Management and case outcome of gastric impaction in four raptors: a case series.
Key words: raptor, gastrointestinal foreign body, gastric impaction, avian
A 3-year-old male American kestrel (Falco sparverius) was referred to College of Veterinary Medicine, North Carolina State University, from the North Carolina Aquarium at Pine Knoll Shores (Pine Knoll Shores, NC, USA) after a 10day history of decreased appetite, described as eating only organ and muscle meat, weight loss, distended coelom, and decreased casting. This nonreleasable bird was acquired from a rehabilitation facility 2 years earlier with a history of unilateral ocular trauma and was being used in a public free-flight education program. The kestrel was housed in an indoor mews with synthetic vinyl flooring substrate. Multiple perches were available with a variety of coverings that included sisal rope, artificial turf, and rubber. Transport between mews and a free-flight area was in a pet carrier lined with a synthetic tightly woven fiber mat used routinely for outdoor household carpeting.
On presentation, physical examination revealed severe abdominal distention associated with a large, firm coelomic mass. The bird weighed 84 g with a body condition score of 1.5/5 (1) and was eupneic. The rest of the physical examination was unremarkable. Results of initial diagnostic tests, including a complete blood count (CBC) and plasma biochemical profile, were unremarkable. Survey radiographs acquired 8 days earlier at the primary institution documented a heterogeneous soft tissue opacity consistent with a foreign body in a distended ventriculus (Fig 1). Results of coelomic ultrasound, completed on the day of presentation, revealed a large amount of foreign material within a dilated, thin-walled ventriculus. A standing fluoroscopic upper gastrointestinal study was completed on the same day, after oral administration of barium sulfate (25 mL/kg; 2.25 mL diluted to 35% wt/vol). (2,3) A large filling defect was seen within the ventriculus; however, contrast media was observed distal to the ventriculus in the intestinal loops (Fig 2). Immediate intervention was suggested, but at the request of the governing institution, supportive care consisting of lactated Ringer's solution (LRS; 50 mL/kg SC ql2h) and gavage feeding (2.8 mL [3% body weight]; Emeraid Carnivore; Lafeber, Cornell, IL, USA) (4) was administered for the next 7 days rather than performing an invasive procedure. On representation, the kestrel weighed 72 g; however, results of the remaining physical examination were otherwise unchanged. The kestrel was anesthetized by mask induction with 5% isoflurane and oxygen flow at 4 L/min for endoscopic evaluation and to potentially alleviate the partial obstruction. Once induced, the kestrel was intubated with a 2.0-mm uncuffed endotracheal tube and maintained with isoflurane at 2.5% to 3% and oxygen flow at 4 L/ min. Using a flexible endoscope (Olympus GIF XP 180N; Olympus America, Central Valley, PA, USA; Karl Storz Flex X2; Karl Storz Veterinary Endoscopy-America, Goleta, CA, USA), a fibrous mass within the ventriculus was visualized, but the material was too large and densely packed to be removed.
Supportive care, similar to the week before, consisting of subcutaneous fluids and gavage feeding, was continued for 2 days before the kestrel was considered stable for surgery. A standard approach ventriculotomy was performed via a 2 x 1 cm, L-shaped, left lateral coeliotomy, described in detail previously. (5-7) The anesthesia protocol for the ventriculotomy mirrored that of the anesthetic protocol for the fluoroscopy, with the addition of preoperative hydromorphone (0.5 mg/kg IM) (8) and a right ulnar intraosseous catheter. The ventriculus was severely distended and thin walled. An 8 g dense fibrous mat of blue and green artificial turf material was surgically removed. The ventriculus was closed with 5-0 PDS (Ethicon; Johnson & Johnson, Somerville, NJ, USA) in a continuous apposing pattern oversewn with 6-0 PDS in a Lembert pattern. The body wall and skin were each closed with 5-0 PDS. The surgery was completed without complication in just under 1 hour; however, during recovery the bird experienced cardiopulmonary arrest. Several minutes of cardiopulmonary resuscitation restored a spontaneous heart rate, but spontaneous ventilation never resumed. After 3 hours of ventilatory support, ventilation was ceased at the request of the governing facility and the bird died. At postmortem examination the suture line of the ventriculus was grossly intact. Abnormal histologic changes included generalized thinning of the ventricular muscularis and koilin layer, and diffuse vascular congestion with perivascular infiltration of heterophils and thrombocytes at the ventricular wall surgical site. No other abnormalities were noted and the underlying cause for the gastrointestinal impaction was not determined. Postmortem liver lead analysis was not completed.
