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Ileo-ceco-rectal intussusception requiring intestinal resection and anastomosis in a tawny eagle (Aquila rapax).

Abstract: A 23-year-old male tawny eagle (Aquila rapax) was examined because of sudden onset of lethargy, regurgitation, and hematochezia. An intestinal obstruction was suspected based on radiographic findings, and an ileo-ceco-rectal intussusception was confirmed by coelioscopy. A 14.3-cm section of intestine was resected before an intestinal anastomosis was done. Coelomic endoscopic examination confirmed a postsurgical complication of adhesions between the intestinal anastomosis and the dorsal coelomic wall, resulting in a partial luminal stricture and requiring surgical removal of the adhesions. Rectoscopy was useful in diagnosing a mild luminal stricture related to the second surgery. Complete recovery was observed 2 months after surgery. Lack of further complications in the 2 years after surgery demonstrates good tolerance of intestinal resection and anastomosis of a large segment of bowel in an eagle. This report is the first reported case of intussusception in an eagle and emphasizes the potential use of endoscopic examination in the diagnosis as well as in the management of complications.

Key words: ileo-ceco-rectal intussusception, anastomosis, avian, tawny eagle, Aquila rapax

Clinical Report

A 23-year-old imprinted male tawny eagle (Aquila rapax) was examined because of sudden onset of lethargy, regurgitation, anorexia, and hematochezia. The eagle was a working bird kept indoors at night and outdoors during the day. The bird was fed commercially sourced day-old chicks and rats. Toxin exposure was unlikely.

On examination, the eagle was active and alert and weighed 1.8 kg. It presented with a body condition score of 2.5 (0-5), an empty crop, and an abnormal posture (minimal flexion of the vertebral column along the back). No parasites or ova were observed on examination of fecal samples provided by the owner.

For ease of diagnostic testing and treatment, general anesthesia was induced with 3%-5% isoflurane in 2 L/min oxygen administered by face mask and followed by endotracheal intubation and maintenance with l%-2% isoflurane. A blood sample was collected, and a 22-gauge intravenous catheter was placed in the basilic vein. Fluid administration was initiated at 15 mL/kg IV of a 20% solution containing vitamin B complex, amino acids, and dextrose (Duphalyte, Pfizer, Sandwich, Kent, UK) diluted in Flartmann solution (compound sodium lactate; Aquapharm, Pfizer, Dunnington, York, UK). Whole-body radiographs revealed a tubular soft-tissue opacity in the dorsocaudal aspect of the coelomic cavity. Results of the complete blood count (CBC) revealed mild leukocytosis (10,000 cells/[micro]L [10 x [10.sup.9] cells/L]; reference interval, 5000-9500 cells/[micro]L [5-9.5 x [10.sup.9] cells/L]) with a normal hematocrit and thrombocyte count. (1,2) No hemoparasites were observed. Serum biochemical analysis revealed hypoproteinemia (2.7 g/dL [27 g/L]; reference interval, 2.9-4.14 g/dL [29.0-41.4 g/L]), hypoalbuminemia (0.8 g/dL [8 g/ L]; reference interval, 1.11-1.35 g/dL [11.1-13.5 g/ L]), hypoglobulinemia (1.9 g/dL [19 g/L]; reference interval, 2.35-2.84 g/dL [23.5-28.4 g/L]), hypouricemia (3.13 mg/dL [186 [micro]mol/L]; reference interval, 6.94-9.68 mg/dL [413-576 [micro]mol/L]), low bile acids (0.82 [micro]g/mL [2 pmol/L]; reference interval, 8.17-36.76 [micro]g/mL [20-90 [micro]mol/L]), hyperglycemia (419 mg/dL [23.3 mmol/L]; reference interval, 183.8-261.3 mg/dL [10.2-14.5 mmol/L]), and hypocalcemia (8 mg/dL [2 mmol/L]; reference interval, 8.8-10.64 mg/dL [2.21-2.66 mmol/L]). (1) Hematochezia in combination with the hematologic and radiographic findings were consistent with enteritis, gastrointestinal ulcers, or obstruction (neoplasia, foreign body, volvulus, or intussusception). Fluid therapy (20 mL/kg IV q5h of 20% Duphalyte diluted in Hartmann solution) and marbofloxacin (15 mg/kg IM q12h; Marbocyl, Vetoquinol, Buckingham, UK) administration were begun. The eagle was discharged.

