Acute Necrotizing Pancreatitis in a Yellow-Naped Amazon Parrot (Amazona Auropalliata)

Acute Necrotizing Pancreatitis in a Yellow-naped Amazon Parrot (Amazona auropalliata)

Authors: Donnelly, Kyle A., Le Roux, Alexandre, Donovan, Taryn A., Grodio, Jessica, and Quesenberry, Katherine Source: Journal of Avian Medicine and Surgery, 32(3) : 232-239 Published By: Association of Avian Veterinarians URL: https://doi.org/10.1647/2017-268

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Clinical Report

Acute Necrotizing Pancreatitis in a Yellow-naped Amazon Parrot (Amazona auropalliata) Kyle A. Donnelly, DVM, MPH, Alexandre Le Roux, DVM, MS, Dipl ECVDI, Dipl ACVR, Taryn A. Donovan, DVM, Dipl ACVP, Jessica Grodio, DVM, PhD, and Katherine Quesenberry, DVM, MPH, Dipl ABVP (Avian)

Abstract: A 25-year-old female yellow-naped Amazon parrot (Amazona auropalliata) was presented for an acute onset of lethargy, ptyalism, and regurgitation. Results of hematologic testing and plasma biochemical analysis revealed severe leukopenia and heteropenia with toxic heterophils and marked hyperamylasemia and hypoproteinemia, consistent with gastrointestinal dysfunction. Survey radiograph findings were suggestive of coelomic effusion. Results of a contrast-enhanced computed tomography (CT) scan revealed a tubular, irregularly marginated structure along the medial aspect of the duodenum, consistent with an inflamed pancreas. The bird died soon after CT imaging, and acute necrotizing pancreatitis and pancreatic coagulative necrosis were observed at necropsy. This report describes the use of a less-invasive modality such as CT to aid in the antemortem diagnosis of acute pancreatitis in a psittacine bird. Pancreatitis should be considered a differential diagnosis in birds with gastrointestinal signs and coelomic effusion visualized on radiography, and the observation of an enlarged inflamed pancreas in the absence of a defined pancreatic mass on CT. Key words: pancreatitis, computed tomography, avian, yellow-naped Amazon parrot, Amazona auropalliata

Clinical Report markedly lipemic, and measured analytes revealed mildly increased creatine kinase concentration (766 A 25-year-old female yellow-naped Amazon U/L; reference interval, 132–402 U/L).1 Plasma parrot (Amazona auropalliata) was examined at a lipid values were not measured at this facility. referring veterinary facility for an acute onset of At the referring facility, the bird was treated lethargy, ptyalism, and regurgitation. The parrot with lactated Ringer’s solution (30 mL/kg SC had no previous health issues reported by the q12h), enrofloxacin (15 mg/kg in SC fluid pocket owners and was fed a commercial pelleted diet, q12h; Baytril 2.27%, Bayer, Shawnee Mission, KS, fresh fruits and vegetables, and cooked egg whites USA), and metronidazole (25 mg/kg PO q12h; on a regular basis. The patient was seen shredding metronidazole 500 mg, compounded in Versa Free paper and chewing on cage toys more frequently in sugarless syrup vehicle, Humco Texarkana, TX, the 2 weeks before presentation. A blood sample USA, and Ora-Plus suspending vehicle, Perrigo, collected at the referring facility was noted to be Minneapolis, MN, USA) because of concern for coelomitis while pending results of diagnostic tests; From Avian and Exotic Pet Service (Donnelly, Quesen- calcium gluconate (100 mg/kg in SC fluid pocket berry), Diagnostic Imaging Service (Le Roux), and Anatomic Pathology Service (Donovan), The Animal Medical Center, 510 q12h) because of concern for reproductive disease; E62ndSt,NewYork,NY10065,USA;andSouthWilton and sucralfate (25 mg/kg PO 1 hour after oral Veterinary Group, 51 Danbury Rd, Wilton, CT 06897, USA medications q12h; Carafate, Aptalis Pharma US (Grodio). Present address: University of Florida College of Inc., Bridgewater, NJ, USA) because of the Veterinary Medicine, Zoological Medicine Service, PO Box presence of gastrointestinal signs. The patient was 100126, 2015 SW 16th Ave, Gainesville FL 32610, USA (Donnelly); The Center for Avian and Exotic Medicine, 562 administered 1 dose of leuprolide acetate (800 lg/ Columbus Ave, New York, NY 10024, USA (Grodio). kg IM; Lupron Depot, AbbVie Inc., Chicago, IL,

