Anatomy and Physiology of the Avian Lower Gastrointestinal Tract

Stomach

The stomach contains a cranial, glandular portion (proventriculus) and a muscular, caudal portion (ventriculus or gizzard). The anatomic region between the two portions is termed the intermediate zone or isthmus. Carnivorous birds have thin-walled, saclike stomachs with an intermediate zone that is difficult to distinguish on external exam. Insectivores, herbivores, and granivores have a ventriculus which is very muscular and well developed. Specifically, their ventriculus is composed of 4 major muscle groups: two thick muscles (caudodorsal and cranioventral) and two thin muscles (caudoventral and craniodorsal). These muscles perform crushing and rotatory movements that help with mechanical digestion of food. The mucosal surface of the ventriculus is covered by a koilin layer (cuticle) which is a carbohydrate-protein complex that may be brown, green, or yellow in color (due to regurgitation of bile pigments from the duodenum).⁷

In general, the psittacine gastric cycle can be divided into six phases: peristaltic wave of the proventriculus, closure of the isthmus, horizontal contraction of the ventricular thin muscles, vertical contraction of the ventricular thick muscles, ejection in the duodenum, and opening of the isthmus. Occasionally, reflux from the ventriculus into the proventriculus can occur at the end of a gastric cycle when the isthmus opens. Retroperistalsis is commonplace in avian digestion, particularly in the colon and rectum as well as reflux from the duodenum into the ventriculus. A contrast fluoroscopic study in awake Hispaniolan Amazon parrots has described this process in detail and reported normal gastrointestinal (GI) tract measurements and transit times in this species.² The sequence is much less complicated in carnivorous birds of prey, but also includes egestion of non-digestible items. In great horned owls, gastric digestion occurs in 4 phases: filling of the stomach, chemical digestion (4–8 hours), fluid evacuation (1–2 hours of slowing increasing gastric contractions), and pellet egestion (high frequency contractions in ventriculus for 4–10 minutes, followed by antiperistalsis of the esophagus, and pellet egestion). Pellets of owls contain hair and bones, while those of hawks contain predominantly hair due to the lower stomach pH of birds in the Falconidae and Accipitridae families. Owls also egest approximately one pellet per meal, whereas hawks and falcons tend to egest one pellet per 2–3 meals.⁹

Small Intestines

In most species, the duodenal loop is located to the right of the ventriculus with a proximal descending portion, a distal ascending portion, and the pancreas located between the two limbs. The jejunum and ileum are arranged in several U-shaped loops in the right side of the coelom. The remnant of the yolk sac and yolk duct (Meckel's diverticulum) is located between the jejunum and ileum and is contained in the axial intestinal loop. The supraduodenal loop is the most distal loop of the ileum, but in some species (pelicans, falcons, hawks, and penguins) there is an additional supracecal loop, which is located in the distal ileum, proximal to the ileorectal junction.⁷ The intestinal villi in carnivorous birds are more developed than those in noncarnivorous birds, which help to compensate for the shorter length of their small intestines.

Large Intestine and Cloaca

Paired ceca and a short segment of intestine, equivalent to the mammalian rectum, comprise the avian large intestine. The avian ceca are classified into four types: intestinal, glandular, lymphoid, and vestigial. Psittacines, passerines, and columbiformes have very reduced, vestigial ceca. Accipitriforms and falconiformes have small, lymphoid ceca, but owls have very large, glandular ceca, which are thought to play a role in water balance. Cecal contents are passed separately from and less frequently than normal feces. They are usually softer in consistency, dark in color, and voluminous. The actual rectum in birds is short and extends from the ileocecal junction to the coprodeum of the cloaca. As stated earlier, antiperistalsis occurs between the cloaca and rectum, where water and sodium chloride are absorbed prior to defecation. The cloaca has three compartments (coprodeum, urodeum, proctodeum), separated by two mucosal folds (coprourodeal fold and uroprotodeal fold). The cloacal bursa is a lymphoid organ unique to birds and is located in a dorsal diverticulum of the proctodeum. It reaches maximum size just before sexual maturity, and involution usually occurs at about 2–3 months of age. The bursa is the site of differentiation of immunologically competent bursal (B) lymphocytes.⁹

