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Endoscopic Removal of Gastrointestinal Foreign Bodies in Two African Grey Parrots (Psittacus erithacus) and a Hyacinth Macaw (Anodorhynchus hyacinthinus).

Abstract: Two African grey parrots (Psittacus erithacus) and one hyacinth macaw (Anodorhynchus hyacinthinus) were examined because of varying clinical signs ranging from general lethargy to seizure-like episodes and regurgitation. Radiography and fluoroscopy in the 3 birds demonstrated variable degrees of gastric abnormalities, suggesting the presence of foreign material or stricture-like defects. Upper gastrointestinal rigid endoscopy by ingluviotomy revealed foreign bodies that were removed endoscopically. Minor postoperative complications were pulmonary congestion or mild aspiration and cardiac arrhythmia, both of which resolved, and no serious deleterious effects were associated with endoscopy in the short or long term. Endoscopy is recommended for examination and removal of foreign bodies from the upper gastrointestinal tract because it is less invasive and traumatic than traditional surgical approaches.

Key words: endoscopy, foreign body, ingluviotomy, proventriculus, African grey parrot, Psittacus erithacus, hyacinth macaw, Anodorhynchus hyacinthinus

Clinical Reports

Case 1

A 3-year-old female African grey parrot (Psittacus erithacus) weighing 361 g was presented to the University of Georgia Zoological Medicine Service with a history of seizure-like episodes. The bird was adopted by the owner 10 months before presentation and, during the preceding month, had experienced four seizure-like episodes, during which the bird was nonresponsive to any stimuli. Physical examination was unremarkable except for evidence of feather picking on the ventral aspect of both wings and on the dorsum. Results of routine hematologic testing and plasma biochemical analysis were unremarkable except for mild hypokalemia (2.4 mEq/L; reference interval, 2.6-4.2 mEq/ L), (1) mild hypophosphatemia (2.7 mg/dL; reference interval, 3.2-5.4 mg/dL), (1) minor increase in bile acid level (73 [micro]mol/L; reference interval, 18-71 [micro]mol/L), (1) and minor decrease in uric acid concentration (3.4 mg/dL; reference interval, 4-10 mg/ dL). (1) Results of serologic and polymerase chain reaction testing for Chlamydia psittaci were negative. Orthogonal, whole body radiographs revealed a tubular structure of soft tissue to mineral opacity in the area of the ventriculus (Fig 1). Given the radiographic changes, ingluviotomy and endoscopic evaluation was performed the next morning after fasting the bird overnight for 12 hours. The bird was premedicated with butorphanol tartrate (1 mg/ kg IM) and meloxicam (0.5 mg/kg 1M). After induction with 5% isoflurane in 100% oxygen, the parrot was intubated with a 3.5-mm uncuffed endotracheal tube and maintained with isoflurane and a nonrebreathing circuit, adjusted to patient requirements. Fluid therapy with lactated Ringers solution (10 mL/kg/h by intraosseous catheter) was continued throughout anesthesia. Intraoperative monitoring consisted of pulse oximetry, respiratory and heart rates, capnography, and body temperature. Thermal support also was provided throughout the procedure. The bird was placed in a reverse Trendelenburg position with the head and neck elevated by 30[degrees]. The ingluvial region was plucked and prepared surgically. A crop tube was placed into the oral cavity and advanced into the crop to identify the position for ingluviotomy. A 4-mm incision was made into the anterior crop, above the coelomic inlet. The crop was isolated using stay sutures (3-0 PDS; Ethicon, Inc, Somerville, NJ, USA; Fig 2A). A 2.7-mm, 18-cm, 30[degrees] rigid telescope, housed within a 4.8-mm operating sheath (Karl Storz Veterinary Endoscopy America, Inc, Goleta, CA, USA), was introduced into the ingluviotomy opening. A 1-L bag of warm (105[degrees]F, 40.5[degrees]C) sterile saline was connected using an intravenous delivery line to one of the sheath ports, and a second intravenous line connected to the second sheath port emptied to a bucket under the table (Fig 3). Repeated, gravity-fed, sterile saline irrigation and aspiration were used to clear debris from within the gastrointestinal tract and facilitate examination of the crop, intracoelomic esophagus, proventriculus, and ventriculus. A 21 X 5-mm rubber tube, presumably of feeding tube origin, was identified within the ventriculus (Figs 2B and 2C). Endoscopic retrieval forceps were used to grasp and remove the object from within the ventriculus. Inspection of the proventriculus and ventriculus revealed evidence of inflammation and mild ulceration. The crop and skin were closed in separate layers using 4-0 poliglecaprone 25 suture (Monocryl, Ethicon) in a simple continuous pattern. Towards the end of the procedure, a progressive arrhythmia developed, which resolved on recovery. Except for mild feather picking at the surgery site, recovery was unremarkable and no further clinical signs were reported. The patient was discharged the next day on meloxicam (0.5 mg/kg PO ql2h) and cephalexin (100 mg/kg PO ql2h) for 7 days. Given the resolution of the seizure-like episodes after foreign body removal, we considered it likely that the owner was confusing vomiting and regurgitation behavior as neurologic disease. Based on diet (50% pelleted feed and 50% fresh vegetables) and normal plasma calcium levels (8.6 mg/dL; reference interval, 7.6-12.0 mg/dL), (1) hypocalcemia was considered unlikely; however, there was no ionized calcium reading to definitively rule this out. No further abnormalities were reported after foreign body removal.