232

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Figure 1. (A) Right lateral and (B) ventrodorsal whole-body radiographs of an Amazon parrot that presented with acute onset of lethargy, ptyalism, and regurgitation. Coelomic serosal detail is severely decreased, with effacement of most of the caudal coelomic organ margins and distension of the caudal coelomic cavity (black asterisk). An increased amount of body fat is also noted radiographically (white arrowheads). Coelomic effusion is considered most likely based on these radiographic ﬁndings. Note the decreased pulmonary/air sac inﬂation, likely secondary to caudal coelomic distension (white # signs).

USA) in light of the recent reproductive behaviors tachypneic with normal heart and lung sounds and and concern for reproductive disease. The next the coelom was full on palpation, suggestive of day, the bird was sedated with midazolam (1.5 mg/ fluid; however, no discrete masses were discern- kg IM) and whole-body survey radiographs were able. The bird was passing only urates with no obtained. Severe decreased coelomic serosal detail fecal material, with occasional small amounts of was present radiographically, with effacement of hemorrhagic mucous. A blood sample was sub- most of the caudal coelomic organ margins and mitted for hematologic testing, plasma biochemical distension of the caudal coelomic cavity (Fig 1). analysis, and measurement of blood lead and zinc Poor inflation of the lungs and air sacs was also levels, and the bird was admitted to the hospital for observed and was considered a consequence of the further supportive care and diagnostic testing. coelomic distension. Because of the increased Treatments administered consisted of parenteral amount of body fat and the caudal coelomic fluids (20 mL/kg SC q12h, lactated Ringers distension in this patient, coelomic effusion was solution), ranitidine (1 mg/kg IM q12h), sucralfate considered the primary differential diagnosis for (25 mg/kg PO q12h), metoclopramide (0.5 mg/kg the loss of coelomic serosal detail, followed by a IM q12h; Baxter Healthcare Corp., Deerfield, IL, caudal coelomic mass. A definitive origin for the USA), calcium EDTA (30 mg/kg SC once; suspected coelomic effusion was not determined Diamondback Drugs, Scottsdale, AZ, USA) pend- radiographically. The patient subsequently was ing results of blood lead and zinc levels, enroflox- referred to the Animal Medical Center for further acin (10 mg/kg SC q12h), meloxicam (0.5 mg/kg diagnostic imaging. IM q12h), and gavage feedings (7 mL/kg; Exact On presentation, the bird was quiet and Hand Feeding Formula, Kaytee, Chilton, WI, responsive, with its eyelids partially closed and USA). feathers fluffed. It weighed 657 g and was obese, Results of plasma biochemical analysis revealed with a body condition score of 7/9. The parrot was moderately increased activity of aspartate amino-

