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Treatment of nonepitheliotropic cutaneous b-cell lymphoma in an umbrella cockatoo (Cacatua alba).

Abstract. A 3.5-year-old umbrella cockatoo (Cacatua alba) was presented because of the development of widely disseminated subcutaneous nodules. The diagnostic work-up included a complete blood count, plasma biochemical analysis, and whole body radiographs. Biopsy samples of the skin lesions were submitted for histopathologic evaluation, bacterial culture and sensitivity testing, immunohistochemistry staining, and acid-fast staining. The diagnosis was nonepitheliotropic cutaneous B-cell lymphoma with a leukemic blood picture. The bird was treated with a chemotherapeutic regimen consisting of vincristine and chlorambucil for 17 weeks. During treatment, the complete blood count was monitored every 1-3 weeks, and the plasma biochemical analysis was monitored every 3-4 weeks. The bird was in partial remission on week 9. On week 17, the bird became acutely ill and was fluffed, depressed, anorectic, and anemic. The chemotherapeutic regimen was discontinued. At this time, the bird had a consistent lymphocytosis but no neoplastic lymphocytes were seen in the general circulation. At week 29 the bird was in complete remission and remains in complete remission 8 years after chemotherapy was discontinued.

Key words: nonepitheliotropic, cutaneous lymphoma, chemotherapy, vincristine, chlorambucil, avian, umbrella cockatoo, Cacatua alba

Clinical Report

A 3.5-year-old female umbrella cockatoo (Cacatua alba) was presented for examination because of the development of multifocal subcutaneous nodules. The owner had first noticed the nodules 1 week previously. During the following week, the owner reported that the nodules had increased in both number and size.

On presentation, the bird appeared bright and alert, was well hydrated, and weighed 517 g. On physical examination, multifocal subcutaneous nodules ranging in diameter from 3 mm to 2 cm, some of which were coalescing, were observed (Fig 1). Large, longitudinal yellow plaques extended along the skin on the abdomen from the caudal aspect of the keel to the vent (Fig 1). Approximately 80% of the feather follicles on the proventer region were enlarged. No other abnormalities were observed. The bird was kept in a room with 4 other cockatoos (2 clutch mates and the 2 parents). According to the owner, all the other birds in the household appeared healthy.

The initial diagnostic work-up included a complete blood count (CBC), plasma biochemical analysis, whole body radiographs, direct fecal examination, and fecal Gram's stain. Hematologic abnormalities included a leukocytosis (75 000 cells/[micro]l; reference range, 4000-10 000 cells/[micro]l) (1) characterized by a lymphocytosis (49 500 cells/[micro]l;; reference range, 1800-5000 cells/[micro]l). (1) Approximately 10% of the lymphocyte population was composed of lymphoblastic cells. Results of the plasma biochemical analysis revealed hypoproteinemia (2.8 g/dl; reference range, 3-5.5 g/dl) with hypoalbuminemia (0.7 g/dl; reference range, 1.2-3.2 g/dl) and increased concentrations of aspartate anainotranferase (AST; 513 U/L; reference range, 20-350 U/L) and creatinine phosphokinase (CPK; 1104 U/L; reference range, 50400 U/L).1 Results of a direct fecal examination and fecal Gram's stain were unremarkable. On survey radiographs, a widening of the hepatic silhouette was observed.


