Avian Medicine: Princilpes and Applicationavianmedicine.net/wp-content/uploads/2013/03/19.pdftect Histomonas meleagridis, Hexamita spp., Giardia intestinalis, Cochlosoma sp. and Chi-lomastix

iseases of the alimentary tract occur fre-quently in birds. Nonspecific clinical signsof gastrointestinal diseases may includeanorexia, dysphagia, regurgitation, vomit-

ing, constipation, diarrhea and tenesmus. Withpolyuria, the feces are normal and are surrounded bya large volume of clear fluid, while with diarrhea thefeces are abnormal (see Color 8). The compositionand quality of food and ingestion of bedding material,poisonous plants or chemicals may influence gastro-intestinal signs. Weight loss and generalized weak-ness are characteristic of chronic diseases.

Fecal evaluation, hematology, blood chemistry, radiol-ogy and esophago-ingluvio-(gastro)scopy or laparo-scopy are considered indispensable diagnostic tools inavian gastroenterology. Diseases that may affect thegastrointestinal system are listed in Table 19.1.

Cytologic examination of a fresh ingluvial aspirate isbest for detecting flagellates (Trichomonas spp.). Ex-amination of freshly voided feces is essential to de-t e c t Histomonas meleagridis, Hexamita sp p . ,Giardia intestinalis, Cochlosoma sp . an d Chi-lomastix gallinarum. Direct microscopic examina-tion of feces may reveal helminthic ova and protozoaloocysts. Flotation and sedimentation techniques arebest for detecting the low number of eggs or oocyststhat occur in an early parasitic infection (see Chapter36). Parasites infecting the liver, kidney, uterus andpancreas can deposit ova or oocysts that can be de-tected in the feces. Parasite ova originating from therespiratory tract may be coughed up, swallowed andfound in the excrement.28,78

DC H A P T E R

19GASTRO-

ENTEROLOGY

J. T. Lumeij

TABLE 19.1 Differential Diagnosis of Clinical Signs Associated with the Gastrointestinal Tract

Regurgitation or Vomiting in AdultsIatrogenic - apomorphine, levamisole, trimethoprim/sulfadiazine(macaws), ketoconazole, doxycycline suspension (particularlymacaws and Amazons)

Fear and excitement (vultures, pelicans, penguins)

Courtship behavior (male psittacines)

Crop milk feeding in pigeons

Physiological cast formation - (raptors)

Goiter (particularly budgerigars)

Callus formation after coracoid fracture

Neuropathic gastric dilatation (NGD)

Food allergies

Motion sickness

Viral diseases - looping ill virus, Pacheco’s disease virus, pigeonherpesvirus, avian polyomavirus, avian viral serositis (togavirus),poxvirus (diphtheritic form)

Bacterial diseases - megabacterial infection, most Enterobacte-riaceae, Pasteurella, Serratia

Mycotic diseases - candidiasis, aspergillosis

Helminths (oropharynx/ingluvies/esophagus) - capillariasis, ser-ratospiciliasis

Protozoal disease - trichomoniasis of upper digestive tract, Plas-modium (penguins, gyrfalcon)

Poisoning - alcohol, arsenic, copper, lead, organochlorine (lin-dane), organophosphate, carbamate, organomercurial, ro-tenone, phosphorus, polytetrafluoroethylene (Teflon), sodiumchloride, thallium, zinc

Plants - Yew (Taxus baccata), Philodendron spp., Rhododen-dron spp. (azalea), Solanaceae (green berries and roots)

Obstructed alimentary tract - stricture, foreign body, neoplasia,intussusception, volvulus, hernia, stenosis, parasites, impaction,paralytic ileus

Organopathy - renal disease, hepatopathy, pancreatitis, peritoni-tis, egg binding, electrolyte disturbances

Regurgitation in Neonatal Psittacines (Sour Crop)Overgrowth of bacteria oryeast (improper food storage)

Overheated formula

Underheated formula

Crop burns

Foreign body ingestion(eg, substrates)

Improper formula consistency

Over-stretching the crop

Aerophagia

Fear and excitement

Infectious agents Avian polyomavirus Avian viral serositis Candida spp. Gas-producing bacteria

Diarrhea28,78

Use of antibiotics

Dietary changes

Bowel obstruction

Toxins

Obstruction

Foreign bodies

Organopathy - hepatopathy, renal disease, pancreatitis

Viral diseases - Newcastle disease virus, paramyxovirus type 3,influenza, adenovirus, astrovirus, calicivirus, coronavirus, en-terovirus, Pacheco’s disease virus, pigeon herpesvirus, duckvirus enteritis, herpesvirus (Ciconiidae), herpesvirus (gruiformes),Marek’s disease virus, orthoreovirus, parvovirus, reovirus, rota-virus, togavirus-like agent, retrovirus (leukosis/sarcoma group)

Bacterial diseases - borreliosis, spirochaetosis, most Enterobac-ter iaceae, Campylobacter spp. , Streptococcus spp. ,Erysipelothrix rhusiopathiae, Listeria monocytogenes, megabac-teria, Clostridium spp., Mycobacterium avium, Yersinia pseudo-tuberculosis, Aeromonas hydrophila, Pasteurella multocida, Pas-teurella anatipestifer (new duck disease)

Chlamydia

Mycoplasma

Candida albicans

Protozoa - Histomonas meleagridis, Hexamita spp., Giardia spp,,Cochlosoma sp., Chilomastix gallinarum, coccidiosis

Helminths - nematodes, trematodes, cestodes

HematocheziaCloacal papillomas ■ Aflatoxicosis

Egg laying ■ Coagulopathies

Ulcers ■ Heavy metal intoxication

Hepatitis ■ Foreign bodies

Infectious enteritis - bacterial, ■ Cloacal neoplasiasviral, parasitic

Passing Undigested FoodGastric foreign body ■ Pancreatitis

Gastrointestinal dysfunction ■ Use of antibiotics

Neuropathic gastric dilatation ■ Food allergies

Enteritis - bacterial, viral, ■ Hepatitisparasitic

TenesmusEgg-laying problems (binding) ■ Uterine prolapse

Abdominal mass ■ Rectal prolapse

Goose venereal disease ■ Enteritis - diarrhea

Cloacal pathology ■ Bacteria

Prolapse ■ Parasites

Papilloma ■ Fungi

Stricture ■ Viruses

Cloacolith ■ Toxins

Cloacitis ■ Decreased bacteria (eg, in-

Intestinal obstruction discriminate antibiotic use)

(eg, constipation)

CHAPTER 19 GASTROENTEROLOGY

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Bacteriologic cultures of the gastrointestinal tractmust be interpreted with respect to the normalflora.78 Gram-positive microorganisms including lac-tobacilli, staphylococci, streptococci and Bacillusspp. are common in the oropharynx of healthy psit-tacine birds. Mycoplasma spp. and Aspergillus spp.are sometimes encountered.168,176 Enterobacteriaceaeare normally not found in the feces of Psittaciformesand Passeriformes, where gram-positive organisms,especially Corynebacterium sp. and Bacillus sp., pre-dominate.17 The isolation of a large number of En-terobacteriaceae in pure culture from Psittaciformesor Passeriformes is suggestive of a primary or secon-dary infection. E. coli and other Enterobacteriaceaeare normal inhabitants of the gastrointestinal tractin Galliformes, Columbiformes, Falconiformes,Strigiformes and Corvidae.140

Routine bacteriologic examination of the feces mayfail to reveal some important microbes that can causediarrhea, including mycobacteria, campylobacterand chlamydia. A technique for identifying mycobac-teria is described in Table 19.2. Detection of campy-lobacter can be augmented by the use of Hemacolor;the bacteria appear S-shaped or in gull-wing form.Chlamydia is best detected using an antigen capturesystem.21,102

The Beak

Anatomy and Physiology

The avian beak is a continuously growing, dynamicstructure composed of bone, vascular layers, keratin,dermis, joints and a germinative layer. In psittacinebirds, the upper and lower jaws are connected to theskull via a kinetic joint. The keratinized sheath cov-ering the upper and lower beaks is called rhamphoth-eca and can be divided into the rhinotheca (maxillarykeratin) and the gnatotheca (mandibular keratin).

The median dorsal border of the rhinotheca is calledthe culmen, and the median ventral border of thegnatotheca is called the gonys. The cutting edges ofthe rhamphotheca are called the tomia. The rhino-theca is perforated by the paired nostrils. Avicultur-ists classify caged birds into hardbills (eg, most psit-tacine birds) and softbills (eg, mynahs, starlings).

In ducks and parrots, the tip of the bill contains welldeveloped mechanoreceptor nerve endings. The beakis used for prehension, for the physical preparationof food, and in some species such as parrots, forlocomotion.130

The rate of keratin replacement is strongly depend-ent on the use of the beak. In large parrots, thecomplete rhinotheca is replaced in about six months,while in toucans the rhinotheca grows approximately0.5 cm over a two-year period. The rate of growth ofthe gnatotheca is about two to three times fasterthan that of the rhinotheca.38 Shedding and replace-ment of the rhinotheca has been described in caper-caillie (annually)4 and Suriname finches.

Beak Diseases

A variety of congenital and acquired defects, includ-ing scissor beak and mandibular prognathism, caninterfere with normal beak function. In gallinaceousbirds, a deformed upper mandible has been associ-ated with embryonic deficiencies of folic acid, biotinor pantothenic acid. Crusty, scab-like lesions in thecorners of the mouth are considered a definite sign ofbiotin or pantothenic acid deficiency in these birds.5Examples of acquired lesions that can lead to malfor-mations or necrosis of the beak include punctures,lacerations, splits and avulsions. Traumatic frac-tures, especially of the mandible, occur frequently inpsittacine birds that get caught in hooks suspendedfrom the ceiling of their enclosures or as a result offighting.

Any bacterial, mycotic, viral or parasitic pathogenthat damages the germinative layers of the beak cancause developmental abnormalities.108 Examples in-clude Candida albicans, psittacine beak and featherdisease virus, Knemidokoptes spp. in Psittaciformesor Oxyspirura spp. in cranes. Rhinothecal over-growth in psittacines, especially budgerigars, hasbeen associated with liver disease (Figure 19.1).133

The rhinotheca may overgrow in hardbills main-tained in an indoor environment and provided softfoods. “Rubber bill,” caused by insufficient minerali-zation of the upper beak, has been described with

TABLE 19.2 Detection of Acid-fast Bacteria in Feces78

Combine 4 grams of feces and 12 ml of 15% sputofluol (Merck)

Gently mix for 30 minutes

Centrifuge for 5 minutes 10,000 rpm

Make smear of sediment

Stain with Ziehl-Neelsen

SECTION FOUR INTERNAL MEDICINE

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vitamin D and calcium deficiencies. Necrotic lesionsat the commissure of the beak have been describedwith trichotecene mycotoxicosis, avian poxvirus andtrichomoniasis (cockatiels).137

Beak deformation consisting of loss of normal epithe-lium on the surface of the beak, upturning of thetomia and shortening of the upper beak have beenreported secondary to photosensitization in ducksfollowing ingestion of seeds from Ammi visnaga, A.majus and the plant or seeds from Cynopterus wat-sonii and C. longipes.152 Photosensitization has beensuspected in many cases of vesicular dermatitis, butthe precise etiologic agents are frequently undeter-mined.

Chronic rhinitis may lead to permanent defects inthe adjoining germinative layer of the rhinotheca(Figure 19.2). Dysphagia, which may be recognizedclinically as an accumulation of food under thetongue, can be an indication of rhamphothecal dys-function.

The Oropharynxand Salivary Glands

Anatomy and Physiology49,101

Birds lack an oropharyngeal isthmus, and the oraland pharyngeal cavities are combined to form anoropharynx. The walls of the oropharynx containnumerous mucus-secreting salivary glands (Figure19.3). The palate contains a median fissure called thechoana, which connects the sinuses to the glottis.Just caudal to the choana is the infundibular cleft,which is the common opening of the auditory tubes.Tongue anatomy varies widely among avian species.Parrots have intrinsic muscles in the tongue, whileother birds have only extrinsic tongue muscles. Swal-lowing involves a rapid rostrocaudal movement of thetongue and the larynx, assisted by sticky saliva andcaudally directed papilla on the tongue, laryngealmound and palate. During swallowing, the choana,infundibular cleft and glottis are closed. The salivaryglands secrete mucus and, in some species, amylase.During the breeding season, the salivary gland ofswifts temporarily enlarges to produce an adhesiveliquid used in nest construction. The nests of some ofthe cave swiftlets of Southeast Asia are made entirelyof this edible secretion (birds’ nest soup). The GreyJay produces large quantities of mucus that areformed into boluses and stored on the sides of treesas a winter food supply. The mucosa of the oral cavity

FIG 19.1 A two-year-old budgerigar, maintained on an all-seeddiet in a strictly indoor environment, was presented for a beaktrim. The bird was obese and was passing bile-tinged urates. Thisclinical presentation is suggestive of a hepatopathy.

FIG 19.2 An eight-year-old Umbrella Cockatoo was presentedwith a nine-month history of progressive sneezing and nasal dis-charge. The feathers around the beak were moist from a serousnasal discharge. The rhinotheca had a deep groove that extendedfrom the nostril to the rostral commissure of the upper beak(arrows). The extent of this defect suggests that the germinativelayer of the rhinotheca had been involved in a disease process forover six months. This bird belonged to a heavy smoker. A mixedpopulation of gram-positive and gram-negative bacteria were cul-tured from a sinus aspirate. The bird responded to nasal flushing,systemic antibiotics, frequent exposure to fresh air and sunlightand being removed from a smoke-filled environment.


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in some passerine chicks is brightly colored, withdistinctive markings that disappear when the chickis weaned. These markings appear to stimulate theparents to feed the chick.

Oropharyngeal Diseases

Table 19.3 lists common upper gastrointestinal tractdiseases, the typical anatomic sites affected, thetypes of lesions induced and the common speciesaffected.

PoxvirusPoxvirus may cause proliferative caseous lesions(diphtheritic form) in the mouth and esophagus in avariety of avian species. Diagnosis can be achieved byidentifying elementary bodies (Bollinger bodies) inimpression smears prepared from lesions andstained with Wright’s stain or by the Gimenezmethod. Trichomoniasis lesions may have a similargross appearance.

Pigeon Herpesvirus Infection (Smadel’s Disease)Pigeon herpesvirus (PHV) infection has been associ-ated with pharyngeal and esophageal diphtheriticmembranes, which are attached to the underlyingtissues. Lesions are most severe when secondarilyinfected with Trichomonas spp.105 Other clinical signsinclude dyspnea, mucopurulent rhinitis and conjunc-tivitis. Histologic identification of basophilic and eos-inophilic intranuclear inclusion bodies is suggestive.

GranulomasGranulomas caused by Mycobacterium spp. or otherbacterial or fungal agents frequently occur in the oralcavity. A diagnosis can be made by staining suspectedmaterial with the Gram’s or Ziehl-Neelsen methods(see Table 19.2).50,71,202 Surgical removal in conjunc-tion with appropriate antimicrobial agents is usuallyeffective in resolving non-mycobacterial-inducedgranulomas. A case of malignant fibrohistiosarcomalocated on the tip of the tongue in a seven-year-oldBrown-throated Conure was successfully removed byradiosurgery.