transferase (733 U/L; reference interval, 150–390 tate brown fluid. The oral cavity was suctioned U/L),1 severely increased activities of amylase until normal breathing resumed. An intravenous (7113 U/L; reference interval, 187–546 U/L)1 and butterfly catheter was placed in the right basilic creatine kinase (6505 U/L), 1 mild hypertriglycer- vein and a bolus of 2 mL lactated Ringer’s solution idemia (379 mg/dL; reference interval, 10–300 mg/ was administered. The bird began to regurgitate dL),2 and moderate hypoproteinemia (2.1 g/dL; again and subsequently went into respiratory reference interval, 2.6–5.9 g/fL)3 characterized by arrest. Epinephrine (0.1 mg/kg IV) and atropine mild hypoalbuminemia (0.7 g/dL; reference inter- (0.2 mg/kg IV) were given to no effect. The body val, 0.9–3.3 g/dL).3 Cholesterol level was normal at was submitted for a cosmetic necropsy. 197 mg/dL (reference interval, 87–364 mg/dL)2 and The CT images revealed a moderate volume of glucose level was normal at 267 mg/dL (reference coelomic effusion distending the coelom (Fig 2). interval, 246–3378 mg/dL).1 Results of plasma The gastrointestinal tract was homogeneously protein electrophoresis and measurement of bile moderately dilated with fluid, and segmental mild acid levels were within reference intervals. Abnor- thickening and increased enhancement of the small mal results of hematologic testing revealed moder- intestinal wall were noted. A tubular, irregularly ate leukopenia (4000 cells/lL; reference interval, marginated, soft-tissue attenuating structure, mod- 6000–17 000 cells/lL) with severe heteropenia (720 erately enhancing, was observed within the right cells/lL; reference interval, 3844–9052 cells/lL) cranial coelom, coursing along the medial aspect of with a left shift (560 cells/lL; reference interval, 0 the duodenum, consistent with a diffusely enlarged cells/lL), toxic change in heterophils characterized pancreas. The liver was heterogeneously enhanc- by decreased numbers of cytoplasmic granules, ing, with ill-defined hypoattenuating areas ob- rounding of the granules, increased cytoplasmic served predominantly within the right hepatic basophilia, and purple coloration to some of the parenchyma on the postcontrast images. The granules. The lymphocytes were reactive with spleen appeared mildly enlarged. The oviduct was deeper blue cytoplasm and an oval nucleus with prominent and moderately enhancing. Bilaterally, clumped to lacy chromatin and occasionally a within the caudal and peripheral aspect of the discernable nucleolar ring or nucleolus. These lungs, increased soft-tissue attenuations were changes were consistent with severe inflammation.1 noted, effacing the normal pulmonary architecture. All other test results were unremarkable, and Finally, the amount of fat was increased within the blood lead and zinc levels were normal. coelomic cavity. The CT findings were consistent The parrot continued to regurgitate overnight. with acute pancreatitis, with secondary severe The next day, the bird was anesthetized for a coelomitis, diffuse enteritis, and predominantly whole-body computed tomography (CT) scan. right-sided hepatopathy (suspected to represent Anesthesia was induced and maintained with hepatitis, lipidosis or a combination of both) in an isoflurane delivered by facemask at 2%. The bird obese parrot. Even though neoplasia was not was then intubated with a 3.5-mm uncuffed completely ruled out, it was considered less likely endotracheal tube, and positive-pressure ventila- because of the lack of defined pancreatic mass. The tion was delivered intermittently during the scan. increased prominence and enhancement of the The CT images were acquired with a third- oviduct on the postcontrast images were consid- generation CT Toshiba Aquilion 64 unit (Canon ered to be secondary to inflammation. Medical Systems, Tustin, CA, USA), as a volume Gross necropsy examination revealed approxi- of data (120 kVp, 100 mAs), and then reconstruct- mately 30 mL of cloudy, yellow effusion within the ed in transverse, sagittal, and dorsal planes in a 1- coelom. This fluid was not cultured or analyzed. mm slice thickness, to obtain high-resolution The intestines were diffusely, markedly dilated and images. Pre- and postcontrast images were ac- reddened with multifocal petechial serosal hemor- quired in soft-tissue and lung algorithms, with rhages, indicative of enteritis. Multiple intestinal nonionic iodinated contrast (2.2 mL/kg; Omni- loops were adhered to one another by pale tan, paque 300, GE Healthcare, Princeton, NJ, USA) manually removable tissue (fibrin). Similar mate- administered by intravenous injection through the rial was observed in the region of the pancreas, left basilic wing vein after acquisition of the initial with yellow, red, and tan stippling, interpreted as precontrast images. Poor perfusion was noted in pancreatitis, fibrinous coelomitis, mesenteric stea- the peripheral veins during anesthesia, which was titis, and steatonecrosis (Fig 3). No foreign discontinued after the scans were complete, 30 material was observed throughout the gastrointes- minutes after induction. During anesthetic recov- tinal tract lumen. The crop contained liquid, ery after extubation, the patient began to regurgi- yellow ingesta. The hepatic parenchyma was