Case 2

A 2.5-year-old male hyacinth macaw (Anodorhynchus hyacinthinus) weighing 1.26 kg was presented with a lifetime history of regurgitation and foul-smelling liquid in the oral cavity. The bird was purchased from a United States breeder at 3 months of age. The referring veterinarian previously had performed crop cytologic examination, plain and contrast radiography, and crop biopsy. Crop biopsy showed no evidence of proventricular dilatation. A gastrointestinal contrast study indicated a possible abnormality in the distal esophagus or proximal proventriculus. Several treatments with antifungals, antibiotics, and motility modifiers were tried with no improvement. The bird was referred to the University of Georgia Zoological Medicine Service, physical examination was unremarkable. Initial hematologic testing, plasma biochemical analysis, and measurement of plasma zinc and whole blood lead levels were unremarkable. C psittaci titer was negative. Cytologic examination of a crop swab sample demonstrated a predominance of gram-negative bacterial rods. Contrast gastrointestinal radiography was performed using iohexol (20 mL/kg, Omnipaque 240 mg/mL; GE Healthcare Inc, Princeton, NJ, USA) diluted with 10 mL water and administered into the crop. Fluoroscopic images and videos were acquired immediately after administration and intermittently over the next 45 minutes. Additional radiographs were taken at 60 and 90 minutes after contrast administration. Radiographic results revealed a filling defect and narrowing of the proventriculus, consistent with a stricture, wall thickening, or other defect within the proventriculus (Figs 4A and 4B). Gastrointestinal motility appeared unremarkable. Given the radiographic changes, ingluviotomy and endoscopic evaluation was performed. Patient premedication, anesthesia, monitoring, positioning, surgical preparation, ingluviotomy, and endoscopy were performed as described previously for the African grey parrot. No obvious abnormalities associated with the crop and esophagus were observed; however, in the region of the distal proventriculus, a large fibrous foreign body was identified (Fig 5A). A wire basket retrieval device (Karl Storz Veterinary Endoscopy America, Inc) was inserted down the instrument channel and used to envelope and remove the foreign body via the ingluviotomy incision (Figs 5B and 5C). Mucosal inflammation with ulceration was visible within the proventriculus, and a generalized loss of koilin was observed within the ventriculus (Figs 5D and 5E). The foreign body was composed of fibers, string, and food items (Fig 6). The crop and skin were closed routinely as described previously. Recovery was uneventful and the bird was discharged the next day on meloxicam (0.5 mg/kg PO ql2h) for 3 to 5 days and cephalexin (100 mg/kg PO ql2h) for 7 days. One month later, the macaw was represented for examination with a complaint of weight loss and regurgitation. On presentation, the bird was bright and in good body condition. The weight was 1.22 kg. No abnormalities were detected on repeat hematologic testing, plasma biochemical analysis, radiography, or crop cytologic examination. The bird was anesthetized using the same anesthetic protocol, and the upper gastrointestinal tract was examined by flexible endoscopy using an 8.6 mm gastroscope (Olympus America Corp, Center Valley, PA, USA). Results were unremarkable. The previously identified ulceration and inflammation within the proventriculus and ventriculus had resolved and koilin was now widespread throughout the ventriculus (Fig 5F). The bird was hospitalized for 1 week for observation, and no regurgitation, vomiting, or other gastrointestinal signs were observed. Serial Gram's stain and cytologic evaluations of the crop swab samples indicated normal crop flora of predominantly gram-positive cocci and rods, with few nonbudding yeasts. The bird maintained weight between 1.22 and 1.26 kg while hospitalized. The bird was discharged and all medications were discontinued. The bird remained clinically healthy for the next 3 months when lost to further follow-up.