NematodesVarious Capillaria spp. may infect the mucosa of thetongue, pharynx, esophagus and ingluvies of Falconi-formes, Psittaciformes, Galliformes, Passeriformesand Anseriformes.78,91,174 Characteristic lesions in-clude hemorrhagic inflammation in the commissureof the beak and diphtheritic membranes in the phar-ynx and tongue. Parasites can be found embedded ininflammatory material. Typical bipolar eggs may befound in esophageal smears or ingluvial washings. InStrigiformes, Synhimanthus (Dispharynx) falconishas been reported in the oropharynx.109

Spirurid infections have been reported in diurnal andnocturnal birds of prey. Lesions containing the adultnematodes can be found in the mouth, esophagus andcrop. The embryonated eggs are thick-walled. As-carides belonging to the genus Contracaecum havebeen found in fish-eating birds, and severe infectionsof the oral cavity have been documented in youngPelecanidae. In birds of prey, Seratospiculum amacu-

FIG 19.3 Anatomy of the oral cavity of an Umbrella Cockatoo. Thedepressor mandibulae muscles (arrows) have been transected bi-laterally to allow the jaws to be opened, revealing the 1) upperbeak, 2) openings of the seromucous glands, 3) choana, 4) rimainfundibuli, 5) esophagus, 6) rima glottis, 7) salivary orifice, 8)tongue, 9) lower beak. Abscesses occur in multiple locations includ-ing a) perichoanal, b) pharyngeal, c) periglottal, d) lingual, e)lateral-ventral lingual and f) sublingual tissues.


486

latum can cause lesions that resemble those of oraltrichomoniasis.212 The adult worms are found in theair sacs. Eggs may be found in the oral mucus orfeces.

Hypovitaminosis AIn psittacine birds, a typical clinical sign of hypovi-taminosis A is metaplasia of the submandibular orlingual salivary glands and clubbing of the choanalpapillae (see Color 8). Affected birds are usually fedall-seed diets with a large percentage of sunflowerseeds. Treatment should include parenteral vitaminA and the use of a formulated diet. Keratogenic cystsin the lingual salivary glands should be differenti-ated from lingual abscesses by biopsy.

Lesions associated with hypovitaminosis A in galli-naceous birds first appear in the pharynx and arelargely confined to the mucous glands and theirducts. The epithelium is replaced by a stratifiedsquamous epithelium that occludes the ducts of themucous glands, causing accumulations of secretionsand necrotic debris. Small, white, hyperkeratotic le-

sions (up to 2 mm in diameter) may be seen in thenasal passages, mouth, esophagus, pharynx andcrop.

Some authors suggest that hypovitaminosis A is un-likely in pigeons because these birds efficiently me-tabolize this vitamin.155,223 Other authors suggest hy-povitaminosis A frequently occurs in pigeons but it isseldom recognized because the histologic lesions arelimited to inflammation of the mucous glands.194 Asthe condition progresses, the duct systems fill withmasses of degenerate lymphoid and inflammatorycells, amorphous debris and mucus.

Sialoliths in PigeonsMucosal lesions that appear similar to those causedby hypovitaminosis A have been described on thepalate of pigeons and are referred to as sialoliths (seeColor 13).223 Sialoliths consisting of a proteinaceoussubstrate mixed with cellular debris are clinicallyrecognized in approximately one percent of pigeons.The etiology of sialoliths remains unknown. How-ever, based on their histologic, histochemical, chemi-

TABLE 19.3 Upper Gastrointestinal Tract Diseases22, 24, 51, 76, 191, 220, 221

Organism Location Lesion Type Species Susceptibility

Candida spp. Oral cavityEsophagus

Ulcerative, necrotic, diphtheritic Most species, particularly neonates,immunosuppressed animals

Duck enteritis virus Oral cavitySublingual salivary glands

Ulcerative Ducks

Herpesvirus Oropharynx, EsophagusProventriculus

Diphtheritic Owls

Lice(Piagetiella peralis)

Oral cavity Stomatitis Penguins

Leeches(Theromyzon spp.)

Nasal cavity, ConjunctivaOropharynx

Hyperemia at attachment site Anseriformes

Mycobacterium spp. Tongue, FrenulumHard palate

Granulomas Psittaciformes, FalconiformesGalliformes

Neoplasias All locations Masses, ulcerative Most species

Papillomas Oropharynx, EsophagusProventriculus

Masses Psittaciformes

Pigeon herpesvirus Pharynx, Esophagus Diphtheritic Pigeons

Poxvirus MouthEsophagus

Diphtheritic Galliformes, Psittaciformes,Passeriformes, Raptors,Columbiformes

Trematodes(Cathaemasia spp.Clinostomum spp.)

Oral cavity Stomatitis Ciconiiformes

Trichomoniasis Oral cavity, EsophagusCrop

UlcerativeProliferative

Raptors, Psittaciformes,Columbiformes, Passeriformes


487

cal and physical characteristics, they are not thoughtto be caused by hypovitaminosis A.223 An associationwith pigeon herpesvirus infection has been sug-gested and seems plausible.110,206,223

Foreign BodiesClinical signs of foreign bodies in the upper GI tractcan include respiratory distress, head shaking,scratching the head with the feet, dysphagia or ano-rexia. A thorough oropharyngeal examination andradiographs may reveal the foreign body.

A string looped around the base of the tongue andpassing down the esophagus has been associatedwith dysphagia and respiratory distress in gallina-ceous birds.71,151 The string tightens and cuts furtherinto the tongue with each swallowing movement,causing edema of the glottis. Ring-shaped foreignbodies (eg, tracheal rings of prey eaten by raptors)can become lodged around the tongue, causing avas-cular necrosis. Wooden, plastic or metal splinters

(originating from toys or enclosures) may lodge in themouth or esophagus of psittacine birds (Figure 19.4).Waterfowl frequently ingest baited fishhooks, whichcan be lodged anywhere in the upper or lower diges-tive tract. Fish bones may lodge in the pharynx orproximal part of the esophagus causing dysphagia.Plant hairs that lodge in the oral or esophageal mu-cosa can cause granulomas.

StomatitisStomatitis in birds has been associated with theconsumption of hot foods, ingestion of oil and inges-tion of caustic substances.51 Birds that chew on silvernitrate sticks may have extensive chemical burns ofthe oropharynx and crop.131 Use of bipolar radiosur-gery is superior to silver nitrate sticks for controllinghemorrhage of the beak and nails. Stomatitis mayoccur secondary to food accumulations caused bybeak deformities (eg, PBFD) (Figure 19.5). Beak ne-crosis has been described in pigeons and gallinaceous

FIG 19.4 A mature Umbrella Cockatoo was presented for evalu-ation of palatine beak necrosis. The bird’s feathers were in poorcondition, and the bird appeared to be hungry but would eatreluctantly. The referring veterinarian had diagnosed PBFD basedon the combination of beak necrosis and feather abnormalities. Onphysical examination, the defect in the palatine area of the beakappeared to contain a foreign body. Magnification indicated thatthe bird had a large wood splinter lodged in the occlusal surface ofthe upper beak. The splinter was removed and the wound wasdebrided and flushed. The bird’s appetite improved within severaldays of presentation, and it began to preen normally within a week.The bird was DNA probe-negative for PBFD virus and polyomavirus.

FIG 19.5 Palatine beak necrosis may occur in some birds withPBFD virus. Once a defect in the oral mucosa occurs, food mayaccumulate in the damaged tissues and create a nidus for secon-dary bacterial and fungal pathogens. In this Umbrella Cockatoo,the rhinotheca was completely necrotic and separated from theunderlying bone. The bird had relatively minor feather pathology.This bird was euthanatized.


488

birds fed a finely ground, high-gluten food. The grad-ual accumulation of fine particles of food along theinner edge of the lower beak leads to secondary infec-tion and necrosis of the beak. Feeding pelleted ra-tions prevents the problem. The tongue of turkeypoults fed a finely ground mash may be curled back-ward by an accumulation of food on the floor of themouth.151

Many trichotecenes, notably T2 toxin, can cause caus-tic injury to the alimentary mucosa. Yellow erosiveand exudative plaques with underlying ulcers lo-cated near the salivary duct openings on the palate,tongue and buccal floor are characteristic lesions.Thick crusts of exudate may accumulate along theanterior margin of the beak. Anorexia is probablycaused by the painful lesions in the beak.87,219

Spirillum pulli may cause stomatitis in chickens.127

The organism can be demonstrated cytologically infresh scrapings from diphtheritic lesions or salivaryglands. Experimental transmission occurs by inocu-lation of tissue suspensions and by direct contact.Moist, slick mucosal membranes have been describedin pheasants with Newcastle disease virus and inchronic cholera.

Lacerations of the TongueLacerations of the tongue have been encountered inpsittacine birds and may be due to mate-inducedtrauma, automutilation during the excitement phaseof post-anesthetic recovery or gnawing on sharp ob-jects. The tongue is highly vascular and bleeds pro-fusely if damaged. Anesthesia, magnification andradiocautery are usually necessary to control bleed-ing and repair the laceration.

Glossitis Gelatinosa CircumscriptaA gelatinous mass may be found on the dorsal aspectof the tongue in five- to twelve-week-old ducklingsand goslings. The precise etiology is undetermined,but a multi-deficient diet has been suggested.103

The Esophagus and Crop

Anatomy and Physiology31,49,101

The esophagus lies immediately under the skin andto the right of the trachea (see Color 13).16 The inter-nal surface of the esophagus is longitudinally folded,increasing its distensibility and allowing carnivorous

and piscivorous birds to consumelarge food items. From a clinical per-spective, the anatomy of the avianesophagus allows for easy introduc-tion of instruments or endoscopes forforeign body removal from theesophagus, crop and proventriculus.In most birds, the esophagus is di-vided by the crop or ingluvies (somebirds do not have a crop) into a cervi-cal and a thoracic component.

In Galliformes and Falconiformes,the crop forms a ventral enlarge-ment of the esophagus at the tho-racic inlet. In Psittaciformes, thecrop is stretched transversely acrossthe neck. In canaries and ducks, thecrop is absent, but there is a spindle-shaped swelling of the esophagus atthe thoracic inlet. In pigeons, theventral diverticulum of the esopha-gus that forms the crop is dividedinto two large lateral sacs. Theesophagus is lined with partly kerat-

FIG 19.6 The shape of the crop varies dramatically depending on the species and theamount and shape of the ingesta. Some crop shapes include a) Great Cormorant, b)peafowl, c) budgerigar and d) domestic pigeon. e-h) Various shapes noted in a cockatoo.Modified in part from King and McLelland.101


489

inized stratified squamous epithelium. Mucousglands are located in the lamina propria, and arenumerous in the thoracic esophagus. The structureof the crop resembles that of the esophagus, exceptthat the mucous glands are restricted to an areaadjacent to the esophagus. The function of the crop isto store food when the ventriculus is full (Figure19.6). When the ventriculus is empty, food can bypassthe crop and move directly into the proventriculus.The entire length of the esophagus can be used tostore food in species that do not have a crop (eg,penguins and gulls). The esophagus and crop producemucus, which softens and moisturizes the food inpreparation for mechanical and chemical digestionlower in the gastrointestinal tract. Initial stages ofcarbohydrate digestion (mediated by salivary amy-lase) may occur in the crop of some species. Thehighly developed crop of the Hoatzin is unusual inhaving a large cervical component and two thoraciccomponents. In this species, the ventriculus is small,and the muscular crop is the main site for the me-chanical dissociation of food.

Adult pigeons of both genders produce a secretioncalled crop milk that is regurgitated and fed to thesquabs during the first week after hatching. Otherfood items gradually replace the crop milk as thebabies mature. Prolactin controls the production ofcrop milk, which consists of desquamated cells of theproliferated stratified squamous epithelium of thecrop. Crop milk physically resembles mammalianmilk and contains a high concentration of fat (6.9-12.7%) and protein (13.3-18.6%), but lacks carbohy-drates and calcium. The crop of Psittaciformes andfinches may also produce some secretions that areregurgitated and fed to neonates. The male EmperorPenguin feeds its chicks a fluid produced bydesquamation of the esophageal epithelial cells,while the merocrine esophageal glands of both gen-ders of Greater Flamingos produce a red nutritivejuice that is regurgitated and fed to the young.

The crop of some birds may be involved in courtshipbehavior. Regurgitation is a common courtship be-havior in some psittacine birds, particularly budgeri-gars, cockatiels and macaws. Males of some avianspecies (eg, pigeon, Great Bustard, ostrich, SageGrouse) have inflatable esophageal diverticula thatact as resonating chambers or display devices.

Investigative Methods

Clinical signs of esophageal or ingluvial disordersmay include dysphagia, anorexia, retching, regurgi-

tation or vomiting. In budgerigars, vomiting may beaccompanied by a rapid flick of the beak, which fre-quently deposits vomitus on top of the bird’s head(Figure 19.7).8 A history of recent drug administra-tion, assisted feeding, poor hygiene or access to toxiccompounds may suggest an etiology for esophagealproblems.

The skin and feathers overlying the crop should beexamined for abnormalities. Wetting of the featherswill help in visualizing lacerations, discolorations ornecrosis of the crop. Hypermotility or hypomotilitymay occur with crop disorders.96 In domestic fowl,peristaltic waves occur in the cervical esophagus atintervals of 15 seconds and in the thoracic esopha-gus, at intervals of about one minute. A psittacinecrop that is partially filled with food should averageone or two contractions per minute.

The esophagus and crop are thin-walled structuresthat are difficult to palpate unless abnormally thick-ened (Color 19.16). The crop can be palpated when itis full of food, fluid, air or abnormal masses. Anenlarged crop with a dough-like consistency that failsto empty is suggestive of a crop impaction (Color19.17). Occasionally, large deposits of fat, and insome cases lipomas, can occur near the crop andshould not be misdiagnosed as a full or impactedcrop. The use of improperly designed feeding cannu-las to provide supportive nutrition to birds can result

FIG 19.7 A two-year-old male budgerigar was presented with athree-week history of regurgitation. The bird was in overall goodcondition and would regurgitate when handled by either of thefemale members of the family. The bird would flick its head whenit regurgitated, causing vomitus to land on the head feathers givingthem a stiff, displaced appearance. Rhinorrhea can cause similarlyappearing feather changes. The regurgitation in this bird waslinked to courtship behavior.


490

in esophageal lacerations, with food being depositedinto the subcutaneous, periesophageal tissues (seeColor 30.8). Discolored necrotic areas, swelling andedema are common clinical findings.

For diagnostic purposes, an esophageal or ingluvialaspirate can be obtained by inserting a catheter andwashing the mucosa with sterile isotonic saline solu-tion. Luer-lock syringes should always be used whentube-feeding or collecting samples from psittacinebirds to prevent them from swallowing the tube.Immediate microscopic examination of a wet mountslide is best for diagnosing trichomoniasis. Materialaspirated from the crop should be centrifuged, andmicroscopic examination of the sediment may revealnematode eggs or Candida spp. (see Color 30 andColor 10). Air-dried smears can be stained with Diff-Quik, Gram’s stain, Wright’s stain, Hemacolor orother stains for specific cytologic examination (seeChapter 10).

A fecal flotation and crop aspirate should be per-formed to detect parasite ova that might indicate anesophageal or ingluvial nematode or trematode infec-tion. Flotation is more likely to detect low concentra-tions of eggs than a direct smear. Endoscopy is usefulfor examining the gastrointestinal mucosa and forremoving some foreign bodies (Color 19.1).