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Figure 2. Select computed tomography (CT) images of the Amazon parrot described in Figure 1, acquired with a third CT generation Toshiba Aquilion 64 unit (Canon Medical Systems, Tustin, CA, USA) as a volume (120 kVp, 100 mAs), and then reconstructed in transverse, sagittal, and dorsal planes, in a 1-mm slice thickness, to obtain high-resolution images. (A) Dorsal multiplanar reconstruction (MPR) in a lung algorithm, precontrast. Bilateral soft-tissue attenuations are visible within the caudal lungs (black arrows), considered to represent either pneumonia or pulmonary thromboemboli. On images (B) to (E) (multiplanar reconstruction images in a soft-tissue algorithm, postcontrast), moderate coelomic effusion is present (white asterisk), with a tubular, irregularly marginated, soft-tissue attenuating structure, moderately enhancing, observed within the right cranial coelom, (D) coursing along the medial aspect of the duodenum, and consistent with an enlarged inflamed pancreas (white arrows). The gastrointestinal tract is homogeneously moderately dilated with fluid, and segmentally, mild thickening and abnormal enhancement of the small intestinal wall is noted on these images, consistent with enteritis. (B, D, E) Additionally, the liver is heterogeneously enhancing, as visualized on these images, with ill-defined hypoattenuating areas observed within the right hepatic parenchyma (white arrowheads), and suspected to represent hepatitis, lipidosis, or a combination of both.The image inset associated with each subfigure represents the plan of the displayed CT images. (A–D) The right of the patient is on the left on images.

rial were present. In the lungs, heterophilic, histiocytic parabronchial pneumonia with intralesional proteinaceous and anisotropic material was observed, consistent with aspiration. Regional airsacculitis was also present. There was no histologic evidence of thrombosis in the lungs. The cause of death in this case was interpreted to be a combination of aspiration and disseminated coelomic inflammation, including necrotizing pancreatitis, mesenteric steatitis, transmural enteritis, and airsacculitis, resulting in a widespread inflammatory response and systemic sequelae. Figure 3. The intestines and mesentery at necropsy of the Amazon parrot described in Figure 1. The intestines are Discussion diffusely, markedly dilated and reddened with This clinical report is the first description of CT multifocal petechial serosal hemorrhages. Multiple findings in a case of acute necrotizing pancreatitis intestinal loops are adhered to one another by pale tan, manually removable material (fibrin). Similar in an adult Amazon parrot, confirmed at necropsy. material is observed in the region of the pancreas Compared with the gold standard of surgical or (arrow), with yellow, red, and tan stippling (asterisk), endoscopic biopsy, CT scanning may prove to be a consistent with pancreatitis, coelomitis, fibrinous valuable, less-invasive modality to support the mesenteric steatitis, and steatonecrosis (bar 1 cm). diagnosis of pancreatitis in birds. Additional ¼ antemortem diagnostic tools are needed for this diffusely mottled pale tan to dark brown, more disease process, as pancreatitis is often anecdotally prominently in the right lobe. The lungs had locally described in birds, but comparatively few reports extensive regions of dark red parenchyma in the have been published. This case adds support to the caudal regions, and sections of lung floated in previously described association of pancreatitis formalin. Representative tissue samples from all with hyperamylasemia,4 but it also offers an organs were obtained, placed in 10% neutral- additional modality to aid in diagnosis. buffered formalin, routinely embedded in paraffin, Similar to other animals, the avian pancreas lies sectioned at 5 lm, and stained with hematoxylin between the ascending and descending loops of the and eosin. duodenum and has both exocrine and endocrine Histologic evaluation of the pancreas revealed functions. Most avian species have a trilobed coagulation necrosis of entire lobules; severe pancreas with the third lobe, or splenic pancreas, regional necrotizing, fibrinous, heterophilic, histio- located independent from the other two.5 Al- cytic mesenteric steatitis; and multifocal, peripher- though the intestinal wall mucosa produces some al involvement of the viable pancreatic of the digestive enzymes, the pancreatic ducts also parenchyma (pancreatitis) (Fig 4). Occasionally, drain exocrine pancreatic enzymes into the ascend- few sharply demarcated, round vacuoles (lipid) ing duodenal loop. In healthy birds, these digestive were observed within the cytoplasm of pancreatic enzymes are secreted into the intestine as inactive acinar cells. The duodenum exhibited transmural, precursors, preventing autodigestion of the pan- fibrinous, heterophilic and lymphoplasmacytic creas. Acute pancreatitis is characterized by enteritis with multifocal necrosis. Histiocytic, activation of these enzymes outside of the intestine, heterophilic airsacculitis was present in air sacs resulting in coagulation necrosis of the pancreas surrounding the pancreas and throughout the and surrounding tissue.6 The presence of such large coelom. Similar inflammation was observed in regions of coagulation necrosis in this case may the capsule of the spleen. Given the type of reflect the severity of the pancreatitis or possible inflammation (heterophilic, histiocytic), special concurrent ischemic damage, although no histo- stains for fungi (Gomori’s methenamine silver) logic evidence of thrombosis was found. Other and acid-fast bacteria (Ziehl-Neelsen) were per- sources of pancreatitis may be coelomitis originat- formed on the pancreas, mesentery, and duode- ing from elsewhere influencing inflammatory num, the results of which were negative. In the changes in the pancreas. liver, lipidosis was marked with concurrent hepa- Acute necrotizing pancreatitis is rarely reported titis, cholangitis, and necrosis. Granulomatous in birds and warrants further clinical investigation oophoritis with intralesional lipid and yolk mate- to determine causal or associated factors in specific