Proventricular and Ventricular Diseases

Proventricular Dilation Disease (PDD)

Proventricular dilation disease (PDD), or neuropathic ganglioneuritis, was historically referred to as macaw wasting disease and was first reported in the late 1970s. Since that time, it has been identified in over 50 avian species including psittacines, passerines, honeycreepers, weaver finches, waterfowl, toucans, and birds of prey. In 2008, avian bornavirus was discovered and identified as the causative agent of PDD. However, avian bornavirus has not been confirmed as the one and only cause of this syndrome. This RNA virus is shed intermittently in the feces, and transmission is usually fecal-oral (vertical transmission has also been proven). The incubation period is still unknown, and appears to be anywhere from days to decades. There are 10 known viral genotypes, and seven of them are known to infect psittacines. Virulence varies amongst these genotypes and they are not cross-protective. The host mounts an inappropriate immune response, which causes progressive destruction of brain, spinal cord, and peripheral nerves. The nerves that supply the GI tract (proventriculus, ventriculus, and intestines) are most commonly affected. Progression of disease is also variable and can range from days to years. Gastrointestinal and neurologic signs are most common - one or both can be noted within a patient.

Definitive diagnosis of PDD is very challenging, as some birds that test positive for the virus do not develop clinical disease, and some that test negative will become acutely ill, while only testing positive during the terminal stages of the disease. Current diagnostic options include PCR (on feces, feathers, and blood), serology, antiganglioside antibodies, and histologic evaluation of a crop biopsy. Recommendations for antemortem diagnostics from the Schubot Exotic Bird Health Center at Texas A&M University include a combination of cloacal or feather RT-PCR in combination with a serologic assay. Also, they consider a bird negative for disease after three negative PCR results. They strongly recommend to determine the genotype of bornavirus-positive birds and keep birds infected with different genotypes separate. It is impossible to predict if individual birds housed with a positive bird will become bornavirus-positive and/or clinically ill. It is not currently recommended to automatically euthanatize positive birds, as many have remained clinically healthy for years. Treatment with COX-2 inhibitors (such as meloxicam or celecoxib) have been proposed, but no clinical trials to examine efficacy for PDD exist.

Avian Gastric Yeast (AGY)

The causative agent, Macrorhabdus ornithogaster, is an ascomycetes yeast that grows at the isthmus (junction of the proventriculus and ventriculus) in birds. There is a large host range amongst avian species, including psittacines, passerines, poultry, and several others - both wild and captive. Amongst psittacines, budgerigars, lovebirds, and cockatiels are the most commonly infected. Canaries, zebra finches, and Gouldian finches are the most commonly infected passerine species. Vomiting, diarrhea, and chronic weight loss are the most commonly reported clinical signs, and AGY should be considered as a differential for any psittacine presented with GI tract signs. This yeast infection can affect birds of any age, but disease in budgerigars occurs most frequently in middle-aged birds. Antemortem diagnosis is best done via direct, wet mount of feces with saline using 40x magnification. Alternatively, a fecal smear can be stained with Gram stain, quick stain, or a fecal PCR can be performed. Avian gastric yeast organisms are long, straight rods with rounded ends which range in length from 20–80 µm and 2–3 µm in diameter. Not all infected birds shed the organism consistently; however, if the bird has clinical signs, the likelihood of shedding increases. There are several published treatments for AGY, but no clinically controlled studies have been performed to determine safety and efficacy. Amphotericin B (25–100 mg/kg PO BID x 14–30 days) is the most commonly prescribed treatment.¹⁰

Cryptosporidiosis

A recent retrospective study examined the prevalence of gastrointestinal cryptosporidiosis in captive psittacine birds in the US.¹¹ There are three main Cryptosporidium species which affect birds, including C. meleagridis, C. baileyi, and C. galli. The first two primarily infect the small and large intestine, whereas the third, C. galli, mainly affects the proventriculus. Avian cryptosporidiosis is often a secondary, opportunistic disease. In this retrospective study, approximately 50% of all cases had another primary cause of death, and most lesions were confined to the proventriculus and ventriculus. Lovebirds were the most common species seen, and a majority had chronic GI signs prior to death. Two birds had contrast radiographs performed which demonstrated thickened proventricular walls and a dilated proventriculus. Only three birds had intestinal cryptosporidiosis without a gastric component.