The primary differential diagnoses for the skin lesions were neoplasia and bacterial or fungal granulomas. The bird was anesthetized with isoflurane, and 2 skin biopsy samples containing abnormal nodules were collected from the proventer region. Sections of the samples were submitted for bacterial culture and sensitivity testing. No bacterial growth was obtained on culture. On histologic evaluation, large coalescing nodules of sheets of neoplastic lymphocytes extending from the dermal epidermal interface to the deep border in the middermis were observed. The cells had a pleomorphic appearance, ranging from cells with small to scant amounts of a fine granular amphophilic cytoplasm to cells with more abundant amphophilic cytoplasm and a more vesicular oval cell nucleus. The cells had indistinct cytoplasmic borders. Heterophils, plasma cells, and macrophages were scattered throughout the section. Occasional cells were identified with large globular, slightly refractile, pale eosinophilic cytoplasmic pigments. These cells were interpreted as Russell bodies (Mott cells). The mitotic index of the neoplastic cells was 0-1 per high-power field. Overlying epithelium and the epithelium of the feather follicles were not involved (Fig 2). Because of the pleomorphic nature of the cellular infiltrates, Ziehl-Nielsen and Fite stains were applied, and results of both stains were negative for acid-fast organisms. The working diagnosis was a nonepitheliotropic cutaneous lymphoma.

The diagnosis of cutaneous lymphoma and the treatment options available were discussed with the owner. The owner elected to pursue a course of chemotherapy, which was begun 7 days after initial presentation. The chemotherapeutic regimen included vincristine (0.1 mg/kg IV every 1-3 weeks; Faulding Pharmaceutical, Elizabeth, N J, USA) and chlorambucil (2 mg/kg PO twice weekly; Leukeran, Catalytic Pharmaceutical, Greenville, NC, USA). The bird received chlorambucil for 17 weeks, which was diluted in water to facilitate administration. The vincristine was administered on weeks 1, 4, 5, 7, 8, 11, 12, and 14. To administer the vincristine, the bird was anesthetized with isoflurane by mask induction, and a 25-gauge butterfly catheter was inserted into the ulnar vein. The vincristine was administered as a slow bolus over a 2 3-minute period, followed by 3 ml of saline to flush the catheter. The treatment regimen was adjusted several times because of the owner's inability to travel the long distance to the clinic. During treatment, the CBC was monitored every 1-3 weeks (Table 1), and the plasma biochemical analysis was repeated every 34 weeks. At weeks 0, 5, 11, 17, and 23, the thrombocyte population was estimated. Results showed the count remained stable (1-3 thrombocytes per oil immersion field) throughout the treatment period, with mild to moderate clumping of thrombocytes. After starting treatment, the leukocytosis gradually decreased (Table 1). The bird was in partial remission on week 9.


Over the course of the therapy, 2 more skin biopsy samples were collected (weeks 5 and 12). Biopsy results were similar to previous results, with the exception of fewer inflammatory cells. The biopsy sample at week 5 was submitted for immunohistochemistry (John Wojcieszyn, PhD, IHC Services, 185 Mountain Valley Drive, Smithville, TX, USA) with a B-cell marker, BLA.36 (monoclonal rabbit antibody), and a T-cell marker, CD3 (polyclonal rabbit antibody). Approximately 90% of the neoplastic lymphocytes were positive for the BLA.36 (Fig 3). Only 10% of the neoplastic lymphocytes stained positive with CD3. The control used was an avian spleen, in which BLA-positive-staining B cells were present in small aggregates interpreted as germinal centers and scattered in areas of the periellipsoid sheaths. Positive CD3 T cells were present in the periarteriolar lymphatic sheaths (follicular white pulp). Electron microscopic examination of formalin-fixed tissue did not reveal the presence of virions.


On week 17 of treatment, the bird presented with severe depression and lethargy and was hospitalized for supportive care and diagnostic testing. Chemotherapy was discontinued at this point. The most relevant hematologic abnormality was anemia (Hct 14%, reference range, 42%- 55%) with 2+ polychromasia. The weight was 507 g. Abnormal results on plasma biochemical analysis were hypoproteinemia (2.6 g/dl), hypoalbuminemia (0.8 g/dl), hypocalcemia (6.6 mg/dl; reference range 7.6-12 mg/dl), increased AST activity (3368 U), increased CPK activity (6500 U/L), and hyperuricemia (64.5 mg/dl; reference range 2-10 mg/dl). (1) The bird was treated with supportive care (lactated Ringer's solution, 20-30 ml SC q12h and oxygen therapy). A CBC and a plasma biochemical analysis done on week 18 (7 days after beginning supportive care) revealed the hematocrit had increased to 35% and the AST activity had decreased to 519 U/L. All other values were within reference ranges. After 9 days of supportive care, the bird showed significant improvement and was discharged to the owner. At week 23 (6 weeks after the discontinuation of chemotherapy), results of a CBC did not show any significant abnormalities, and the bird remained in partial remission. At week 29 (12 weeks after discontinuing treatment) no subcutaneous nodules were observed (Fig 4). The bird has been in complete remission for 8 years.



