Diagnosis and management of inflammatory bowel disease in a harpy eagle (Harpia harpyja) with suspected fenbendazole toxicosis

Grayson A. Doss Department of Surgical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

Search for other papers by Grayson A. Doss in
Current site
Google Scholar
PubMed
Close
 DVM
,
Christoph Mans Department of Surgical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

Search for other papers by Christoph Mans in
Current site
Google Scholar
PubMed
Close
 Dr med vet
,
Laura Johnson Tender Care Animal Hospital, 1420 E Lessard St, Prairie du Chien, WI 53821.

Search for other papers by Laura Johnson in
Current site
Google Scholar
PubMed
Close
 DVM
,
Marie E. Pinkerton Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

Search for other papers by Marie E. Pinkerton in
Current site
Google Scholar
PubMed
Close
 DVM
,
Robert J. Hardie Department of Surgical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

Search for other papers by Robert J. Hardie in
Current site
Google Scholar
PubMed
Close
 DVM
, and
Kurt K. Sladky Department of Surgical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

Search for other papers by Kurt K. Sladky in
Current site
Google Scholar
PubMed
Close
 MS, DVM

Click on author name to view affiliation information

Abstract

CASE DESCRIPTION A 14-year-old 4.1-kg (9.02-lb) male harpy eagle (Harpia harpyja) was evaluated because of vomiting, anorexia, lethargy, and weight loss (decrease of 0.35 kg [0.77 lb]) of 4 weeks' duration. The bird had previously been treated orally with fenbendazole after the initial onset of clinical signs.

CLINICAL FINDINGS An initial CBC revealed marked heteropenia and anemia, but whole-body contrast-enhanced CT images and other diagnostic test findings were unremarkable. Clinical signs persisted, and additional diagnostic testing failed to reveal the cause. During celiotomy, a biopsy specimen of the duodenum was obtained for histologic examination, which revealed lymphoplasmacytic inflammation, consistent with inflammatory bowel disease (IBD).

TREATMENT AND OUTCOME Prior to histopathologic diagnosis of IBD, barium sulfate administered via gavage resulted in a temporary improvement of clinical signs. Following diagnosis of IBD, corticosteroid administration was initiated in conjunction with antifungal prophylaxis. Cessation of vomiting and a return to normal appetite occurred within 3 days. Fifteen months after cessation of corticosteroid treatment, the eagle continued to do well.

CLINICAL RELEVANCE To our knowledge, this was the first report of diagnosis and management of IBD in an avian species. For the eagle of the present report, results of several diagnostic tests increased clinical suspicion of IBD, but histologic examination of an intestinal biopsy specimen was required for definitive diagnosis. Although successful in this case, steroid administration in avian species must be carefully considered. Conclusive evidence of fenbendazole toxicosis was not obtained, although it was highly suspected in this bird.

Abstract

CASE DESCRIPTION A 14-year-old 4.1-kg (9.02-lb) male harpy eagle (Harpia harpyja) was evaluated because of vomiting, anorexia, lethargy, and weight loss (decrease of 0.35 kg [0.77 lb]) of 4 weeks' duration. The bird had previously been treated orally with fenbendazole after the initial onset of clinical signs.

CLINICAL FINDINGS An initial CBC revealed marked heteropenia and anemia, but whole-body contrast-enhanced CT images and other diagnostic test findings were unremarkable. Clinical signs persisted, and additional diagnostic testing failed to reveal the cause. During celiotomy, a biopsy specimen of the duodenum was obtained for histologic examination, which revealed lymphoplasmacytic inflammation, consistent with inflammatory bowel disease (IBD).

TREATMENT AND OUTCOME Prior to histopathologic diagnosis of IBD, barium sulfate administered via gavage resulted in a temporary improvement of clinical signs. Following diagnosis of IBD, corticosteroid administration was initiated in conjunction with antifungal prophylaxis. Cessation of vomiting and a return to normal appetite occurred within 3 days. Fifteen months after cessation of corticosteroid treatment, the eagle continued to do well.

CLINICAL RELEVANCE To our knowledge, this was the first report of diagnosis and management of IBD in an avian species. For the eagle of the present report, results of several diagnostic tests increased clinical suspicion of IBD, but histologic examination of an intestinal biopsy specimen was required for definitive diagnosis. Although successful in this case, steroid administration in avian species must be carefully considered. Conclusive evidence of fenbendazole toxicosis was not obtained, although it was highly suspected in this bird.