Case 3

A 20-year-old female African grey parrot weighing 425 g was presented with a 1-month history of inappetence and weight loss. The bird was adopted 2 months before presentation and was housed with another African grey parrot and a macaw (Ara sp.). The owner reported that the feces appeared to be loose, mucoid-green with an increased urate component and contained undigested seeds. On initial presentation to the referring veterinarian, assisted crop feeding was performed, after which blood was noted on the end of the feeding tube. The bird was promptly referred to the University of Georgia Zoological Medicine Service, where physical examination abnormalities included a prominent keel with an emaciated body condition (1/5) and blunted choanal papillae. Initial plasma biochemical analysis indicated a mild increase in creatine kinase concentration (926 U/L; reference interval, 123-875 U/L), (1) attributed to the patient's muscle wasting. The only hematologic abnormality was lymphopenia (416 cells/[micro]L; reference interval, 2 080-5 200 cells/[micro]L), (1) likely part of a stress response. Results of PCR evaluations for avian bornavirus on blood and fecal samples were negative. Orthogonal, whole body radiographs revealed a moderately enlarged proventriculus with an ill-defined luminal ventral margin. The proventriculus:keel ratio was increased at 0.8 (Fig 7A); ratio values < 0.48 indicated normal proventricular diameter. (2) Positive-contrast gastroenterography was performed with a 50:50 mixture of 5 mL iohexol and 5 mL Omnivore Care (Emeraid Omnivore Care; Emeraid LLC, Cornell, IL, USA), which was administered into the crop. Fluoroscopic and radiographic images and videos were acquired as described previously and revealed proventricular dilatation with a moderate amount of mobile, rounded filling defects within the proventriculus and ventriculus (Fig 7B). These structures initially were dependent in the proventriculus and then began to float as proventricular contractions increased. The material occasionally moved from the proventriculus into the ventriculus. Given the radiographic changes, ingluviotomy for endoscopic evaluation and crop biopsy for possible proventricular dilatation were pursued. Patient premedication, anesthesia, monitoring, positioning, surgical preparation, ingluviotomy, and endoscopy were performed as described previously. However, before endoscopy, a crop biopsy was harvested, taking care to sample an area containing blood vessels and nerves. Approximately 15 to 20 pieces of foreign material, identified as closed-cell extruded polystyrene foam, were removed from the proventriculus and ventriculus using 1.7 mm retrieval forceps (Fig 8). To remove larger items that could not be removed via the instrument channel of the sheath, it was necessary to withdraw the endoscope-sheath-forceps unit while grasping the foreign material. Inflammation and ulceration of parts of the proventriculus were evident. After removal of all visible foreign material, the gastrointestinal tract (crop, proventriculus, ventriculus) was flushed with warm sterile saline solution. The crop and skin were closed routinely as described previously. The patient recovered uneventfully. Postoperative therapy comprised supplemental nutrition with Omnivore Care (15 mL/kg PO ql2h) for 2 days, famotidine (1 mg/kg IM ql2h) for 5 days, sucralfate (25 mg/kg PO q8h, Carafate, Bridgewater, NJ, USA) for 3 days, metoclopramide (0.5 mg/kg PO q8h) for 3 days, and tramadol (30 mg/kg PO ql2h) for 4 days. However, the day after surgery, dyspnea developed with congestion of the lower respiratory tract inferred during auscultation. Given concerns regarding possible aspiration pneumonia, pulmonary edema, and air sacculitis, the bird was treated with furosemide (2 mg/kg IM as needed) for 4 days, N-acetyl-L-cysteine (20 mg/ mL, 60 mg nebulized in 3 mL water q8h) for 3 days, amoxicillin trihydrate/clavulanate potassium (125 mg/kg PO ql2h, Clavamox drops; Zoetis, Inc, Kalamazoo, MI, USA) for 7 days, and itraconazole (5 mg/kg PO ql2h, Sporanox; Janssen Pharmaceuticals, Titusville, NJ, USA) for 7 days. Supplemental oxygen was continued and cardiopulmonary parameters were monitored continually. Clinical signs improved within 48 hours and the bird continued to recover completely. Results of the crop biopsy demonstrated minimal lymphoplasmacytic ingluvitis. No inflammation was identified in any nerve or ganglia in four-step sections, thereby failing to indicate the presence of proventricular dilatation disease. The patient was discharged 1 week after initial admission with continued amoxicillin trihydrate/clavulanate potassium and itraconazole at previously described dosages for an additional 5 days. The weight at the time of discharge was 407 g. The patient was clinically healthy during reexamination a week later and was referred back to the original veterinarian for future care. No further complications were reported.

