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Successful treatment of tracheal xanthogranulomatosis in a red-tailed hawk (Buteo jamaicensis) by tracheal resection and anastomosis.

Abstract: A red-tailed hawk (Buteo jamaicensis) was presented because of dyspnea subsequent to 2 celiotomy procedures. Respiration markedly improved after an air sac cannula was placed. Tracheoscopy revealed a mass firmly adhered to the proximal tracheal wall. Because of lack of response to medical therapy, 5 tracheal cartilages were surgically resected and an end-to-end tracheal anastomosis was performed. On histologic examination of the mass, vacuolated macrophages, fibrosis, and occasional cholesterol clefts were identified, consistent with a diagnosis of xanthogranulomatosis. We propose that a single term, xanthogranulomatosis, replace the varied terms currently used to describe the syndromes in avian species in which intracytoplasmic lipid is found within tissue macrophages.

Key words: trachea, xanthfoma, xanthomatosis, xanthogranuloma, resection, anastomosis, avian, red-tailed hawk, Buteo jamaicensis

Clinical Report

A 5-year-old captive female red-tailed hawk (Buteo jamaicensis) was presented with intestinal intussusception and prolapse through the cloaca. Despite diagnostic investigations, the cause remained undetermined. A celiotomy and intestinal resection and anastomosis were done, but because of postoperative complications, a second celiotomy was performed 4 days later. At surgery, ileus and localized peritonitis originating from the intestinal anastomosis site were identified, and a second intestinal resection and anastomosis was required. For both procedures, anesthesia was induced with 5% isoflurane in 1.5 L/rain oxygen administered by face mask and maintained at 2%-3% isoflurane administered by an endotracheal tube connected to a nonrebreathing circuit. Anesthetic gases were not humidified. A red rubber endotracheal tube with a slanted tip was used for both procedures (size was not recorded). Although the tube was cuffed, the cuff was not inflated after intubation. The bird regurgitated during the second procedure, and on extubation, gastric material was visible in the glottis around the tube. Convalescence after the second celiotomy was unremarkable, and the bird was discharged 10 days later.

One week after discharge, the bird was reexamined because of dyspnea. Anesthesia was induced and maintained as described above, and an air sac cannula was placed in the left caudal thoracic air sac. Respiratory effort immediately improved, and isoflurane and oxygen were subsequently administered through the air sac cannula. A tracheoscopy using a 2.7-mm rigid endoscope (Richard Wolf, Knittlingen, Germany) was done, and results revealed a mass within the proximal third of the trachea, firmly adhered to the tracheal wall and reducing the tracheal luminal diameter by over one half. Results of cytologic examination of swabs taken from the mass showed only cellular debris, and aerobic bacterial culture results were negative. No coelomic or extraluminal tracheal abnormalities were visible on radiographs.

Treatment consisted of enrofloxacin (20 mg/kg IM q12h; Baytril, Bayer PLC, Suffolk, UK), carprofen (4 mg/kg IM q24h; Rimadyl, Pfizer Animal Health, Sandwich, Kent, UK), and intravenous fluids (0.9% NaCl, 10 ml q12h). Hyaluronidase (1 ml diluted in saline to 3 IU/ml; Hyalase, CP Pharmaceuticals Ltd, Wrexham, UK) was administered intratracheally, and the bird was nebulized with gentamicin (50 mg) and hyaluronidase (12 IU) in 5 ml of saline (30 minutes q6h). The next day, the bird was reanesthetized for tracheoscopy through the air sac cannula as described above. The appearance of the lesion had not improved, and diluted hyaluronidase was instilled into the trachea. Three days later, the air sac cannula became obstructed. The hawk was reanesthetized, and a second air sac cannula was placed into the right caudal thoracic air sac while the obstructed cannula was removed. Tracheoscopy again showed minimal change in the appearance of the mass. At this point, given the lack of response to medical treatment, a tracheal resection and anastomosis was scheduled for the next day. Antibiotic therapy was changed to tobramycin (5 mg/kg IM q12h; Nebcin, King Pharmaceuticals, Donegal, Ireland) and piperacillin (200 mg/kg IM q12h; Pipril, Wyeth Pharmaceuticals, Maidenhead, Berkshire, UK), and treatment with carprofen was continued.

