard CW, McDougald LR, Saif YM (eds): Diseases of Poultry 10 ed. Iowa State University Press, Ames, IA 1997, pp. 414-466.

3. Payne LN, Gillespie AM Howes K: Myeloid leukaemogenicity and transmission of the HPRS-103 strain of avian leukosis virus. Leukemia 6:1167-1176, 1992.

4. Gardner MB, Rongey RW, Sarma P, Arnstein P: Electron microscopic search for retrovirus in spontaneous tumors of the parakeet. Vet Pathol 18: 700-703, 1981.

5. Gould WJ, O’Connell PH, Shivaprasad HL, Yeager AE, Schat KA: Detection of retrovirus sequences in budgerigars with tumours. Avian Pathol 22: 33-45, 1993.

6. Reece RL: Some observations on naturally occurring neoplasms in birds in the State of Victoria, Australia. Avian Pathol 21:3-32, 1992.

7. Latimer KS, Rakich PM: Subcutaneous and hepatic myelolipomas in four exotic birds. Vet Pathol 32:84-87, 1995.

8. Andreasen JR, Andreasen CB, Latimer KS, Oliphant JLH: Thoracoabdominal myelolipomas and carcinoma in a lovebird (Agapornis sp. ). J Vet Diagn Invest 7:271-272, 1995.

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