Diagnosis and treatment of proventricular nematodiasis in an umbrella cockatoo (Cacatua alba)

Johanna Mejia-Fava Department of Small Animal Medicine and Surgery, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Stephen J. Divers Department of Small Animal Medicine and Surgery, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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David A. Jiménez Department of Veterinary Biosciences & Diagnostic Imaging, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Dana L. Ambrose Department of Infectious Disease, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Raquel Rech Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Nicole L. Gottdenker Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Jörg Mayer Department of Small Animal Medicine and Surgery, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Abstract

Case Description—A 16-year-old female umbrella cockatoo (Cacatua alba) was referred to the University of Georgia College of Veterinary Medicine for evaluation of a 3-year seasonal history of lethargy and weight fluctuation.

Clinical Findings—Abnormalities detected via clinicopathologic analyses included mild leukocytosis, heterophilia, and lymphopenia consistent with a stress leukogram. Previous fecal examinations failed to diagnose enteric parasite infestation. Results of a fecal flotation test with Sheather sugar solution revealed spirurid eggs (Spiruroidea). Coelomic radiography revealed a widened cardiohepatic waist with increased soft tissue opacity at the level of the hepatic silhouette. The caudal thoracic and abdominal air sacs bilaterally appeared compressed against the coleomic wall. The proventriculus was increased in diameter, with a proventriculus-to-keel ratio of 1.0. Coelomic ultrasonography and positive-contrast upper gastrointestinal radiography revealed severe thickening and irregularity of the proventricular wall. The animal was anesthetized for an endoscopic examination of the upper gastrointestinal tract. Intralesional nematodes were identified on histologic examination of biopsy specimens from the proventriculus.

Treatment and Outcome—Effective fenbendazole treatment (15 mg/kg [6.8 mg/lb], PO, alternating between 5 days of treatment and 5 days of no treatment, which continued for 4 periods) was confirmed by repeated endoscopy and fecal examinations. The bird remained free of clinical signs 27 months after diagnosis and treatment.

Clinical Relevance—Antemortem diagnosis of proventricular nematodiasis has not been reported in psittacines. Spirurid nematode eggs are shed intermittently, which may lead to false-negative results on a single routine fecal examination. In this patient, radiography, endoscopy, and histologic evaluation facilitated antemortem diagnosis. This is the first report of successful treatment of this condition in psittacines.

Abstract

Case Description—A 16-year-old female umbrella cockatoo (Cacatua alba) was referred to the University of Georgia College of Veterinary Medicine for evaluation of a 3-year seasonal history of lethargy and weight fluctuation.

Clinical Findings—Abnormalities detected via clinicopathologic analyses included mild leukocytosis, heterophilia, and lymphopenia consistent with a stress leukogram. Previous fecal examinations failed to diagnose enteric parasite infestation. Results of a fecal flotation test with Sheather sugar solution revealed spirurid eggs (Spiruroidea). Coelomic radiography revealed a widened cardiohepatic waist with increased soft tissue opacity at the level of the hepatic silhouette. The caudal thoracic and abdominal air sacs bilaterally appeared compressed against the coleomic wall. The proventriculus was increased in diameter, with a proventriculus-to-keel ratio of 1.0. Coelomic ultrasonography and positive-contrast upper gastrointestinal radiography revealed severe thickening and irregularity of the proventricular wall. The animal was anesthetized for an endoscopic examination of the upper gastrointestinal tract. Intralesional nematodes were identified on histologic examination of biopsy specimens from the proventriculus.

Treatment and Outcome—Effective fenbendazole treatment (15 mg/kg [6.8 mg/lb], PO, alternating between 5 days of treatment and 5 days of no treatment, which continued for 4 periods) was confirmed by repeated endoscopy and fecal examinations. The bird remained free of clinical signs 27 months after diagnosis and treatment.

Clinical Relevance—Antemortem diagnosis of proventricular nematodiasis has not been reported in psittacines. Spirurid nematode eggs are shed intermittently, which may lead to false-negative results on a single routine fecal examination. In this patient, radiography, endoscopy, and histologic evaluation facilitated antemortem diagnosis. This is the first report of successful treatment of this condition in psittacines.

