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Cutaneous mast cell tumor and mastocytosis in a black-masked lovebird (Agapornis personata).

Abstract: A 12-year-old female black-masked lovebird (Agapornis personata) with a cobalt color mutation was presented for self-mutilation of a mass located on the right lateral neck. Cytologic evaluation of the soft tissue mass revealed a predominance of poorly stained mast cells with metachromatic intracytoplasmic granules. The presumptive diagnosis was cutaneous mast cell tumor. Clinical evaluation, results of a complete blood cell count and biochemical analysis, and radiographs did not reveal systemic manifestation of mast cell disease. The mass was surgically resected, but surgical margins were limited because of the location of the mass and the small size of the patient. The lovebird died the day after surgery. Gross postmortem examination revealed splenomegaly, multifocal pinpoint white nodules throughout the liver parenchyma, severe thickening and yellow coloration of the great vessels, and pale pink swelling of the caudal right kidney. Histopathologic analysis of the resected mass revealed sheets of round cells that contain metachromatic granules, defined as neoplastic mast cells, within a fine fibrovascular stroma. Similar neoplastic cells were seen in the right kidney, hepatic sinusoids, splenic pulp, periovarian connective tissue, and bone marrow. The histopathologic diagnosis was a cutaneous mast cell tumor and disseminated mast cell disease, or mastocytosis. To the authors' knowledge, this is the first reported case of a cutaneous mast cell tumor and mastocytosis in a psittacine bird.

Key words: mast cell, mastocytosis, neoplasia, self-mutilation, avian, psittacine bird, lovebird, Agapornis personata

Clinical Report

A 12-year-old female intact black-masked lovebird (Agapornis personata) with a cobalt color mutation was presented to the University of Illinois Veterinary Teaching Hospital because of a 4-day history of self-mutilation. The lovebird had no history of self-trauma and was reported to be otherwise healthy. The bird was housed alone in a household with exposure to cigarette smoke and was fed a diet that consisted of commercial psittacine pellets and a cockatiel/parrot seed mix (brands unknown by the owner). No recent changes to the environment were reported. On physical examination, the bird weighed 52 g and was bright and alert, with a body condition score of 2/5. An ulcerated soft tissue mass that measured 15 mm x 22 mm and 5 mm in thickness was visible on the right lateral aspect of the neck immediately cranial to the thoracic inlet (Fig 1). The mass involved the underlying musculature, but passage of a gavage feeding tube confirmed that it did not communicate with the crop. The surface of the mass contained a mild serosanguineous discharge, and a small amount of dried blood was evident on the bird's beak.

The owner initially declined extensive diagnostic testing or anesthesia and opted for simple wound management. Butorphanol (2.0 mg/kg IM; Torbugesic, Fort Dodge Animal Health, Fort Dodge, IA, USA) was administered for analgesia, and the ulcerated mass was swabbed for cytologic evaluation. Feathers on the wound periphery were plucked, and the ulcerated tissue was cleansed with sterile saline solution. An aloe vera preparation (Soother Plus cream, Harrisons' Pet Products, Lake Worth, FL, USA) was applied to the ulcerated area, and the neck was bandaged with a film dressing (Telfa pad, Tyco Health Care Group LP, Mansfield, MA, USA), cast padding, and flexible bandaging material (Vetrap, 3M Animal Care Products, St Paul, MN, USA). The bird was discharged with meloxicam (0.5 mg/kg PO q24h; Metacam, Boehringer Ingelheim Vetmedica Inc, St Joseph, MO, USA) and enrofloxacin (15 mg/kg PO ql2h; Baytril, Bayer Health Care, Shawnee Mission, KS, USA). A commercial Romanowsky stain (Diff-Quik, Jorgensen Laboratories Inc, Loveland, CO, USA) applied to the tissue sample revealed a highly cellular infiltrate composed primarily of presumptive mast cells and background erythrocytes (Fig 2A). The presence of mast cells was confirmed by Wright-Giemsa stain (Fig 2B). The presumptive diagnosis was a cutaneous mast cell tumor.

