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Case Report— Acute Lameness in a Roller Pigeon (Columba livia) with Multicentric Lymphosarcoma

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SUMMARY. A 3-yr-old ?1 adult female roller pigeon (Columba livia) used as part of a breeding pair for an ongoing research study presented with acute left limb lameness. Palpation of the left leg and region revealed a large lump near the coxofemoral
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  Case Report—   Acute Lameness in a Roller Pigeon ( Columba livia  ) with MulticentricLymphosarcoma  Susan M. Williams,  AC Robert J. Williams, B and Robert M. Gogal, Jr. B  A  Poultry Diagnostic and Research Center, Department of Population Health, College of Veterinary Medicine, University of Georgia, Athens, GA 30602 B Department of Veterinary Biosciences and Diagnostic Imaging, College of Veterinary Medicine, University of Georgia, Athens, GA 30602Received 4 January 2017; Accepted 17 February 2017; Published ahead of print 3 March 2017SUMMARY. A 3-yr-old ?1  adult female roller pigeon ( Columba livia  ) used as part of a breeding pair for an ongoing research study presented with acute left limb lameness. Palpation of the left leg and region revealed a large lump near the coxofemoral joint. Thebird was able to ambulate in the cage, but would not brood her hatchling. The bird was humanely euthanized and necropsy wasperformed. Grossly, multiple large white to pale tan nodules were noted in the pancreas, lung, rib cage, intestines, and unilaterally in the left kidney. Microscopic examination of the various organs revealed neoplastic proliferation of round cells consistent withlymphoblasts. Immunohistochemistry was performed with the use of antibodies to CD3, CD79a, CD20, and CD21 to phenotypethe cells. The results indicated that the neoplastic infiltrating cells were predominantly of T-cell srcin.RESUMEN. Reporte de caso- Cojera aguda en una paloma (Columba livia) con linfosarcoma multic´entrico.Una paloma adulta de tres a ˜nos de edad (Columba livia) utilizada como parte de una pareja de reproductores para un estudio deinvestigaci´on en curso present´o cojera aguda del miembro izquierdo. La palpaci´on de la pierna izquierda y de la regi´on izquierda revel´o un abultamiento severo cerca de la articulaci´on coxofemoral. El ave fue capaz de moverse en la jaula, pero no cubr´ıa a su cr´ıa.Se practic´o la eutanasia humanitaria del ave y se realiz´o la necropsia. A la necropsia, se observaron m´ultiples n´odulos grandes decolor blanco en el pa ´ncreas, el pulm´on, la caja tora ´cica, los intestinos y unilateralmente en el ri˜n´on izquierdo. El examenmicrosc´opico de los diversos ´organos revel´o proliferaci´on neopla ´sica de c´elulas redondas compatibles con linfoblastos. La inmunohistoqu´ımica se realiz´o con el uso de anticuerpos para CD3, CD79a, CD20 y CD21 para fenotipificar las c´elulas. Losresultados indicaron que el srcen de las c´elulas infiltrantes neopla ´sicas fue predominantemente de c´elulas T.Key words: lymphosarcoma, immunohistochemistry, roller pigeon, CD3 Abbreviations: ALV  ¼ avian leukosis virus; IHC ¼ immunohistochemistry  Lymphoid neoplasia is one of the most common forms of hemolymphatic neoplasms in avian species, especially poultry specieswith viral-induced lymphosarcomas (2) There are rare reports of neoplasia in general, in penguins, pelicans (10), and ratites (4).Lymphoid neoplasms have been reported in pet birds, canaries,budgerigars, and other psittacine species, with male canaries being the most reported, because their singing abilities make them popularpets (2). Neoplasms in pigeons are uncommon in spite of thelongevity of the species (1). However, multiple tumor types havebeen reported and include lymphomas, cutaneous neoplasms,reproductive (both male and female), alimentary, pulmonary,urinary, and endocrine systems (11). This report involved an adultfemale research pigeon. CASE HISTORY AND CLINICAL SIGNS  A 3-yr-old adult female roller pigeon ( Columba livia  ) used as a part of a breeding pair for an ongoing research study was housedwith her mate at the Poultry Diagnostic and Research Center animalfacilities. The housing consisted of a large wire cage with perches,water, and feed. A cardboard nesting box was present for laying eggsand brooding hatchlings. Lighting was kept