A16-year-old female umbrella cockatoo (Cacatua alba) was referred to the University of Georgia Zoological Medicine Service for evaluation of a 3-year seasonal history of lethargy and weight fluctuation. The parrot was offered a seed mixturea and formulated pelleted dietb supplemented with various fruits and vegetables. The cockatoo shared the same air space with, but was housed separately from, a Congo African grey parrot (Psittacus erithacus erithacus). Both birds were also provided with separate outdoor aviaries but did have contact through a common fence. No abnormalities were observed in the African grey parrot, and the owners did not report any environmental changes or prior health problems in either bird.

Previously, the cockatoo had been regularly examined annually by the referring veterinarian. Routine health assessment included hematologic evaluation, plasma biochemical analysis, and routine fecal tests, which did not show relevant abnormalities. Parasites were not seen in previous fecal examinations via both direct smear and fecal flotation with sodium nitrate and centrifugation technique. Previous treatments included enrofloxacinc (5 mg/kg [2.3 mg/lb], PO) every 12 hours for 2 months. The owners noticed that the parrot improved during antimicrobial treatment but never completely returned to its previous level of activity and attitude.

On initial examination upon referral to the Zoological Medicine service (day 1), the cockatoo was bright, alert, and responsive. On palpation, the lower portion of the coelom felt abnormal, with a possible mass effect in the region of the proventriculus. The bird weighed 554 g (1.2 lb) and was thin with a body condition score of 3 of 9. There were no other abnormalities noted on physical examination. Following anesthetic induction with 5% isofluraned in oxygen at 1 L/min delivered via a mask, the bird was intubated with a 4.0-mm uncuffed endotracheal tube and anesthesia was maintained with 3% isoflurane in oxygen, which was adjusted to individual patient requirements. Blood (1.5 mL) was collected from the right jugular vein for routine hematologic and plasma biochemical analysis. Hematologic examination revealed mild leukocytosis (19,700 cells/μL; reference range,1 5,000 to 13,000 cells/μL), heterophilia (14,972 cells/μL; reference range,1 750 to 8,320 cells/μL), and lymphopenia (3,546 cells/μL; reference range,1 1,450 to 10,790 cells/μL). These values were consistent with a stress leukogram. Results of the plasma biochemical analysis were all within reference ranges.

Orthogonal radiographse of the entire coelom were obtained. On the lateral view, an increased soft tissue opacity was identified in the midcoelom. The caudal thoracic and abdominal air sacs bilaterally appeared compressed against the coleomic wall by the resultant mass effect. The proventriculus was increased in diameter, with a proventriculus-to-keel ratio of 1.0 (Figure 1).2,3 The ventrodorsal view revealed a widened cardiohepatic waist with an enlarged soft tissue opacity at the level of the hepatic silhouette (Figure 2). Coelomic ultrasonography was performedf,g to further characterize the coelomic anomalies (Figure 3). A minimal volume of hypoechoic free coelomic fluid was identified, and the liver appeared normal. A heteroechoic mass, approximately 2.6 × 3.0 cm in diameter, was identified just caudal to the liver and filled most of the coelomic cavity. The mass had an undulant, severely thickened wall and thin, irregularly marginated lumen. It contained a small volume of gas caudally and seemed to connect to the small intestine. Few normal small intestinal segments were identified. The spleen and urogenital tract were not seen because of the mass effect. Positive-contrast upper gastrointestinal radiography was also performed via esophageal tube administration of iohexolh (25 mL/kg [11.4 mL/lb] of a 350 mg/mL nonionic iodinated contrast medium diluted 1:1 with water) into the crop. Fluoroscopyi and radiography documented a large filling defect because of severe annular thickening of the proventricular wall. A small amount of contrast was present in the proventricular lumen and between lobular regions of mural thickening. The proventriculus had a thickened wall with an intramural fimbriated to stellate appearance (Figure 4). Subjectively, the small intestines were diffusely, mildly dilated. On the basis of results of diagnostic imaging, complete upper gastrointestinal endoscopy was performed.