[FIGURE 1 OMITTED]

Twelve hours later, the lovebird was returned for a scheduled bandage change. Because of the presumptive diagnosis, the owner elected to pursue staging for neoplasia. A complete blood cell count (CBC), whole blood biochemical analysis, and radiographic evaluation were performed. Results of the CBC showed a decreased packed cell volume (26%; reference range, 39%-51%) and leukopenia (3.5 [10.sup.3]/[micro]L; reference range, 4.5-9 x [10.sup.3]/[micro]L), and results of the biochemical analysis revealed hypoproteinemia (0.9 g/dL [9 g/L]; reference range, 2.8-4.0 g/dL [28-40 g/L]), hypoalbuminemia (0.7 g/dL [7g/L]; reference range, 2.0-2.8 g/dL [20 28 g/L]), and a high concentration of creatine kinase (925 U/L; reference range, 52-245 U/L). (1) Hematogenous mast cells were not observed. The anemia and hypoproteinemia in conjunction with hypoalbuminemia were attributed to recent blood loss associated with self-mutilation.

Whole-body radiographs demonstrated the expansile nature of the soft-tissue mass, which was causing tracheal deviation to the right. No evidence of gross metastatic disease was seen. The wound was cleaned and rebandaged as previously described. Treatment with oral enrofloxacin and meloxicam was continued, and diphenhydramine (2 mg/kg PO ql2h; Benadryl, Pfizer Consumer Healthcare, Morris Plains, NJ, USA) was added.

Three days after staging, the lovebird was admitted for surgical resection of the mass. The bird had remained bright and alert, and no changes were revealed during physical examination. Before surgery, butorphanol (2.5 mg/kg IM once) was administered for analgesia. General anesthesia was induced with 5% isoflurane (Minrad Inc, Orchard Park, NY, USA) delivered by face mask. The lovebird was intubated with a modified 8-Fr red rubber tube (Tyco Health Care Group LP, Mansfield, MA, USA), and anesthesia was maintained with 1.5%-3% isoflurane.

The soft tissue surrounding the mass was circumferentially incised with a scalpel blade, and the tumor was bluntly dissected from the underlying tissue. The mass did not appear to extend through the underlying fascial plane. Because of the location and size of the mass relative to the size of the bird, minimal margins (2-3 mm) were obtained. The skin was closed with 4-0 Vicryl (Ethicon Inc, Somerville, N J, USA) in a Ford interlocking pattern. The mass was submitted for histopathology. The bird had an uneventful recovery from anesthesia and was discharged that night.

The following day, the bird was found dead in its cage at home. A postmortem evaluation was performed, and tissue samples were submitted for histopathology. On gross examination, the spleen was enlarged (5-mm diameter) and dark red, the liver parenchyma contained multiple pinpoint white nodules, and the caudal pole of the right kidney was enlarged and pale pink. The great vessels at the heart base were thickened and yellow. On histologic examination, the mass excised from the neck was well demarcated but unencapsulated and composed of sheets of round cells within a fine fibrovascular stroma. Neoplastic cells contained a moderate amount of slightly granular basophilic cytoplasm and a large round-to-oval nucleus that contained clumped chromatin and a single prominent nucleolus. Giemsa and toluidine stains revealed metachromatic granules in neoplastic cells (Fig 2D). Mitoses were rare. Small numbers of eosinophils and fewer heterophils were scattered throughout the mass. Neoplastic cells of similar morphology also were found within the syringeal marrow (Fig 2C), extending into the adjacent tissue of the neck, and infiltrating the marrow of the long bones. Similar neoplastic cells also effaced the right kidney and infiltrated the hepatic sinusoids, splenic red pulp, and periovarian connective tissue. Other lesions included atherosclerosis and retention of the superficial esophageal mucosa, suggestive of inanition.

[FIGURE 2 OMITTED]

Discussion

This case report describes the presentation of a cutaneous mast cell tumor with secondary self-mutilation and disseminated mastocytosis in an adult female lovebird. Mast cell disease is uncommon in birds, and, to our knowledge, this is the first reported case of a cutaneous mast cell tumor and mastocytosis in a psittacine bird.

Various types of cutaneous and subcutaneous neoplasia have been reported in psittacine birds, including basal cell carcinoma, (2) lymphosarcoma, (3) lipoma, (4) malignant melanoma, (5-7) metastatic renal carcinoma, (8) sarcoma, (9) squamous cell carcinoma, (10,11) nonepitheliotropic B-cell lymphoma, (12) hemangiosarcoma, (13) and granular cell tumors. (14) Mast cell disease has been documented in numerous small domestic mammals and occasional reptilian species, including dogs, (15-20) cats, (15,16,21,22) ferrets, (23-26) hedgehogs, (27) a snake, (28) and a chelonian. (29) Mast cell tumors in birds are rare. Cutaneous mast cell tumors have previously been documented in owls (30,31) and gallinaceous birds. (32,33) Disseminated or metastatic mast cell disease has very rarely been reported in birds, with cases documented in 2 chickens. (32,33)