on a 24-hr cycle toencourage mating, and supplemental heat and cooling was providedto keep study animals comfortable at around 25 C. The breeding pair had produced two eggs laid a couple of days apart (Aug. 26 and28, 2015) and were brooding the eggs. Just after both eggs hatched,the adult female presented with acute left limb lameness. She wasable to ambulate in the cage but would not brood her recenthatchlings, which subsequently died. Palpation of the leg revealed a large lump felt near the coxofemoral joint. She was unable to graspwith her foot on the affected leg. The bird was humanely euthanatized because of concerns about her quality of life. GROSS AND MICROSCOPIC LESIONS Numerous large white to pale tan nodules were noted in thepancreas, lung, rib cage, small intestines, and unilaterally in the leftkidney (Fig. 1). Sections of affected organs were fixed in 10%buffered formalin, routinely processed, sectioned, and stained withhematoxylin and eosin. Microscopic examination of the variousorgans revealed a nonencapsulated, neoplastic proliferation of roundcells consistent with lymphoblasts (Fig. 2). The neoplastic cells hadmoderate cytoplasm with mild anisocytosis and moderate anisokar-yosis with a prominent single nucleolus. There were at least 3–4mitotic figures per high power field per organ, as well as scatteredindividual necrotic cells throughout the neoplastic masses. Immu-nohistochemistry (IHC) staining was performed with the use of goat C Corresponding author. E-mail: smwillia@uga.edu  //titan/Production/a/avdi/live_jobs/avdi-61/avdi-61-02/avdi-61-02-15/layouts/avdi-61-02-15.3d  3 May 2017  1:54 pm  Allen Press, Inc.  Cust # 11577-010317-CaseR Page 1  AVIAN DISEASES 61:000–000, 2017 1  anti-rabbit CD3, CD20, CD21 and horse anti-mouse CD79a monoclonal antibodies on the sectioned tissues of the affected organswith the goal of phenotyping these neoplastic round cells. IMMUNOHISTOCHEMISTRY RESULTS IHC staining had scattered positive staining throughout thenodules for CD3, a T-cell marker (Fig. 3). CD79a (B cell), CD20(B cell), and CD21 (dendritic cell) did not stain the neoplastic cells. DISCUSSION Leg lameness in birds is typically due to trauma or nutritionalcauses such vitamin deficiencies (9). Vitamin D3, calcium orphosphorus deficiencies lead to rickets in young growing birds (9).Osteopenia or osteoporosis is more likely to occur in adult birds andresults in a reduction in bone mass. Typical causes includestarvation, calcium, copper, phosphorus, or vitamin D3 deficiencies(9). Females in production, not having enough calcium in the dietcan lead to bone resorption to acquire calcium for shell formation,leading to a calcium deficiency. Trauma can lead to lameness whenthe leg or foot is affected. Examples would be getting a foot caughtin caging material, flying into objects, improper handling,  etc  . In thiscase, we thought the bird might have gotten her foot trapped in thewire caging and dislocated the femur from the hip joint whilestruggling to get free. Nutritional diseases were ruled out, as the dietsupplied was balanced for egg production. This bird was part of 18breeding pairs in a maternal lead study. She had been orally gavagedwith a single lead pellet. None of the other breeding pairs hadpresented with lameness nor had it been observed in previous birdstudies involving lead exposure (5,6,7). Further, there have been noknown studies linking lead exposure with cancer in any species,including birds, so this etiology was ruled out.Lymphoid neoplasia is not a common tumor found in pigeons.Shimonohara   et al  . (11) reported several types of tumors in theresearch colony at Purdue University. Eighty-three birds weresubmitted for necropsy and 28 (33.7%) had neoplasms orproliferative disorders. Seminoma and thyroid adenoma were themost common tumor diagnosed over an 11-yr period. Lymphosar-coma was documented in four birds, which grossly had multiplenodules in multiple organs. Kidney, spleen, intestine withmesentery, and pancreas were most commonly affected, and theage range was 6–12 yr old. In our case, similar organs except thespleen were affected, and the bird was 3 yr old. Two other reportsdocument lymphosarcoma in the conjunctiva and multiple otherorgans including the kidney, intestines, and pancreas (1,8). Neitherof these reports mentions leg lameness as part of the clinical