Figure 1—
Figure 1—

Radiographic image of a 16-year-old female umbrella cockatoo (Cacatua alba) referred for evaluation of a 3-year seasonal history of lethargy and weight fluctuation and a subsequent diagnosis of proventricular nematodiasis. The lateral radiographic view revealed that the proventriculus was increased in diameter (arrows) with a proventriculus-to-keel ratio of 1.0.

Citation: Journal of the American Veterinary Medical Association 242, 8; 10.2460/javma.242.8.1122

Figure 2—
Figure 2—

Ventrodorsal coelomic radiographic image of the cockatoo in Figure 1, which revealed a widened cardiohepatic waist (arrowheads) with increased soft tissue opacity at the level of the hepatic silhouette. The caudal thoracic and abdominal air sacs bilaterally appeared compressed against the coleomic wall.

Citation: Journal of the American Veterinary Medical Association 242, 8; 10.2460/javma.242.8.1122

Figure 3—
Figure 3—

Coelomic ultrasonographic image of the bird in Figure 1, which revealed a heteroechoic 2.6-cm mass (black vertical line on the image) just caudal to the liver and filling most of the coelomic cavity. This mass was identified as the proventriculus, and numerous, columnar, soft tissue echoic structures (white asterisks) are evident projecting into the narrow, hypoechoic, fluid-filled lumen.

Citation: Journal of the American Veterinary Medical Association 242, 8; 10.2460/javma.242.8.1122

Figure 4—
Figure 4—

Lateral positive-contrast gastrointestinal radiographic image of the bird in Figure 1. A large filling defect (white arrows) caused by severe annular thickening of the wall of the proventriculus was seen.

Citation: Journal of the American Veterinary Medical Association 242, 8; 10.2460/javma.242.8.1122

On day 2 of hospitalization, the bird was again anesthetized and maintained under general anesthesia as described. An intraossoeus catheter was placed into the distal portion of the right ulna to provide vascular access and intraoperative fluids, and intermittent positive pressure ventilation was provided throughout the anesthetic period. The bird was positioned with the head elevated to prevent liquid from entering the pharynx and being aspirated. A surgical ingluviotomy approach was used to facilitate rigid endoscopic evaluation of the upper gastrointestinal tract.4 A 1-cm longitudinal incision was made in the right lower cervical region, at the dorsal border of the crop. Stay sutures were placed, and a 5-mm incision was made into the crop. Endoscopic evaluation proceeded by use of a 2.7-mm rigid telescopej housed within a 4.8-mm operating sheathk and sterile saline (0.9% NaCl) solution infusion. The crop and intracoelomic portion of the esophagus were unremarkable; however, entry into the proventriculus revealed numerous botryoid vesicle-like structures likely caused by nematodes burrowed within proventricular glands (Figure 5). These structures appeared to originate from the cranial and lateral portions of the proventricular mucosa. Grossly normal mucosa on the ventral portion of the proventriculus was noted, but it was not possible to advance further into the ventriculus. A biopsy forceps (1.7 mm)l was used to collect several biopsy specimens from abnormal areas of the proventriculus. Following removal of the endoscopic equipment, the crop was closed with poliglecaprone 25m suture impregnated with triclosan in a continuous appositional pattern. The skin was closed separately over the ingluviotomy incision with the same antimicrobial-impregnated suture material. The bird made an uneventful recovery from anesthesia and, pending laboratory results, was discharged the following day. On the basis of the bird's body condition and malnutrition status during hospitalization, the animal was supplemented with a pediatric multivitamin supplementn (vitamin A concentration, 2,000 U/kg [909 U/lb], PO) every 24 hours. Initial treatments of meloxicamo (0.5 mg/kg [0.23 mg/lb], PO) every 12 hours and trimethoprim-sulfamethoxazolep (40 mg/kg [18.18 mg/lb], PO) every 12 hours were also started.

Figure 5—
Figure 5—

Endoscopic image of the proventriculus of the bird in Figure 1. Notice the numerous botryoid vesicle-like structures.