Mast cells in mammals arise from a heterogenous myelomonocytic cell population originating in the bone marrow. Mature mast cells are normal components of the dermis/subdermis, lungs, liver, and gastrointestinal tract, and have important roles in the mediation of inflammatory responses, promoting hypersensitivity reactions, stimulating T cells in immune responses, and defending the host against tissue parasites. (15,18) Mammalian mast cells are round with a centrally located round-to-oval nucleus and contain varying numbers of intracytoplasmic granules. (18,34) Mast cell tumors can be identified via cytology by using a commercially available Romanowsky stain; however, the staining quality is variable, and mast cells may go unidentified. Mast cells can be cytologically confirmed by using a Wright-Giemsa stain, which demonstrates the characteristic dark metachromatic intracytoplasmic granules. (18) On histologic examination, mast cell granules can be better identified by using Giemsa or toluidine blue stains. (18) Techniques used to diagnose avian mast cell tumors have not been well described, and the methodology used is often extrapolated from mammals. In this case report, a cutaneous mast cell tumor was suspected based on a commercial Romanowsky stain used for cytologic evaluation. However, as depicted in Figure 2A and B, the avian mast cells were not as readily apparent with this stain as with a Wright-Giemsa stain. On histologic examination, granules exhibited a typical, although faint, metachromasia with toluidine blue and Giemsa stains (Fig 2D).

Scant literature is available that describes the distribution and function of avian mast cells, especially with regard to psittacine birds. Mast cells in domestic chickens have been found in highest numbers in the connective tissues of the oviduct, proventriculus, small intestine, peritoneum, crop, thyroid glands, and peripheral nerves. (35) In cockerels, large numbers of mast cells were reported in the dermis, subcutaneous tissues, lung, spleen, and thymus. Relative numbers of mast cells vary among avian species, with larger counts found in chickens than in turkeys, pheasants, or Japanese quail. (36)

Mast cell tumors in domestic mammalian species are highly variable. In dogs, mast cell tumors are common, which represents 7%-20% of all cutaneous tumors, (18, 20,37) and approximately 50% of these tumors are malignant. Cutaneous mast cell tumors in dogs are graded on a scale of 1-3 based on the degree of mast cell differentiation. This grading scale in dogs has been correlated to the biologic behavior of the tumors and, therefore, the prognosis. (15,16,18,38) A grade I (well differentiated) cutaneous mast cell tumor is likely to be completely excised by using the recommended 2- to 3-cm lateral margins and one fascial plane for a deep margin, whereas a grade III (poorly differentiated) tumor is more likely to have metastasized. (19,20,39) In addition to grading, staging of mast cell disease is important to determine the extent of the neoplasia. The World Health Organization has established the Clinical Staging System for canine mast cell tumors: stage I, a single tumor confined to the dermis; stage II, a single tumor confined to the dermis with regional lymph node involvement; stage III, multiple dermal tumors with local infiltration and regional lymph node involvement; and stage IV, any tumor with distant metastasis or recurrence with metastasis. (15, 18,37,38) In dogs, the most common sites for cutaneous mast cell tumor metastasis are the regional lymph nodes, spleen, and liver. (18) As with other neoplastic conditions, clinical staging is accomplished by evaluating bloodwork results, bone marrow cytology, radiographs, regional lymph node cytology or histopathology, and advanced diagnostics, for example, an abdominal ultrasound. (15,18,37,40) Circulating mast cells are concentrated in the buffy coat, which should be evaluated when performing a CBC. However, cytologic evaluation of a bone marrow aspirate provides a more accurate assessment of possible mastocythemia than does a CBC. (15,18)

Although the behavior of mast cell disease and mastocytosis in avian species is poorly described, the lovebird in this case report was staged by extrapolating most of the recommendations used in dogs. Hematologic analysis and radiographic examination were performed; however, the lack of peripheral lymph nodes in birds precluded the evaluation of lymph tissue. In addition, because of case constraints, coelomic ultrasound and bone marrow aspirates were not performed. In this lovebird, the postmortem discovery of neoplastic cells in tissues surrounding the mass as well as in the bone marrow and multiple other sites led to a presumptive assessment of grade III mast cell disease with advanced stage III IV neoplasia.