A 14-year-old 4.1 kg (9.02 lb) male harpy eagle (Harpia harpyja) was referred to the University of Wisconsin-Madison School of Veterinary Medicine for medical evaluation after a 4-week period of lethargy, hyporexia, and weight loss (decrease of 0.35 kg [0.77 lb]; loss of 7.9% of its normal weight). The owner described the eagle as having a normal interest in food, but not eating normal quantities. In addition, minutes to hours after eating, regurgitation or vomiting of undigested or partially digested food occurred. The eagle's diet consisted of frozen-thawed rodents and birds as well as various prekilled wildlife species. Results of a CBC and plasma biochemical profile performed 2 weeks after the onset of clinical signs did not indicate any abnormalities.1,a A routine fecal examination performed at that time (ie, 14 days prior to the referral evaluation) revealed few Capillaria spp, and 3 doses of fenbendazoleb (50 mg/kg [22.7 mg/lb], PO, q 24 h) were administered. Results of previous annual blood analyses had not revealed any notable abnormalities, and no prior medical problems were reported.

During the initial physical examination, the eagle was lethargic but otherwise quiet, alert, and responsive. For safety of the bird and the veterinary staff, the remainder of the examination was performed after the bird was sedated with midazolam hydrochloridec (1 mg/kg [0.45 mg/lb], IM) and butorphanol tartrated (1 mg/kg, IM). Other than a low body condition score (4/9), no other gross abnormalities were observed. Results of a CBC and plasma biochemical profilee revealed low PCV (PCV, 18%; reference range,1 31% to 36%) and marked leukopenia (2.0 × 103 WBCs/μL; reference range,1 11.1 × 103 WBCs/μL to 21.8 × 103 WBCs/μL) with a severe, absolute heteropenia (0.02 × 103 heterophils/μL; reference range,1 6.1 × 103 heterophils/μL to 13.2 × 103 heterophils/μL). All other clinicopathologic variables were within reference ranges. Cloacal and oropharyngeal swab samples were collected for cytologic examination (with Gram staining and Kinyoun acid-fast staining for cloacal samples) and aerobic and anaerobic bacterial culture; the results were negative or unremarkable. Results of a fecal examination (fecal flotation and direct smear assessment) were negative for parasites. The eagle was anesthetized via mask administration of isofluranef in oxygen. Whole-body CT images were obtained before and after IV administration of an iodinated contrast mediumg (2.2 mL of iohexol/kg [1 mL/lb]; 300 mg of iodine/mL). No obvious radiographic abnormalities were identified in any organ system. The midazolam administered for sedation was antagonized with flumazenilh (0.05 mg/kg [0.023 mg/lb], IM), and the eagle's recovery from anesthesia was uncomplicated.

On the basis of the eagle's treatment history and lack of obvious clinical findings to explain the hematologic changes, fenbendazole toxicosis was suspected. Heavy metal toxicosis was also considered as a differential diagnosis. A blood sample was submitted for analyses of plasma lead and zinc concentrations, and results were considered normal, compared with laboratory reference intervals for plasma lead and zinc concentrations in other eagle species. Heavy metal chelation therapy was initiated prior to receiving the results of the metal analyses and discontinued once results became available. Antimicrobial and antifungal medications were prescribed for prophylaxis because of the severe heteropenia. Famotidinei (0.5 mg/kg [0.23 mg/lb], PO, q 24 h for 14 days), metronidazolei (25 mg/kg [11.36 mg/lb], PO, q 12 h for 10 days), enrofloxacinj (20 mg/kg [9.09 mg/lb], PO, q 24 h for 10 days), itraconazolek (10 mg/kg [4.54 mg/lb], PO, q 24 h for 14 days), and calcium disodium EDTAl (35 mg/kg [15.91 mg/lb], IM, q 12 h for 5 days) were prescribed. Meloxicamm (0.5 mg/kg, PO, q 24 h) was previously being administered orally by the owner at home, and this treatment was continued. At the time of the eagle's discharge from the hospital, the owner (who was a veterinarian) was instructed to also provide gavage feeding and SC administration of lactated Ringer solution every 8 hours to maintain adequate nutrition and hydration.

Ten days later, the eagle was reevaluated because of continued vomiting and lethargy. The owner had been successfully gavage feeding a high-protein formulan to the eagle 4 times each day, but it vomited 30 to 90 minutes after formula administration. The eagle's interest in frozen-thawed rodents appeared normal, but it would only pick at them without consuming large portions. On the day of the reevaluation, a small amount of frank blood was observed in the vomitus and feces. The eagle's weight had decreased by 0.3 kg (0.66 lb [loss of 7.5% of its initial weight]) since the previous visit.

Given the lack of improvement, additional diagnostic testing was performed, including repeated CBC and plasma biochemical profile and an endoscopic examination of the upper gastrointestinal tracto and cloaca.p The anesthetic protocol was similar to that previously described. The results of the CBC indicated an improvement in PCV (20%), evidence of polychromasia, and an increase in total WBC (14.6 × 103 WBCs/μL) and heterophil (9.1 × 103 heterophils/μL) counts. Plasma biochemical analysis results indicated low total protein concentration (2.5 g/dL; reference range,a 2.8 to 5.4 g/dL). Results of the endoscopic examination of the oral cavity, esophagus, and proventriculus appeared normal, whereas the mucosa of the ventriculus appeared nodular. Endoscopic examination of the cloaca revealed few pinpoint areas of mucosal erosion or ulceration with adjacent tissue hyperemia. Multiple mucosal biopsy specimens of the ventriculus and cloaca were collected, preserved in neutral-buffered 10% formalin, and routinely processed and stained with H&E stain for histologic examination. Evidence of mild lymphocytic inflammation was detected in the sections of cloaca, and no abnormalities were identified in the sections of the ventriculus.