Heavy Metal Toxicosis

Gastrointestinal signs of zinc and lead toxicosis include regurgitation secondary to crop stasis/dilatation. Ulcerations in the gastrointestinal tract can also cause gastritis and possible perforation of the ventriculus. Tentative diagnosis of heavy metal toxicity can be made based on the presence of metallic objects in the GI tract on a radiograph and concurrent clinical signs. Definitive diagnosis requires blood testing of lead and zinc levels - lead levels greater than 0.2 ppm and zinc levels above 2 ppm confirm toxicosis. Treatment involves removal of the metallic objects, if possible, and chelation therapy. In smaller birds, physical removal of metallic objects is often not possible. A study performed in budgerigars reviewed several treatment protocols that have been recommended to aid natural passage of foreign material (including metallic objects). These protocols included psyllium with grit, acidic drinking water, fine grit, coarse grit, and cathartic emollients (peanut butter and mineral oil). Of these protocols, treatment with either fine or large grit were the most effective in hastening the passage of metallic foreign objects from the ventriculus of budgerigars.⁸ Additional treatment with either oral (dimercaptosuccinic acid [DMSA], D-penicillamine) or parental (CaEDTA) chelators is also recommended. Oral chelators are contraindicated in birds that are regurgitating.⁶

Obstruction

Just like in other species, gastrointestinal obstructions can occur in avian species which ingest foreign substances. A recent case report described a perforating ventricular metallic foreign body in a 4-year-old umbrella cockatoo that was surgically removed. Ventriculotomy has been previously associated with high postoperative complications including leakage from the surgical site, localized infection, and coelomitis. No omentum is present in avian species, precluding its use as a surgical "patch" over the ventriculotomy site. A porcine collagen patch has been previously evaluated for enhancing ventriculotomy healing using Japanese quail as experimental models. Unfortunately, the patch did not enhance wound healing - instead it had quite the opposite effect, contributing to leakage at the incision site due to xenograft rejection.⁵ In addition, regardless of the technique used in that study, there were significant adhesions present postoperatively in the coelomic cavity. A newer study examined ventriculotomy closures with and without the use of a coelomic fat patch in Japanese quail. Birds with the coelomic fat patch had significantly greater serosal inflammation at necropsy; therefore, this technique is not recommended in quail.¹⁷

Neoplasia

Tumors of the proventriculus and ventriculus are rare in psittacines; however, the isthmus between the two gastric components is more commonly affected. Clinical signs of gastric neoplasia are nonspecific and include anorexia, regurgitation, weight loss, passage of undigested seeds, and possibly melena. Diagnosis can be made via contrast radiography or GI endoscopy, depending on patient size. Surgical excision is challenging (see above), and the prognosis is considered poor.⁶

Small and Large Intestinal Diseases

Mycobacteriosis

Mycobacteriosis affects a variety of avian species including domestic poultry, psittacines, and free-living and captive wild birds. The most common isolate is Mycobacterium avium subsp. avium, but over 10 other species have been known to infect birds including non-tuberculosis (M. genavense, M. intracellulare) and tuberculosis mycobacteria (M. bovis, M. tuberculosis, M. africanum). The primary route of infection is oral, as most lesions are found in the intestine and liver. With progression of disease, nodules (not the classic tubercles as seen in mammals) can be found in bone marrow, lungs, air sacs, gonads, and other organs.¹⁶ The most common clinical sign is chronic weight loss, and mycobacteriosis should be a differential for any bird with chronic weight loss, an inflammatory leukogram, and hepato/splenomegaly.³