[FIGURE 1 OMITTED]

For 2 days, the bird was brighter and passing smaller volumes of hemorrhagic diarrhea. However, it remained anorectic and was readmitted because regurgitation recurred. Whole-body radiographs taken with the bird under anesthesia (anesthetic protocol as described previously) revealed a severely dilated, gas-filled proventriculus, ventriculus, and intestines orad to a tubular soft-tissue opacity in the ileo-ceco-rectal area (Figs 1 and 2). At 24 hours after readmission, the bird's weight was 1.43 kg, and a ventrodorsal radiograph obtained under anesthesia confirmed the persistence of the soft-tissue opacity in the ileo-cecorectal region (Fig 3).

Coelomic endoscopic examination was planned to determine the origin of the tubular opacity visible on radiographs. For this procedure, butorphanol tartrate (1 mg/kg IM) and intraoperative fluids (15 mL/kg IV of 20% Duphalyte diluted in Hartmann solution and 6 mL/kg IV of hydroxyethyl starch colloids in isotonic NaCl solution (Voluven 6%, Fresenius Kabi, Runcorn, Cheshire, UK) were administered. The bird was anesthetized as described previously and positioned with the head and cranial coelom elevated 40[degrees] to minimize the risk of potential free intracoelomic fluid entering the lungs. The left leg was restrained craniodorsally, and left flank was prepared for aseptic surgery.

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

Coelomic endoscopy through a left flank approach revealed a severely congested and distended ileo-ceco-rectal region, with adhesions and potential necrosis at the supracecal loop. Because of these findings, the potential risk of intestinal necrosis, and the lack of response to therapy, surgery was elected.

The blunt incision used for the endoscopic examination was extended cranially and caudally with scissors. A surgical retractor (Lone Star retractor system, Veterinary Specialty Products, Inc., Mission, KS, USA) was used to maximize exposure of the coelomic organs. The mass was a pale swelling of the intestine, firm on palpation, and located in the ileo-ceco-rectal region (Fig 4). The adjacent intestine was severely congested, and intraluminal gas and fluid were palpated orad to the mass.

Stay sutures (6/0 polydioxanone, PDS II Taper point, Johnson & Johnson Inti., St. Elevens-Woluwe, Belgium) were placed orad and aborad to the mass. The aborad stay suture was less than 1 cm from the cloaca, preventing the mass from being exteriorized from the coelom. Sterile swabs were used to isolate the affected intestine from the coelom. An area of necrotic and congested intestine perforated, resulting in fecal contamination of the intestinal serosa. The intestines orad and aborad to the firm mass were clamped with atraumatic pediatric bulldog clamps and incised. When the middle of the isolated tissue was incised, the walls were inflamed and congested and did not bleed. Visualization of intestinal telescoping in the mass confirmed the intussusception (Fig 5). A 14.3cm section of nonviable intestine was resected, and an end-to-end ileo-rectal anastomosis was done by opposing the ends of the resected intestine and suturing in a simple interrupted appositional pattern with 6/0 polydioxanone, with extraluminal knots separated by 1 mm. The aborad intestine was severely congested and friable. After closure of the anastomosis, 2 mL of warm fluids were injected into the intestinal lumen to test for leaks. The stay sutures were removed, and the coelomic cavity and skin were closed with 3/0 polyglactin 910 (Vicryl, Johnson & Johnson Intl.) in a continuous apposition and an interrupted horizontal mattress pattern, respectively. An esophagostomy tube was placed after surgery to minimize the stress associated with repeated restraint for forcefeeding.

Postoperative analgesia was maintained with butorphanol (1 mg/kg IM q4h for 3 days) followed by meloxicam (0.1 mg/kg PO q24h for 5 days; Metacam, Boehringer Ingelheim, Rhein, Germany). Amoxicillin-clavulanate (125 mg/kg, 1 dose IM, then PO q12h, Noroclav tablets, Norbrook Laboratories, County Down, Northern Ireland), enrofloxacin (15 mg/kg PO q12h. Baytril 10% oral solution. Bayer, Kiel, Germany), and itraconazole (5 mg/kg PO q12h, Sporanox 100-mg capsules, Janssen-Cilag, High Wycombe Bucks, UK) were administered to control and prevent infection.