A 4-year-old female peregrine falcon (Falco peregrinus) was presented to the NCSU CVM Exotic Animal Medicine Service after a 4-day history of anorexia, vomiting, regurgitation, and increased respiratory effort. The captive-raised falcon was owned by a falconer and alternately housed either outside in a mews with pea gravel substrate or indoors on a block perch or in a transport carrier. The indoor substrate usually was newspaper; however, the owner had recently substituted an absorbent paper with plastic backing that was marketed for urine absorption in dog crates. The falcon was fed the meat and internal organs of one commercially purchased thawed frozen quail daily, with the head, feathers, and bones removed. No previous medical history or history of reduced casting was reported.
On presentation, the falcon was thin (667 g) with a body condition score of 1.5/5, (1) was 5% to 7% dehydrated, and had a concave ventral coelomic wall on palpation. Respiratory effort was characterized as increased and tachypneic, exacerbated by handling. The falcon was administered LRS (60 mL/kg SC) and maintained in an oxygen-enriched environment for up to 1 hour before performing diagnostic tests. The bird was anesthetized with isoflurane via mask induction for venipuncture and radiographs. A heterogeneous soft-tissue opacity was observed within a severely dilated proventriculus and mildly dilated ventriculus (Fig 3). After completion of radiographs, the falcon experienced cardiopulmonary arrest, and resuscitation efforts were unsuccessful. Postmortem examination revealed aboral esophageal and proventricular impaction with 22 g of densely packed paper and thin plastic material. The extrapulmonary primary bronchi were compressed by the underlying distended proventriculus, and the cranial half of the lungs were congested bilaterally. Reduced fat stores and decreased body condition were corroborated, but there were no other abnormal findings. Histologic examination revealed a severe, segmental, transmural, and ulcerative heterophilic esophagitis with numerous intralesional bacterial cocci and moderate multifocal pulmonary hemorrhage. Phlebotomy was not completed before anesthesia because of tachypnea, dyspnea, and efforts to reduce stress; however, at anesthetic induction, a blood sample was obtained for routine hematologic and biochemical testing and blood lead levels. However, only blood lead levels were measured pursuant to the owner's directions, and results showed blood lead levels were below the detection limit of the assay (<5 [micro]g/dL).
A juvenile female golden eagle (Aquila chrysaetos), between 1 and 5 years of age, was presented to the Clinic for Birds, Reptiles, Amphibians & Ornamental Fish, University Ludwig-Maximilian of Munich, Germany, with a 2-day history of lethargy and inappetence. The eagle was kept by a falconer to hunt European brown hare. Housing was either a mews with pea gravel substrate or on an outside perch over grass. The eagle's diet was wild caught hare and rabbit that had been killed by means other than firearm, and fed every 2 to 3 days. There was no reported history of reduced casting and no previous medical history.