Antemortem diagnosis of mycobacteriosis is challenging - histopathology, culture, or PCR techniques are the preferred methods, but there are disadvantages to each. In naturally infected ring-neck doves, more endoscopic splenic biopsies contained acid-fast organisms than liver biopsies, and liver biopsy alone could not rule out infection.¹³ The authors also found that taking multiple biopsies increased the likelihood of diagnosis of mycobacteriosis. Many practitioners used to rely on acid-fast stains of feces for diagnosis, but this has been shown to have a very low sensitivity (~ 7%) due to inconsistent shedding of the organisms.¹⁸ A recent study examined a nested PCR for antemortem diagnosis of Mycobacterium in Amazon parrots and found that particular PCR was specific, faster, and more sensitive than acid-fast stains, culture, and regular PCR.¹ Various treatment protocols have been proposed; however, no published clinical studies have demonstrated treatment success in any avian species. A recent uncontrolled clinical study evaluated the use of azithromycin, rifampin, and ethambutol for treatment of 16 naturally infected ring-neck doves with Mycobacterium avium subsp. avium for 180 days. Five birds died during treatment (all confirmed positive for mycobacteriosis on necropsy), and of the remaining birds, 81% had evidence of infection and disease at the end of the treatment period. Toxicity associated with drug therapy was not noted, but this protocol was deemed to have poor efficacy for treatment of mycobacteriosis.¹⁴

Enteritis/Intestinal Disease

Common causes of enteritis in psittacine birds include Clostridium and Campylobacter species. Diagnosis is made through fecal cytology and/or isolation of those organisms on fecal culture.⁶ A recent publication described an outbreak of E. coli in a colony of captive budgerigars with increased mortality, and hepatitis and enteritis noted on necropsy.¹⁵ Other factors that contributed to mortality included environment, nutrition, and concomitant pathogens. Antibiotics were not included in their treatment plan; instead, husbandry changes were implemented (cleaning protocols and alterations to the physical structure of the aviary), their diet was changed to decrease the amount of seeds (millet) offered, and a probiotic was added to the feed. Columbid herpesvirus-1 and adenoviral infections can also lead to hepatitis and enteritis in raptors. Clinical signs of both infections include anorexia, regurgitation, and possibly diarrhea.⁹ A recent case report described an intestinal obstruction secondary to ileocecorectal intussusception, confirmed via coelioscopy, in a 23-year-old male tawny eagle.¹² Surgical resection and intestinal anastomosis were performed, but intestinal adhesions formed postoperatively, which resulted in another partial luminal stricture and required a second surgical procedure. Ultimately, the eagle had a complete recovery and was asymptomatic 2 years after surgery.

Cloacal Diseases

Cloacal prolapse may involve the oviduct, ureters, intestines, or coprodeum. Prolapses occur secondary to egg laying, excessive sexual/masturbating behavior, constipation/tenesmus, or idiopathic/behavioral (especially in cockatoos). Cloacitis, cloacaliths, severe enteritis, or GI obstruction have all been documented as causes for cloacal prolapse secondary to tenesmus. Ideally, the primary cause of the cloacal prolapse should be identified and corrected in addition to replacement of the cloacal tissue (if still viable). Two lateral vent sutures can be placed to help maintain the cloacal tissue in the proper position, but recurrent prolapses may require more permanent surgical fixation including ventplasty, cloacopexy, or salpingectomy (if the oviduct is affected). Papillomatosis also affects the cloaca, but is due to a herpesvirus infection rather than papillomavirus. Presumptive diagnosis is made by placing acetic acid on the lesions, which will blanch the tissue in cases of papillomatosis. Definitive diagnosis requires a surgical biopsy and histopathology. Recurrence is common following surgical removal. Many practitioners perform fecal Gram staining as part of routine physical examinations to assess general health. A recent publication examined the level of agreement between fecal and cloacal Gram staining and fecal aerobic bacterial cultures in Hispaniolan Amazon parrots.⁴ Most of the bacteria on the Gram stain were Gram-positive, and Gram-negative organisms were identified in ~33% of samples. Agreement between culture and Gram stain was fair, and there was a tendency for culture to underestimate the true diversity of bacterial flora.