Histopathologic examination of the intussusception revealed severe, subacute, transmural intestinal necrosis and hemorrhage. The intestinal mucosa had extensive ulceration with a thick layer of fibrin mixed with numerous karyorrhectic and karyopiknotic debris, degenerated polynucleated heterophils, erythrocytes, and large pleomorphic bacterial colonies. The underlying lamina propria was severely edematous and hemorrhagic, containing numerous macrophages, polynucleated heterophils, and some multinucleated giant cells. The necrosis and inflammation extended through the intestinal submucosa and the muscularis to the serosa with vascular thrombosis and severe acute multifocal hemorrhage. No parasitic or bacterial elements were identified.

[FIGURE 4 OMITTED]

The bird was discharged 3 days after surgery. The owner administered a critical care diet (30 mL PO; Emeraid Carnivore Care, Lafeber, Cornell, IL, USA) followed by 10 mL of 20% Duphalyte in Hartmann solution and oral medications via the esophagostomy tube twice daily. The bird passed small amounts of fecal material with large volumes of urates within 6 hours after the first administration of formula. By 2 days after surgery, the eagle was brighter and ate some chopped skinned chicks. Nonhemorrhagic voluminous feces were observed during the 4 days after discharge. Four days after surgery, the eagle regurgitated solid food, and its administration was discontinued. When regurgitation recurred 24 hours later, enrofloxacin intolerance was suspected, and it was replaced by marbofloxacin in crushed tablet form (15 mg/kg PO q12h). Further episodes of regurgitation were not reported, and solid food was reintroduced gradually during the next 3 days.

[FIGURE 5 OMITTED]

At 10 days after surgery, the eagle weighed 1.43 kg and was eating 7 chopped skinned chicks daily. The sutures and the esophagostomy tube were removed with the eagle under anesthesia, and a blood sample was collected for a repeat CBC and biochemical analysis. Results revealed anemia (hematocrit, 30%; reference interval, 37-47%), polychromasia and anisocytosis, hypoalbuminemia (0.9 g/dL [9 g/L]), hypouricemia (1.19 mg/dL [71 [micro]mol/L]), decreased bile acids (2.86 [micro]g/dL [70 [micro]mol/ L]), and increased lactate dehydrogenase (1757 U/L; reference interval, 211-369 U/L), creatine kinase (1017 U/L; no reference reported), and aspartate aminotransferase (581 U/L; reference interval, 124-226 U/L). (1) All medications were discontinued.

At 12 days after surgery, the eagle vomited once and was lethargic, although still passing feces. Radiographs obtained with the bird under anesthesia revealed a soft-tissue density dorsal to the anastomosis site. Coelomic endoscopy revealed fibrinous material immediately aborad to distended intestinal loops. A sample of this material was submitted for bacterial culture, but results yielded no growth. The fibrinous adhesions between the anastomosis site and the dorsal coelomic wall were carefully cut by electrosurgery. Treatment with amoxicillin-clavulanate 1M and butorphanol IM were restarted, and supplemental fluids were given IV for 24 hours. The critical care diet (30 mL q8h) was administered via a feeding tube for the next 4 days. Twenty days later, the eagle was active and alert, eating, gaining weight, and passing feces without difficulty. Rectoscopy was performed with the eagle under general anesthesia, and a mild degree of stricture was observed at the anastomosis site, although it was not blocking the intestinal lumen. Lactulose (200 mg PO q12h for 7 days) was started. The bird recommenced flying duties several days later. Except for 1 transient episode of hematochezia 20 days later, no more incidents were reported in the 2 years after surgery.

Discussion

We describe the first reported case of intussusception in an eagle. The clinical signs and diagnostic and therapeutic approaches for intussusception in birds and the potential utility of endoscopic examination in the diagnosis, as well as in the management of complications related with this condition, are highlighted.