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Figure 4. The pancreas and mesentery of the Amazon parrot described in Figure 1. Coagulation necrosis of an entire pancreatic lobule (asterisk) with severe regional necrotizing, fibrinous, heterophilic, histiocytic mesenteric steatitis (arrows). (Hematoxylin and eosin, 340 magnification, bar 200 lm.) Inset: High-magnification view of heterophilic, ¼ histiocytic, necrotizing mesenteric steatitis (arrow). (Hematoxylin and eosin, 3500 magnification, bar 20 lm.) ¼ cases so that ultimately treatment and prevention diabetes mellitus, 11–13 toxicities,14,15 and neopla- guidelines can be established. Quaker parrots sia.16 (Myiopsitta monachus) appear particularly prone Viral infections have historically been docu- to developing acute necrotizing pancreatitis of mented as a frequent cause of pancreatitis in birds. unknown cause.7 Interestingly, Quaker parrots Specific viruses associated with pancreatitis are coronavirus,17 herpesvirus,18 paramyxovirus 3,19 seem to be especially prone to developing hyper- 20 lipidemia, although there are individuals as well as and flavivirus (West Nile virus). A case of herpesviral-associated pancreatitis in a cockatiel other species that develop hyperlipidemia but not (Nymphicus hollandicus) yielded inclusion bodies of pancreatic problems.8 This case demonstrated a the pancreatic acinar and duct cells and was also mild hypertriglyceridemia with normal serum accompanied by diabetes mellitus.18 Coronavirus cholesterol level. High-density lipoproteins, low- in pigeons (Columba livia) is associated not only density lipoproteins, and very-low-density lipopro- with pancreatitis but also excess mucus in the teins were not evaluated. Various clinical condi- trachea, as well as pulmonary lesions.17 Paramyxo- tions that have been associated with acute virus has been associated with pancreatitis and also pancreatitis in birds include obesity and a high- neurologic pathology in birds.19 Some avian fat diet,4,9 viral infections, chlamydial infection,10 species infected with West Nile virus present with