Diseases of the Esophagus and Crop

TrichomoniasisTrichomonas gallinae infections commonly occur inpigeons and raptors, and may also occur in Passeri-formes (particularly canaries and Zebra Finches)115

and Psittaciformes (particularly budgerigars andcockatiels).8,61,137 In pigeons, the proliferative necroticlesions caused by trichomoniasis are called “canker,”while in falcons the disease is called “frounce.”Trichomoniasis lesions appear similar to thosecaused by poxvirus; however, in cockatiels, poxvirusinfections are uncommon.137 Table 19.4 compares theclinical presentation of trichomoniasis in budgeri-gars and pigeons.

Samples for detecting T. gallinae can best be collectedby introducing a slightly moistened cotton-tipped ap-plicator into the esophagus, and moving it up anddown several times against the mucosal lining. Thecotton tip is then compressed between the thumb andindex finger to produce one drop of fluid, which isplaced on a slide for direct examination. A clinicaldiagnosis in Psittaciformes can be difficult because oflow parasite numbers in the early stages of the dis-ease137 and the intracellular location of the parasite.8

Trichomoniasis can cause inflammation of the upperintestinal tract and mouth resulting in dysphagia orvomiting, and may be an underdiagnosed cause ofingluvitis in budgerigars. Historically, idiopathicvomiting, diarrhea and death with yellow caseousplaques and papilliform projections in the esophagusand crop have been defined in many budgerigars.These lesions resemble those caused by trichomoni-asis.3,154 Trichomoniasis was documented in 70% of agroup of budgerigars with clinical signs of vomitingand diarrhea.8 There was no gender predisposition,but the majority of cases occurred in birds from oneto three years of age. The cervical part of the esopha-gus was most frequently affected, but many birdsalso had crop involvement. Histologic examinationrevealed that the increased thickness of the crop andesophagus was the result of an increase in depth ofthe mucosa. The intracellular occurrence of tricho-moniasis has not been reported in other avian gen-era, and this unique feature of infection in budgeri-gars may contribute to the underdiagnosis oftrichomoniasis as a cause of morbidity and mortalityin Psittaciformes.

Trichomoniasis-induced ingluvitis and stomatitishave been reported in a cockatiel and budgerigarflock, respectively.138,162 Trichomoniasis was consid-ered the cause for 80% morbidity and 72% mortalityin a flock of 60 cockatiels exhibiting regurgitation,diarrhea and depression.222 A large caseous mass inthe distal trachea caused by Trichomonas sp. wasreported in a ten-week-old Blue-fronted Amazon par-rot.61

Trichomoniasis was diagnosed in neonatal cockatiels,Lilac-crowned Amazon Parrots, Mexican Red-headedAmazon Parrots, Sun Conures and Blue-crownedConures that were fed from a single food source withthree syringes. Clinical signs included necrotic der-matitis at the commissure of the beak, depression,crop stasis and white caseous plaques on the tongueand pharynx. Histopathology was negative in allcases. The diagnosis was made by identifying tricho-

TABLE 19.4 Differences in Clinical Presentation of Trichomoniasis in Budgerigars and Pigeons

Budgerigars Pigeons

Anatomic Location Esophagus, crop Mouth, cloaca, umbilicus,liver, generalized

Lesions Proliferative Diphtheritic

Age Mainly adults Squabs


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Gastroenterology

Color 19.1 A >20-year-old Amazon parrot was pre-sented with a six-month history of intermit-tent dyspnea that had become progres-sively worse. Survey radiographs indicateda soft tissue mass in the area of the caudalthoracic esophagus. Laparoscopy indicateda diffuse air sacculitis (that was not de-tected on radiographs), and the soft tissuemass was determined to be a dilated por-tion of the esophagus. Endoscopy of thetrachea revealed thick mucus from whichKlebsiella spp. and Pseudomonas spp. wererecovered. The bird responded to systemicantibiotics but would relapse with the ces-sation of antibiotic therapy. Endoscopy ofthe esophagus revealed a large mass in theesophagus. Histologically, the surface ofthe mass contained hyperplastic mucus-producing cells. The etiology of the massremains undetermined.

Color 19.2 An eight-year-old Sulphur-crested Cocka-too was presented with a five-week historyof vomiting and progressive weight loss.Contrast radiographs indicated a mucosalfilling defect in the proventriculus. Gastro-scopy with a 3.5 mm flexible endoscope wasperformed. a) The opening from the cropinto the thoracic esophagus is clearly vis-ible. b) The opening from the proventricu-lus to the ventriculus is visible. Note thekoilin layer (dark green areas), which canpartially extend into the proventriculus. c)Bile-stained koilin layer of the ventriculus.d) Ulcers on the proventricular mucosa.Note barium sulfate is still adherent tosome of the sites of ulceration. The bird didnot respond to supportive therapy. Histo-pathology indicated marked myocardial de-generation and necrosis of undeterminedetiology.

Color 19.3 A mature Scarlet Macaw was presented forintermittent regurgitation and weight loss.The bird was maintained in an outdoorenvironment and was frequently exposed

(every hour) to an automatic pesticide fog-ger. The bird had been in this environmentoff and on for several years. Abnormal clini-cal pathology findings includedWBC=22,000, AST=750 and LDH=800. Ra-diographs indicated a rough appearance tothe dorsal serosal surface of the proven-triculus, suggestive of inflammation. Theclient chose to treat the bird at home withonly antibiotics. The bird died several daysafter presentation. At necropsy, a large per-forating ulcer was present in the proven-triculus.

Color 19.4 Hemorrhagic, necrotizing, gram-negativebacterial colitis in an Umbrella Cockatoowith a chronic PBFD virus.

Color 19.5 Several different nematodes can causenodular-type lesions and mucosal hyper-trophy in the proventriculus and ventricu-lus. In this case, proventricular hypertro-phy was caused by Dyspharynx sp. in acrane that died following a period of weightloss, depression and anemia (courtesy ofRobert E. Schmidt).

Color 19.6 A cockatoo with PBFD virus was founddead in its enclosure. The bird was in excel-lent overall condition and was of normalweight. Necropsy findings included hyper-emia of the intestinal tract with distendedvessels. Histopathology indicated a gram-negative bacterial enteritis and septicemia.

Color 19.7 A mature Yellow-collared Macaw hen diedfollowing a period of unseasonably low tem-peratures well below freezing. The bird hadexhibited several days of depression beforedeath. At necropsy, the cloaca and lowerintestinal tract were filled with blood-tinged, poorly digested food. Histopathol-ogy indicated severe necrosis of the villi andcrypt cells with a minimum inflammatoryresponse. An etiologic agent was not iden-tified.


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Gastroenterology

Color 19.8 The pericloacal area of birds is normallydry and the feathers are of normal color.Accumulations of excrement or bile-stainedfeathers are indications of enteritis or cloa-cal dysfunction. In this case, a maturecockatiel had biliverdinuria from hepa-topathy and enteritis associated withgiardiasis.

Color 19.9 a) A cloacal papilloma appears as multiple,pink-to-red masses on the cloacal mucosa.Large lesions may protrude from the cloacaand be misidentified as a cloacal prolapse.Five percent acetic acid will cause papil-lomatous tissue to appear white while nor-mal mucosa will stay pink. Stage cauteriza-tion with silver nitrate may be the easiestand most efficacious way to remove papil-lomatous tissue. Large masses should beremoved with repeated treatments severalweeks apart to prevent excessive damage tothe cloacal mucosa. b) The silver nitratestick is placed in direct contact with thepapillomatous tissue and moved gentlyover the lesion. When the tissue turns grey,the silver nitrate is inactivated by flushingwith water. The undiluted silver nitratemust not be allowed to run inside the clo-aca, or nonspecific chemical burns will oc-cur.

Color 19.10A mature pigeon was presented for depres-sion and anorexia of two days’ duration.The feathers around the vent and lowerabdomen were covered with excrement andfly larvae. The contaminated feathers wereremoved. The cloaca was impacted withdry, firm feces and urates. The feces wereremoved from the cloaca with forceps, andthe cloaca was flushed with dilute chlor-hexidine solution. A Gram’s stain of therostral cloacal wall revealed a moderatenumber of short, gram-negative bacteria.The bird responded to parenteral enroflox-acin.

Color 19.11A female Amazon parrot was presentedthree days after egg laying when she wasfound on the bottom of the enclosure. Thebird was depressed and emaciated. A cloa-cal prolapse had occurred, and the mucosahad multifocal, dry, necrotic areas. The ne-crotic tissues were cleansed with a dilutechlorhexidine solution and surgically re-moved. The cloaca was placed back in theabdomen and was held in place with a cloa-copexy. The bird was placed on oral en-rofloxacin, and the cloaca was flushed BIDwith dilute chlorhexidine solution followedby the installation of Preparation H. Thebird responded to the therapy. The prolapsewas considered to have occurred followingthe passage of an unusually large egg.

Color 19.12 A mature male budgerigar was presentedwith a three-week history of intermittent

regurgitation. Several masses (inglu-violiths) were palpated and were removedsurgically from the crop.

Color 19.13 A mature budgerigar was presented for aswelling in the thoracic inlet area. The cropwas severely distended with food, and thebird had an audible click on inspiration.Goiter was the presumptive diagnosis andthe bird responded to iodine therapy (cour-tesy of Elizabeth Hillyer).

Color 19.14 A >25-year-old rosella died acutely. Thegastrointestinal tract was dilated and con-tained poorly digested ingesta. The birddied from severe atherosclerosis.

Color 19.15 Typical “turkish towel” appearance of thecrop in a bird with a severe Candida spp.ingluvitis. Compare to Color 19.16 in whichthe crop is transparent.

Color 19.16 In Psittaciformes, the normal crop andesophagus are thin, milk-colored, partiallytransparent membranes with a few distin-guishable, small blood vessels. Note thatthe trachea can be seen through the crop.

Color 19.17 A 15-week-old Hyacinth Macaw was pre-sented for necropsy following a brief periodof depression. The client had noticed thatthe bird’s crop had not emptied over atwelve-hour period. The bird was being feda commercial hand-feeding formula sup-plemented with a liquid vitamin and min-eral supplement. At necropsy, the crop washyperemic and distended with food, and thevessels were congested. The kidneys werecalcified. Macaws appear particularly sen-sitive to hypervitaminosis D3. This bird’sdiet was estimated to have four to six timesthe necessary level of vitamin D3.

Color 19.18 A 23-year-old Scarlet Macaw hen was pre-sented two weeks after the referring veteri-narian had surgically removed an impactedegg from the distal uterus. The bird wasseverely depressed and emaciated, and theabdomen was distended. Radiographs indi-cated gaseous distention of the intestinaltract. Abnormal clinical pathology findingsincluded WBC=45,000 (toxic heterophils),PCV=25, TP=2.2 and AST=900. Fluid col-lected by abdominocentesis was charac-teristic of an exudate (SpGr=1.025, Pro-tein=4.5 g/dl and numerous heterophils).An exploratory laparotomy was performed,a section of strangulated colon was re-moved and a side-to-side anastomosis wasperformed. The bird did not recover fromthe surgery. Note the congested, distendedbowel loops and the presence of granulationtissue on the abdominal wall.


495

monas in impression smears of the lungs of a birdthat died one hour before examination.137

In another case, six Yellow-naped Amazon Parrotbabies were affected. Clinical signs included whitishgray plaques on the tongue, choana and pharynx.Wet mount examination of scrapings from these le-sions, crop lavage and transtracheal wash were nega-tive. Postmortem examination of one of the Amazonparrots revealed a caseous plaque partially occludingthe syrinx and lungs and filled with a yellowish, clearexudate containing abundant trichomonads thatwere demonstrated by a wet mount impressionsmear.137 These cases suggest that trichomoniasis isa severely underdiagnosed cause of upper gastroin-testinal disease in psittacine birds. Histopathologicexamination is of limited diagnostic value becausethe causative organisms float away from the tissuein formalin.137 Nitroimidazole drugs like metronida-zole, ronidazole, dimetridazole and carnidazole areusually effective in treating trichomoniasis; however,nitroimidazole-resistant strains of trichomoniasis oc-cur in The Netherlands because of the improper useof these drugs by pigeon fanciers.56

Nematode and Trematode InfectionsMany nematodes including Capillaria sp p . ,Echinura uncinata, Gongylonema ingluvicola andDis-pharynx nasuata can invade the esophageal orcrop mucosa. The thorny-headed worm (Oncicolacanis) has been reported in turkeys.78,174

Ingluvial/Esophageal Stasis and DilatationThe suggestive causes of crop stasis include heavymetal toxicity, crop impaction, callus formation aftera coracoid fracture, thyroid enlargement, atonic crop,sour crop, overstretching of the crop, esophagitis(candidiasis, trichomoniasis, capillariasis, ser-ratospiciliasis), ingluvioliths and esophagealstenosis (Color 19.13). If the fluid in the crop remainsstagnant, it will decay and have a foul odor (oftenreferred to as sour crop). Regurgitation of proven-tricular fluid may be a contributing factor. Feeding aliquid formula to granivorous birds can induce cropstasis, possibly as a result of a lack of mechanicalstimulation.

In turkeys, there is thought to be a hereditary predis-position to developing a pendulous crop after in-creased liquid intake during the first wave of sea-sonal hot weather. The majority of affected birds donot recover, but continue to have pendulous crops. Ithas been shown that feeding cerelose as a substitutefor starch increases the incidence of pendulous crop

in gallinaceous birds. Affected birds had large quan-tities of the gas-producing yeast Saccharomyces tel-lustris. Large quantities of gas may have initiatedthe crop dilatation.151

Crop ImpactionCrop impaction is occasionally seen in Galliformesand Anseriformes that have sudden access to anabundant supply of lush grasses and sproutedgrains.79,122 Dried oatmeal and soybeans swell whenthey absorb water and can impact the crop. This is amajor cause of mortality in free-ranging CanadaGeese.80,92 About 2000 Canada Geese died from im-paction of the cervical esophagus accompanied bynecrosis and ulceration of the esophageal mucosafollowing the ingestion of fox tail grass (Setaria lutes-cens). Lead poisoning, acute fowl cholera and ven-tricular worm infections can cause similar clinicalsigns.122 Crop impactions can occur in birds providedad libitum grit. Food substances that are difficult todigest, such as raw potatoes, beets, apple skins, sau-sage skins and large pieces of animal tissues, mayalso cause crop impaction. In captive raptors, inglu-vial impaction may occur when roughage is suddenlyadded to a low roughage diet, or when the moisturecontent of the diet is inadequate. Crop impactionmay be complicated by secondary Clostridium per-fringens infection in the European Kestrel.91

Impacted material in the crop can be softened by theadministration of warm water followed by massagingthe crop. However, an ingluviotomy will generally bethe method of choice for removing impacted material.Foreign bodies may be removed endoscopically. Ex-pressing the ingluvial contents through the mouth byturning the bird upside down is a dangerous proce-dure that may lead to irritation of the nasal mucosa,sinusitis or aspiration pneumonia. Packing the cho-ana with cotton and intubating with an endotrachealtube will help eliminate this problem.