At surgery, anesthesia was induced and maintained with isoflurane administered by a nonrebreathing circuit connected to the air sac cannula. The bird was placed in dorsal recumbency with the head elevated at 45[degrees] from the horizontal. After aseptic preparation, the skin was incised over the affected area of trachea and the crop bluntly dissected from the surgical site and reflected to the right. The proximal aspect of the surgical site was delineated by the light from an endoscope positioned within the trachea at the site of the lesion. Stay sutures were placed in the trachea, and 5 cartilage rings, incorporating the mass, were resected en bloc by incising the annular ligaments between adjacent cartilage rings. The resected ends of the trachea were apposed with 3 sutures of 5-0 (1 metric) polydiaxonone (PDS, Johnson and Johnson International, St-Stevens-Woluwe, Belgium) placed with the knots external to the tracheal lumen and spanning 2 tracheal rings on either side of the resection site. The crop was tacked over the area to provide an airtight seal with the same suture material, and the skin was closed with 2-0 (3 metric) polyglactin 910 (Vicryl, Johnson and Johnson International) in a simple continuous pattern. The mass was placed in 10% formalin and submitted for histopathologic examination.

Recovery after surgery was uneventful, and the air sac cannula was removed the next day. Treatment with itraconazole (10 mg/kg PO q12h, Sporanox, Janssen-Cilag, High Wycombe, Buckinghamshire, UK) was instituted. The bird was discharged 1 week after presentation on amoxycillin/clavulanic acid (125 mg/kg PO q12h for 5 days), meloxicam (0.1 mg/kg PO q24h for 7 days, Metacam, Boehringer-Ingelheim, Ingelheim, Germany), and itraconazole (10 mg/kg PO q12h for 10 days).

Tracheoscopy performed 10 days after surgery demonstrated good healing, with no evidence of stenosis. The bird has had no recurrence of stenosis for at least 2 years, despite having had 3 further anesthetic episodes for the diagnosis and repair of a fractured wing.

The formalinized mass was processed, sectioned, and stained with hematoxylin and eosin. Histologically, in transverse sections of trachea, at least one half of the tracheal lumen was occupied by a mass beneath the lining of the epithelial surface. This epithelium was metaplastic, with the normal ciliated columnar surface replaced by stratified squamous epithelium, 3-5 layers thick, with focal areas lined by stratum corneum. No distinct keratin was seen. Beneath the epithelium and occupying the area between it and the tracheal cartilages was a solid lesion that was well vascularized and consisted of connective tissue (including bands of fibroblasts), foamy macrophages, clumps of giant cells, a minimal to moderate lymphocytic infiltration, and a few cholesterol clefts. The tracheal cartilage appeared normal and showed a moderate degree of mineralization. Tissues external to the cartilage consisted of loose, areolar connective tissue, muscle, and dilated blood vessels. Free blood was present.

Discussion

In this report we describe the surgical treatment of a red-tailed hawk that presented with dyspnea due to a proximal tracheal mass. The mass had developed after 2 anesthetic events, performed 17 days and 21 days previously, for the surgical treatment of intestinal intussusception. The mass was successfully removed en bloc by resecting 5 tracheal cartilages and anastomosing the resected ends of the trachea. Histologic examination of the mass showed a combination of chronic inflammation and xanthomatous change, consistent with tracheal xanthogranulomatosis.

With the increased use of anesthetic and diagnostic techniques in avian medicine, endotracheal intubation for maintenance of avian general anesthesia is now common. As the number of these procedures increases, so does the number of reported adverse complications secondary to endotracheal intubation. (1) In humans, the most common complication of endotracheal intubation is tracheal stenosis. (2) This results from tracheal inflammation or necrosis, secondary to overinflation of the endotracheal cuff or prolonged intubation. (2) In veterinary medicine, chemical irritation from cold sterilization of endotracheal tubes between patients is an additional risk. (1) The marked mobility of the avian neck may also predispose to mucosal trauma from the endotracheal tube tip during patient positioning.