The intestinal morphology of the tawny eagle has not been previously described. From orad to aborad, we observed the following: 1) the duodenum, a large and wide simple loop followed by a relatively symmetric Meckel track presenting the Meckel diverticulum at its extreme; 2) the supraduodenal or ileac loop, which is closely attached to the duodenal loop by mesenterium and vascularly supplied by branches of the duodenal vessels; 3) a large supracecal kink formed by the aborad portion of small intestine; 4) a pair of vestigial ceca; and 5) a short and straight rectum (colon) closely attached to the dorsal coelomic wall, all of which are supplied by the caudal mesenteric blood vessels. Comparative studies in other members of the genera Aquila and Buteo reported intestinal morphologic peculiarities shared by both genera that may differentiate the family Accipitriformes from closely related families such as Falconiformes. The minimal attachments of the supracecal kink to the rest of intracoelomic structures may be a predisposing factor for its intussusception in buzzards and eagles. (3,4)

In birds, intestinal intussusception has been previously reported in poultry, 4 macaws (Ara species), 2 red-tailed hawks (Buteo jamaicensis), and 1 red-shouldered hawk (Buteo lineatus). (5-12) Multiple intussusceptions have been only reported in poultry. (6) Also, in the nonpoultry avian cases reported, intussusception involved the ileo-cecorectal area, with a single exception also involving the aborad jejunum. (6,12)

In small mammals, intussusception may be caused by enteritis, prokinetic drugs, or exercise, or it may be an agonal event. Parasitic infection is a common cause of intussusception in young dogs and cats but this association has never been reported in birds other than poultry. Differential diagnoses for intussusception in nonavian species are intestinal foreign bodies, volvulus or torsions, incarcerations, adhesions, strictures, abscesses, granulomas, hematomas, neoplasia, congenital malformations, and ileus. (13)

Clinical signs in birds may include hemorrhagic diarrhea, vomiting, coelomic pain, a coelomic palpable mass, a portion of rectum protruding from the cloaca, inability to pass feces, hyporexia, anorexia, lethargy, depression, and emaciation. (11)

Results of a CBC and serum biochemical analysis are nonspecific but may reveal dehydration, stress leukograms, anemia, and electrolyte and acid-base abnormalities. (13) The use of radiology in locating an intestinal intussusception in birds has only been reported in a red-tailed hawk (radiographed after contrast enema) and in a blue-and-gold macaw (Ara ararauna; plain radiographs and radiographs after oral contrast administration). (9-12) In birds with complete and sometimes with partial obstruction, survey radiographs may reveal a pattern of mechanical obstructive ileus characterized by the presence of severely dilated intestines filled with intraluminal gas or fluid orad to a tubular soft-tissue mass. Fluoroscopy has been reported as a useful diagnostic test for intussusception in a red-tailed hawk. (9) Ultrasonography is a useful diagnostic tool in small mammals, although the presence of air sacs may complicate the utility of this technique in birds, depending on the location of the intussusception. (14) This report is the first case in birds describing the use of coelomic endoscopy instead of exploratory coeliotomy (a more invasive technique) to diagnose the ileo-cecorectal intussusception. Rectoscopy may aid in the diagnosis of an aborad intussusception by revealing an invaginated intestine protruding into the rectum, although this technique has never been reported in birds. (13)

Both spontaneous and manual reduction of intestinal intussusception by external manipulation have been reported in small mammals. Intraoperative manual reduction was unsuccessful in a blue-and-gold macaw. (12) Intestinal surgical resection and anastomosis, with or without ancillary procedures to prevent recurrence, showed a successful outcome in 4 of 5 avian case reports (2 blue and gold macaws [1 died], 1 red-shouldered hawk, and 2 red-tailed hawks). (9,11,12)

In small mammals, possible complications of surgical treatment of intussusception are dehiscence, intestinal perforations or strictures, adhesion formation, recurrence of intussusception, peritonitis, leakage, and death. (15) Risk of dehiscence is increased in hypoalbuminemic patients with preexisting peritonitis or gastrointestinal foreign bodies. (15) Complications reported in birds are limited to 1 case of excessive intraoperative hemorrhage and 1 case of postoperative mural abscess formation at the anastomosis site, blocking the intestinal lumen (diagnosed by contrast radiography and exploratory coeliotomy) and requiring intestinal resection and temporary jejunostomy, followed by reanastomosis. (12) In this eagle, coelomic endoscopy revealed adhesions at the anastomosis site, causing a partial obstruction and requiring surgical removal of the adhesions. Jejunostomy has been reported as a temporary alternative to intestinal anastomosis in an adult blue-and-gold macaw in which the serosal defects could not be closed by primary intention after removing a fibrinous plug. (12) In this eagle, a stricture at the anastomosis site not associated with clinical signs was confirmed by rectoscopy during the second surgical recheck.