Because of the histopathologic findings and the suspicion of an underlying inflammatory disorder, changes to the treatment protocol were made as follows: meloxicam, metronidazole, and enrofloxacin treatments were discontinued; oral administrations of famotidine and itraconazole were continued; and treatments with ceftiofur crystalline-free acidq (10 mg/kg, IM, q 72 h for 12 days) and sucralfater (25 mg/kg, PO, q 8 h for 14 days) were added. Gavage feedings and SC administration of fluid were continued as previously prescribed, although the dosing frequency was changed to twice daily to reduce stress associated with frequent handling.

A recheck examination was performed 1 week later. Results of a CBC and plasma biochemical profile indicated continued increase in PCV (25%) and normalization of the total WBC count (20.6 × 103 WBCs/μL), heterophil count (12.4 × 103 heterophils/μL), and total protein concentration (3.4 g/dL). There was no change in the frequency of vomiting, and most of the gavaged food was expelled each time.

With the eagle conscious and perched wearing a falconry hood, a fluoroscopic examination of the gastrointestinal tract was performed. Survey images were first acquired. Then 30% (wt/vol) barium suspensions (20 mL/kg) was administered via gavage into the eagle's crop, and static images and a video recording were obtained up to 180 minutes thereafter. No abnormalities were observed during review of the obtained images and video recording, and peristalsis appeared adequate. Gastrointestinal transit time appeared appropriate, with contrast material reaching the cloaca within 180 minutes after administration, although a reference range for gastrointestinal transit time in this species does not currently exist, to our knowledge.

Owing to the eagle's poor clinical response to treatment, administrations of famotidine and ceftiofur crystalline-free acid were discontinued. Treatment with sucralfate was continued, and administration of terbinafinet (25 mg/kg, PO, q 24 h) was initiated for antifungal prophylaxis, replacing the previously prescribed itraconazole. Interestingly, gavage feedings performed the same day after barium administration did not result in vomiting.

Seventeen days later (5 weeks after the initial evaluation), the eagle was hospitalized for supportive care and further diagnostic testing because of continued cachexia, weight loss, vomiting, and lethargy. The body condition score had decreased to 3/9, and body weight had decreased to 3.7 kg (8.1 lb [loss of 9.6% of its initial weight]). Cloacal and oropharyngeal swab samples were collected for cytologic examination, and swab samples from the oropharynx were also submitted for fungal culture. No cytologic abnormalities were detected, and fungal culture of the oropharynx swab samples failed to yield growth of any organisms. Results of repeated fecal examination (fecal flotation and direct smear assessment) and infectious disease testing (including PCR assay of whole blood samples to detect Chlamydia psittaci antigen, assessment of serum titers of anti-avian herpesvirus antibodies and anti-avian bornavirus antibodies, and PCR assays of whole blood samples and breast contour feathers to detect West Nile virus antigen and avian bornavirus antigen, respectively) were all negative. A CBC and plasma biochemical profile revealed that the heteropenia and anemia had resolved.

Because of the suspected therapeutic response to barium administration, a 30% (wt/vol) barium suspensions (20 mL/kg) was administered intermittently via gavage and occasionally resulted in decreased frequency of postgavage-feeding vomiting for several hours. In addition, gavage feedings were continued 2 to 3 times a day with various feeding formulas.n,u,v Oral administration of terbinafine was replaced with oral administration of fluconazole (10 mg/kg, PO, q 24 h), and ranitidine (0.8 mg/kg [0.36 mg/lb], PO, q 12 h) and meloxicam (0.25 mg/kg [0.11 mg/lb], PO, q 24 h) were also prescribed. However, despite changing of feeding formulas and frequency of gavage feeding, the eagle continued to vomit after most feedings and frequently vomited several hours later. A licensed veterinary acupuncturist performed several sessions of acupuncture, focusing on generalized inflammation and gastrointestinal tract motility sites derived from sites used in mammalian species, but these procedures did not result in any apparent improvement.