Discussion and Conclusion

In the cases described, gastrointestinal foreign bodies were identified and removed by rigid endoscopy in 3 psittacine birds. When performed by a clinician who is familiar with the use of appropriate endoscopic equipment and techniques, endoscopic foreign body removal proved to be an effective, safe, and minimally invasive procedure, considered superior to traditional proventriculotomy/ventriculotomy. The rigid endoscope inserted via an ingluviotomy provided an important visual aid in identifying and removing all foreign material from the proventriculus/ventriculus.

Gastrointestinal obstruction and associated conditions are described frequently in birds. Common conditions seen are toxicosis, foreign body ingestion, papillomatosis, neoplasia, and infection due to bacterial, fungal, viral, or parasitic causes. (3) Foreign objects generally are encountered in ratites, gallinaceous birds, waterfowl, and psittacine birds. (4) However, any species can present with foreign bodies regardless of sex or age. (5) Items ingested can include hair, cloth fibers, parts of toys, and heavy metals. Foreign body ingestion can lead to partial or complete gastrointestinal obstruction and often represents an emergent condition. Consumption of foreign material by psittacine birds may be the result of their curious, foraging nature, or in the case of neonatal birds, their compulsive pumping for food. (6) Some reports indicate that environmental stressors, such as dramatic alterations of housing, also may encourage foreign body ingestion. (7) Gastrointestinal foreign bodies often pose a challenge to practitioners, as the condition often is seen in association with enteritis, and deciding the primary cause can be difficult. (8) Foreign bodies in the gastrointestinal tract are diagnosed based on the history, clinical signs, and results of laboratory tests and imaging modalities. (9) Clinically, gastrointestinal foreign bodies may cause lethargy, anorexia, weight loss, vomiting and/or regurgitation, crop stasis, and hemorrhagic enteritis. In cases of perforation, affected birds may exhibit signs of shock or severe depression. (5) Although most foreign objects are found frequently in the proventriculus and ventriculus, they can be found anywhere along the length of the gastrointestinal tract. (8) Radiography is useful for visualizing foreign material, particularly radiopaque objects, such as metal. Foreign bodies often are associated with functional ileus and gaseous dilatation proximal to the obstruction. (5)

Management of foreign bodies should be based on the clinical signs of the individual bird, species affected, nature and location of the foreign body, available tools, and preference and experience of the veterinarian. (10) Proventriculotomy may be used to access the proventriculus and muscular ventriculus; however, to avoid the risks of invasive surgery, a flexible or rigid endoscope with appropriate retrieval forceps or device may be used to remove ingested objects. (11)

Proventriculotomy or ventriculotomy has been reported as an effective means for removing gastric foreign bodies in several avian species, including an ostrich (Struthio camelus), (12) a brown kiwi (Apteryx australis mantelli), (13) and a sarus crane (Grus antigone). (14) These standard surgical approaches are indicated most commonly for removal of foreign bodies that are not removed easily with endoscopy or proventricular lavage. (15) Ventriculotomy is considered more susceptible to postoperative complications, particularly leakage. Additionally, birds lack an omentum to help seal enterotomy incisions. (16) The most substantial limitation to successful soft tissue surgery involving the coelomic cavity is the relative small size of most avian patients and the limited surgical access afforded by standard coeliotomy techniques. (16) Both limitations often can be overcome by endoscopy, which provides focal magnification, illumination, and non- to minimally-invasive access to the gastrointestinal tract and coelom. (17)

The advantage of endoscopic removal is that no surgical approach to the coelom, air sacs, or proventriculus are required, making it a less invasive option compared to surgery. From a clinical perspective, in addition to an oral approach in smaller birds (<400-500 g), the crop permits the minimally-invasive insertion of rigid endoscopes via an ingluviotomy into the proventriculus and ventriculus of larger parrots (>400-500 g) where the traditional 2.7 X 18-cm telescope is of insufficient length.Is The benefits of upper gastrointestinal endoscopy and foreign body removal over traditional coeliotomy techniques are not dissimilar from those reported in companion mammals. (19,20) Reduced visibility has been suggested with endoscopic techniques; however, the use of a 30[degrees] telescope (that can be rotated around its longitudinal access) and saline infusion largely overcomes these obstacles, while flexible gastroscopes can be used in large birds (>l-2 kg). (21)