In conclusion, intussusception is a rarely reported condition in birds of prey. The 3 previous cases reported involved specimens belonging to the genus Buteo, whereas the present case involves a tawny eagle (genus Aquila). Similar to previous reports in nonpoultry avian species, the primary cause of intussusception remains unknown. Eagles and buzzards share the anatomic characteristic of a minimal attachment of the supracecal kink, which may be a predisposing factor to its intussusception, although further studies are warranted. In suspected cases of intussusception, coelomic endoscopy is preferable to exploratory coeliotomy as a diagnostic tool as it is less invasive. Intestinal ileo-cecorectal resection and ileo-rectal anastomosis was well tolerated and should be considered as an effective treatment for this syndrome in eagles. Rectoscopy and coelomic endoscopy may aid in identifying postoperative complications.

References

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(3.) Mitchell PC. On the intestinal tract of birds. Proc Zoo! Soc Lond. 1986;136-159.

(4.) Beddard FE. On the alimentary tract of certain birds and on the mesentery relations of the intestinal loops. Proc Zool Soc Lond. 1911;47-93.

(5.) Sharma UK. Intussusception in poultry. Indian Vet J. 1971;48(4):337-341.

(6.) Williams RB. On the aetiology of intestinal intussusception in the fowl. Avian Pathol. 1986; 15(2):301-304.

(7.) Okoye JO. Cases of intestinal intussusception in young fowls. Avian Pathol. 1985;14(2):275-279.

(8.) Takeshi K. A case of intussusception of a chicken small intestine. J Japan Vet Med Assoc. 2002;55(5):285-287.

(9.) Greenwood AG, Storm J. Intestinal intussusception in two red-tailed hawks (Buteo jamaicensis). Vet Rec. 1994; 134(22): 578-579.

(10.) Forbes NA. Avian gastrointestinal surgery. Semin Avian Exotic Pet Med. 2002; 11(4): 196-207.

(11.) Scott DE. Surgical correction of a colonic prolapse/ intussusception in a red-shouldered hawk (Buteo lineatus). Proc Annu Conf Assoc Avian Vet. 2012:45-49.

(12.) VanDerHeyden N. Jejunostomy and jejuno-cloacal anastomosis in macaws. Proc Annu Conf Assoc Avian Vet. 1993:35-37.

(13.) Fossum TW. Surgery of the digestive system. In: Fossum TW, ed. Small Animal Surgery. 3rd ed. St. Louis, MO: Mosby Elsevier. 2007:399-530.

(14.) Riedesel EA. The small bowel. In: Thrall DE, ed. Textbook of Veterinary Diagnostic Radiology. 6th ed. St. Louis, MO: Elsevier Saunders; 2013:801.

(15.) Tobias KM. Intestinal resection and anastomosis. In: Tobias KM, ed. Manual of Small Animal Soft Tissue Surgery. Ames, IA: Wiley-Blackwell; 2010:175-182.

Mikel Sabater, LV, MRCVS, CertZooMed, Minh Huynh, DVM, MRCVS, and Neil Forbes, BVetMed, Dipl ECZM (Avian), FRCVS

From Great Western Exotics, Unit 10, Berkshire House, County Business Park, Shrivenham Road, SN1 2NR, Swindon, UK (Sabater, Forbes); Exoticsvet, Marques de San Juan, 23, 46015, Valencia, Spain (Sabater); and Centre Hospitalier Veterinaire Fregis, 43 Avenue Aristide Briand, 94110 Arcueil, France (Huynh).
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Author:Sabater, Mikel; Huynh, Minh; Forbes, Neil
Publication:Journal of Avian Medicine and Surgery
Article Type:Clinical report
Date:Mar 1, 2015
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