signs.Both report excessive lacrimation with swelling of the conjunctiva and surrounding periorbital tissues. After treatment failure for a suspected respiratory infection, euthanasia was selected andmulticentric lymphosarcoma was diagnosed. In the present case,the neoplasia in the left kidney was most likely applying pressure tothe sciatic nerve, resulting in lameness. The mass that was palpatedbefore euthanasia was determined to be lymphosarcoma thatsurrounded the ribs and infiltrated the skeletal muscle of the Fig. 1. Gross lesions from adult female pigeon. (A) Gastrointestinaltract with numerous white raised nodules (arrows) in the duodenum andpancreas. (B) Unilateral large white raised nodule in the left kidney (arrow).Fig. 2. Microscopic lesions in various organs. (A) Expansile nodulein the kidney composed of neoplastic lymphocytes (arrows). H&E.200 3 . (B) Similar neoplastic lymphocytes (arrows) in the liver. H&E.400 3 . (C) Neoplastic lymphocytes in the mucosal and on the serosalsurfaces of the duodenum (arrows). H&E. 100 3 . (D) Neoplasticlymphocytes (arrows) adjacent to the rib and expanding into the skeletalmuscle wall of the coelomic cavity. H&E. 100 3 .  //titan/Production/a/avdi/live_jobs/avdi-61/avdi-61-02/avdi-61-02-15/layouts/avdi-61-02-15.3d  3 May 2017  1:54 pm  Allen Press, Inc.  Cust # 11577-010317-CaseR Page 2 2 Lymphosarcoma-induced acute lameness in a pigeon  coelomic wall. The femur and hip were not dislocated, nor affectedgrossly by the mass.Reports of other nonpoultry avian species with lymphosarcomasdescribe organ distribution similar to the present case. Gregory   et al  .(4) described a hepatic lymphoma with leukemia in a 2-yr-old emu.In addition to the liver, neoplastic lymphoblasts were found in thekidneys and spleen that were characterized as mostly large immaturelymphocytes. Clinical chemistry values indicated evidence of liverdamage with increased liver enzyme activity, serum cholesterol, andbile acids. In another report by Coleman and Oliver (3), an 8-mo-old blue and gold macaw was euthanatized after not responding totreatment. Necropsy revealed hepatomegaly, splenomegaly, andrenomegaly. Microscopic examination revealed diffuse neoplasticpleomorphic lymphocytes in the liver and spleen. The kidney hadplump immature lymphoblasts effacing the normal parenchyma. A second bird (different owner), an adult male canary, was alsodescribed to have been euthanatized after not responding totreatment. Necropsy revealed an enlarged liver. Histologic exami-nation revealed multiple foci of small neoplastic lymphocytes thateffaced the parenchyma. A report by Wade  et al  . (12) documentedmulticentric lymphosarcoma in a European starling with an enlargedliver and spleen grossly. Microscopically, neoplastic lymphoid cellswere seen in the heart, spleen, pleura, air-sac wall, kidneys, testes,skeletal muscle, and bone marrow. PCR was negative forreticuloendotheliosis virus. However, the authors were able toamplify a   pol   gene similar to avian leukosis virus (ALV) Prague Cstrain and other ALV viruses and mouse retroviruses. Lack of freshtissues prevented the authors from expanding their investigation toassess whether an ALV-like retrovirus was involved. Finally, a reportby Schmidt  et al  . (10) performed IHC with various lymphoidmarkers on tissues from a Humboldt penguin and a pink-backedpelican. Both of these birds had pleomorphic neoplastic lymphocyticinfiltrates throughout multiple organs. Immunoreactivity waspresent with the CD3 marker, a pan T-cell marker in the neoplastictissues, whereas CD45 (leukocyte common antigen) and CD79 werenegative in the neoplastic areas and in normal lymphoid aggregatesin the spleen and gut. However, it was suggested that these twomarkers may not cross react with these bird species. IHC in thepresent case was positive for CD3. None of the other reportsexamined the srcin of the neoplastic lymphoid cells by IHC.Immunohistochemistry for lymphosarcoma is typically performedto determine whether a neoplasia is of T-cell or B-cell srcin. Formammals, this knowledge can help guide the selection of chemotherapeutic regimes to treat the cancer. Only one of thereports cited here characterized the lymphosarcoma as T-cell insrcin (10). For the present case, the IHC results obtained from the Athens Diagnostic Laboratory indicated that CD3 þ T cells were inthe