Given the eagle's lack of clinical improvement, it was decided to perform an exploratory celiotomy for further examination and biopsy of the gastrointestinal tract. The eagle was premedicated with midazolam and butorphanol; anesthesia was induced and maintained with isoflurane in oxygen. A 22-gauge intraosseous catheter was placed in the distal portion of the right ulna for intraoperative administration of fluids and antimicrobials; this catheter ultimately had to be replaced within 72 hours because of damage from wing movement. Piperacillin-tazobactamw (200 mg/kg [90.9 mg/lb], q 6 to 8 h) was perioperatively administered via the catheter. Following local infiltration with lidocaine, a ventral midline celiotomy was performed. Coelomic exploration did not reveal any gross or palpable abnormalities of the gastrointestinal tract, liver, pancreas, or kidneys. A full-thickness biopsy specimen of the proximal portion of the duodenum was obtained, and the enterotomy site was closed with absorbable suturex in a simple interrupted pattern (Figure 1). Because of the duration of the procedure and concerns for postoperative healing, biopsies of other organs were not performed. The coelomic membrane, muscle layer, and subcutaneous tissues were each apposed with polyglyconate suture in simple continuous patterns,y and the skin was closed with staples.z The eagle recovered from anesthesia without complications. Intraosseous administration of butorphanol (0.5 mg/kg, q 4 h) was performed for postoperative analgesia. This butorphanol dosage was used because higher dosages administered for chemical restraint often resulted in moderate sedation in this eagle. Intraosseous administration of piperacillin-tazobactam was continued for 3 days after surgery.

Figure 1—
Figure 1—

Intraoperative photograph of a closed duodenal biopsy site in a harpy eagle (Harpia harpyja) that was evaluated because of vomiting, anorexia, lethargy, and weight loss (decrease of 0.35 kg [0.77 lb]) of 4 weeks' duration. The suture tags were trimmed before this portion of the intestines was replaced into the coelom.

Citation: Journal of the American Veterinary Medical Association 252, 3; 10.2460/javma.252.3.336

Histologic examination of sections of the duodenal biopsy specimen revealed moderate numbers of lymphocytes and plasma cells expanding the lamina propria (Figure 2). In sections in which the muscularis externa was present, perivascular lymphocytes and plasma cells were identified at the interface of circular and longitudinal muscles. No infectious organisms were observed. The final histopathologic diagnosis was mild lymphoplasmacytic enteritis consistent with IBD.

Figure 2—
Figure 2—

Photomicrograph of a section of the duodenal biopsy specimen obtained from the harpy eagle in Figure 1. Notice the evidence of lymphoplasmacytic inflammation within the epithelium. H&E stain; bar = 50 μm.

Citation: Journal of the American Veterinary Medical Association 252, 3; 10.2460/javma.252.3.336

The route of administration of the fluconazole, meloxicam, and famotidine was changed from oral to intraosseous. An intraosseous constant rate infusion of metoclopramideaa (0.08 mg/kg/h [0.036 mg/lb/h]) was initiated to determine whether gastrointestinal tract motility was a factor in the continued vomiting. Intraosseous fluid therapy (lactated Ringer solution administered at a rate of 3.3 mL/kg/h [1.5 mL/lb/h]) was also provided. Ultimately, the intraosseous catheter was removed after 72 hours because of bending of the needle, likely secondary to the frequent episodes of manual restraint.

Despite intensive supportive care and medical treatment for nearly 7 weeks, the eagle continued to have weight loss, lethargy, and episodes of vomiting. After discussing the eagle's quality of life and long-term prognosis with the owner, in-hospital administration of all medications was stopped, and the eagle was monitored in the hospital for an increase in appetite. The eagle continued to show interest in frozen-thawed rodents but would only consume very small amounts, which were frequently expelled in vomit. After 12 days of hospitalization, the owner elected to continue supportive care at home. Oral administration of prednisone (0.5 mg/kg, PO, q 24 h) with concurrent administration of terbinafinet (25 mg/kg, PO, q 24 h) was prescribed. The eagle's body weight at discharge from the hospital was 3.7 kg.

Over the next 6 days, the eagle continued to vomit all forms of nutrition and lose weight, regardless of multiple gavage feedings each day. Because of advanced cachexia and worsening lethargy, the owner increased the oral prednisone dosage to 1 mg/kg every 24 hours. Within 3 days of starting the increased dosage, the eagle began to eat normal amounts of food and vomiting ceased. Administration of prednisone at this dosage was continued for 5 to 6 weeks, and a gradual dosage reduction was performed over the next 5 weeks. The concurrent oral administration of terbinafine was continued as initially prescribed and ultimately discontinued simultaneously with the reduced dosage of prednisone. During corticosteroid treatment, the eagle regained all previously lost weight and was eating normally. At 29 months after cessation of the prednisone treatment, the eagle continued to do well and had no residual effects of the prior illness or recurrence of clinical signs.