IngluviolithsIngluvioliths have occasionally been reported inbirds (Figure 19.8).3,10,12 Urate (excreta) calculi withseed husk centers were described in the crops ofseveral budgerigars.12 It was speculated that thecalculi originated from the ingestion of excreta andseed husks in birds provided no food. Other inglu-violiths have been found to contain potassium phos-phate, oxalate and cystine, and were not consideredto have occurred secondary to urate ingestion (Color19.12).3


496

Foreign BodiesUnweaned psittacine neonates (especially macawsand Eclectus Parrots) frequently ingest foreign bod-ies.11 Any ingested foreign body, including rubber ormetal feeding tubes, should be removed immediatelyfrom the ingluvies before it has an opportunity toalign with the thoracic esophagus and pass into the(pro)ventriculus. The type of foreign body is depend-ent on the species (Figure 19.9). Fishing hooks arecommon in waterfowl. Perforating or obstructingbones are encountered in raptors.

Crop and Esophageal Lacerations and FistulaPenetration of the pharynx or esophagus by feedingcannulas, or esophageal-ingluvial burns caused by

ingestion of overheated feeding formulas or causticmaterials can result in deposition of food subcutane-ously and lead to extensive foreign body reactions. Inbirds of prey, sharp bones from prey animals maycause an esophageal or ingluvial fistula.20,153 Trau-matic lacerations of the chest including the ingluviesare often seen in racing pigeons. The most likelycause for these lacerations is a collision with antennawires. Bite wounds from mates or cats and dogs mayalso cause crop lacerations. A bird with a crop fistulamay be presented with weight loss despite a raven-ous appetite. The feathers surrounding the fistulaare usually matted with dried food. Subcutaneouspockets of food should be surgically drained and fre-quently flushed. A feeding tube can be passed fromthe esophagus directly into the proventriculus toallow enteral feeding while the esophagus and cropheal (see Chapters 15, 16 and 41).81

Esophageal StrictureA ten-year-old Hyacinth Macaw developed a stricturein the thoracic esophagus after ingesting severallarge pieces of hard plastic. The most obvious clinicalsign was regurgitation of mucus. A barium studyrevealed a filling defect in the caudal esophagus.Endoscopic examination through an ingluvial inci-sion revealed an annular ring of exudate and hyper-plastic tissue. The stricture was resolved by periodicmechanical dilation.203 Esophageal strictures mayalso occur secondary to burns. A cockatoo with severeself-mutilation syndrome damaged the perieso-

FIG 19.8 An ingluviolith is evident in theseradiographs of a cockatiel (courtesy of JeanParé).

FIG 19.9 An adult female Umbrella Cockatoo was presented with an acute onset oflethargy and regurgitation. Several small solid masses could be palpated in the crop. Thebird was producing small amounts of excrement and had tenesmus. The bird was main-tained in an earthen-floored flight enclosure and was fed wild bird seeds. Abnormal clinicalpathology findings were limited to hypokalemia and mild anemia (PCV=34%). Radio-graphs indicated several metallic densities in the crop. In addition, an excessive numberof mineral densities (small rocks, grit) were present in the ventriculus and intestinal tract.The metallic densities (pieces of wire) were removed using an endoscope and forceps. Theventriculus was flushed with copious amounts of warmed LRS, which resulted in theremoval of about 20 to 30 small rocks. The bird was given corn oil by crop tube three timesa day for three days, and rocks were noted in the stool on the day after the first corn oiltreatment. The bird’s diet was corrected and no further problems were noted.


497

phageal skin to such a degree that the esophagus wasoccluded and the bird died from asphyxiation.

The Proventriculusand Ventriculus


The avian stomach consists of a cranial glandularpart (proventriculus) and a caudal muscular part(ventriculus). The proventriculus in birds is situatedin the left dorsal and left ventral regions of thethoraco-abdominal cavity, and is covered ventrally bythe fat-laden posthepatic septum (see Color 14). Thepyloric part of the ventriculus joins the duodenumand is located on the right side of the midline. Ingranivorous, insectivorous and herbivorous birds,the muscular wall of the ventriculus is highly devel-oped and is clearly distinct from the proventriculus.The two organs are divided by an intermediate zone,or isthmus, which can be seen grossly as a constric-tive band (Figure 19.10). The ventriculus can bepalpated in granivorous birds on the left ventral sideof the abdomen just caudal to the sternum.

The proventriculus has two types of glandular epi-thelial cells. Mucus-producing, columnar epithelialcells line the proventricular mucosa and the luminaof the ducts from the proventricular glands. Thesecells contain numerous periodic acid Schiff (PAS)-positive mucin granules. The multilobular glands ofthe proventriculus are lined by oxynticopeptic cells.These cells have ultrastructural features similar toboth the parietal (acid-secreting) and the peptic (en-zyme-secreting) cells of the mammalian stomach,and secrete both pepsinogen and hydrochloric acid.The ducts from these glands empty from numerouspapillae that can be found in the proventricular wall.These oxynticopeptic cells possess a very eosinophilicand somewhat granular cytoplasm and do not con-tain PAS-positive mucin granules.

The wall of the ventriculus is composed of smoothmuscle arranged into four semi-autonomous masses.The caudodorsal and cranioventral thick musclesand the craniodorsal and caudoventral thin musclesattach to the right and left tendinous centers in thelateral walls of the ventriculus. The asymmetric ar-rangement of the muscles enables rotary and crush-

ing movements during ventricular contractions. Thethin muscles form the cranial and caudal blind sacs.The caudal blind sac is a good point for gastrotomyincision in granivorous birds because incisions in thethick muscles heal poorly. The inner surface of theventriculus of granivorous birds is lined by a carbo-hydrate-protein complex (koilin layer or cuticle).This koilin layer is composed of vertical rods secretedby the mucosal glands of the lamina propria and ahorizontal matrix, which is a secretion of the surfaceepithelium that hardens after spreading around therods. Desquamated cells of the surface epitheliumare trapped within the horizontal matrix. Hydrochlo-ric acid from the proventriculus causes precipitationof the protein complex to form a tough, water-resis-tant lining. The brown, green or yellow color of thekoilin is caused by regurgitation of bile through thepylorus.

The intermediate zone that divides the proventricu-lus and ventriculus has histologic characteristics

FIG 19.10 The isthmus (arrow) is distinguished as a constrictiveband separating the proventriculus (p) from the ventriculus (v).The proventriculus can be seen laying dorsal to the caudal thoracicair sac. This bird died from myocardial degeneration.


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similar to both organs. Compound glands are absent,and the internal surface is relatively smooth. Thecolumnar epithelium lining the proventriculusgradually changes into ventricular glands. There is amixture of proventricular-like mucoid secretions andventricular-like glandular secretions. Most gastricneoplasms in birds occur in the intermediate zone,and use of PAS stains appears useful in determiningthe types of epithelial cells that have been trans-formed.113,161

The ventriculus is the site of gastric proteolysis, andin many species also of mechanical digestion. In car-nivorous and piscivorous birds, the proventriculus ismore adapted for storage than for physical digestion.In these species, the ventriculus is thin-walled andsac-like, and the ventriculus and proventriculus aredifficult to differentiate grossly. The koilin layer isrelatively thin and softer than in granivorous birds.The muscularis is relatively thin. In raptorial species(eg, owls), the ventriculus is involved in the forma-tion and regurgitation of pellets or “castings,” whichare composed of undigestible fur, feathers or bones.Intermediate forms of proventricular and ventriculardifferentiation are found in many avian species in-cluding frugivorous (fruit-eating) and testacivorous(shellfish-eating) birds.

In certain frugivorous pigeons, the koilin layer iscomposed of rows of hard, pointed, conical projectionsthat facilitate crushing firm fruits such as nutmeg.In some species (magpie and starling), massive shed-ding and excretion of the koilin layer occur peri-odically. Male hornbills may regurgitate the koilinlayer as a seed-filled sac that is fed to the nestingfemale.

The proventriculus in an ostrich is a large, thin-walled structure. In contrast to other birds, the oxyn-ticopeptic cells are restricted to a patch on thegreater curvature. The distal extremity of the ostrichproventriculus passes dorsal to the ventriculus andempties on the caudal aspect of this organ. The os-trich ventriculus is a thick-walled muscular organ.The isthmus between the proventriculus and ven-triculus is large, which makes it easy to removeforeign bodies from the ventriculus through aproventricular incision. In emus and nandus, theproventriculus is large and spindle-shaped, and theventriculus is slightly larger and more lightly mus-cled than that of the ostrich.

Proventricular and Ventricular Diseases

Most diseases of the proventriculus or ventriculus pro-duce similar clinical signs and make differentiationdifficult. For example, an enlarged proventriculus maybe found in many of the diseases in Table 19.1. Thefollowing is a discussion of some of the diseases thataffect the proventriculus and ventriculus.

Megabacterial Proventriculitis“Going light” syndrome in budgerigars, a diseasecharacterized by emaciation, weakness, high morbid-ity and low mortality, has been described in canariesand budgerigars. Vomiting of slimy material is seenin advanced stages of the disease.64,177,197,201 Postmor-tem findings include proventriculitis and proven-tricular dilatation. Histologically, gram-positive,PAS-positive, acidophilic (with Giemsa), rod-shapedbacteria can be identified, especially in the area be-tween the proventriculus and ventriculus. The or-ganisms have been characterized as large bacteria(not fungi), hence the name “megabacteria” (see Fig-ure 33.13).

A diagnosis can be made by cytologic demonstrationof the organisms in a proventricular washing. ThepH of the proventriculus is markedly elevated inaffected birds. The pH of the proventriculus fromnormal canaries was found to range from 0.7 to 2.4compared to severely infected canaries in which thepH was 7.0 to 7.3. In birds with moderate numbers ofmegabacteria, the pH of the proventriculus rangedfrom 1.0 to 2.0.201 The most important differentialdiagnosis is trichomoniasis.

Proventricular and Ventricular NematodesMany nematode species have been reported to occurin the proventriculus (Echinura uncinata, Gongy-lonema ingluvicola, Cyrnea spp., Dyspharynx nasu-ata and Tetrameres spp.). Amidostomum spp., Cheilo-spirura spinosa and Epomidiostomum uncinatumare found under the horny layer of the ventriculus(Color 19.5).60,174,179 Lesions vary considerably de-pending on the host and the parasite, and may bequite extensive (see Chapter 36). Clinical signs maybe absent or include emaciation, anemia and mortal-ity. Diagnosis can often be made by detecting para-site eggs using a fecal flotation technique. Treatmentcan be attempted with levamisole (20 mg/kg orally, or10 mg/kg parenterally) or ivermectin (200 µg/kg par-enterally). It should be stressed that experience withivermectin in many avian species is absent. Acutedeath has been reported after the use of ivermectinin some mammalian and reptilian species.


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Neuropathic GastricDilatation and Encephalo-

myelitis of PsittacinesNeuropathic gastric dilatation(NGD)123 has been given manynames since it was first recog-nized as a clinical entity in 1971(Table 19.5).

The descriptive term myentericganglioneuritis and encephalo-myelitis of Psittaciformes bestdefines the following histologiclesions that can be observed inaffected animals: lymphocyticand monocytic infiltration of intrinsic and extrinsicsplanchnic nerves of the muscularis tunics of thealimentary tract; in some cases, leiomyositis in or-gans innervated by affected nerves and non-suppura-tive encephalitis, myelitis and radiculoneuritis havebeen described.68 Many psittacine species can be af-fected, including macaws, cockatoos, conures, Afri-can Grey Parrots, Senegal Parrots, Amazon parrots,Eclectus Parrots, Thick-billed Parrots and cocka-tiels.68

Clinical signs are related to (pro)ventricular andsometimes neurologic dysfunction, and may includeanorexia, regurgitation, undigested seeds in the fecesand weight loss. The occurrence of neurologic signs isvariable. In advanced cases, proventricular dilata-tion can be visualized on abdominal radiographs,with or without contrast media (Figure 19.11). In theclinical patient, a tentative diagnosis of NGD can bemade based on clinical signs and radiographic find-ings. It should be stressed that other diseases canmimic NGD and should be ruled out before a defini-tive diagnosis is considered (Table 19.6).69,90,197 NGD

TABLE 19.5 Synonyms for Neuropathic Gastric Dilatation*

Psittacine proventricular dilatation syndrome (PPDS)

Macaw wasting syndrome

Myenteric ganglioneuritis

Psittacine encephalomyelitis

Proventricular dilatation of psittacines

Proventricular dilatation and wasting syndrome

Myenteric ganglioneuritis and encephalomyelitis of psittacines

Wasting/proventricular dilation disease (WPDD)

Proventricular dilatation disease

Proventricular dilatation syndrome

Macaw fading syndrome

* References 37,45,68,89,94,121,123,157,167,172,195,221

FIG 19.11 A three-year-old female cockatiel was presented with atwo-week history of passing undigested seeds. Survey radiographssuggested a dilated proventriculus. Barium contrast study indi-cated a slowed gastric emptying time (VD and lateral radiographseight hours after the administration of barium by crop tube). Notethe numerous filling defects (ingesta and undigested seeds) in thecrop, proventriculus and intestines. The client chose to have thebird euthanatized. Histopathology confirmed a diagnosis ofneuropathic gastric dilatation.


500

can be confirmed by histologic identification of char-acteristic lesions in the splanchnic nerves from aventricular biopsy (Figure 19.12). However, a nega-tive result derived from a small biopsy of the ven-tricular wall does not rule out NGD.68

Although the etiology is presently unclear, a viraletiology has been suggested because of epidemiologichistories of affected aviaries and the demonstrationof intranuclear and intracytoplasmic inclusion bod-ies in affected t issue of some birds.26,63,84,123

Paramyxovirus-like inclusions have been describedby some researchers123 but could not be identified byothers.68 The “avian viral serositis” virus producesexperimental lesions that are similar to those de-scribed with NGD (see Color 32).

Affected animals invariably die after a more or lessprotracted course of the disease. Controlled studiesto document the effects of treatment on the prognosisof NGD have not been reported. General therapyincluding supportive care, a liquid diet, vitamin sup-plementation and treatment of secondary diseaseshas been recommended. It has been suggested thatbirds can survive on a liquid diet,78 but no case re-ports could be found that document long-term sur-vival of birds confirmed by ventricular biopsy to haveNGD. Treatment of NGD should be considered withcaution, given that the disease may be caused by aninfectious agent.

It has been suggested that a virus may induce anautoimmune reaction that would be responsible forthe lesions observed in NGD.67 The inciting viruswould no longer be present when the disease becameclinically obvious or was diagnosed at necropsy. Ifthis scenario is true, then administration of an anti-

inflammatory dose of corticosteroids might be indi-cated.161

Ganglioneuritis and Encephalitis in GeeseProventricular impaction with non-suppurative en-cephalomyelitis and ganglioneuritis morphologicallysimilar to NGD in psittacine birds has been reportedin two Canada Geese.43

Proventriculitis in ChickensProventricular enlargement and infiltration of theproventricular interglandular tissue with mononu-clear cells has been described106 as part of the infec-tious runting and stunting syndrome in broiler chick-ens.