Cutaneous mast cell tumors are not reported as frequently in cats as in dogs; however, they still comprise 12%-20% of all feline skin tumors. (15,21) Cutaneous mast cell tumors in cats are most often located on the head and neck, (15,16) with one paper citing these locations in 43% of cats with mast cell tumors. (21) Currently, the histologic grading system used to evaluate canine mast cell tumors is not recommended for cats because the correlation of histologic findings with prognosis differs in cats. (16,21,22) Unlike dogs, cats have a higher propensity to develop mastocytosis, which is the visceral or systemic form of the disease. (16) Mastocytosis in domestic mammals has a predilection for the spleen, liver, and abdominal lymph nodes. (16,22) By using these same criteria in the lovebird, the discovery of mast cells in the liver and spleen confirmed the presence of mastocytosis.

Previously documented mast cell tumors in birds have been confined to the head: cutaneous mast cell tumors in a great horned owl (Bubo virginianus) were located adjacent to the right orbit and near the left auditory meatus, (30) a mast cell tumor in a burrowing owl (Athene cunicularia) involved the oral mucosa, (31) a lump on the margin of the right upper eyelid in Hawaiian owl (Asio flammeus sandwichensis) was later confirmed to be a mast cell tumor, (31) and a periocular mast cell tumor was reported in a white leghorn cock. (32) The mast cell tumor found on the neck of the lovebird described in this case report mirrored the distribution documented in cats.

Complications of mast cell disease in domestic animals include gastroduodenal ulceration secondary to histamine release and subsequent stimulation of gastric H2 receptors, excessive acid secretion, and hypermotility. Additional complications include pruritus, prolonged coagulation times, and delayed healing of surgical sites. (15,18,37,38) The lovebird described here originally presented for self-mutilation, which may have been induced by pruritus.

Treatment for mast cell disease in small animals involves surgical removal of the tumor and/or a combination of radiation therapy and chemotherapy. Surgical margins recommended for mast cell tumor removal are 3 cm laterally and a deep margin of one fascial plane. (15,16,18) A study in dogs reported complete excision of grade I and II cutaneous mast cell tumors by using 2-cm lateral margins in conjunction with a deep margin of one fascial plane. (20) Adjunct radiation therapy is recommended if the location of the tumor prevents complete surgical excision. Radiation therapy for grade I and II mast cell tumors reportedly achieves a 1- to 2-year disease-free interval in 79%-97% and 77% 85% of cases, (15) respectively, or 85% 95% of cases with low- or intermediate-grade mast cell differentiation. (16) In cases of poorly differentiated mast cell disease or documented dissemination, surgical excision and radiation therapy may only be palliative, and additional treatment with chemotherapy may be warranted. However, the prognosis is poor in many of these cases, because mast cell disease appears to be fairly resistant to chemotherapy. (15,18) In the case of the lovebird, disseminated disease was not suspected when the tumor was excised. Because of the patient's small size, as well as the location of the tumor on the lateral aspect of the neck in close proximity to the trachea, esophagus, and jugular vein, complete surgical resection with recommended margins was not possible. Although mastocytosis was not revealed until postmortem examination, local adjunct radiation therapy may have been an option. Treatment for mastocytosis has not been documented in birds. In spite of radiation therapy and possible chemotherapy, the extent of disease described in this lovebird relative to the prognosis for mastocytosis in domestic mammals was not likely to have resulted in a good prognosis.

This case report describes both a cutaneous mast cell tumor and disseminated mastocytosis in a lovebird. Because this bird presented for self-mutilation, a diagnostic workup, including cytology, is recommended for all avian patients being presented for self-trauma, and mast cell disease should be included in the differential diagnosis.

Acknowledgments: We thank Jodi Matheson, DVM, Dipl ACVR, Avery Bennett, MS, DVM, Dipl ACVS, and Kim Byrne, CVT, for their assistance with this case.

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Rebecca K. Dallwig, DVM, Julia K. Whittington, DVM, Karen Terio, DVM, PhD, Dipl ACVP, and Ann Barger, MS, DVM, Dipl ACVP

From the Zoological Medicine Service (Dallwig), Department of Veterinary Clinical Medicine (Whittington), Zoological Pathology Program (Terio), and Veterinary Diagnostic Laboratory (Barger), University of Illinois, College of Veterinary Medicine, Urbana, IL 61802, USA.
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Author:Dallwig, Rebecca K.; Whittington, Julia K.; Terio, Karen; Barger, Ann
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Geographic Code:1USA
Date:Mar 1, 2012
Words:3936
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