In this clinical report, we describe the successful treatment of nonepitheliotropic cutaneous B-cell lymphoma in an umbrella cockatoo. Lymphoid neoplasia is the most common neoplastic condition reported in the avian patient. (2-19) Neoplasms of lymphoid origin have been described in birds from the following orders: Anseriformes, Charadriiformes, Columbiformes, Ciconiiformes, Galliformes, Passeriformes, Psittaciformes, and Struthioniformes. (3,5,6,11,12,14,16-19) Lymphoid neoplasia is generally classified into 2 forms: lymphoma and lymphoid leukemia. (20) Lymphoma usually originates in primary or secondary lymphoid tissue and can involve multiple sites in the body. Furthermore, neoplastic lymphocytes might appear in the peripheral circulation. (5,8 10,15,21) Lymphoid leukemia originates in the bone marrow and could affect other organs, such as the spleen and liver to a lesser degree. It is characterized by an elevation of circulating lymphocytes, many of which are blast cells. White blood cell counts can exceed 100 000 cells/[micro]l, with a predominant lymphocytosis. (22) In psittacine birds, lymphoma is the most common form of lymphoid neoplasia reported. (2-4,8,11,18,21-23)

Lymphoma can present as a disseminated, multisystemic disease involving multiple tissues of the body or as isolated lesions on the skin. (2-4,8,11,18,21-23) It is characterized by the formation of white to yellow tissue discolorations, sarcomatous masses, or both. The most consistent clinical finding associated with cutaneous lymphoma in psittacine birds is the presence of multifocal or localized cutaneous nodule(s) with or without ulceration.> In this cockatoo, the clinical presentation, CBC results, and histopathologic findings confirmed the diagnosis of cutaneous lymphoma with a leukemic blood picture. Because a bone marrow biopsy was not performed, we cannot completely rule out the bone marrow as the source of the neoplastic lymphocytes. It is unlikely that the bursa of Fabricius was the source, although this also cannot be completely excluded. Four cases of lymphoma involving the bursa of Fabricius in adult psittacine birds (>1 year old) have been identified (D. R. R., unpublished data, 2008). All these birds with bursal involvement had significant clinical signs associated with the tumor mass forming within the cloaca. The origin of the neoplastic cells identified within the peripheral circulation was not known.

Lymphoid neoplasia has been studied extensively in poultry because of the economic impact on the food industry. In chickens, lymphoid neoplasia has been associated with infections by a herpes virus (Marek's disease), avian leukosis virus, and reticuloendotheliosis virus. (24) Molecular investigations suggested a retroviral cause for multicentric lymphoma in a starling. (14) Retroviral-induced lymphoma has been suspected in other passerine birds but remains to be proven. Research is limited on the cause of lymphoid neoplasia in psittacine birds. Results of attempts to identify viral particles in tumors from budgerigars (Melapsittacus undulatus) were negative. (25) In another study, antigen from avian leukosis virus was found in sera from budgerigars suspected of having renal tumors. (26) However, the authors did not demonstrate a direct correlation between the presence of avian leukosis antigen in the sera and tumor formation. Avian leukosis DNA sequences have been detected in tumors from budgerigars by hybridization techniques. (27) However a correlation between the presence of the viral DNA and tumor formation was not established. Ramos-Vara et al (11) failed to identify exogenous avian retrovirus (RAV-1) in a lymphoma lesion from a scarlet macaw (Ara macao). Currently, no conclusive evidence correlates lymphoid neoplasia with viral infection in psittacine birds. (25,27) In this cockatoo, virions were not found within the neoplastic cells on electron microscopic evaluation of formalin-fixed tissue.