On presentation, the eagle was weak, lethargic, and slightly thin (body condition score 2-2.5/5), (1) and it had a firm, distended coelom. Initial diagnostic tests included a CBC and serum biochemical profile, measurement of blood lead level, and survey radiographs. Abnormal findings were increased blood lead level (110 [micro]g/dL; <20 [micro]g/dL is considered background levels in golden eagles), (9) and radiographic evidence of a severely dilated proventriculus and ventriculus containing material of soft tissue opacity (Fig 4). Medical therapy consisted of chelation with calcium ethylenediaminetetraacetic acid (Ca-EDTA; 100 mg/kg IV q12h for 1 day then SC q12h for 3 days; Ca-EDTA diluted in 50 mL 0.9% NaCl). Additional therapy included supplemental fluids (LRS, 20 mL/kg SC q12h) and vitamin-B complex (10 mg/kg SC q24h). Food was withheld before sedation the next day because of the gastric impaction. One day after presentation, the eagle was anesthetized with isoflurane in a protocol similar to that used for the kestrel, intubated, and positioned in sternal recumbency for gastric lavage. The bird was secured to a tilted surgery table at a 45[degrees] angle with the head towards the floor. A plastic orogastric tube was marked at one end, measured from the tip of the beak to the distended coelom. The tube was positioned such that the end passed into the eagle's esophagus extended at least to the proventricular lumen, and the free end exited the oral cavity and reached a warm water reservoir. Copious amounts of lukewarm water were flushed into the proventriculus and ventriculus by a bilge-style "stomach pump" similar to that used widely for equine and canine gastric lavage. The refluxed water from the gastric lavage was allowed to flow by gravity via the esophagus and out the mouth; however, gastric lavage to remove the impaction was unsuccessful. Therefore, the day after gastric lavage, a ventriculotomy, using a similar approach and procedure as described with the kestrel, was completed. A large packed mat of grass was removed from the ventriculus and proventriculus (weight was not recorded). Postoperative therapy consisted of continued lead chelation, B-vitamin complex supplementation, and supplemental fluids (LRS), identical to the previous regimen, and the addition of amoxicillin and clavulanic acid (125 mg/kg PO q12h), meloxicam (0.1 mg/kg IM ql2h), and gavage feeding (20 mL/kg PO ql2h, Eukanuba Veterinary Diet High Calorie; Mars, Inc, McLean, VA, USA). The eagle survived surgery, but died unexpectedly 4 days later despite continued supportive care. Necropsy was declined by the owner.
A 4-year-old male barn owl (Tyto alba) was presented at the North Carolina Aquarium at Pine Knoll Shores (Pine Knoll Shores, NC, USA) after a 1-day history of anorexia, lethargy, and decreased fecal output. Other related history included several recent casts containing small fragments of wood shavings and straw. The owl was purpose-bred for use as a captive education bird in a free-flight program at the same institution as the kestrel (case 1) and began to exhibit clinical signs 6 weeks after the kestrel surgery. It had no previous history of medical conditions. The owl had been moved recently from an indoor mews similar to that described for the kestrel into an outdoor mews with pea gravel substrate, and it was fed 25 g of thawed frozen mice once daily obtained from a commercial supplier. Management, including transport and perch options, was similar to that for the kestrel. Enrichment items were offered routinely, including shredable items, such as phone books. A first-time enrichment item described as newspaper wrapped around a food item had been offered recently.
Management and treatment was completed within the primary institution in which the owl was housed, with no referral to a secondary institution. On physical examination, the owl had a 3/5 body condition score, (1) weighed 385 g, and had a firm, 3 cm palpable mass in the mid coelom. Results of an initial CBC and biochemical profile were unremarkable. Radiographs revealed a soft tissue opacity in a distended ventriculus that displaced the proventriculus and liver cranially (Fig 5). Medical management included supplemental fluids (0.9% NaCl; 15 mL/kg SC q24h for 2 days), gavage feeding (Emeraid Carnivore; 30 mL/ kg PO q24h for 2 days), and mineral oil (0.5 mL) added to the gavage feeding formula. After 2 days of medical intervention, the owl casted 3 pellets consisting of 36 g of shredded newspaper. No further complications were noted and no further intervention was necessary.