mass. Cell markers for B-cells and dendritic cells were negative.Because not all of the neoplastic cells stained with the CD3, thetumor composition being from pure T cells is rather unlikely. Another possibility as to why not all the neoplastic cells stained forCD3 is that some of neoplastic cells were too immature or anaplasticto exhibit the CD markers or the stained cells are inflammatory Tlymphocytes responding to the neoplastic cells. Although treatmentin mammals has been well documented and dependent on staging and pathological grade of the tumor at time of diagnosis, none of thechemotherapeutic agents or protocols are approved in avian species,nor at present are there grading schemes for neoplasia in birds (2). REFERENCES 1. Chalmers, G. A. Neoplasms in two racing pigeons. Avian Dis.30:241–244. 1986.2. Coleman, C. W. Lymphoid neoplasia in pet birds: A review. J. AvianMed. Surg. 9:3–7. 1995.3. Coleman, C. W., and R. Oliver. Lymphosarcoma in a juvenile blueand gold macaw (  Ara araruana  ) and a mature canary ( Serinus canarius  ). J. Assoc. Avian Vet. 8:64–68. 1994.4. Gregory, C. R., K. S. Latimer, E. A. Mahaffey, and D. Thomas.Lymphoma and leukemic blood picture in an emu ( Dromaius novaehollan- diae  ). Vet. Clin. Pathol. 25:136–139. 1996.5. Holladay, J. P., M. Nisanian, S. Williams, R. C. Tuckfield, R. Kerr,T. Jarrett, L. Tannenbaum, S. D. Holladay, A. Sharma, and R. M. Gogal, Jr.Dosing of adult pigeons with as little as one #9 lead pellet caused severedelta-ALAD depression, suggesting potential adverse effects in wildpopulations. Ecotoxicology 21:2331–2337. 2012.6. Kerr, R. P., T. M. Krunkosky, D. J. Hurley, B. S. Cummings, S. D.Holladay, and R. M. Gogal, Jr. Lead at 2.5 and 5.0  l M induced aberrantMH-II surface expression through increased MII exocytosis and increasedautophagosome formation in Raw 267.4 cells. Toxicol.  In Vitro   27:1018–1024. 2013.7. Nisanian, M., S. D. Holladay, E. Karpuzoglu, R. P. Kerr, S. M. Williams, L. Stabler, J. V. McArthur, R. C. Tuckfield, and R. M. Gogal, Jr.Exposure of juvenile Leghorn chickens to lead acetate enhances antibioticresistance in enteric bacterial flora. Poult. Sci. 93:891–897. 2014.8. Rambow, V. J., C. J. Murphy, and J. G. Fox. Malignant lymphoma in a pigeon. J. Am. Vet. Med. Assoc. 179:1266–1268. 1981. Fig. 3. Immunohistochemistry for CD3. (A) Kidney. Arrows point out some positive staining neoplastic cells. 200 3 . (B) Liver. Arrows point outsome positive staining cells in clumps and others that are scattered in the parenchyma. 100 3 . Insert. Higher magnification of positive staining cells200 3 . (C). Lung. Solid mass disrupting parenchyma with a few positive staining cells. 50 3 . Insert. Positive staining cells at the junction of normaland neoplastic parenchyma 200 3 .  //titan/Production/a/avdi/live_jobs/avdi-61/avdi-61-02/avdi-61-02-15/layouts/avdi-61-02-15.3d  3 May 2017  1:54 pm  Allen Press, Inc.  Cust # 11577-010317-CaseR Page 3 S. M. Williams  et al  . 3  9. Schimdt, R. E., D. R. Reavill, and D. N. Phalen. Pathology of petand aviary birds. Blackwell, Oxford, United Kingdom. 2003.10. Schmidt, V., H.-C. Phillip, J. Thielebein, S. Troll, C. Hebel, andH. Aupperle. Malignant lymphosarcoma of T-cell srcin in a Humboldtpenguin ( Spheniscus humboldt  ) and a pink- backed pelican ( Pelecanus rufescens  ). J. Avian Med. Surg. 26:101–106. 2012.11. Shimonohara, N., C. H. Holland, T. L. Lin, and W. L. Wigle.Naturally occurring neoplasms in pigeons in a research colony: A retrospective study. Avian Dis. 57:133–139. 2013.12. Wade, L. L., E. W. Polack, P. H. O’Connell, G. S. Starrak, N. Abou-Madi, and K. A. Schat. Multicentric lymphoma in a European starling ( Sturnus vulgaris  ). J. Avian Med. Surg. 13:108–115. 1999.  //titan/Production/a/avdi/live_jobs/avdi-61/avdi-61-02/avdi-61-02-15/layouts/avdi-61-02-15.3d  3 May 2017  1:54 pm  Allen Press, Inc.  Cust # 11577-010317-CaseR Page 4 4 Lymphosarcoma-induced acute lameness in a pigeon  Queries for avdi-61-02-151. Author: This article has been lightly edited for grammar, style, and usage. Please compare against your srcinaldocument and make corrections on these pages. Please limit your corrections to substantive changes that affectmeaning. If no change is required in response to a question, please write  ‘‘ OK as set ’’  in the margin. Copy editor
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