The development of a tracheal mass so soon after 2 prolonged anesthetic events involving endotracheal intubation suggests iatrogenic complications as the cause of the lesion in this hawk. In a study in humans, iatrogenic tracheal stenosis due to prolonged placement of cuffed endotracheal tubes accounted for one third of tracheal resection and anastomosis procedures. (2) Although the endotracheal tube used in this bird was cuffed, the cuff was left uninflated, as is the accepted procedure for avian anesthesia. Prolonged contact of the endotracheal tube tip with the tracheal mucosa alone has been suggested as sufficient cause of irritation. (1) In a study in dogs, electron microscopy demonstrated damage to endotracheal endothelial cells after short periods of intubation with uncurled tubes. (3) The position of the lesion in the bird we describe was similar to the expected position of the endotracheal tube tip. Breathing nonhumidified air is sufficient to cause tracheal mucosal damage in guinea pigs. (4) Tracheal mucosal injury may have been caused or exacerbated by aspirated gastrointestinal fluid from regurgitation during the second celiotomy. The endotracheal tube had been used for other patients, although it was cold-sterilized after each use in a 1:250 solution of F10 SC Disinfectant (Health and Hygiene Pty Ltd, Florida, South Africa). Either residual bacterial contamination or insufficient rinsing after sterilization may have contributed to tracheal irritation. However, this sterilizing agent has been used for nebulizing birds at a similar dilution. (5)

Treatment of stenotic tracheal lesions includes medical therapy, bougienage, corticosteroid therapy, endoscopic debulking, laser resection, tracheal stenting, and tracheal resection and anastomosis. (6-8) Endoscopic debulking of tracheal stenosis after intubation in a blue and gold macaw (Ara ararauna) has been described, although it required 2 treatments. (7) A case of successful tracheal resection and anastomosis was reported in a goose (Anser anser) with membranous tracheal stenosis secondary to trauma. (9) The lesion in this hawk was firmly adhered to much of the tracheal mucosa, and we feared that endoscopic debulking might cause excessive iatrogenic damage. Although tracheal stenosis has been treated with bougienage in mammalian species, (6) this has not been described in birds. Given the anatomy of the avian trachea, with its complete tracheal rings, bougienage may have a high risk of complications in avian species. Laser debulking was not available in this case. Tracheal resection and anastomosis was deemed the most appropriate treatment technique for this bird.

In small animal medicine, the split-cartilage technique of tracheal resection and anastomosis is preferred over the annular ligament-cartilage technique. (8) In the first technique, the cartilage rings immediately distal and proximal to the resection site are circumferentially split in half. (8) The 2 "half cartilages" are then brought into apposition during anastomosis. In the annular-ligament technique, the resection and anastomosis sites are between tracheal cartilages. (8) The split-cartilage technique is thought to provide more accurate apposition and thus less risk of stenosis formation. (8) In this bird, because of size constraints and the concern of iatrogenic damage while trying to split the tracheal cartilages, the annular ligament-cartilage technique was used. Because no tension was apparent on the suture site after anastomosis, tension-relieving sutures were not placed. The insertion of excessive suture material may predispose to inflammation. (8)

Appropriate surgical technique includes handling tissues gently by using stay sutures or atraumatic forceps, minimizing tension at the surgical site, and aligning the tracheal edges as accurately as possible. (1,8) Polydioxanone, a monofilament absorbable suture material, was used in the trachea to minimize the risk of granulation tissue formation. Although polydioxanone is slowly absorbed, it caused the least tissue reaction of 5 tested suture materials in pigeons. (10) Additionally, in a study of tracheal anastomosis in rabbits (Oryctolagus cuniculus), results with polydioxanone were superior to those with polypropylene. (11) In the report of tracheal anastomosis and resection in a goose, polydioxanone was also used without complications. (9) In a study of tracheal resection and anastomosis in rabbits, an interrupted suture pattern provoked less stenosis than a continuous one. (11) To reduce intraluminal irritation in this hawk, a simple interrupted suture technique, using as few sutures as possible, was used, and all knots were tied external to the tracheal lumen. To ensure accurate placement, all sutures were preplaced before tracheal closure.

Surgical complications of tracheal resection and anastomosis can be immediate or delayed; but both can be considerable. Immediate complications include tracheal obstruction due to secretions, edema, or inflammation at the site of anastomosis. (12) Extratracheal hematoma formation can also cause obstruction. (12) Delayed complications are dehiscence and stenosis formation. (8) Appropriate surgical technique reduces the likelihood of both complications, while the placement and maintenance of an air sac cannula helps reduce morbidity associated with temporary tracheal obstruction.