Discussion

The term IBD defines a group of complex idiopathic disorders often encountered in both humans and small animals. The underlying cause is considered multifactorial, and pathogenesis is most commonly associated with one or more of the following: an exaggerated or abnormal innate immune response, genetic predisposition, dietary factors, and host interactions with either commensal or pathogenic gastrointestinal bacteria.2–4 In dogs and cats, clinical signs often reflect the area of the gastrointestinal tract affected and can include anorexia, vomiting, diarrhea, weight loss, tenesmus, hematochezia, hematemesis, and melena.2,3 Diagnosis is achieved through exclusion of other potential disease processes and, in many cases, is dependent on response to various medical interventions or results of histologic examination of intestinal biopsy specimens.2–4 Treatment is based on the subset type and severity of the disease and may range from treatments with antimicrobials and diet modification to immunosuppressive therapy.2–4

Inflammatory bowel disease in birds is poorly described. The only published comment regarding this disorder in avian species of which the authors were aware described it as rare in incidence.5 For the harpy eagle of the present report, compatible clinical signs, the exclusion of other potential diseases, and histopathologic findings of a full-thickness duodenal biopsy specimen led to a diagnosis of IBD. Another indication of the likely presence of gastrointestinal tract inflammation in this eagle was the temporary but apparently therapeutic effect of oral administration of barium. The potential of barium sulfate as an intestinal protectant in small animals has been described,6 and it is possible that the barium suspension adhered to ulcerated areas in the eagle's gastrointestinal tract, resulting in diminished local irritation and the observed decreased frequency of vomiting.

Histologic diagnosis of IBD in cats and dogs is challenging because of the subjective nature of grading lesion severity, differences in tissue sample processing, and difficulty in interpretation of changes in the small tissue samples obtained via endoscopy.4,7 Although standards for diagnosis of IBD in canine and feline biopsy specimens have been published,8 pathologists' interpretations of histologic findings may still vary widely.7 Because IBD is rare in birds, histopathologic diagnostic criteria do not exist; hence, the diagnosis for the eagle of the present report was presumptive. Ideally, because diagnostic criteria are nonexistent, the histologic findings for this eagle would have been compared with those for a similar biopsy specimen obtained from a healthy, aged-matched harpy eagle. Such harpy eagle tissue samples were not available for comparison in this case, and the presumptive diagnosis was based on standard criteria for IBD diagnosis in dogs and cats.7

Given the normal findings for the CBC and plasma biochemical profile performed immediately prior to administration of fenbendazole and the subsequent onset of marked hematologic changes after administration of the drug, fenbendazole toxicosis was highly suspected in the case described in the present report. Fenbendazole toxicosis in several animal species, including rabbits, porcupines, pigeons, doves, storks, and vultures, has been reported.9–13 In addition, abnormal changes in clinicopathologic variables in tortoises administered fenbendazole orally have been described.14 Toxicosis is a result of the drug's mechanism of action. Fenbendazole binds tubulin and affects cellular division, which can then lead to severe suppression of rapidly dividing cells, such as bone marrow precursors and intestinal crypt cells.12 Affected birds may have signs of anorexia, weight loss, lethargy, dehydration, marked leukopenia or heteropenia, thrombocytopenia, and sudden death within days after fenbendazole administration.10–13 Birds may become rapidly septicemic or develop secondary infections during treatment.12,13 Although some birds may recover after provision of aggressive supportive care, the overall mortality rate associated with fenbendazole toxicosis in avian species is high.10–13 Morbidity and death induced by fenbendazole are known to be dose related in pigeons and doves.10 The dose administered to the eagle of the present report was based on published dosage recommendations for raptors and was therefore assumed appropriate.15

In the harpy eagle of the present report, changes in hematologic and plasma biochemical variables over time were similar to those reported for painted storks (Mycteria leucocephala) following fenbendazole administration.12 Painted storks with fenbendazole toxicosis initially had decreased PCV and marked leukopenia secondary to severe heteropenia, which was followed by a slow increase in PCV and rebound leukocytosis; the heterophil count in those birds normalized several weeks later.12

It remains unclear whether fenbendazole toxicosis resulted in the marked heteropenia and anemia observed in the eagle of the present report. Definitive diagnosis would have required histologic evidence of intestinal crypt necrosis and bone marrow suppression. A bone marrow biopsy was not performed in this case. Duodenal biopsy was performed several weeks after discontinuation of fenbendazole administration, making it unlikely that crypt necrosis would be detected during histologic examination of the duodenal biopsy specimen. If the clinical signs were secondary to fenbendazole toxicosis, it remains unknown whether the findings for this eagle were consistent with an idiosyncratic drug reaction or a drug reaction applicable to all birds of the species H harpyja. To the authors' knowledge, no published information exists in the veterinary medical literature regarding the use of fenbendazole in this species. Inquiries were made with several zoological institutions housing captive harpy eagles throughout the United States and in Central and South America regarding fenbendazole usage in this species. Information received revealed that although fenbendazole does not appear to be a commonly used anthelmintic in harpy eagles, compared with usage of other antiparasitic compounds, dosages similar to that used in the case described in the present report have been administered to other individuals of this species without signs of adverse effects.bb

For the eagle of the present report, thrombocyte counts were not routinely performed, making it difficult to identify thrombocytopenia secondary to possible fenbendazole toxicosis. Electron microscopic evaluation of the affected tissue in the duodenal biopsy specimen may also have proven useful for determining any potential virologic cause of the intestinal inflammation. Unfortunately, however, the small amount of duodenal tissue in the biopsy specimen precluded its use for diagnostic tests other than histologic examination.