This case series describes proventricular or ventricular gastric foreign body impactions and management in 4 captive raptors. All 4 raptors in this case series developed lumen-filling gastric impaction caused by a large amount of foreign fibrous material despite having a natural behavior of casting nondigestible material. Gastrointestinal foreign bodies have been reported in multiple avian taxonomic groups. Several cases of gastrointestinal foreign bodies were reported in psittacine birds, including a perforating wire in the ventriculus of an umbrella cockatoo (Cacatua alba), (10) a splintered wood foreign body in the proventriculus of an umbrella cockatoo, (11) and a fibrous and string intestinal foreign body in an umbrella cockatoo and an eclectus parrot (Eclectus roratus), respectively. (12,13) However, none of these psittacine bird cases involved lumen-filling impactions. Reports of gastric foreign bodies in nonpsittacine birds, also resulting in nonlumen-filling impactions, include common mynas (Acridotheres tristis) (14,15) and kori bustards (Ardeotis kori). (16) Lumen-filling impactions containing natural and artificial fiber in the ventriculus of three Micronesian kingfishers (Halcyon cinnamomina cinnamomina) (17) and a captive-bred, 8-year-old male gyrfalcon (Falco rusticolus) were reported, respectively. (18) Ventricular impactions with feathers and litter substrate resulting in death were reported in gentoo penguin chicks (Pygoscelis papua) (19) and broiler chicks, (20) respectively, while ventricular diverticula as a sequela of ventricular foreign bodies were reported in captive parakeet auklets (Aethia psittacula). (21)
Gastrointestinal foreign bodies and impactions across avian taxa are often a life-threatening condition that may have multifactorial etiologies, including medical and behavioral causes. One possible behavioral cause is pica, which is the consumption of nonnutritive substances. (22) With the exception of the eagle that ingested grass, synthetic material used for perches, substrate, or enrichment was the source of impaction in the other 3 birds. Pica leading to ventricular impactions of shredded plant material in Micronesian kingfishers, (17) plastic and woody plant material in farm-raised ostriches (Struthio camelus), (23,24) gravel and grass in captive Oriental white storks (Ciconia boyciana), (25) and proventricular impactions of grass and other food material in wild trumpeter (Cygnus buccinator) and tundra (Cygnus columbianus columbianus) swans has been reported. (26) Lead toxicosis has been associated with pica and secondary proventricular impactions in waterfowl. (26-28) Systemic absorption of lead when dissolved in an acidic environment, such as the proventriculus or ventriculus, can lead to functional ileus and secondary neuropathic gastric dilatation. (29,30) Grass impaction in the lead-poisoned eagle was similar to proventricular impaction described in lead-poisoned waterfowl and may represent a form of pica associated with lead toxicosis. (31) The source of lead in the eagle was presumed, but not confirmed, to be lead ammunition in wild caught prey. Another possible source of lead, but not documented in these cases, includes some types of artificial turf. Extra care must be taken to use substrate that is nontoxic in the event of ingestion. In these cases, radiographic evidence of ingested heavy metal was not apparent; however, discrete metallic opacities are not always observed on radiographs, or the metal fragments could have dissolved completely or were expelled in a casted pellet before examination. Only 1 of 4 birds in this report was confirmed to have concurrent lead toxicosis and gastric impaction. Two birds, the kestrel and owl, were not tested for lead due to the very low likelihood that they were exposed to lead in their environment or via commercially available food.
We hypothesize that a lack of environmental enrichment for birds managed in captivity may contribute to behavioral pica due to boredom. (32) Ingestion of substrate or environmental enrichment materials by the peregrine falcon, kestrel, and owl may have been a behavioral response to boredom, stress, or frustration. Although not confirmed, a behavioral problem could have contributed to the artificial turf impaction in the captive gyrfalcon (18) and ingestion and impaction of plant material provided for aesthetics and enrichment in the enclosure of 3 captive kingfishers. (17) Appropriate diet, housing, and environmental enrichment may decrease the likelihood of behavioral pica. While it may not be possible to remove everything that could possibly be ingested from the captive raptor environment, none of the ingested foreign materials in this case series was considered inappropriate for their intended purposes. If captive raptors are known to exhibit behavioral pica, their caretakers should increase behavioral monitoring, especially when new enrichment items are presented.