Given the prolonged suppression of the adrenocortical axis after corticosteroid use in some species, with consequences such as aspergillosis, a nonsteroidal inflammatory drug was used to reduce postoperative inflammation in this hawk. (13) Other authors have used topical or systemic corticosteroids. (1,9)

Reports of xanthomatosis in birds include xanthomatosis in commercial chickens attributed to fat-related toxic hydrocarbons in feed (14); oral xanthoma in a budgerigar (Melopsittacus undulatus) (15); xanthomas overlying the carporadial-carpoulnar joint (16) and leg (17) of racing pigeons (Columba livia); a case series of xanthomas in 8 budgerigars and 1 rose-breasted cockatoo (Cacatua roseicapilla) (18); periarticular xanthomatosis in an American kestrel (Falco sparverius) (19); and xanthomatosis of the liver in an Amazon parrot. (20) Xanthomatosis has been experimentally induced in the feet of Japanese quail (Coturnix japonica) susceptible to dietary cholesterol-induced atherosclerosis. (21) Periosseous xanthogranulomatosis in a free-living fledging great horned owl (Bubo virginianus) eventually resolved without treatment. (22) A recent report described a novel cutaneous neoplasm that exhibited xanthomatous characteristics in a hyperlipidemic goose. (23)

In mammals, the term xanthoma has historically referred to a yellow cutaneous mass formed by lipid deposited within tissues and associated with hyperlipidemia. In a hyperlipidemic state, blood vessel trauma allows lipid extravasation into surrounding tissues. (24) Areas prone to trauma, such as extremities or injection sites, are considered sites predisposed to xanthoma formation. (24) Histologically, multinucleated giant cells, cholesterol clefts, and tissue macrophages (also called fixed macrophages or histiocytes) with intracytoplasmic lipid vacuolations are usually present. (24)

Currently in human medicine, many diverse xanthomatous syndromes, both with and without hyperlipidemia, appear similar histologically. These syndromes are now separated by signalment, clinical appearance, the presence or absence of hyperlipidemia, histopathologic appearance, and immunohistochemical phenotype. (25,26) Many believe that the various xanthomatous lesions in people are simply different manifestations of a spectrum of disorders resulting in lipid-laden tissue macrophages. (26,27) One view is that, excluding spontaneous xanthomas that develop in hyperlipidemic states and immunologic or storage disorders resulting in defective phagocytosis, all other instances of xanthogranulomatous reactions are the consequence of lipid phagocytosis by macrophages secondary to hemorrhage, suppuration, or necrosis. (28) The emerging view appears to be that once macrophages have phagocytosed lipid, the inflammatory process is similar, regardless of the initiating cause. (26-28)

In avian medicine, the syndromes of xanthoma, xanthomatosis, and xanthogranulomatous inflammation have not been consistently defined or separated (Table 1). Xanthomas and xanthomatosis are most commonly recognized as disorders of the avian integument, with lesions often overlying deeper tissue masses. (29) Xanthoma has been defined as a discrete mass of highly vacuolated macrophages and multinucleated giant cells, while xanthomatosis has been defined as a similar process but lacking discrete margins and often situated in the skin. (30) Xanthogranulomatous inflammation has been defined as a process with the histologic features of xanthoma as well as variable features of inflammation. (22) This contrasts with the emerging view in human literature described above, in which these categories are presumed to be variations of the same pathophysiologic phenomenon, occurring after macrophages phagocytose lipid. Only the presence of vacuolated or foamy macrophages is universal. The presence of multinucleated giant cells, inflammatory cells, and fibrous tissue does not clearly differentiate between the different histologic categories of xanthomatous change, as has been reported in avian medicine. Given these considerations, we propose that the term xanthogranulomatosis be used to describe avian lesions in which intracytoplasmic lipid vacuoles are seen within macrophages. We recognize that individual lesions may have varied numbers of the different histologic components, but adopting a single term will help to avoid confusion and inconsistency in categorizing lesions and may allow a more systematic examination of the syndromes in avian species that result in such changes.