Gastric Impaction and Gastric Foreign BodiesGastric impaction is common in psittacine babiesthat consume bedding material such as crushed wal-nut shell, ground corncob, shredded paper pulp, sty-rofoam packing, kitty litter and excess grit. Thesebedding materials should not be used with neo-nates.35,39

Ventricular impaction secondary to litter ingestionhas been reported to cause high mortality during thefirst three weeks of life in turkey poults. Affectedanimals were emaciated and had empty intestinaltracts, distended impacted ventriculi and foreignbodies in the first part of the duodenum.170

Gastric obstruction caused by phytobezoars or de-tachment of the koilin layer of the ventriculus hasbeen reported in chickens, a goose, ducks and a pi-geon.51 Gastric rupture may occur secondary to animpaction. In raptors, ventricular impaction causedby a hard mass of fur can also occur. Gastric impac-tion is more common in captive raptors fed earlyduring the day in hot weather. Those fed late in theday are less likely to retain their casting.66

In ostriches, (pro)ventricular impaction is a seriousmanagement problem.209 The condition occurs usu-ally two to three weeks after moving the birds to anew environment containing a novel substrate orfood. Most affected birds are under six months of age,but the condition can also occur in adults. Clinicallythe birds are sluggish and produce small, firm fecalballs. Some affected birds may be lame. Cloacal pro-lapse may occur in young birds several days to fourweeks old. Early diagnosis through abdominal palpa-tion and radiographs followed by immediate surgicalcorrection are imperative for successful resolu-tion.88,187 A 17-inch string of beads could be palpated

TABLE 19.6 Differential Diagnosis of Neuropathic Gastric Dilatation

Heavy metal poisoning

Fungal infection of ventriculus or koilin mycosis

Nematode infection of the (pro)ventriculus

Megabacteria infection of the proventriculus

Gastric impaction

Pyloric obstruction by a foreign body

Ventriculus perforation by a foreign body

Myoventricular dysgenesis

Proventricular foreign body

Koilin dysgenesis

Myoventricular calcinosis

Intestinal papillomatosis

Proventricular and ventricular neoplasia

Vitamin E and selenium deficiencies


501

FIG 19.12 A one-year-old male Eclectus Parrot was presented for severe emaciation, depression, diarrhea and a distended abdomen. Thebird had a ravenous appetite. Abnormal clinical pathology findings included AST=1637, LDH=4049 and WBC=3000. a) Survey radiographsindicated a severely dilated proventriculus and hepatomegaly. The bird was fasted for eight hours and a barium contrast study wasperformed. b) Ventrodorsal and lateral radiographs were taken two hours post-barium administration and c) lateral radiograph representseight hours post-barium administration. The proventriculus was markedly reduced in size following fasting. Contrast studies indicated adelayed gastric-emptying time, hepatomegaly (causing the proventriculus to be displaced dorsally) and retention of barium in theproventriculus, suggestive of mucosal inflammation. The bird responded to treatment with broad-spectrum antibiotics and lactulose. Itshould be stressed that the survey radiographs were suggestive of NGD; however, a dilated proventriculus and slowed gastric-emptyingtime are not pathognomonic for NGD. A biopsy is necessary to confirm a diagnosis.


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in the crop of an Amazon parrot.Barium contrast radiographswere used to confirm that thestring of beads passed into thesmall intestines. The string wasextracted through the mouth us-ing sponge forceps.213

Although poorly documented inbirds, emetics might be useful toremove foreign bodies that wouldnot damage the gastrointestinalmucosa during the regurgitationprocess. Apomorphine inducedemesis in 55% of treated birds36

and in another study, a 0.5% solu-tion of tartar emetic was effec-tive.114

Metallic Foreign Bodies: TraumaticGastritis, Heavy Metal Poisoning

Ingestion of metallic foreign bod-ies is relatively common in Galli-formes, Anseriformes, Columbi-f o r mes , Gr ui f or mes ,Pelecaniformes, Psittaciformesand ratites.51,71,205, 209,210 In captive Psittaciformes andfree-ranging Anseriformes, ingestion of lead is ex-tremely common. Paralysis of the intestinal tractfrom nerve damage may occur secondary to leadpoisoning. In Anseriformes, this is clinically recog-nized as esophageal and proventricular dilatation. Inthe other orders, ingestion of ferrous metal objects,such as nails, wire, hairpins and needles, account forthe majority of cases. This is particularly common ingallinaceous birds.151 In one case, each affected birdhad a piece of one-inch wire penetrating the ventricu-lus (see Figure 45.2). It was discovered that theowner used a wire brush to clean the water container.

Ingestion of ferrous objects may cause perforation ofthe ventriculus (majority of cases) or proventriculus,leading to an acute, generalized, purulent peritonitisor to a local peritonitis with abscess formation on theserosal surface of the (pro)ventriculus or duodenum.The powerful contractions of the ventriculus musclesin the domestic fowl can result in a pressure of 100-200 mmHg, which can easily force sharp objectsthrough the tough muscular wall. Occasionally, pene-tration of a large (hepatic) artery or vein can resultin fatal hemorrhage. In some rare cases, the ferrousforeign body will be resorbed by the inflammatoryreaction without permanent deleterious effects.Cases have been documented in which a foreign body

was exteriorized by penetration through the bodywall.51,205

Foreign body penetration of the ventricular wallcauses a decrease in ventricular contraction and aninsufficient digestion of food, which may be recog-nized clinically by the passage of undigested seeds inthe feces. In the racing pigeon, passing undigestedseed is considered pathognomonic for a traumaticgastritis. In chronic cases, anorexia, weight loss anda palpable abscess on the left side of the abdominalwall may be noted.205 Radiology is the method ofchoice to confirm a tentative diagnosis.

Noninvasive treatments for removal of gastric metalforeign bodies should be attempted before (pro)ven-triculotomy. Ferrous metals may be removed fromthe (pro)ventriculus using a powerful magnet of neo-dymium-ferro-borium alloy (The Magnet Store 1-800-222-7846) attached to a small-diameter polyvi-nyl catheter with a removable steel guide wire(Figure 19.13).120 The size of the polyvinyl probe andmagnetic disk can be varied according to the size ofthe animal. A probe with a length of two meters, adiameter of 18 mm and an attached cylinder magnetof 17 x 70 mm (derived from a bovine cage magnet)has been used to remove thirteen large staples fromthe ventriculus of an ostrich. Fluoroscopy or en-doscopy can be used to guide grasping forceps in the

FIG 19.13 A mature African Grey Parrot was presented for evaluation of depression andanorexia several days after destroying a panel of chicken wire placed over a screened-in-porch.Radiographs indicated that the ventriculus was full of metallic densities. Because the wirewas composed of a ferrous metal, a) the foreign bodies were removed by repeatedly insertinga red rubber feeding catheter equipped with several neodymium-ferro-borium alloy magnets(arrows). b) The metal removed from the bird is firmly attached to the magnet containedwithin the tube.


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removal of gastric foreign bod-ies.117,119 Most cases of lead and zincingestion can be managed medicallyand do not require surgery.

Myoventricular DysgenesisProventricular dilatation secondaryto ventricular abnormalities causedby feeding finely ground food low infiber is commonly observed as an in-cidental finding in chickens. The en-larged proventriculus has a dis-tended thin wall and is full of food.The ventriculus in affected birds ispoorly developed, and there is nosharp demarcation between theproventriculus and ventriculus.169 The postmortemfindings are similar to those with pyloric obstructionor gastroesophageal paralysis (ie, dilatation of thefood-filled ventriculus, proventriculus, esophagusand crop). In the latter condition, the ventricularmuscles are of normal thickness.

Vitamin E and Selenium DeficienciesVitamin E and selenium deficiencies may cause de-generative lesions in the smooth muscle of the ven-triculus of domestic and free-ranging Anserifor-mes.135,178,219

Gastric Ulceration, Ventriculus Erosion,Gastritis, Koilin Dysgenesis

Idiopathic proventricular ulcers do occur in psittac-ine birds. Many affected animals are “high strung” orin what could be called stressful environments (Fig-ure 19.14); (Color 19.3).

High dietary levels of certain types of fish meal orfinely ground, low-fiber diets can cause erosions andulcers in the koilin layer of gallinaceous birds.71,144

Infectious and parasitic agents may damage the ven-tricular wall causing dysfunction. Penetration of for-eign bodies may cause localized lesions. Zoalene(DOT) toxicosis may cause gastric erosion.71 Ven-triculus erosion with a heavy infiltration of hetero-phils has been reported with zinc poisoning.46,48,216

Copper PoisoningExcessive dietary copper leads to roughening andthickening of the koilin layer. The marked thickeningand folding may have a wart-like appearance. Hem-orrhages may be seen under the koilin layer.53,216

FIG 19.14 An eight-year-old Sulphur-crested Cockatoo was pre-sented with a five-week history of vomiting and progressive weightloss. Survey radiographs indicated gaseous distention of the pro-ventriculus (arrows). Contrast radiographs indicated mucosal fill-ing defects in the proventriculus. Gastroscopy with a 3.5 mmflexible endoscope indicated numerous proventricular ulcers(Color 19.2). The bird did not respond to supportive therapy.Histopathology indicated marked myocardial degeneration andnecrosis of undetermined etiology.


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Neoplasias2,68,74,113,161

The clinical effects of (pro)ventricular neoplasia mayvary, depending on the size of the tumor and thepresence or absence of active bleeding from the ulcer-ated tumor. Clinical signs may include weight loss,vomiting, passing of whole seeds in the feces, regen-erative anemia, hypoproteinemia and melena. Al-though hypoproteinemia may occur, the albu-min/globulin ratio is not affected, which togetherwith the anemia and melena is strongly indicative ofgastrointestinal blood loss (Table 19.7). Death usu-ally ensues when massive gastric bleeding occursfollowing erosion of a major vessel. Contrast radiog-raphy using both positive and negative contrast maybe helpful in outlining the (pro)ventricular neo-plasm.196 Endoscopic-guided biopsy may be used toconfirm a tentative diagnosis.

Tumors are frequently located at the isthmus on theboundary between the proventriculus and ventricu-lus. Gross lesions in the (pro)ventriculus may besubtle, and histologic examination is needed to differ-entiate tumors from other causes of ulceration orhypertrophy. The use of specific staining methods(Alcian blue and periodic acid Schiff) facilitates dif-ferentiation between tumors of proventricular andventricular origin.113,161

Presently, no reports of successful treatment of(pro)ventricular tumors have been published, but ithas been suggested that early diagnosis and surgicalexcision are feasible.161

TABLE 19.7 Documented Cases of Gastrointestinal Neoplasias in Psittaciformes (P), Galliformes (G) and Other (O).

Rhamphotheca P P P P P

Oropharynx P G,P P G G G,P

Esophagus G G G,P G,P,O

Crop G P G,P

Proventriculus G,P,O G P G

Ventriculus G,P,O G G G G P G

Intestines G,P G,P G G,P G G G

Rectum O G

Cloaca G,P,O P P P

Pancreas G G G

Squamous cell carcinomas are the most common tumor in the oral cavity of Galliformes. Oropharyngeal tumors may be painful, ulcerative and infiltrative but rarelymetastasize. Clinical signs may include dysphagia, regurgitation, vomiting, diarrhea, tenesmus and cloacal prolapse. A definitive diagnosis can be made by biopsy.Prognosis depends on the location of the tumor, the degree of tissue infiltration and the occurence of metastasis. Many connective tissue tumors in gallinaceous birdsmay be caused by the leucosis sarcoma group of viral infections.149 There is a high incidence of pharyngeal and esophageal squamous cell carcinoma in humans andchickens in northern China suggesting a common etiology.34, 180 The incidence of gastric neoplasia seems higher in psittacine birds compared to other species. Intestinaltumors must be differentiated from metastatic oviductal or ovarian tumors by demonstrating that no primary tumors of these organs exist and that the tumor originatesfrom intestinal mucosal epithelium or glands, rather than growing inward from the serosal surface.29 Obstruction of the pancreatic ducts can occur with pancreaticneoplasias. Islet cell carcinomas can cause diabetes mellitus.74, 196

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505

The Small andLarge Intestines

Anatomy and Physiology101

In the majority of avian species, the duodenum is anarrow, U-shaped organ that originates from thepylorus on the right side of the ventriculus. The palepink or yellow lobulated pancreas is located betweenthe proximal descending and distal ascending duode-nal loops (see Color 14). In some species (eg, White-tailed Sea Eagle and Jackass Penguin), secondaryfolds are present in the duodenum. In the BlackStork, the duodenum is twisted, while in other spe-cies (eg, Northern Fulmar and Gannet), the duode-num consists of more than one loop. The bile andpancreatic ducts often open near each other at thedistal end of the duodenum. There are one, two(ducks and geese) or three (domestic fowl) pancreaticducts and two bile ducts. When a gallbladder is pre-sent, this organ drains the right liver lobe via theright hepatocystic duct and empties into the duode-num via the cysticoenteric duct. In species where agallbladder is absent (most pigeons, many parrotsand the ostrich), the right liver lobe drains directlyinto the duodenum via the right hepatoenteric duct.In gallinaceous birds, the common hepatoentericduct drains bile from both liver lobes to the duode-num. The jejunum and ileum are arranged in a num-ber of loops, and are suspended by a long, distalmesentery on the right side of the abdominal cavity.

The vitelline diverticulum (Meckel’s diverticulum),which is the remnant of the yolk duct, is locatedopposite the distal end of the cranial mesentericartery. The duct of the yolk sac opens into the smallintestine on a small papilla. The yolk provides nour-ishment, minerals, fat-soluble vitamins and mater-nal immunoglobulins to the embryonic bird and tothe chick during the first few days of life. Just beforehatching, the yolk sac is internalized and the umbili-cus is closed. Precocial birds have a yolk sac thatranges from 10 to 25% of body weight at hatching,while in altricial species these values range from 5 to10% of body weight.99 Precocial birds must learn toeat during the first few days of life, while altricialbirds are fed by their parents. In altricial species,resorption of the yolk is faster than in precocialspecies and takes about four days.

In gallinaceous birds, the yolk sac should not persistbeyond six to nine days and should not be larger thanpea-size between six to eight days of age.71 In theostrich, yolk sac absorption may require eight ormore days. In the emu and cassowary, a yolk sac canbe palpated for at least one week, but it should bereduced in size. It should be noted that at hatching,the liver of some birds is a bright yellow color due toabsorption of pigments from the yolk sac (see Color30). The liver gradually changes to the mahoganycolor of the adult between eight and fourteen days ofage in gallinaceous birds.130 In the adult chicken, thevitelline diverticulum has been found to contribute toextramedullary myelopoiesis, and it has been sug-gested to have a lymphoepithelial function.130

The large intestine usually consists of paired cecaand a short, straight rectum. The ceca arise at theileorectal junction. The anatomy of the ceca variesamong species. In Galliformes, the ceca are large andcurve in a caudodorsal direction. Tetraonids (eg, ca-percaillies grouse that eat branches and twigs oftrees) have the largest ceca of any species because oftheir high cellulose diet.4 The ostrich has a largesacculated cecum while other ratites have only ves-tigial ceca. Passeriformes, Columbiformes and somePsittaciformes also have vestigial ceca. Budgerigarshave no ceca. Vestigial ceca usually contain largeamounts of lymphoid tissue. In Galliformes, the lym-phoid cecal tissue is located in the proximal part ofeach cecum and is called the cecal tonsil. Large cecaare involved in the bacterial fermentation of cellu-lose, and are also important in water reabsorptionfrom ureteral urine. The type of food consumed by abird influences intestinal length. Red Grouse fed apelleted ration have a cecal length 50% shorter thanthose of free-ranging birds.136 This is extremely im-portant when one considers the problems with diges-tion that could occur if captive-raised birds werereleased into the wild.