The diagnosis of lymphoma in psittacine birds is made by cytologic or histopathologic evaluation of lesions. Differential diagnoses include other neoplasia and bacterial or fungal granulomas. Results of bacterial culture and sensitivity testing in this case did not produce evidence of bacterial involvement. The acid-fast stain of the biopsy sample was negative for acid-fast organisms. Furthermore, on histopathologic evaluation, neither granuloma formation nor fungal elements were evident at the lesion sites.

A CBC, a plasma biochemical analysis, and survey radiographs are essential diagnostic tools in assessing an ill avian patient. In this cockatoo, the results of the CBC identified a severe leukocytosis, characterized by a lymphocytosis and abnormal lymphocytes in the general circulation. The initial abnormal findings in the plasma biochemical results were unremarkable and nonspecific. Hypoalbuminemia is generally associated with chronic malnutrition or hepatic disease. However, the method of laboratory analysis could influence the test results. Determination of albumin concentration is more accurate by plasma or serum protein electrophoresis; however, bromcresyl green dye binding usually results in false low test results in avian samples when compared with a bovine serum albumin standard. The radiographs revealed widening of the hepatic silhouette. We suspect this abnormality was caused by hepatomegaly because of the caudodorsal displacement of the proventriculus.

However, hepatic involvement cannot be completely ruled out because liver aspirates or biopsy samples were not collected. Even though hepatomegaly was suspected, the bird did not show any signs nor did laboratory findings suggest hepatic function compromise. Hepatomegaly due to the infiltration of neoplastic cells into the hepatic parenchyma has been reported in birds with lymphoma. (4,6,9,14,23)

Immunocytochemistry with monoclonal antibodies against cell surface glycoproteins is frequently used in canine medicine to identify lymphoid malignancies as either B-lymphocyte or T-lymphocyte origin. (28) Other modalities being developed for use in small mammal medicine are flow cytometry and polymerase chain reaction for antigen receptor rearrangement. However, at this time, these tests are neither available nor validated for use in avian species. In small animal medicine, assessing phenotype is of prognostic significance, because dogs with T-cell lymphoma have shorter remission and survival times than dogs with B-cell tumors. (29,30) The avian lymphocytes can be differentiated through immunohistochemistry with the use of T- and B-cell specific antibodies. (7,8) However, the differentiation of avian lymphoma into cell subpopulations has been poorly documented. Latimer et al (8) described a case of cutaneous T-cell-rich B-cell lymphoma in an umbrella cockatoo. The cell population consisted of small, well-differentiated, reactive T cells and neoplastic B cells. The tumors in our patient consisted of mostly B cells, with few scattered T cells. The second biopsy was used for the immunohistochemistry because less inflammation effaced the neoplastic population. In birds, it is unknown whether response to treatment differs on the basis of cell type of the lymphoid malignancy. The positive response seen in this cockatoo correlates with what is known in small animal medicine, wherein response to treatment and long-term prognosis are more favorable with B-cell tumors than with T-cell tumors. (29,30)