In avian medicine, celioscopy is a well-established diagnostic tool that can be used to examine and biopsy various organ systems within the coelomic cavity. In the eagle of the present report, other diagnostic tests were preferentially chosen because of the localization of the clinical signs to the gastrointestinal tract. However, although more invasive, celiotomy was ultimately performed instead of celioscopy to obtain a full-thickness duodenal biopsy specimen.

Antiemetics are routinely used in veterinary medicine. However, little information exists concerning use of these drugs in avian species. To the authors' knowledge, there are no systematic studies in birds evaluating the effectiveness of any of the antiemetic compounds commonly used in dogs and cats. Because of this, the authors chose not to prescribe antiemetics because of the lack of established dosage recommendations for these compounds in birds. Metoclopramide has been used anecdotally as an antiemetic drug in birds, but its use is controversial owing to a lack of studies demonstrating its efficacy and the potential for possible adverse effects.16,cc Further research is needed to investigate the use of antiemetic compounds in avian species.

In the case described in the present report, histologic examination of biopsy specimens of the cloaca revealed mild lymphocytic inflammation, which differed from the lymphoplasmacytic infiltrate present in the full-thickness biopsy specimen of the duodenum. It is plausible that the lymphoplasmacytic inflammation within the gastrointestinal tract was limited to the small intestine alone. Other possible explanations are that the lymphoplasmacytic inflammation was also present within the cloaca and that the endoscopic biopsy specimens were nonrepresentative or that the lymphocytic inflammation within the cloacal samples denoted an unrelated process. Although the ventriculus appeared nodular on endoscopic evaluation, it is possible that this appearance is normal in harpy eagles, which may explain the lack of histopathologic abnormalities in the mucosa of the ventriculus.

Readily available psittacine tests were used to detect herpesviral or bornaviral infection in the eagle of the present report, and those tests were most likely of low diagnostic yield. The West Nile virus PCR assay was also performed on a whole blood sample, which limited the usefulness of this diagnostic test. The obvious limitations of these infectious disease tests were understood prior to use; nevertheless, they were performed because of the lack of a diagnosis, despite numerous other tests having been previously performed. On the basis of the clinical situation, the likelihood of the eagle having an infection with one of these viral agents seemed low.

Although fenbendazole toxicosis was highly suspected as the cause of the hematologic abnormalities in the eagle of the present report, gastrointestinal signs were observed prior to administration of the drug; thus, it was unlikely that fenbendazole administration resulted in the development of IBD. It is conceivable that an insult to the gastrointestinal tract, such as enteritis, may have led to increased mucosal barrier permeability in the eagle. This, in combination with the diversity of this eagle's diet, may have increased the potential for exposure to novel antigenic stimuli after the mucosal barrier function of the gastrointestinal tract was compromised. Increased contact with bacteria or other antigens may have resulted in an enhanced or inappropriate immune response, leading to continued dysfunction of the enteric tract. In humans, increased mucosal barrier permeability with persistent exposure to luminal antigens may lead to an enhanced or irregular immune response with secondary dysfunction of the gastrointestinal tract.17,18 This abnormal interaction between the host's immune system and luminal microorganisms, especially bacteria, is believed to be a major part of the pathogenesis of IBD.19 It is also well documented that irritable bowel syndrome in people can develop secondary to acute infectious gastroenteritis, which is often contracted from a contaminated water source.17,20 Although attractive, this hypothesis requires careful interpretation and further validation.

Administration of anti-inflammatory or immunosuppressive medication is a common method of treating IBD in dogs and cats. Oral administration of intermediate-acting corticosteroids, such as prednisolone or prednisone, is often prescribed because of the ease of administration and decreased potential for severe adverse effects.2–4 The corticosteroid dosages used for treatment of the eagle of the present report (0.5 to 1.0 mg/kg, PO, q 24 h) were within the ranges of anti-inflammatory to low-level immunosuppressive dosages recommended for use in dogs.21 Little information about the use of corticosteroids in birds exists. However, a survey of exotic animal practitioners indicated that glucocorticoid administration may not be uncommon in the treatment of avian patients and may hold beneficial effects in certain circumstances.dd Although the outcome in the case described in the present report was positive, the authors advocate caution when administering any form of corticosteroid treatment in avian species. Administration of exogenous corticosteroids in birds can easily result in infections (secondary to immunosuppression), deleterious physiologic effects, and death.22–24 Use of corticosteroid treatment in this eagle was carefully considered before implementation, and ultimately, it was decided that the potential benefits outweighed the risks. Further research is necessary to better understand the role of corticosteroid treatment in birds with IBD.