The rectum lies in the dorsal part of the abdominalcavity and is a continuation of the ileum. It is usuallya short, straight organ, but in some species, includingthe rhea, the rectum is looped or folded. In the emu,the rectum is adapted to preserve water. The highresorptive capacity may be related to increased fold-ing of the mucosal surface, which increases the sur-face area by a factor of five. The emu has a limitedrenal concentrating ability with a maximalurine:plasma osmotic ratio of only 1.4:1.5.182


506

Intestinal Diseases

EnteritisMany infectious agents can cause enteritis. Table19.1 lists some infectious causes of diarrhea. Infec-tious stunting syndrome (ISS) in chickens (probablyof viral etiology) is associated with an enteritis andinflammation of the pancreatic ducts. Most affectedbirds recover completely after a period of diarrhea.However, some birds develop exocrine pancreatic de-ficiency secondary to blockage of the pancreatic ducts(Colors 19.4 and 19.6).93

IleusIleus (intestinal obstruction) can be defined as acondition wherein the passage of intestinal contentsis arrested or severely impaired. The cause of intes-tinal obstruction may be physical or it may be due toimpaired motor function (paralytic ileus) (Color19.18). Physical causes may be located within thelumen, in the intestinal wall or outside the intestine.Occlusion of the intestinal lumen may be caused byforeign bodies, enteroliths or parasites. Intestinalwall lesions that have been reported to cause stenosis

in birds include tumors, granulomas and strictures(eg, cicatrization tissue induced by foreign bodies).Extraluminal compression may occur from intus-susception, volvulus mesenterialis, volvulus nodo-sus, incarcerated hernia mesenterialis, pseudoli-gaments and adhesions due to tumors or peritonitis.Vascular causes of ileus include embolism and throm-bosis of a splanchnic artery or vein with infarction ofa bowel segment.

Neurogenic causes (paralytic ileus) include lead poi-soning, peritonitis, neuropathic gastric dilatationand enteritis (Figure 19.15).

Once the intestine is obstructed it dilates, and fluidis collected in the intestinal lumen and lost from thecirculation. Clinical signs depend on the site andseverity of the obstruction. The birds become rapidlydehydrated and are severely depressed. In many con-ditions ischemic necrosis of the intestinal wall oc-curs, leading to increased permeability and proteinloss into the intestinal lumen. Resorption of intesti-nal contents, including endotoxins released fromgram-negative bacteria, can cause shock. Usuallycomplete intestinal obstruction in birds caused byintussusception or volvulus is fatal within 24 to 48hours. A more protracted course is common withother causes of intestinal obstruction. Vomiting isusually present in complete mechanical obstruction,although this sign may be absent when the obstruc-tion is in the caudal part of the intestinal tract. Thepassage of feces is diminished or absent. Diarrhea maybe present with partial obstruction. Emaciation is seenwhen the obstruction occurs gradually from a progres-sive disease.

Plain radiographs may show the extent and locationof the gas-filled intestinal loops. A barium enema orupper GI contrast study may be used to determinethe exact location of the obstruction. The use of dou-ble contrast techniques facilitates visualization oflesions in the intestinal wall. Early diagnosis andrapid surgical correction may successfully resolvemany intestinal obstructions. Birds should be stabil-ized with fluids and antibiotics before surgery.

IntussusceptionIntussusception of the distal part of the small intestineis occasionally reported in young gallinaceous birdssecondary to enteritis or spasmodic antiperistalsiscaused by a nematode infection or coccidiosis. The af-fected part of the intestine rapidly becomes necrotic,inducing adhesions with neighboring tissues. Deathusually occurs from peritonitis and toxemia.93

FIG 19.15 A twelve-week-old Blue and Gold Macaw chick waspresented for anorexia, depression and regurgitation of three days’duration. The abdomen was severely distended and doughy. Heartsounds were muffled dorsally, and severe dyspnea occurred follow-ing minimal exercise. A modified transudate was collected byabdominocentesis. Abnormal clinical pathology findings included:WBC=4500, AST=800 and LDH=1200. Radiographs indicatedgaseous distention of the bowel. The bird did not respond to suppor-tive care. At necropsy, the abdomen was filled with yellow fluid,and the bowel loops were distended with gas and were blue-blackin coloration. Histologic findings were suggestive of avian viralserositis. The bird’s sibling died following a similar clinical disease.


507

In 19 cases of intestinal intussusception in gallina-ceous birds and ducks, 15 cases involved the smallintestine, three cases involved the ceca and one caseinvolved the rectum. The middle and distal parts ofthe small intestine were usually involved. The begin-ning of the intussusception was usually located about30 cm proximal to the ileocecal junction in chickensand 10-20 cm proximal in ducks. In one bird thedistal end of the small intestine was invaginated intothe rectum, while in another bird, 5 cm of the smallintestine was prolapsed through the cloaca. In onecase of cecal intussusception, the cecum passedthrough the rectum, and the black-red color of theapex could be seen in the cloaca. In the other cases ofcecal invagination, part of the cecum was invagi-nated into itself. Invagination leads to partial ob-struction with accumulation of fluid and gas proxi-mal to the affected site. Rectal intussusception,which can lead to rectal prolapse, has been reportedin gallinaceous birds and has been noted in Psittaci-formes.51

Volvulus MesenterialisVolvulus mesenterialis can be defined as the twistingof a portion of the intestine around its mesentericattachment. Volvulus mesenterialis jejuni has beenreported in chickens, ducks and pigeons.51 The pres-ence of stalked tumorous egg follicles with associatedadhesions and stalked mesenteric cysts are commonpredisposing factors. In one case (pigeon), a heavyascarid infection was present. In the other cases,enteritis was present, which may have predisposedthe birds to mesenteric torsion. In one case, a fecalithcaused obstruction and torsion of the rectum justproximal to the junction with the cloaca. The entirerectum was filled with fecal material and gas. In theostrich, torsion of the large bowel has also been re-ported.209 It is speculated that an abrupt change infeed may be a predisposing factor.

Volvulus NodosusVolvulus nodosus can be defined as twisting of anintestinal loop around itself. Volvulus nodosus is usu-ally seen in conjunction with a volvulus mesenteri-alis jejuni but may occur independently. Predispos-ing factors include adhesions and antiperistalticmovements induced by intestinal ulcerations, heavyascarid infestations, accumulation of sand, foreignbodies and tumors.

Occlusion of the bowel can occur if intestinal loopsherniate through tears in the mesentery or throughthe abdominal wall.51 Abdominal herniation is par-ticularly common in egg-laying hens, and may be

associated with trauma, abdominal masses, eggbinding, tenesmus or endocrine abnormalities.

Other reported causes of intestinal obstruction in-clude a stone lodged near the boundary between theduodenum and jejunum, sloughed koilin layer in apigeon obstructing the distal part of the rectumwhere it joins the cloaca, and phytobezoars lodged inthe distal part of the ileum or distal part of therectum. Acute death was caused by rupture of anintestinal diverticulum in two of these cases andintestinal hemorrhage in one case. Other affectedbirds died eight to ten days after developing clinicalsigns, probably due to shock and absorption of intes-tinal toxins.51 Sarcoma of the small intestine, anabscess or a cyst in the distal part of the rectum,diphtheritic enteritis with obstruction in the distalpart of the small intestine and a stenosis caused bycircular cicatrization tissue in the small intestine orrectum have also been reported as causes of intesti-nal obstruction.

Persistently feeding voluminous feedstuffs of poornutritional value caused intestinal impaction in agroup of Galliformes, Anseriformes and Columbifor-mes. In some cases, the entire gastrointestinal tractwas involved. In others, the small intestine, rectumor cecum was the major site of impaction. Obstruc-tion of the small intestine, which may progress torupture, may be caused by ascarids or cestodes inGalliformes, Anseriformes, Falconiformes, Psittaci-formes or Passeriformes (see Figure 36.30).91,93,154

Esophageal and intestinal perforations in turkeysoccurred following the ingestion of grasshoppers.215

Intestinal perforation by fir cones and glass havebeen reported in Tetraonidae.4

Coligranuloma: Hjarre’s DiseaseA coliform-induced granulomatous disease (Hjarre’sdisease) has been reported in captive75 and free-rang-ing Galliformes. Clinical signs are not specific andinclude emaciation and diarrhea. Large lesions maycause intestinal obstruction. Granulomas may also oc-cur in the liver, ceca (which may be very large), duode-num and mesentery. The lesions should be differenti-ated from leukotic neoplasms and tuberculosis.


508

The Cloaca


The cloaca consists of three compartments: the co-prodeum, which is directly continuous with the rec-tum; the urodeum, which contains the openings ofthe ureters and genital ducts; and the proctodeum,which opens to the outside through the lips of thevent.130 The coprodeum is separated from theurodeum by the coprourodeal fold, while theurodeum and proctodeum are separated by the uro-proctodeal fold (Figure 19.16). A striated sphinctermuscle controls the action of the vent. In the cock, thephallus, if present, lies on the crest of the ventral lipof the vent. It consists of a median phallic bodyflanked on either side by a lateral phallic body andlymphatic folds. Tumescence of the phallus is due to

lymph, which f lows from theparacloacal vascular bodies that liein the ventrolateral walls of theurodeum. In the detumescent state,the phallus is directed toward theinterior of the cloaca. This type ofphallus is called non-intromittent,because it does not enter the cloaca ofthe female but is merely applied tothe protruded oviduct of the female.In adult male ducks and ratites, adistinct phallus is present that is in-serted into the female cloaca duringcoitus. The male Vasa Parrot also hasa large copulatory organ that swellsconsiderably during the breedingseason. This physiologic phenome-non in the Vasa Parrot should not beconfused with cloacal pathology.

The cloacal bursa (bursa of Fabricius)is a dorsomedian pear-shaped diver-ticulum of the cloacal wall (see Figure5.6). In chickens, it reaches its maxi-mum size at six weeks when it meas-ures 3 x 2 x 1 cm and weighs about 4grams. It then begins to regress atabout 8 to 12 weeks of age, and by 20months it weighs only 0.5 g. In theadult, a nodular remnant of thebursa can be identified. In ratites,the neck of the bursa has a wide lu-

men, which does not occur in other avian species. Inthese birds, the proctodeum and cloacal bursa formone single cavity. The unusually wide entrance to thebursa is often incorrectly identified as a urinary blad-der. The bursa is the site of differentiation of B-lym-phocytes, which play an important role in the hu-moral defense system of the body (see Chapter 5).

During defecation, the coprourodeal fold protrudesthrough the vent to prevent fecal contamination ofthe urodeum and proctodeum. Similarly, the uroproc-todeal fold protrudes through the vent during egglaying. Urine deposited in the urodeum moves retro-grade into the rectum (and ceca, if present), wherereabsorption of water takes place. Often birds willhave watery excreta when they are excited, becausethey defecate before water reabsorption is complete.

Clinical Examination

Clinical signs indicative of cloacal disorders may in-clude flatulence, tenesmus, soiled pericloacal area,

FIG 19.16 The cloaca is composed of the 1) coprodeum, 2) urodeum and 3) proctodeum.The 4) openings of the ureter and 5) vagina can be seen in the urodeum. Other structuresassociated with the cloaca include the 6) rectum, 7) cloacal bursa, 8) oviduct and 9) vent.


509

protruding tissue from the cloaca and foul-smellingfeces. Examination of the cloaca should start withthe feathers and skin around the vent. Normallythese structures should be clean, and there should beno signs of inflammation (Color 19.8). An abnormalacidic smell can be a sign of cloacitis, which is oftenassociated with cloacal papillomatosis.

Cloacal Diseases

Cloacal ProlapseA prolapse involving the cloaca may contain intes-tines, oviduct and one or both ureters. The appear-ance of smooth, glistening, pink tissue is an indica-tion that the cloaca has prolapsed, which may becaused by sphincter problems, chronic irritation ofthe rectum or tenesmus. A cloacal prolapse maycause severe constipation and toxemia (Color 19.10).In gallinaceous birds, cannibalism by cage matesmay result in cloacal rupture and evisceration of theaffected individual.

Acute cloacal prolapse associated with egg layinggenerally responds to manual reduction, followed by

application of two simple transverse stay suturesperpendicular to the vent. Postoperative strainingcan be prevented by applying xylocaine gel in thecloaca BID. The cause of the straining or increasedabdominal pressure should be corrected to preventfurther prolapsing.

In cockatoos, chronic cloacal prolapse may be associ-ated with sexual behavior in the presence of theowner, or can be caused by idiopathic straining (Fig-ure 19.17). A combination of ventral cloacopexy173 andcloacal mucosal “reefing” has been used to correctchronic cloacal prolapse (see Chapter 41).

CloacitisA sporadically occurring, chronic inflammatory pro-cess of the cloaca with a very offensive odor, com-monly known as “vent gleet,” may occur in layinghens and occasionally in males. A yellow diphtheriticmembrane may form on the mucosal surface, andurates and inflammatory exudate contaminate theskin and feathers around the vent. The cause isunknown. Treatment consists of cleaning the areaand applying a local antibiotic ointment.93

A similar condition has been reported in ducks. Scar-ring, which reduces the elasticity and diameter of thecloaca and may prevent egg laying and, in extremecases, defecation, is a complication of cloacitis (Fig-ure 19.18).71,93

FIG 19.17 A two-year-old Umbrella Cockatoo was presented witha four-day history of tenesmus. The bird was fed a seed-based dietand was constantly demanding affection from its owner. Physicalexamination findings included the accumulation of excrementaround the vent and protrusion of a smooth, glistening, pinkcloaca. The bird had a moderate number (15%) of gram-negativebacteria in the feces and was placed on injectable enrofloxacin andmedroxyprogesterone acetate. The mucosa of the cloaca was coatedwith apple cider vinegar to check for papillomas. None were de-tected. The bird responded to the antibiotic and hormone therapyas well as to a change in diet to a formulated product and behaviormodification. The tenesmus stopped, and there were no furtherproblems with cloacal prolapsing.

FIG 19.18 A four-year-old male Amazon parrot was presentedwith a history of straining to defecate and emitting a foul odor. Alarge pericloacal mass was palpable on physical examination. Themass was ulcerated, hyperemic, moist and associated with a yel-lowish-green discharge. Cytologic evaluation of samples collectedfrom within the mass revealed gram-negative rods, degranulatingheterophils and macrophages containing bacteria. Radiographsshowed an extensive pericloacal mass that was causing cloacaldistention (arrows) and cranial displacement of the intestines. Themass was surgically debrided, and the bird was successfullytreated with piperacillin.


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Neisseria, Mycoplasma spp.and Candida albicans

Bacteria (especially Neisse-ria and Mycoplasma spp.),and Candida albicans havebeen associated with a vene-real disease affecting gan-ders.9,14,188 It seems likelythat the cloacitis observed indrakes has a similar etiology,but an association has notbeen confirmed.

Cloacal infections may occa-sionally be observed in otherspecies and may result fromtrauma, surgery or infectiousdiseases. Uroliths or fe-caliths may form during theprocess. Cloacitis is often seen in psittacine birdssuffering from cloacal papillomatosis.