Treatment of lymphoma in small animal medicine is based on several factors, including clinical stage (I, II, III, IV, V) and substage (a, b), tumor histologic grade, and the owner's commitment. The response to treatment is classified as complete remission, partial remission, stable disease, or progressive disease. (31) The treatment of lymphoma in canine medicine can be very rewarding. In small animal oncology, standard chemotherapeutic protocols are used successfully to prolong survival time and preserve a high quality of life. Reports of lymphoma treatment in birds are scant. Currently, no standard protocols have proved successful in the long-term management of lymphoma in psittacine birds. Chemotherapy and radiation therapy have been used to treat lymphoid neoplasia in psittacine birds with varying results. (3,18,21) An Amazon parrot treated with prednisone twice daily survived for 32 weeks? An African grey parrot (Psittacus erithacus) treated with orthovoltage x-ray teletherapy survived 8 weeks. (18) A Moluccan cockatoo (Cacatua moluccensis) with lymphoma was treated with a cyclic chemotherapeutic regimen comprising prednisone, cyclophosphamide, vincristine, doxorubicin, L-asparagine, and alpha-interferon. The authors reported a complete response to treatment of the solid tumors, but only a stable disease state was reached in the leukemic phase of the disease. (21) The protocol we used was a modification of one described to treat lymphoma in a pekin duck (Anas platyrhynchos domesticus). (9) We elected to treat this patient with vincristine and chlorambucil because of their known efficacy in the treatment of lymphoid neoplasia in mammalian species. These drugs are usually combined with a corticosteroid to increase the efficacy of the treatment protocol. In this case, we decided not to include a corticosteroid in the treatment protocol because of their reported adverse effects in avian species. (32)

Our treatment goal was to achieve remission of the cutaneous lesions without adversely affecting the patient. The initial plan was to treat the bird for 23 weeks with a cyclic treatment protocol consisting of vincristine IV (every 1-3 weeks) and chlorambucil PO (twice weekly). The vincristine administration schedule varied because of owner-related conflicts that precluded compliance with our set schedule. The patient was only treated for 17 weeks. It received a total of 8 IV vincristine injections and twice weekly doses of oral chlorambucil. During 16 weeks of treatment, the bird did not show any abnormal clinical signs or abnormal results on the plasma biochemical analysis. The most consistent abnormality on the CBC, in addition to the leukocytosis with lymphocytosis, was heteropenia (see Table I). Artifactual decrease in the percentage of heterophils can be caused by severe leukocytosis because of lymphocytosis. This is often the case when the differential count is reported by percentages. (33) The heteropenia observed during chemotherapy was partly attributed to myelosuppression from the chemotherapeutic regimen. However, thrombocytopenia was not evident during the treatment period. Accurate thrombocyte counts are difficult to determine because of clumping. We relied on rough estimates (thrombocytes seen per oil immersion field, reference range 2-3 per oil immersion field) (34) to assess the thrombocyte population during chemotherapy. Myelosuppression is the most common toxicosis associated with chemotherapy. In dogs and cats, neutropenia is the most common cytopenia associated with chemotherapy-induced myelosuppression. The effect of chemotherapy on neutrophils is related to their rapid bone marrow transit time and short circulating half-life. The neutrophil counts usually return to normal values within 36-72 hours after the nadir. Sepsis is the most common complication associated with neutropenia (35) Even though it was a potential complication in this case, this bird did not show evidence of sepsis. However, on week 17, the bird became severely ill. The most significant finding was anemia, which could have been attributed to the cumulative effects of the chemotherapeutic agents. The most common adverse effects associated with chlorambucil therapy include myelosuppression and gastrointestinal toxicity. In this case, bone marrow suppression or blood loss through gastrointestinal ulceration could have contributed to the anemia. Chemotherapy was halted at week 17 of treatment when the bird became ill, which was 6 weeks earlier than was planned. The leukemic blood picture resolved; however, a few small cutaneous lesions were still present. No further clinical signs of illness or abnormal hematologic or biochemical results were seen on follow-up examinations. The remaining subcutaneous tumors continued to decrease in size after cessation of chemotherapy and were not seen at 12 weeks after chemotherapy was discontinued. Residual drug effect may have contributed to the continued decrease in tumor size. Furthermore, the tumors were associated with inflammation; the destruction of the neoplastic cells and decreased tumor growth might have led to reduced inflammation, and hence decreased tumor size. The 17-week chemotherapy regimen was sufficient to achieve complete remission of the cutaneous lymphoma in this patient.

The field of psittacine bird oncology is still in its infancy. Data regarding effectiveness or treatment of choice are limited. In this report, we describe the successful chemotherapeutic treatment of cutaneous lymphoma in an umbrella cockatoo. The bird remains in remission 8 years after discontinuing chemotherapy.