The harpy eagle of the present report was evaluated because of persistent, nonspecific clinical signs associated with the gastrointestinal tract as well as clinicopathologic changes consistent with fenbendazole toxicosis. Results of routine diagnostic testing failed to determine a cause of those signs, and histologic examination of a full-thickness duodenal biopsy specimen was required to make the diagnosis of lymphoplasmacytic enteritis. Treatment with prednisone was ultimately successful in alleviating clinical signs, but was not initiated until numerous other differential diagnoses were ruled out. Inflammatory bowel disease should be considered as a differential diagnosis in harpy eagles with prolonged, refractory gastrointestinal signs. In addition, the authors believe that caution should be exercised when administering fenbendazole to harpy eagles at the dosage used in the bird of the present report (ie, three 50-mg/kg doses of fenbendazole, PO, 24 hours apart) until additional information regarding safe use of this drug in this species is available.

Acknowledgments

The authors thank Marta Curti, Dr. Magaly Linares, Dr. Pilar Alexander Blanco Márquez, Angel Muela, Dr. Meredith Persky, Dr. Ryan Sadler, Dr. Miguel Saggese, Dr. Carlos Sanchez, and Dr. Rick Watson for information regarding fenbendazole usage in harpy eagles.

Abstract published in the Proceedings of the First Annual ExoticsCon, San Antonio, Tex, August–September 2015.

ABBREVIATIONS

IBD

Inflammatory bowel disease

Footnotes

a.

ISIS Physiological Data Reference Values Project. Apple Valley, Minn: International Species Inventory System (ISIS), 2013.

b.

Panacur, Merck Animal Health, Summit, NJ.

c.

Midazolam hydrochloride injection, Hospira Inc, Lake Forest, Ill.

d.

Torbugesic, Fort Dodge Animal Health, Fort Dodge, Iowa.

e.

Avian/Reptilian Profile Plus, VetScan VS2, Abaxis, Union City, Calif.

f.

IsoFlo, Abbott Laboratories, North Chicago, Ill.

g.

Omnipaque injection, GE Healthcare Inc, Princeton, NJ.

h.

Flumazenil, West-Ward Pharmaceuticals Corp, Eatontown, NJ.

i.

Pharmacy, School of Veterinary Medicine, University of Wisconsin, Madison, Wis.

j.

Baytril, Bayer Animal Health, Shawnee Mission, Kan.

k.

Sporanox (itraconazole) oral solution (10 mg/mL), Janssen Pharmaceuticals, Titusville, NJ.

l.

Calcium disodium EDTA, Sigma Chemical Co, St Louis, Mo.

m.

Metacam, Boehringer Ingelheim Vetmedica, St Joseph, Mo.

n.

Oxbow Carnivore Care, Oxbow, Murdock, Neb.

o.

Olympus model GIF-XP160 endoscope, Olympus America Inc, Lombard, Ill.

p.

64019BA and 64018US, Karl Storz Veterinary Endoscopy America Inc, Goleta, Calif.

q.

Excede, Pharmacia and Upjohn Co, New York, NY.

r.

Carafate, Aptalis Pharma US Inc, Bridgewater, NJ.

s.

Liquid E-Z-Paque, E-Z-EM Inc, Lake Success, NY.

t.

Terbinafine HCl, Harris Pharmaceuticals Inc, Fort Myers, Fla.

u.

Emeraid Carnivore, LaFeber Co, Cornell, Ill.

v.

Prescription Diet a/d, Hill's Pet Nutrition Inc, Topeka, Kan.

w.

Zosyn, Wyeth Pharmaceuticals Inc, Philadelphia, Pa.

x.

5-0 Maxon, Covidien, Mansfield, Mass.

y.

3-0 Maxon, Covidien, Mansfield, Mass.

z.

Appose ULC 35-W, Covidien Ltd, Mansfield, Mass.

aa.

Metoclopramide injection, Baxter Healthcare Corp, Deerfield, Ill.

bb.

Blanco Márquez PA, Director, Harpy Eagle Conservation Program, Bolívar, Venezuela: Personal communication, 2016.

cc.

Bowman M, Paré J, Ziegler L, et al. Effects of metoclopramide on the gastrointestinal tract motility of Hispaniolan parrots (Amazona ventralis) (abstr), in Proceedings. Annu Conf Am Assoc Zoo Vet 2002;117–118.

dd.

Heatley JJ, Slater MR, Hoppes S. Glucocorticoid use in avian species: a survey of veterinary practitioners (abstr), in Proceedings. Am Assoc Zoo Vet Assoc Reptilian Amphib Vet Joint Conf 2008;169–170.