Phallus Prolapse and Venereal Disease in AnseriformesThe phallus may not retract into the cloaca in somesexually mature drakes. The problem is usually as-sociated with an extensive infection in the erectiletissue at the base of the phallus. It has been sug-gested that the etiology of this condition is traumatic,because the incidence is higher under conditionswhere the drakes have to mate with the females outof the water.71 Drakes with females that have cloaci-tis may have a phallus infection, suggesting that aninfectious agent can play a role in phallus prolapse.

Cloacal StrictureInfections, surgical manipulation of the cloaca (par-ticularly for removal of papillomas) and trauma maycause stricture of the vent, requiring surgical recrea-tion of an opening and appropriate aftercare to pre-vent a recurrence.173

Cloacal ImpactionCloacal impaction may occur from foreign bodies (eg,potato chunks in Galliformes), fecaliths, concre-ments of urates and retained necrotic eggs (Figure19.19). Uroliths can vary from six to eight millimeter-thick concrements on the cloacal wall to solid massesthe size of a chicken egg. In any case of cloacalimpaction, passing excrement is difficult or impossi-ble and can cause congestion of the ureters and dila-tation of the intestines as far proximal as the duode-num. Renal failure and visceral gout may occur if theureters are blocked.51

Cloacoliths composed of urates have been observed innumerous psittacine birds, particularly macaws andAmazon parrots.173 The etiology is unknown. Treat-ment consists of segmenting and removing the con-crements. Cloacal impaction may also occur secon-dary to cloacal infections and cloacal stricture(Figure 19.20).

Cloacal papillomatosis is a well known disease inpsittacine birds and is recognized clinically as a glis-tening red or pink cauliflower- or strawberry-likemass rising from the cloacal orifice (Color19.9).42,67,86,112,173,190,196,200 Early lesions are charac-terized by a rough-appearing mucosa at the mucocu-taneous junction of the cloaca. Other presentingsigns may include tenesmus, melena, foul-smellingfeces, flatulence, pasting of the vent and cloacoliths.The abnormal odor is likely to be caused by bacterialproliferation in the crypts caused by the papillomas.The incidence of disease is higher in New Worldparrots, but Old World parrots may also be affected.69

The condition is frequently misdiagnosed as a cloacalprolapse. Applying an acetic acid solution (apple ci-der vinegar) to cloacal epithelium will change thecolor of papillomatous tissue to white. A definitivediagnosis can be made after histopathologic exami-nation of a biopsy. Cloacal papillomas are often asso-ciated with similar lesions in the oropharynx, cho-ana, esophagus, crop, proventriculus, ventriculusand occasionally mucosa of the eye and nose.67 Theetiology is presently unknown. There seems to be ahigh correlation between neoplasia of bile ducts andpancreatic ducts and papillomatosis in psittacinebirds.41,69,86,159

FIG 19.19 A mature Amazon parrot was presented with a two-day history of depression, anorexiaand straining to defecate. The abdomen was distended. When a cotton swab was inserted into thecloaca, excrement would “squirt” out. When the swab was removed, no excrement would be released.Several uroliths that were functioning as a valve were identified at the opening of the cloaca. Whenthe uroliths were removed, the bird was able to defecate normally.


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Various techniques have been used to treat cloacalpapillomas, including cryosurgery, chemical cautery,radiosurgery and autogenous vaccination,173 but thereported spontaneous remissions and intermittentnature of the disease67,69,129,200 makes evaluation ofthe various treatments difficult. The introduction ofbirds with papillomas to a breeding facility should beprevented by performing a thorough physical exami-nation at the beginning and end of the quarantineperiod. Of 41 papillomatous lesions, growth was be-nign in 40, but one single case was diagnosed ascarcinoma in situ.190 Other tumors should be consid-ered in the differential diagnosis.13,58,15,163 Papillomasare most easily removed from the cloaca with careful,staged cauterization with a silver nitrate stick. Thesilver nitrate must come in contact only with thetissue intended to be removed to prevent severeburns of normal cloacal mucosa (Color 19.9).

The Pancreas


The pancreas is situated on the left ventral side ofthe abdominal cavity between the descending andascending loops of the duodenum. There are threelobes: dorsal, ventral and splenic. The dorsal andventral lobes are usually connected (except in theMallard and pigeon). The splenic lobe extends crani-ally from the dorsal or ventral lobe. There are one,two or three pancreatic ducts, which usually drainthe pancreatic secretions into the ascending part ofthe duodenum. The exocrine pancreatic enzymesthat are present in the duodenum include amylase,lipase, trypsin and chymotrypsin, which facilitatedegradation of carbohydrates, fats and proteins, re-spectively. Trypsin and chymotrypsin are secreted asinactive precursors, and they become active onlywhen they enter the duodenum. The activator is thelocally produced enzyme, enterokinase, whichchanges trypsinogen to trypsin. This prevents thepancreas from being digested by its own enzymes.49

FIG 19.20 A ten-year-old Blue-fronted Amazon Parrot was presented with depression, failure to defecate and a distended abdomen. Thereferring veterinarian had placed a purse-string type suture to correct what was diagnosed as a cloacal prolapse three days beforepresentation. The abdomen was distended and tight. Unproductive tenesmus was noted by a constant “winking” of the cloaca. Thepurse-string suture was removed and the bird released a large quantity of excrement; however, the tenesmus continued. Survey radiographsrevealed several elongated mineralized masses in the cloacal area (arrows). Three large uroliths were removed from the cloaca with forceps.The cloacal mucosa was hyperemic and ulcerated. A large cloacal papilloma was evident in the left lateral wall of the cloaca. The papillomawas cauterized by specific application of silver nitrate, and the cloaca was flushed with a dilute povidone-iodine solution. Removal of thepapilloma required two further treatments. Papillomas that protrude from the cloaca must not be confused with a cloacal prolapse, asinitially occurred in this case.


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Diagnostic Considerations

The pancreas has both endocrine and exocrine func-tions. The former are discussed in Chapter 23. Manypostmortem lesions have been reported in avian pan-creata.70 There are two major clinical manifestationsof pancreatic disease. If no pancreatic enzymes areavailable in the duodenum, maldigestion and pass-ing of feces with excessive amylum and fat will occur.Affected animals may have voluminous, pale or tan,greasy feces (see Color 8). Fat in the feces can bedemonstrated by Sudan staining. Interpretation ofmicroscopic examination of feces for undigested foodsuch as fat, starch grains and muscle fibers is compli-cated by variation in diets and by changes due tointestinal causes of malabsorption. Measurement offecal proteolytic activity can be performed in severalways. The X-ray film gelatin digestion test is anunreliable assay of fecal proteolytic activity.217 A testfor fecal proteolytic and amylase activity is probablymore reliable for use in birds.214

Pancreatic Diseases

Acute Pancreatic Necrosis/Acute PancreatitisThe pathogenesis of acute pancreatitis involves theactivation of pancreatic enzymes in and around thepancreas and in the bloodstream, resulting in coagu-lation necrosis of the pancreas, and necrosis andhemorrhage of peripancreatic and peritoneal adiposetissue (see Color 14). Affected birds may be in shock,and radiographs may show loss of abdominal detaildue to peritonitis and fluid accumulation in the peri-toneal cavity. Dilatation of the small intestine may bevisible due to an accompanying ileus. Increasedplasma amylase activity (secondary to destruction ofexocrine pancreatic cells) has been reported inchronic active pancreatitis in birds. Elevated plasmaamylase may also occur with occlusion of the mainpancreatic duct,164 and might be a component of theinfectious stunting syndrome in chickens.181 Lipemiamay be present. A diagnosis of pancreatitis can beconfirmed by endoscopy or exploratory laparotomy.

Obesity seems to be a predisposing factor of pancrea-titis in birds. Treatment should include withholdingfood and oral medication for 72 hours, correction offluid and electrolyte balance and prophylactic use ofantibiotics. Dietary fat intake should be restricted todecrease the secretory load of the pancreas.70,158

Chronic Pancreatic Fibrosis/Chronic Pancreatitis/Pancreatic Exocrine Insufficiency

A decrease in pancreatic glandular tissue or fibrosismay occur as the result of a chronic inflammatoryprocess and cause clinical changes suggestive of pan-creatic exocrine insufficiency (PEI).70,160 Furtherstudies on the relation between pancreatic diseaseand plasma amylase and plasma lipase activities inbirds are needed to facilitate clinical diagnosis; how-ever, birds with a malabsorption syndrome and highamylase and lipase levels may respond to therapywith pancreatic enzymes, suggesting PEI. Fre-quently, the cause of PEI is undetermined. Pancre-atic fibrosis was reported in two psittacine birds withchronic chlamydiosis.70

High dietary levels of zinc may cause dilation ofacinar lumina and degenerative changes in acinarcells including depletion of zymogen bodies, cytoplas-mic vacuolization, the presence of hyaline bodies andother electron-dense debris, necrosis of individualacinar cells and fibrosis.46,48,98,204,216 Excess levels ofzinc also interfere with exocrine pancreatic func-tion.118

Pancreatic atrophy and fibrosis accompanied by im-paired fat digestion have been reported in chickenson a selenium-deficient diet.192,193 It has been shownthat addition of 0.1 ppm selenium to the diet couldreverse the clinical signs and cause complete pancre-atic acinar regeneration.72

Infectious Stunting Syndrome (ISS)Infectious stunting syndrome (ISS)93,1709 has manysynonyms including runting and leg weakness,104

runting syndrome,147 infectious stunting,19,171 palebird syndrome,65,116,142 malabsorption syndrome,142

brittle bone disease,199 diarrhea and stunting,93 runt-ing and stunting syndrome,165 and stunting and runt-ing syndrome.125 Clinical signs include growth retar-dation, steatorrhea, polyphagia, coprophagia, softbones, swollen tibial epiphyses, rachitic ribs and ab-normal feather development. The latter is possiblyrelated to decreased circulating concentrations ofthyroxine (see Chapter 23).93,170

Although the etiology of this disease is not known, avirus is likely to be the etiologic agent,170 but myco-toxins, other toxins, Campylobacter spp. and spiro-chetes may also be involved.93,189 Chickens, turkeysand guineafowl have all been documented with thisdisease. Most birds develop enteritis and inflamma-tion of the pancreatic ducts and recover completelyafter a prolonged period of diarrhea.93


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Pancreatic lesions are thought to be incited by in-flammatory reactions in the pancreatic ducts, whichmay result in complete blockage of the pancreaticducts in a small proportion of affected birds. Blockageleads to vacuolization and shrinkage of exocrine cellsand atrophy of the acini. As the disease progresses,much of the exocrine tissue is obliterated by fibro-plasia. The changes are similar to those induced afterexperimental ligation of the pancreatic ducts.124,126

The resulting exocrine pancreatic insufficiency leadsto maldigestion,173 steatorrhea and inappropriate ab-sorption of fat-soluble vitamins. The skeletal changesare likely to be related to reduced absorption of vita-min D and calcium, the latter being bound to theexcessive amounts of fat and excreted in the feces.93

Paramyxovirus Infections inPsittaciformes and Passeriformes

Paramyxovirus type III is a common infection inNeophema spp. and Platycerca spp., and is also en-countered in some passerine birds, especiallyEstrildidae.184,198 Torticollis, other neurologic signs,cachexia and death are common. Some infected birdsdevelop a yellow-to-white chalky stool that containslarge amounts of starch. In almost all cases, a pan-creatitis can be detected. Histologically, the lesionscan vary from a few lymphoid follicles to massiveinfiltration with lymphocytes and plasma cells. Insome cases, this is clinically manifested as pancreaticexocrine insufficiency.

Campylobacter infections in Estrildidae cause simi-lar discoloration of the feces. Histologically, atrophyof the microvilli of the small intestine, which maycause a malabsorption syndrome, can be found.47

Pancreatic TumorsA high correlation between neoplasia of bile ductsand pancreatic ducts and internal papillomatous dis-eases in psittacine birds has been suggested.41,69,86,159

The Pleuro-peritoneum


The coelomic cavity in birds is subdivided by perito-neal, pleural and pericardial reflections into eightdifferent cavities, excluding the eight cavities thatare formed by the air sacs. Birds do not have a

diaphragm. They have two pleural cavities and fiveperitoneal cavities (Table 19.8). Clinically, these cavi-ties dictate the location and spread of pathologicprocesses within the coelomic cavity and are impor-tant when considering surgical approaches to theabdominal organs (see Color 13, Anatomy Overlay).

As in mammals, both the parietal and the visceralpleura are reflected over the lungs, but in birds alarge surface of the parietal pleura is joined to thevisceral pleura by fibrous strands. The degree ofobliteration of the pleural space depends on the spe-cies. In some birds, including the domestic fowl, ex-tensive areas of pleural cavity persist in the adult (inthe chicken, dorsolateral). In these areas the lungscan collapse inward when the pleural cavity isopened. Some fluid can accumulate in these areasunder certain disease conditions.

The pericardium in birds is essentially similar tothat in mammals. Because the lungs are situateddorsally and there is no diaphragm, the heart is notenclosed by the lungs. The liver lies on both sides ofthe heart, and the parietal pericardium becomes con-tinuous with the peritoneum. During embryonic de-velopment, the pleural cavity becomes separatedfrom the peritoneal cavity by the pulmonary fold,which is a double-layered sheet formed by the parie-tal pleura (dorsal) and the parietal peritoneum (ven-tral). The cranial and caudal thoracic air sacs developas dilatations from the bronchi and penetrate intothis double-layered sheet, splitting the dorsal fromthe ventral layer. The dorsal layer becomes fusedwith the adjacent wall of the thoracic air sac, be-comes tough and tendinous and acquires fascicles ofstriated muscle along its lateral edge that attach tothe ribs (costoseptal muscle). This is called the hori-zontal septum, saccopleural membrane or pulmo-nary aponeurosis. The ventral layer becomes fusedwith the ventral walls of the thoracic air sacs and iscalled the oblique septum, which occurs bilaterally.

TABLE 19.8 Reference Guide to the Coelomic Cavities in Birds

Right pleural cavity (RPC)

Left pleural cavity (LPC)

Pericardial cavity (PC)

Left ventral hepatic peritoneal cavity (LVHPC)

Right ventral hepatic peritoneal cavity (RVHPC)

Left dorsal hepatic peritoneal cavity (LDHPC)

Right dorsal hepatic peritoneal cavity (RDHPC)

Intestinal peritoneal cavity (IPC)


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Unlike the horizontal septum, the oblique septae orsaccoperitoneal membranes remain thin and looklike air sac walls.

The partitions in the peritoneal cavity proper areformed by five sheets of peritoneum which, apartfrom the mesentery, do not occur in mammals.

The combined dorsal and ventral mesentery form acontinuous midline vertical sheet from the dorsal tothe ventral body wall as far caudally as the ventricu-lus. Caudal to this level, only a dorsal mesentery ispresent supporting the intestines. Cranially, themesentery is continuous with the pericardium.

The posthepatic septum is composed of a left and aright double-layered sheet. It extends caudal to theliver from the last thoracic vertebra in a ventro-caudal direction to the caudal wall of the peritoneum.The posthepatic septum has connections with thevisceral peritoneum enclosing the liver.