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Samuel Rivera, DVM, MS, Dipl ABVP (Avian), James R. McClearen, DVM, and Drury R. Reavill, DVM, Dipl ABVP (Avian), Dipl ACVP

From the Department of Animal Health, Zoo Atlanta, 800 Cherokee Avenue SE, Atlanta, GA 30315-1440, USA (Rivera): Bells Ferry Veterinary Hospital, 6410 Highway 92, Acworth, GA 30102, USA (McClearen), and Zoo/Exotic Pathology Service, 2825 KOVR Drive. West Sacramento, CA 95605, USA (Reavill).
Table 1. Hematologic results from an umbrella cockatoo
undergoing chemotherapy to treat cutaneous lymphosarcoma. Week 0
represents the values at presentation.


Parameter                                         0      3      4

White blood cells, x [10.sup.3] cells/[micro]l    75     70     76
  Heterophils, x [10.sup.3] cells/[micro]l       22.5   11.2   13.7
  Lymphocytes, x [10.sup.3] cells/[micro]l       49.5   58.8   62.3
  Monocytes, x [10.sup.3] cells/[micro]l          0      0      0
  Eosinophils, x [10.sup.3] cells/[micro]l       2.3     0      0
  Basophils, x [10.sup.3] cells/[micro]l         0.8     0      0
Packed cell volume, %                             44     45     45


Parameter                                         5      7      8

White blood cells, x [10.sup.3] cells/[micro]l    42     72     29
  Heterophils, x [10.sup.3] cells/[micro]l       5.9    20.2   4.4
  Lymphocytes, x [10.sup.3] cells/[micro]l       36.1   51.8   24.7
  Monocytes, x [10.sup.3] cells/[micro]l          0      0      0
  Eosinophils, x [10.sup.3] cells/[micro]l        0      0      0
  Basophils, x [10.sup.3] cells/[micro]l          0      0      0
Packed cell volume, %                             45     47     50


Parameter                                         11     12     14

White blood cells, x [10.sup.3] cells/[micro]l    37     30     19
  Heterophils, x [10.sup.3] cells/[micro]l       1.1    0.9    3.0
  Lymphocytes, x [10.sup.3] cells/[micro]l       35.9   29.1   15.8
  Monocytes, x [10.sup.3] cells/[micro]l          0      0     0.2
  Eosinophils, x [10.sup.3] cells/[micro]l        0      0      0
  Basophils, x [10.sup.3] cells/[micro]l          0      0      0
Packed cell volume, %                             45     50     43


Parameter                                         15    17    18

White blood cells, x [10.sup.3] cells/[micro]l    30    11    13
  Heterophils, x [10.sup.3] cells/[micro]l       1.2    4.7   2.6
  Lymphocytes, x [10.sup.3] cells/[micro]l       28.8   5.5   9.9
  Monocytes, x [10.sup.3] cells/[micro]l          0     0.3    0
  Eosinophils, x [10.sup.3] cells/[micro]l        0     0.2   0.5
  Basophils, x [10.sup.3] cells/[micro]l          0     0.3    0
Packed cell volume, %                             38    14    35

Parameter                                         21    range (1)

White blood cells, x [10.sup.3] cells/[micro]l    26      4-10
  Heterophils, x [10.sup.3] cells/[micro]l       4.2     4.5-8.0
  Lymphocytes, x [10.sup.3] cells/[micro]l       21.6    1.8-5.0
  Monocytes, x [10.sup.3] cells/[micro]l          0       0-0.3
  Eosinophils, x [10.sup.3] cells/[micro]l       0.3      0-0.2
  Basophils, x [10.sup.3] cells/[micro]l          0       0-0.1
Packed cell volume, %                             43      42-55
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Title Annotation:Clinical Reports
Author:Rivera, Samuel; McClearen, James R.; Reavill, Drury R.
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Geographic Code:1USA
Date:Dec 1, 2009
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