Citation: Journal of the American Veterinary Medical Association 242, 8; 10.2460/javma.242.8.1122

Cytologic evaluation of the saline solution in which the endoscopic biopsy specimens had been submitted revealed no etiologic agents. There was a small quantity of extracellular, refractile, and linear material of unknown origin in the background, but it was nondiagnostic. The biopsy specimens from the proventriculus consisted of large amounts of amorphous basophilic material (mucus), clusters of epithelial cells admixed with few randomly scattered lymphocytes and plasma cells, and partial longitudinal sections of nematodes. The nematodes were characterized by a thick cuticle with cross striations, coelomyarian musculature, and relatively large intestines. The sections were tangential, so it was difficult to accurately determine whether a particular nematode was likely in a larval or subadult stage. However, because of the lack of reproductive structures seen, the nematodes were most likely in the larval stage and this was the reason eggs were not seen in the sections (Figure 6). Following the identification of nematodes, a repeated fecal sample was collected and submitted for more specialized evaluation. One gram of feces was mixed with a small amount of Sheather sugar solution (specific gravity, 1.27 to 1.30). The mixture was then strained through a layer of cheesecloth and added to a 15-mL conical test tube. The test tube was filled to the top with Sheather sugar solution. A coverslip was added, and the test tube was centrifuged for 10 minutes at 280 × g. The coverslip was placed on a slide, and individual eggs were counted at 10× power. The initial fecal test revealed 257 spiurid eggs/g of feces.

Figure 6—
Figure 6—

Photomicrographs of spirurid nematodes. A—Partial longitudinal section of 2 spirurid nematodes surrounded by mucus and inflammatory cells. The undulating cuticle, coelomyarian musculature, and relatively large intestines are apparent. H&E stain; bar = 500 μm. B—Spiruid nematode egg; bar = 20 μm.

Citation: Journal of the American Veterinary Medical Association 242, 8; 10.2460/javma.242.8.1122

Treatment with fenbendazoleq was initiated for 20 days (15 mg/kg [6.8 mg/lb], PO, q 24 h), alternating between 5 days of treatment and 5 days of no treatment. A second fecal evaluation 3 weeks after cessation of treatment revealed a decrease in fecal egg counts from 257 to 12 eggs/g. The same treatment protocol was continued for another 20 days, and at the end of treatment, no eggs were seen on fecal examination.

The cockatoo was reexamined 4 months after initial examination and 6 weeks after the last treatment. At this time, weight was recorded as 558 g (1.3 lb). The owner reported that the bird had returned to normal appetite, vocalization, and behavior. Gastroscopy with a flexible gastroscoper and workstations revealed a normal proventriculus and ventriculus without any evidence of the parasitic cysts (Figure 7). However, there was some mucosal scarring over 1 area of the proventriculus. The ventriculus appeared normal.

Figure 7—
Figure 7—

Images obtained by use of a flexible endoscope of the proventriculus (p) and ventriculus (v) of the bird in Figure 1 after treatment with fenbedazole. Note the areas of mild mucosal scarring (black arrowheads).

Citation: Journal of the American Veterinary Medical Association 242, 8; 10.2460/javma.242.8.1122

Given the bird's regular access to an outside aviary and arthropods, anthelmintic treatment was continued with ivermectint (0.4 mg/kg [0.18 mg/lb], PO) monthly in an attempt to prevent reinfection. Spirurids have an indirect life cycle that includes a ground-living arthropod intermediate host, so the importance of maintaining a hygienic environment was stressed to the client. The bird was most recently reexamined by the referring veterinarian 22 months after the initial examination. At that time it weighed 449g (1.0 lb) and continued to receive ivermectin prophylaxis. Twenty-seven months after the initial diagnosis, the bird appeared healthy and in good body condition, as reported by the owner.