References

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2.  Beaufrere H, Nevarez J, Taylor WM, Jankowski G, Rademacher N, Gaschen L, Pariaut R, Tully TN. Fluoroscopic study of the normal gastrointestinal motility and measurements in the Hispaniolan Amazon parrot (Amazona ventralis). Vet Radiol Ultrasound. 2010;51:441–446.

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4.  Evans EE, Mitchell MA, Whittington JK, Roy A, Tully TN. Measuring the level of agreement between cloacal Gram's stains and bacterial cultures in Hispaniolan Amazon parrots (Amazona ventralis). J Avian Med Surg. 2014;28:290–296.

5.  Ferrell S, Werner J, Kyles A, Lowenstine L, Kass P, Tell L. Evaluation of a collagen patch as a method of enhancing ventriculotomy healing in Japanese quail (Coturnix coturnix japonica). Vet Surg. 2003;32:103–112.

6.  Hadley TL. Disorders of the psittacine gastrointestinal tract. Vet Clin North Am Exot Anim Pract. 2005;8:329–349.

7.  King A, McLelland J. Digestive system. In: King A, McLelland J, eds. Birds, Their Structure and Function. East Sussex, UK: Billiere Tindall; 1984: 84–109.

8.  Lupu C, Robins S. Comparison of treatment protocols for removing metallic foreign objects from the ventriculus of budgerigars (Melopsittacus undulatus). J Avian Med Surg. 2009;23:186–193.

9.  Murray M. Raptor gastroenterology. Vet Clin North Am Exot Anim Pract. 2014;17:211–234.

10. Phalen DN. Update on the diagnosis and management of Macrorhabdus ornithogaster (formerly Megabacteria) in avian patients. Vet Clin North Am Exot Anim Pract. 2014;17:203–210.

11. Ravich ML, Reavill DR, Hess L, Childress AL, Wellehan JF. Gastrointestinal cryptosporidiosis in captive psittacine birds in the United States: a case review. J Avian Med Surg. 2014;28:297–303.

12. Sabater M, Huynh M, Forbes N. Ileo-ceco-rectal intussusception requiring intestinal resection and anastomosis in a tawny eagle (Aquila rapax). J Avian Med Surg. 2015;29:63–68.

13. Saggese MD, Tizard I, Phalen DN. Comparison of sampling methods, culture, acid-fast stain, and polymerase chain reaction assay for the diagnosis of mycobacteriosis in ring-neck doves (Streptopelia risoria). J Avian Med Surg. 2010;24:263–271.

14. Saggese MD, Tizard I, Gray P, Phalen DN. Evaluation of multidrug therapy with azithromycin, rifampin, and ethambutol for the treatment of Mycobacterium avium subsp. avium in ring-neck doves (Streptopelia risoria): an uncontrolled clinical study. J Avian Med Surg. 2014;28:280–289.

15. Seeley KE, Baitchman E, Bartlett S, DebRoy C, Garner MM. Investigation and control of an attaching and effacing Escherichia coli outbreak in a colong of captive budgerigars (Melopsittacus undulatus). J Zoo Wildl Med. 2014;45:875–882.

16. Shivaprasad H, Palmieri C. Pathology of mycobacteriosis in birds. Vet Clin North Am Exot Anim Pract. 2012;15:41–55.

17. Simova-Curd S, Foldenauer U, Guerrero T, Hatt JM, Hoop R. Comparison of ventriculotomy closure with and without a coelomic fat patch in Japanese quail (Coturnix coturnix japonica). J Avian Med Surg. 2013;27:7–13.

18. Tell LA, Leutenegger CM, Larsen RS, Agnew DW, Keener L, Needham ML, Rideout BA. Real-time polymerase chain reaction testing for the detection of Mycobacterium genavense and Mycobacterium avium complex species in avian samples. Avian Dis. 2003;47:1406–1415.