The histologic findings in this case were those of a chronic inflammatory lesion affecting the subepithelial tissues of the trachea. The presence of cholesterol crystals with a mononuclear cell infiltration adds weight to a specific diagnosis of xanthogranulomatosis. Interestingly, intestinal intussusception requiring surgery has been de scribed in 2 red-tailed hawks, one of which died a few months later of acute tracheal obstruction. (31) The cause was not identified.

In this report, we describe a successful tracheal resection and anastomosis procedure in a raptor performed to relieve tracheal obstruction caused by a xanthogranulomatous reaction. Xanthogranulomas affecting the trachea are not common in birds of prey. The lesion likely occurred as a complication of intubation during multiple, prolonged anesthetic events for an unrelated problem. We propose that a single term, xanthogranulomatosis, replace the terms currently used to describe the syndromes in which intracytoplasmic lipid is found within tissue macrophages.

Acknowledgments: We thank J.M. Hamilton, DVM, PhD, Idexx Laboratories Ltd, West Yorkshire, UK, for making the initial diagnosis and the staff of Clockhouse Veterinary Hospital for their care and treatment of this bird.

References

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(3.) Klainer AS, Turndorf H, Wu WH, et al. Surface alterations due to endotracheal intubation. Am J Med. 1975;58:674-683.

(4.) Barbet JP, Chauveau M, Labbe S, et al. Breathing dry air causes acute epithelial damage and inflammation of the guinea pig trachea. J Appl Physiol. 1988;64:1851-1857.

(5.) Chitty J. A novel disinfectant in psittacine respiratory disease. Proc Annu Conf Assoc Avian Vet. 2002:25-27.

(6.) Smith MM, Gourley IM, Antis TC, Kurpershoek C. Management of tracheal stenosis in a dog. J Am Vet Med Assoc. 1990;196:931-934.

(7.) Parker D. Endoscopic repair of tracheal stenosis in a blue and gold macaw (Ara ararauna). Proc Annu Conf Assoc Avian Vet. 2003;95.

(8.) Hedlund CS. Tracheal resection and reconstruction. Probl Vet Med. 1991;3:210-228.

(9.) Clippinger TL, Bennett RA. Successful treatment of a traumatic tracheal stenosis in a goose by surgical resection and anastomosis. J Avian Med Surg. 1998;12:243-247.

(10.) Bennett RA, Yaeger MJ, Trapp A, Cambre RC. Histologic evaluation of the tissue reaction to five suture materials in the body wall of rock doves (Columba livia). J Avian Med Surg. 1997;11: 175-182.

(11.) McKeown PP, Tsuboi H, Togo T, et al. Growth of tracheal anastomoses: advantage of absorbable interrupted sutures. Ann Thorac Surg. 1991;51: 636-641.

(12.) LaMuraglia MV, Meister M, DiBona N. Tracheal resection and reconstruction: indications, surgical procedure, and postoperative care. Heart Lung. 1991;28:245-252.

(13.) Westerhof I, Van den Brom WE, Mol JA, et al. Sensitivity of the hypothalamic-pituitary-adrenal system of pigeons (Columba livia domestica) to suppression by dexamethasone, cortisol and prednisolone. Avian Dis. 1994;38:435-445.

(14.) Sanger VL, Lagace A. Avian xanthomatosis: etiology and pathogenesis. Avian Dis. 1966;10:103-111.

(15.) Ridgeway RL. Oral xanthoma in a budgerigar Melopsittacus undulatus. Vet Med Small Anim Clin. 1977;72:266-267.

(16.) Ciampi L. Fibroxanthogranuloma of a pigeon wing. Clin Vet. 1979;102:669-677.

(17.) Yang SY, Lee SH. Case report of xanthomatosis in racing pigeon. J Chinese Soc Vet Sci. 1987;13: 169-171.

(18.) Petrak ML, Gilmore CE. Neoplasms. In: Petrak ML, ed. Diseases of Cage and Aviary Birds. 2nd ed. Philadelphia, PA: Lea and Febiger; 1982:606-637.

(19.) Haley PI, Norrdin RW. Periarticular xanthomatosis in an American kestrel. J Am Vet Med Assoc. 1982;181:1394-1396.

(20.) Sandmeier P. Xanthomatosis of the liver in an Amazon parrot. Proc Conf Europ Assoc Avian Vet. 2001:170-173.