Discussion

Although proventricular nematodiasis has been reported in various avian species, most cases are associated with high morbidity and mortality rates and diagnosed after death.5–7 Nematodes known to infect the proventriculus of birds include spirurids (Geopetita spp, Dispharynx spp, Habronema spp, and Tetrameridae). To our knowledge, this is the first report detailing the antemortem diagnosis and successful treatment of spiruridiasis in a psittacine. Fatal infections of Synhimantus (Dispharynx) nasuta have been reported in 2 of 5 African jacanas (Actophilornis africana).8 In wrinkled hornbills (Aceros corrugatus) with proventricular nematode infection, there were no eggs seen in the feces, nodules were seen in the proventriculus, and adult female nematodes were present within the primary and secondary glands of the proventriculus.5 In the biopsy tissue examined in this cockatoo, we were unable to determine the exact location of the nematodes within the proventricular mucosa because the sections of tissue were very small and did not include the full thickness of the mucosa. Additionally, in the cockatoo of the present report, the species of spirurid was not identified because a whole adult was not retrieved from the proventriculus. Results of histologic examination were highly suggestive of spirurid infection,9 and this was confirmed by fecal testing.

Spirurid nematodes have an indirect life cycle requiring an arthropod intermediate host such as a cockroach (Blattodea), grasshopper (Orthoptera), or crustacean (Crustacea).5 Avian species appear to react differently to nematodiasis, with some having no clinical signs, others developing clinical signs, and some dying acutely.10 Clinical signs range from lethargy, diarrhea, and decreased appetite to more severe signs such as proventricular ulceration, mucosal proliferation, anemia, and adenomatous proliferative proventriculitis.6,11,12

Gastric lavage and fecal examination can help to identify spirurid eggs and adult worms but are not always reliable.8,11 Fecal eggs can be intermittently shed, which can lead to false-negative results on fecal examination, as in this case. Sodium nitrate is not an appropriate flotation medium for spirurid eggs because the specific gravity of the solution is too low (1.18 to 1.12) to reliably float them.4 Specific gravity of at least 1.25 is recommended for spirurid eggs.4 They often need to be identified by a direct smear or sedimentation techniques, such as the one described.

Aviary design should include efforts to decrease parasite exposure and break the life cycle of nematodes. Grass and dirt floors should be avoided; concrete or gravel substrate allow for easier cleaning, making intermediate hosts and eggs unlikely to remain accessible to hosts.11 This case also indicates that proventricular nematodiasis is another differential diagnosis for proventricular dilatation in psittacines.

a.

Seed mixture, Central Garden & Pet, Kaytee Products Inc, Chilton, Wis.

b.

Harrison's Bird Foods, HBD International Inc, Brentwood, Tenn.

c.

Baytril, Shawnee Mission, Kan.

d.

IsoFlo, Abbott Laboratories, North Chicago, Ill.

e.

Siemens Digital Radiography, Eklin Medical Systems Inc, Santa Clara, Calif.

f.

ATL HDI 5000, Philips, Amsterdam, The Netherlands.

g.

Sono CT, Universal Diagnostic Solutions, Oceanside, Calif.

h.

Omnipaque, GE Healthcare Inc, Princeton, NJ.

i.

Sireskop 5, Siemens, Santa Clara, Calif.

j.

64018BSA, autoclavable Hopkins rigid telescope, 2.7 mm × 18-cm working length, 300, Karl Storz Veterinary Endoscopy America Inc, Goleta, Calif.

k.

67065C, operating sheath for 64018BSA telescope, 14.5F outer diameter, Karl Storz Veterinary Endoscopy America Inc, Goleta, Calif.

l.

6716Z, flexible biopsy forceps, 5F × 34 cm, Karl Storz Veterinary Endoscopy America Inc, Goleta, Calif.

m.

Monocryl Plus Suture, Johnson & Johnson Medical Ltd, Livingston, West Lothian, Scotland.

n.

Enfamil Poly-Vi-Sol (without iron), Mead Johnson Nutritionals, Evansville, Ind.

o.

Metacam, Boehringer Ingelhelm Vetmedica Inc, St Joseph, Mo.

p.

Trimethoprim-sulfamethoxazole, Hi-Tech Pharmacal Co Inc, Amityville, NY.

q.

Panacur, Intervet/Shering-Plough Animal Health, Millsboro, Del.

r.

5.9-mm × 1-m gastroscope with 2-mm channel (GIF XP160), Olympus, Shinjuku, Tokyo, Japan.

s.

WM-N60 Workstation, Olympus, Shinjuku, Tokyo, Japan.

t.

Ivomec, Merial Ltd, Duluth, Ga.

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