No pathognomonic clinical signs of gastric impaction have been established, although raptors with gastric impaction may exhibit a range of clinical signs from nonspecific indicators, such as alterations in appetite, anorexia, and lethargy, to marked signs including changes in casting behavior and leg paresis. (18) Appetite alterations, such as selective ingestion and complete anorexia, similarly seen in parakeet auklets (21) and Oriental white storks, (25) were exhibited by the owl and kestrel, and eagle and peregrine, respectively. Casting is a natural behavior that functions to eliminate nondigestible material, such as feathers, hair, and/or bones, from the ventriculus in raptors. (33) Although changes in casting behavior, as reported for the kestrel, may help diagnose possible gastric impaction in raptors, casting varies by species, diet, and husbandry. (34-37) This natural behavior is beneficial when foreign material is mixed with natural, but nondigestible material, as documented in bald eagles (Haliaeetus leucocephalus) that cast pellets containing lead shot. (38) Absence of casting behavior in raptors can be caused by absence of nondigestible material in the diet (e.g., as in the peregrine falcon), underlying gastrointestinal foreign body impaction (eg, as in the kestrel), alterations in gastrointestinal motility with or without underlying lead toxicosis, or various other causes, such as infectious or structural disease. Unfortunately, the casting history was not reported in the eagle, and no apparent changes in casting frequency was reported in the owl, possibly because of rapid diagnostic and medical intervention. Left leg paresis, presumably due to compression of the kidney and ischiatic nerve roots secondary to the distended ventriculus, reported in the gyrfalcon was not observed in any of the raptors in this report. (18)
Physical examination revealed no consistent abnormal findings among all 4 birds. Three of the 4 birds had a decreased body condition score (<2.5/5), although 2 of those birds that were being flown for falconry could be expected to have a lower body condition score, while the third bird's decreased body condition score may have been associated with decreased dietary intake. All but one bird in this report had a distended coelom, which corresponded to a dilated ventriculus identified radiographically, similar to the gyrfalcon case. (18) However, on palpation, the distended coelom could be mistaken for a neoplastic mass or reproductive tract enlargement. (39,40) The lack of coelomic distension in the peregrine falcon was likely because of the location of the impaction in the proventriculus and lower esophagus.
Noninvasive diagnostic tests at the time of decreased casting or changes in dietary preference should include radiographs (with or without contrast) and could include ultrasound examination and positive contrast fluoroscopy. Obtaining a full history and completing a physical examination always should precede diagnostic tests. Additionally, a complete blood count, serum biochemical analysis, and measurement of blood lead levels may be helpful to detect underlying disease, such as lead toxicosis, hemodynamic shock, or electrolyte imbalances. Provided the patient is stable, radiographs should be acquired as soon as alterations in dietary or casting patterns occur and were very useful in confirming proventricular or ventricular dilation in all 4 birds in this report, as described in a similarly affected gyrfalcon. (18) Ultrasound and positive contrast fluoroscopy can help further characterize gastrointestinal abnormalities and differentiate between gastric impactions with partial or complete obstruction. The kestrel is the only bird in this series in which positive contrast fluoroscopy documented lack of a complete obstruction.
Reported avian gastrointestinal foreign bodies have resulted in multiple intervention techniques; however, treatment plans should be tailored individually to each case and may depend on the cause of impaction and underlying disease (i.e., lead toxicosis). Medical management, including gastric lavage, was performed in wild swans (Cygnus species), (27) staged endoscopic intervention in a gyrfalcon, (18) and surgical intervention was performed in several other bird species. (10-17,21,23,24) Medical management alone was sufficient for the owl, but this approach was not attempted in the other 3 birds. Oral lubricants, such as mineral oil and peanut butter, may be successful if used early in the disease process when casting stops or when foreign material is known to have been ingested. (17) Providing casting material, such as a quail with feathers, to the gyrfalcon, was successful in removing a residual small volume of foreign material (i.e., artificial turf). (18) Gastric lavage is another noninvasive option to alleviate a proventricular impaction. While gastric lavage was unsuccessful in the eagle with the grass impaction, that technique was used successfully to remove loosely packed lead shot, grit, and fibrous material from the proventriculus and ventriculus of impacted and/or lead poisoned waterfowl and vultures (Gyps fulvus). (27,41) However, the impacted material in these raptor cases may have been too densely compacted secondary to ventricular contractions and, therefore, less likely to be broken down and flushed out with the lavage technique.
Removal of an artificial fiber impaction by gastric endoscopy was successful in a gyrfalcon during a series of endoscopic procedures over 9 weeks. (18) Endoscopic removal was unsuccessful in a Micronesian Kingfisher (17) and the kestrel in this report because of poor visualization and the size and density of the impacted material, respectively. For the same reasons, endoscopy was not likely to have been successful in the peregrine falcon or eagle, both of which had a large amount of densely compacted foreign material in their proventriculus or ventriculus. Ultimately, raptor cases with a very large, densely compacted gastric foreign body may require surgical intervention. In this case series, ventriculotomy was used to relieve the gastric impactions in the kestrel and eagle, but both patients died after surgery. The cause of death of these birds is unclear. The deaths of the peregrine falcon, kestrel, and eagle may have been secondary to an underlying debilitated physiologic state, although sequela secondary to lead toxicosis (i.e., lead encephalopathy) may have contributed to the eagle's death. Surgical intervention should be considered once the patient's physiologic stability is maximized and if the foreign material impaction is too large or too dense to be removed by medical or endoscopic techniques.