The ventriculus is enclosed between the two layers ofthe left sheet of the posthepatic septum. The princi-pal peritoneal fat depot is located between the twoperitoneal layers of the posthepatic septum. The lat-eral layers of the right and left sheet form the medialwall of the right and left hepatic peritoneal cavities.Because the right and left sheets are fused craniallyand unite in the midline ventrally, the liver is sepa-rated from the rest of the viscera by this posthepaticseptum. The posthepatic septum (together with themesentery) divides the peritoneum into three princi-pal cavities: the intestinal peritoneal cavity dorsome-dially, and two lateral hepatic cavities that enclosethe liver. The left and right hepatic cavities are fur-ther subdivided by the left and right hepatic liga-ments, which run horizontally and are continuouswith other peritoneal sheets (medially with the mes-entery, cranially with the parietal peritoneum,caudally with the posthepatic septum and laterallywith the oblique septum), thus forming the LDHPC,LVHPC, RDHPC and RVHPC, respectively. TheLVHPC and RVHPC are large, elongated cavitiesextending from the left and right liver lobe, respec-tively, to the caudal body wall. The LDHPC andRDHPC are much smaller and are in contact with thecraniodorsal aspects of the left and right liver lobes.The IPC is enclosed between the left and right he-patic cavities and extends from the liver to the vent.The intestines and gonads are suspended by mesen-teries within the IPC. Each peritoneal cavity is blindand has no connections, except for one that existsbetween the IPC and the LDHPC. The peritoneum

plays an important role in the defense system of thebody by closing perforations, containing infection andproviding blood supply. The peritoneum heals rapidlyafter damage. Peritoneal injuries normally healwithout the formation of adhesions, but in the pres-ence of infection, ischemia or foreign bodies, fibrousadhesions may occur. The peritoneal surface allowsthe passive diffusion of water and solutes of lowmolecular weight between the peritoneal cavitiesand the subperitoneal vasculature. Larger moleculesand particulate matter enter the bloodstream via thelymphatics. Healthy birds have a thin film of fluid inthe peritoneum, which facilitates organ movement.The presence of free fluid in the peritoneal cavities isconsidered pathologic.

From the anatomic relationships outlined above, it isclear that diseases associated with the female genitaltract (ovarian adenocarcinoma with implant metas-tasis on the peritoneum, egg-related peritonitis) areoften confined to the IPC and LDHPC. Peritonitisfrom gastric perforation may be restricted to theLVHPC. Rupture of the liver can lead to accumula-tion of blood in one of the hepatic peritoneal cavities.Accumulation of transudate is most often seen in theLVHPC and the RVHPC and the PC, although thedorsal hepatic and peritoneal cavities may some-times be involved. It is even possible to see some fluidaccumulate in the RPC and LPC.

Ascites

Ascites is defined as the accumulation of serous fluidwithin one or more of the peritoneal cavities and maybe caused by peritoneal and extraperitoneal diseases.Accumulation of fluid in one or more peritoneal cav-ity can result in abdominal distention. Largeamounts of ascitic fluid may compress the pulmonaryair sac system, causing dyspnea. During physicalexamination, abdominal distention can be recognizedby the increased distance from carina to pubic bones.A bird with ascites should be handled carefully toprevent rupture of the air sacs, which can lead toimmediate asphyxiation. Clinical signs may or maynot occur with abdominal fluid accumulations. Inliver disease, yellow or green feces may be seen. Inneoplastic or liver disease, palpable masses may bepresent in the abdomen (Figure 19.21).

In ascites associated with liver disease (includinghepatic congestion due to cardiac disease), increasedportal venous hydrostatic pressure and decreasedportal venous colloid osmotic pressure are importantfactors. Increased subperitoneal capillary permeabil-


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ity, decreased peritoneal lymphatic drainage andleakage from disrupted abdominal viscera (bile,urine) may cause non-liver-related ascites. Some-times the definition of ascites is restricted to non-in-flammatory transudate,44 but the distinction be-tween transudate and exudate is not always clearunder clinical conditions. Conditions where an in-flammatory exudate is present can be defined asperitonitis.

Although it has been suggested that chylous ascites(ascites due to the presence of lipoproteins and chy-lomicrons in the peritoneal cavity) can occur inbirds,44 current information on avian physiology sug-

gests that the absorption of fat from the intestine inbirds is different from what occurs in mammals. Thelymphatic system is not as well developed in birds asin mammals. The lymphatic vessels are small, thelargest being hardly more than 1 mm in diameter,and the thoracic duct is only 1.5 mm across.148 Be-cause there is no functional intestinal lymphatic sys-tem in birds, absorbed lipids enter the portal systemas large, very low-density lipoproteins. These lipo-proteins have been defined as “portomicrons” in con-trast to “chylomicrons” (the fat-rich particles that areabsorbed by mammals).16 Chylous peritonitis, whichoccurs in mammals secondary to rupture of the lym-phatic vessels or lymphatic congestion, is thereforetheoretically not possible in birds.

Blockage of lymph drainage can be an importantfactor in the development of ascites in birds. Forexample, implantation of oviduct carcinoma on theintestinal peritoneal cavity rapidly induces ascitesfrom portal hypertension secondary to pulmonaryhypertension. Right ventricular failure with valvularinsufficiency results in increased pressure in thevena cava where the lymph ducts connect to thecirculatory system.93

Pseudochylous ascites is the condition whereby tur-bid or milky abdominal fluid is seen. This may becaused by cellular debris and is associated with ab-dominal malignancies and infections.57 A goose witha severe fatty degeneration of the liver accompaniedby extreme hepatomegaly and hyperlipemia devel-oped severe dyspnea secondary to pseudochylous as-cites of unknown origin. A milky-appearing asciticfluid was demonstrated in the ventral hepatic perito-neal space by laparotomy. Removal of 0.5 liter ofascitic fluid and diuretic therapy decreased the dysp-nea. The concentration of total triglycerides in theascitic fluid was 55 mmol/l, while total triglyceridesin the plasma was 77 mmol/l. The ascit icfluid:plasma triglyceride ratio in this bird was oppo-site to what would be expected in chylous ascites,although the physical characteristics of the fluidwere highly suggestive for this condition.

Edema may occur in organs and tissues in conjunc-tion with ascites caused by hypoalbuminemia. It maybe recognized clinically as edema of subcutaneoustissues of the abdomen or pitting edema on the feet(ducks with amyloidosis).

FIG 19.21 A mature caique was presented with a two-week historyof progressive dyspnea and abdominal swelling. Note the distalprotrusion of the abdomen. Fluid collected by abdominocentesiswas yellow and was characterized as a transudate (SpGr=1.012,Protein=1.8 mg/dl, few cells). The liver was swollen and the bloodwas lipemic. An exploratory surgery was performed, at which timea soft-shelled egg was removed from the uterus. Soft-shelled eggsare most often related to a primary etiology of malnutrition, whichresults in the fatty liver, lipemia and dystocia leading to possibleegg-related peritonitis.


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Diagnostic Methods

Radiographically, ascites is characterized by a dif-fuse, ground-glass haziness in the abdomen, and spe-cific organs are often impossible to delineate. Ad-ministration of furosemide for several days or ab-dominocentesis will increase the diagnostic value ofthe radiographs. The cardiohepatic silhouette mayappear widened, and the air sacs may appear nar-rowed laterally on the ventrodorsal view. Occasion-ally, ileus or enlargement of the heart, liver, spleen orother abdominal organs may be detected, providinginformation with respect to the primary disorder.Ultrasonography is a noninvasive technique that isvaluable in the differential diagnosis of abdominalenlargement and ascites (see Chapter 12).27,100

Abdominocentesis provides diagnostic information inbirds with ascites (see Chapter 10).33 Peritoneal lav-age is possible, but extreme caution should be prac-ticed to prevent iatrogenic puncture of the pulmonaryair sac system and asphyxiation of the bird. Abdomi-nocentesis should be performed when one is certainthat free fluid is present to prevent inadvertent organpuncture. Transudate is characterized by a clear topale-yellow color, a low specific gravity (<1.020), lowprotein (1 g/dl) and a low cellularity. Exudate is char-acterized by a high specific gravity (>1.020), a highprotein content (3 g/dl) and possible presence of manyinflammatory and mesothelial cells. Exudates mayclot during sampling and may require an anticoagu-lant for proper cytologic examination. Septic exu-dates contain intracellular bacteria. Identifying awide variety of bacteria suggests perforation of thegastrointestinal tract or the abdominal wall.

Clinical Biochemistry and HematologyLaboratory investigations in birds with ascitesshould include plasma chemistries for hepatic andrenal disease (AST, CPK, LDH, bile acids, proteinelectrophoresis, uric acid, urea). Renal protein lossshould be evaluated by a quantitative determinationof protein in the urine. Additionally, a PCV and totalWBC and differential are indicated. When peritonitisis present, a marked leucocytosis can be observed,with the predominant cell type being heterophilicleukocytes. Juvenile heterophils (band cells) are nor-mally not present in the peripheral blood and indi-cate severe inflammation. Granulomatous diseasesand avian tuberculosis are often associated withmonocytosis.

In neoplastic disease, exfoliated neoplastic cells maybe encountered. Hemorrhagic effusions may have the

appearance of peripheral blood and have leukocyteand erythrocyte numbers comparable to peripheralblood. Chronic hemorrhagic effusions may showsigns of erythrophagocytosis. Urine in the abdominalcavity can be recognized by the presence of sphericalurate crystals.

In mammals, LDH and the ascites serum protein andLDH ratios are helpful in differentiating betweenexudates and transudates.15 The ascitic fluid amy-lase:plasma amylase ratio is useful for the diagnosisof pancreatic ascites. Ascitic fluid with a milky ap-pearance and a triglyceride:plasma triglyceride ratio<1 is suggestive of pseudochylous ascites becausechylous ascites does not occur in birds.

Differential Diagnosis44,62,71,89,97,112,170

Abdominal enlargement due to ascites should be dif-ferentiated from other causes of abdominal enlarge-ment such as obesity, neoplasia, herniation, egg-re-lated peritonitis, granuloma, gravid uterus, gastroin-testinal dilatation, hepatomegaly, splenomegaly andrenomegaly. A cystic right oviduct can also pose adiagnostic challenge to the clinician because thesefluid-filled cysts may reach a size up to 10 cm indiameter and may compress the abdominal viscera,mimicking ascites.

Chronic liver disease can cause ascites through intra-hepatic portal hypertension due to hepatic fibrosis(aflatoxicosis, coal tar poisoning, plant toxins fromCrotalaria spp. or rapeseed, bacterial or viral cho-langiohepatitis). The accompanying hypoalbu-minemia contributes to ascites formation. Bloodchemistries, bile acids, low plasma albumin and liverbiopsies are useful diagnostic techniques. Ascitesfrom chronic liver disease is common in Anseriformeswith amyl-oidosis and in mynahs, toucans and birdsof paradise with iron storage disease.

Ascites may occur as part of generalized edema sec-ondary to hypoalbuminemia caused by chronic liverdisease, nephrotic syndrome and protein-losing en-teropathy.

Neoplasias, particularly abdominal carcinomas (es-pecially ovarial adenocarcinoma with implants onintestinal peritoneal cavity), may block lymph drain-age, causing ascites with a high-protein content thatcontains neoplastic cells.

Congestive heart failure (right ventricular failure;RVF) is a common cause of ascites in gallinaceousbirds and ducklings that are raised at high altitudes


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and forced to grow at a rapid rate. Low environ-mental temperature and high-sodium diets havebeen associated with RVF and ascites in chickensand turkeys. Furazolidone causes cardiomyopathy inturkeys, ducks and chickens. Fusarium moniliformevar. subglutans produces the mycotoxin monili-formin that induces myocardial degeneration withassociated hydropericardium and ascites in chicks,ducklings and turkey poults. RVF and ascites mayalso be associated with rickets. Congenital ventricu-lar septal defect can cause a left to right shunting ofblood and result in RVF and ascites. Numerous drugshave been shown to cause cardiovascular malforma-tions in chick embryos.

Exposure to chlorinated biphenyls, dioxin (toxic fatsyndrome), creosol and coal tar products can damagethe endothelial lining of blood vessels, causing hy-dropericardium and ascites.

Viral infections such as Marek’s disease tumors mayoccur in the heart, and viruses of the leukosis-sar-coma group can cause various tumors associatedwith ascites (hemangioma and hemangiosarcoma ofmesentery, erythroblastosis, mesotheliomas). Otherviruses including avian polyomavirus and avian viralserositis can cause myocarditis and pericarditis lead-ing to RVF and ascites.

Bacterial endocarditis and myocarditis may result incardiac insufficiency (RVF) and ascites. Staphylococ-cus, Streptococcus and Erysipelothrix spp. have beenassociated with endocarditis, while bacterial myo-carditis may occur in listeriosis, pullorum disease,fowl typhoid and other bacterial infections. E. coliperitonitis may be associated with ascending infec-tions from the female genital tract.

Mycobacterium spp. infections can cause blockage oflymph drainage in some cases. Acid-fast (Ziehl-Neel-sen) staining organisms may be noted in ascitic fluid.Peritonitis can occur from foreign bodies penetratingthe intestinal tract and secondary to infections in thelungs, air sacs, pericardium, female reproductive or-gans and gastrointestinal tract. E. coli, staphylococciand streptococci can often be isolated in serofibrinousperitonitis in females as a result of ascending infec-tions from the uterus. Aspergillosis air sacculitis canalso involve the peritoneum.

Penetrating or nonpenetrating trauma to the abdo-men can cause urate ascites, bile ascites, pancreaticascites and hemoperitoneum (rupture of liver, spleenor kidney). Enlargement of an organ or other space-

occupying masses can block lymph drainage, result-ing in ascites.

Cystic right oviduct occurs if the right Muellerianduct does not regress normally. The oviduct remnantis attached to the cloaca by a narrow stalk. Ultra-sonography can differentiate between free fluid andfluid encapsulated within a cyst (see Chapter 12).

Therapy for ascites should be aimed at the primarydisorder. Therapeutic removal of ascitic fluid is indi-cated only if ascites is accompanied by a life-threat-ening dyspnea. If hypoproteinemia is present, ab-dominocentesis will remove protein from a bird thatmay have compromised liver or kidney function. Diu-retic therapy (furosemide) can be administered toeffect. Low-sodium diets may be helpful.

Accumulation of fat in the peritoneal cavity cancause dyspnea through compression of the thoracicand abdominal air sacs. Obesity is an importantdifferential diagnosis in birds with dyspnea and ab-dominal enlargement. It is commonly seen in par-rots, cockatoos and pigeons on high-energy diets withrestricted exercise, but many other species can beaffected.

Ventral abdominal hernias are common in budgeri-gars and racing pigeons (particularly hens). A causalrelationship with hyperestrogenism, which causesweakening of the abdominal muscles, has been sug-gested. The hernia may contain fat, loops of bowel orother abdominal organs. Incarceration of the intesti-nal tract is a rare but possible complication. A diag-nosis can be made by physical examination and radi-ology. Treatment involves surgical closure of theabdominal hernia. Removal of excess fat that is pri-marily located between the sheets of the posthepaticseptum facilitates the procedure. A perineal herniacontaining a persistent right oviduct was observed bythe author in a budgerigar.

The most common causes of peritonitis in birds areforeign bodies (from alimentary tract or through ab-dominal wall) and egg-related peritonitis. The lattercondition can be the result of oviduct or ovariandysfunction. Conditions such as false layer, internallayer, impaction of oviduct and torsion of egg yolkfollowed by infarction should be considered. Abdomi-nocentesis is indicated to collect samples for furtherexamination (cytology, culture).


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