In previous reports of psittacine birds with gastrointestinal foreign bodies, blood test results were nonspecific and included leukocytosis characterized by a heterophilia and abnormal plasma protein concentrations. (22) The birds in this report did not display any major hematologic changes suggestive of acute or chronic inflammation. The major complications encountered were associated with anesthesia and the chronic presentation. The importance of medical stabilization and a thorough preoperative evaluation cannot be overemphasized. (23)

The most significant postoperative complication encountered was pulmonary congestion, which may have been associated with overhydration or minor aspiration in Case 3, but this resolved with appropriate medical treatment. Therefore, packing the oropharynx with moistened gauze is recommended when using lavage with rigid endoscopy to prevent saline from welling up into the oral cavity. An arrhythmia of unknown origin occurred in the first case that resolved during anesthetic recovery.

Cephalexin was prescribed in the first case after surgery at a dosage of 100 mg/kg PO ql2h; however, according to the pharmacokinetic data available for cephalexin in birds, 35 to 50 mg/kg 4 times a day would be expected to establish and maintain therapeutic plasma concentrations in large birds (pigeons, cranes, and emus). (24) Additionally, meloxicam was used for analgesia (0.5 mg/kg IM ql2h). Pharmacokinetic information for meloxicam, which was published after these cases were seen, indicates that a dosage of 1 mg/kg IM q 12h provides an optimal therapeutic regime in African grey parrots. (25)

Ultimately, as in companion animal medicine, gastrointestinal endoscopy is recommended in clinical situations to facilitate examination and removal of foreign bodies from the avian upper gastrointestinal tract in a manner that is less traumatic and less invasive compared to standard coeliotomy approaches. Recently, gastroscopy and biopsy has been evaluated in the pigeon (Columba livia). (26)


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Robert J. Cotton III, DMV, and Stephen J. Divers, BVetMed, DZooMed, Dipl ECZM (Zoo Health Management, Herpetology), Dipl ACZM, FRCVS

From the Department of Small Animal Medicine and Surgery (Zoological Medicine). College of Veterinary Medicine, University of Georgia, 2200 College Station Road, Athens. GA 30602, USA.

Caption: Figure 1. Right lateral survey radiograph of a foreign body (arrows) within the ventriculus of an African grey parrot.

Caption: Figure 2. (A) Surgical view of the coelomic inlet of an African grey parrot demonstrating 2-mm stay sutures elevating the crop (arrows), and the insertion of the 4.8-mm operating sheath (1) into the crop through an ingluviotomy. (B) Endoscopic view of the rubber tube foreign body (2) being grasped with 1.7-mm retrieval forceps (3). (C) View of the 21 X 5 mm removed rubber tube.

Caption: Figure 3. Diagrammatic illustration of the saline infusion and irrigation system used for avian upper gastrointestinal endoscopy (Courtesy of Kip Carter, Educational Resources, University of Georgia).

Caption: Figure 4. Right lateral radiograph (A) and right standing lateral fluoroscopic view of a hyacinth macaw after the administration of iohexol. Note the filling defect (1) visible in both images.

Caption: Figure 5. (A) Endoscopic view of the fibrous foreign body (1) within the ventriculus of the hyacinth macaw described in Figure 4. (B) Deploying the wire basket retrieval device--note the three metal prongs of the device (arrows). (C) Fibrous foreign body (1) secured with wire basket retrieval device (2) and being withdrawn from the proventriculus. (D) View of the proventriculus immediately after removal of the foreign body demonstrates inflammation and superficial ulceration of the proventricular mucosa (arrows). (E) View of the ventriculus immediately after removal of the foreign body demonstrating lack of koilin. (F) Flexible endoscopic view of the ventriculus 1 month later, demonstrates a return of the normal koilin layer.

Caption: Figure 6. View of the 32 X 11 mm proventricular foreign body removed from the hyacinth macaw described in Figure 5 (mm scale).

Caption: Figure 7. (A) Right lateral plain radiograph of the central coelom of an African grey parrot demonstrates proventricular dilatation (proventricular measurement = 18.3 mm, keel = 22.8 mm, and proventriculankeel ratio of 0.8). (B) Right standing fluoroscopic images after administration of iohexol, which demonstrate proventricular dilatation and multiple filling defects (asterisks).

Caption: Figure 8. Foam foreign bodies removed from the proventriculus of the African grey parrot described in Figure 7 (cm scale).
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Title Annotation:Retrospective Study
Author:Cotton, Robert J., III; Divers, Stephen J.
Publication:Journal of Avian Medicine and Surgery
Date:Dec 1, 2017
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