References

  • 1. Oliveira MJ, Nascimento IA, Ribeiro VO, et al. Haematological values for captive harpy eagle (Harpia harpyja). Pesqui Vet Bras 2014;34:805809.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Simpson KW, Jergens AE. Pitfalls and progress in the diagnosis and management of canine inflammatory bowel disease. Vet Clin North Am Small Anim Pract 2011;41:381398.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Jergens AE. Inflammatory bowel disease: current perspectives. Vet Clin North Am Small Anim Pract 1999;29:501521.

  • 4. Allenspach K, Kathrani A. Inflammatory bowel disease. In: Bonagura J, Twedt D, eds. Kirk's current veterinary therapy XV. St Louis: Saunders-Elsevier, 2014;536540.

    • Search Google Scholar
    • Export Citation
  • 5. Souza MJ, Newman SJ, Greenacre CB, et al. Diffuse intestinal T-cell lymphosarcoma in a yellow-naped Amazon parrot (Amazona ochrocephala ouropalliata). J Vet Diagn Invest 2008;20:656660.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Willard M. Digestive system disorders. In: Nelson R, Couto C, eds. Small animal internal medicine. 5th ed. St Louis: Mosby-Elsevier, 2014;367500.

    • Search Google Scholar
    • Export Citation
  • 7. Jergens AE, Evans RB, Ackermann M, et al. Design of a simplified histopathologic model for gastrointestinal inflammation in dogs. Vet Pathol 2014;51:946950.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Day MJ, Bilzer T, Mansell J, et al. Histopathological standards for the diagnosis of gastrointestinal inflammation in endoscopic biopsy samples from the dog and cat: a report from the World Small Animal Veterinary Association Gastrointestinal Standardization Group. J Comp Pathol 2008;138:S1S43.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Graham JE, Garner MM, Reavill DR. Benzimidazole toxicosis in rabbits: 13 cases (2003 to 2011). J Exot Pet Med 2014;23:188195.

  • 10. Howard LL, Papendick R, Stalis IH, et al. Fenbendazole and albendazole toxicity in pigeons and doves. J Avian Med Surg 2002;16:203210.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Gozalo AS, Schwiebert RS, Lawson GW. Mortality associated with fenbendazole administration in pigeons (Columba livia). J Am Assoc Lab Anim Sci 2006;45:6366.

    • Search Google Scholar
    • Export Citation
  • 12. Weber MA, Terrell SP, Neiffer DL, et al. Bone marrow hypoplasia and intestinal crypt cell necrosis associated with fenbendazole administration in five painted storks. J Am Vet Med Assoc 2002;221:417419.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Bonar CJ, Lewandowski AH, Schaul J. Suspected fenbendazole toxicosis in 2 vulture species (Gyps africanus, Torgos tracheliotus) and marabou storks (Leptoptilos crumeniferus). J Avian Med Surg 2003;17:1619.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Neiffer DL, Lydick D, Burks K, et al. Hematologic and plasma biochemical changes associated with fenbendazole administration in Hermann's tortoises (Testudo hermanni). J Zoo Wildl Med 2005;36:661672.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Hawkins M, Barron H, Speer B, et al. Birds. In: Carpenter JW, Marion CJ, eds. Exotic animal formulary. 4th ed. St Louis: Elsevier Saunders, 2012;183437.

    • Search Google Scholar
    • Export Citation
  • 16. Grosset C, Guzman DS-M, Keating MK, et al. Central vestibular disease in a blue and gold macaw (Ara ararauna) with cerebral infarction and hemorrhage. J Avian Med Surg 2014;28:132142.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Marshall JK, Thabane M, Garg AX, et al. Intestinal permeability in patients with irritable bowel syndrome after a waterborne outbreak of acute gastroenteritis in Walkerton, Ontario. Aliment Pharmacol Ther 2004;20:13171322.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Villani A-C, Lemire M, Thabane M, et al. Genetic risk factors for post-infectious irritable bowel syndrome following a waterborne outbreak of gastroenteritis. Gastroenterology 2010;138:15021513.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008;134:577594.

  • 20. Zanini B, Ricci C, Bandera F, et al. Incidence of post-infectious irritable bowel syndrome and functional intestinal disorders following a water-borne viral gastroenteritis outbreak. Am J Gastroenterol 2012;107:891899.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Plumb DC. Prednisone. In: Plumb DC, ed. Plumb's veterinary drug handbook. 8th ed. Hoboken, NJ: Wiley-Blackwell, 2015;883887.

  • 22. de Matos R. Adrenal steroid metabolism in birds: anatomy, physiology, and clinical considerations. Vet Clin North Am Exot Anim Pract 2008;11:3557.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Verstappen FALM, Dorrestein GM. Aspergillosis in Amazon parrots after corticosteroid therapy for smoke-inhalation injury. J Avian Med Surg 2005;19:138141.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Deem SL. Fungal diseases of birds of prey. Vet Clin North Am Exot Anim Pract 2003;6:363376.

All Time Past Year Past 30 Days
Abstract Views 514 0 0
Full Text Views 1014 852 365
PDF Downloads 350 181 21
Advertisement