nonspecific clinical signs and variable reports of ter of the inflammation between organ systems was systemic inflammation, including pancreatitis.20 also different, with a granulomatous oophoritis Although this bird did not exhibit clinical neuro- versus heterophilic pancreatitis. logic deficits, the brain was not assessed because of The severity of the inflammation associated with the cosmetic necropsy performed. Viral culture and the pancreas in this parrot likely accounts for the molecular diagnostic tests also were not per- regional air sac and intestinal inflammation. The formed. intestinal inflammation may explain the hypopro- Pancreatitis has been associated with diabetes teinemia secondary to a protein-losing enteropa- mellitus in psittacine birds in several reports.11–13 thy; however, the heterophilic inflammation was In a report of diabetes in a chestnut-fronted macaw most severe over the intestinal serosa compared (Ara severa),12 pancreatitis was characterized as with the mucosa, indicating an extraintestinal mild and considered chronic, in contrast to the source of inflammation. The coelomic effusion clinical presentation of the parrot we describe. No may be secondary to the pancreatitis, a primary evidence of diabetes, such as hyperglycemia, insult that then caused pancreatitis such as weight loss, polyuria, or polydipsia, was observed hepatitis or salpingitis, protein-losing enteropathy, in the case described here. Occasional reports link or a combination of all. The severe inflammatory heavy metal toxicosis to pancreatitis;14,15 however, leukogram supports the marked inflammation results in this bird were negative for both zinc and observed at necropsy. One study suggested amylase lead on blood measurements and gastrointestinal levels above 1500 U/L may be associated with metallic foreign material on imaging. Obesity and avian pancreatitis, which is consistent with the hepatopathy or concurrent egg yolk coelomitis amylase level of 7113 U/L present in this case.4 may have been contributing factors in this case. Lipase is often measured concomitantly with In captivity, Amazon parrots appear particular- amylase in small animal patients; however, this ly prone to developing obesity and secondary test is not useful in cats and only specific in dogs if consequences including atherosclerosis and hepatic results are orders of magnitude above the reference lipidosis.2,21 In this parrot, fat accumulation was interval.24,25 Although there are no reference occasionally present within the exocrine pancreas intervals available in psittacine birds, lipase may but was not a prominent feature. The role that prove useful for further supporting a diagnosis of hypertriglyceridemia played in this case is unclear; pancreatitis. Development of a pancreas-specific however, consideration should be given to its lipase assay for use in birds would be a useful next relationship with the hepatic lipidosis, obesity step. pancreatitis, and reproductive disease observed at Treatment of acute pancreatitis is not well necropsy. In people, hypertriglyceridemia is the described in birds. In canine patients, treatment most common cause of acute pancreatitis after is supportive, typically aimed at replacing fluid alcohol and gallstone disease.22 Underlying path- losses, preserving hydrostatic pressure, controlling ophysiology includes hydrolysis of triglycerides by nausea, and providing pain relief.26 Although this pancreatic lipase and excessive formation of free patient was started on appropriate supportive fatty acids with associated inflammation.22 Con- treatments, hypotension and aspiration com- comitant hyperviscosity and ischemia also likely pounded by general anesthesia likely led to the play a role.22 In birds, the liver is stimulated during bird’s death. the process of egg formation to produce egg yolk Histopathology is considered the test of choice precursors such as yolk-targeted, very-low-density for the diagnosis of pancreatitis. Historically, lipoproteins, which are then reflected in circulation antemortem diagnosis of pancreatitis in birds has as a hypertriglyceridemia.23 This bird’s hypertri- only been achieved by endoscopy or exploratory glyceridemia paired with oophoritis and hepatic laparotomy.4 Patient history can provide useful lipidosis observed at necropsy may suggest some supporting information during assessment of influence of the reproductive status in the devel- suspected cases of avian pancreatitis. In this case, opment of pancreatitis. visceral coelomic pain may have contributed to the The salpingitis cannot be ruled out as the initial abnormal behaviors observed in this parrot, inflammatory insult that then led to the pancrea- specifically chewing of cage items. Body condition titis; however, this is considered less likely given score and high-fat diet are possible predisposing the relative difference in severity of inflammation factors for pancreatitis in birds; however, more between the mild inflammation observed in the data are needed to add to existing reports.4,9 This reproductive tract compared with the severe case is of particular importance to highlight the necrotizing pancreatitis. Additionally, the charac- potential use of less-invasive modalities such as CT

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