Considerations for appropriate management to improve survival of raptors with gastric impaction should include early diagnosis and intervention. Of the 4 birds in this series, only the owl that was managed medically recovered from the gastrointestinal impaction. That bird was very likely diagnosed and treated earlier in the disease process, since the education facility had recent experience with the impacted kestrel. Astute observation by personnel who manage captive birds of prey can help reduce the potential of foreign material ingestion by removing items that seem to be a target before a problem develops. It is unrealistic to consider an enclosure without any potential risk, since anything in the captive environment is potentially a source if the material can be shredded or if it is small enough to be swallowed. Careful consideration should be given to substrate, enrichment items, and availability of potential foreign material that could be ingested. Owners and keepers should be cognizant of potential problems, and be proactive at the first signs of decreased casting, lethargy, or changes in appetite, since early intervention is more likely to be successful in raptors with gastric impactions.
Jeffrey R. Applegate, Jr., DVM, Arnaud Van Wettere, DVM, MS, PhD, Dipl ACVP, Emily F. Christiansen, DVM, MPH, Dipl ACZM. and Laurel A. Degernes, DVM, MPH, Dipl ABVP (Avian)
From the Department of Clinical Sciences (Applegate, Degernes); and the Department of Population Health and Pathobiology (Wettere), NCSU College of Veterinary Medicine, 1060 William Moore Dr. Raleigh. NC 27607, USA; and the North Carolina Aquariums, 3125 Poplarwood Ct, Raleigh, NC 27604. USA (Christiansen). Present address (Wettere): Utah Veterinary Diagnostic Laboratory, School of Veterinary Medicine. Department of Animal, Dairy & Veterinary Sciences, Utah State University, 950 East 1400 North. PO Box 6338, Logan, UT 84341. USA.
Acknowledgments: We thank the husbandry and educational staff at the North Carolina Aquarium at Pine Knoll Shores for their compassion and support with animal care. We thank Laura Adamovicz, DVM, Brianne Phillips, DVM, Craig Harms, DVM, PhD. Dipl ACZM, and Jessica McMurrer, CVT for assistance in case management and report preparation. We thank the NCSU Internal Medicine and Diagnostic Imaging Services for assistance with endoscopy and advanced imaging.
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Caption: Figure 1. Lateral radiograph of American kestrel (case 1) that was presented because of decreased appetite and casting, weight loss, and a distended coelom. Arrows outline the ventriculus distended with material of homogenous soft tissue opacity.
Caption: Figure 2. Lateral projection fluoroscopic image of the kestrel (case 1) described in Figure 1. Ventricular impaction outlined by contrast media (barium sulfate) coating the foreign material in ventriculus (V). Contrast can be seen distal to the ventriculus in the small intestine (SI) and cloaca (C).
Caption: Figure 3. Lateral radiograph of peregrine falcon (case 2) that was presented because of anorexia, vomiting, and regurgitation. Arrows outline a distended proventriculus (PV) containing material of soft tissue opacity and a mildly dilated ventriculus (V).
Caption: Figure 4. Lateral radiograph of a golden eagle (case 3) that was presented because of lethargy and inappetance. Arrows outline the proventriculus (PV) and ventriculus (V) distended with homogenous material of soft tissue opacity.
Caption: Figure 5. Lateral radiograph of a barn owl (case 4) that was presented because of lethargy, anorexia, and decreased fecal output. Arrows outline the distended ventriculus.
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|Author:||Applegate, Jeffrey R., Jr.; Van Wettere, Arnaud; Christiansen, Emily F.; Degernes, Laurel A.|
|Publication:||Journal of Avian Medicine and Surgery|
|Date:||Mar 1, 2017|
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