(21.) Hoekstra KA, Nichols CR, Garnett ME, et al. Dietary cholesterol-induced xanthomatosis in atherosclerosis-susceptible Japanese quail (Coturnix japonica). J Comp Pathol. 1998;119:419-427.

(22.) Raynor PL, Kollias GV, Krook L. Periosseous xanthogranulomatosis in a fledgling great horned owl (Bubo virginianus). J Avian Med Surg. 1999;13:269-274.

(23.) Jaensch SM, Butler R, O'Hara A, et al. Atypical multiple, papilliform, xanthomatous, cutaneous neoplasia in a goose (Anser anser). Aust Vet J. 2002;80:277-279.

(24.) Walton KW, Thomas C, Dunkerley DJ. The pathogenesis of xanthomata. J Pathol. 1972; 109: 271-289.

(25.) Hernandez-Martin A, Baselga E, Drolet B, Esterly NB. Juvenile xanthogranuloma. J Am Acad Dermatol. 1997;36:355-367.

(26.) Jaffe R. The histiocytoses. Clin Lab Med. 1999;19:135-155.

(27.) Ferrando J, Campo-Voegeli A, Soler-Carrillo J, et al. Systemic xanthohistiocytoma: a variant of xanthoma disseminatum? Br J Dermatol. 1998; 138:155-160.

(28.) Cozzutto C, Carbone A. The xanthogranulomatous process; xanthogranulomatous inflammation. Path Res Pract. 1998;183:395-402.

(29.) Latimer KS. Oncology. In: Ritchie BW, Harrison G, Harrison L, eds. Avian Medicine: Principles and Application. Lake Worth, FL: Wingers Publishing; 1994:640-672.

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From Great Western Referrals, Unit 10 Berkshire House, County Park Business Park, Shrivenham Road, Swindon, WILTS SN1 2NR, United Kingdom (Monks, Zsivanovits, Forbes), and Department of Pathology, School of Veterinary Medicine, University of the West Indies (UWI), St Augustine, Trinidad, West Indies (Cooper).
Table 1. Comparison of histologic reports of xanthoma, xanthomatosis,
and xanthogranulomatosis in birds.

 Multinucleated Inflammatory
Species Macrophages giant cells cells

Amazon Lipid-laden Present Granulocytes
 parrot (20)
Budgerigar (15) Large clear ND (a) ND
 foam cells
Domestic Dense Present ND
 chicken (14) infiltrations
 of foamy
 macrophages
Domestic Foamy ND Heterophils and
 goose (23) macrophages lymphocytes
 present near areas of
 ulceration
Great Macrophages, Present Granulomatous
 horned some of tissue
 owl (22) which had
 vacuolation
Japanese Present Present Granulomatous
 quail (21) inflammation
 and eruptive
 lesions
Kestrel (19) Densely packed ND Some areas with
 with varying lymphocytes
 sizes and and
 numbers of non-vacuolated
 vacuoles macrophages
Pigeon (16) Lipid-laden Present Granulocytes
 and
 mononuclear
 cells
Pigeon (17) Present Present Small numbers
 of lymphocytes
 and small areas
 of necrosis

 Cholesterol
 Fibrous clefts or
Species tissue crystals Diagnosis

Amazon No Present Xanthomatosis
 parrot (20)
Budgerigar (15) Connective ND Xanthoma
 tissue
 infiltration
Domestic Present ND Xanthomatosis
 chicken (14)
Domestic ND Reference to Atypical multiple
 goose (23) needle-like papilliform
 clefts xanthomatous
 cutaneous
 neoplasia
Great Dense Present Xanthogranulomatosis
 horned capsule
 owl (22)
Japanese ND ND Xanthomatosis
 quail (21)
Kestrel (19) ND ND Xanthomatosis
Pigeon (16) Present ND Fibroxantho-
 granulotna
Pigeon (17) ND Present Xanthomatosis

(a) ND indicates not determined or stated.
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Article Details
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Title Annotation:Clinical Reports
Author:Monks, Deborah J.; Zsivanovits, H. Petra; Cooper, John E.; Forbes, Neil A.
Publication:Journal of Avian Medicine and Surgery
Article Type:Case study
Geographic Code:4EUUK
Date:Dec 1, 2006
Words:3778
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