| | The anatomy, physiology, and diseases of the avian proventriculus and ventriculus
The morphology of the avian proventriculus and ventriculus is unique among vertebrates, and has evolved to accommodate a wide range of nutritional needs. The proventriculus and ventriculus play a crucial role in providing an adequate environment for the physical and chemical reduction of the size and molecular complexity of a bird's diet. The physiology of avian digestion has been studied primarily in Galliformes, but the knowledge gained from this research offers a valuable starting point in understanding the motility, the release of gastric secretions and the absorption mechanisms of most companion avian species. A variety of diseases can affect the proventriculus and ventriculus. Their respective clinical signs are often difficult to differentiate from one another and from diseases affecting other parts of the gastrointestinal tract. It is important for the practitioner to have an understanding of the conditions affecting the avian proventriculus and ventriculus to determine appropriate diagnostic and therapeutic procedures.
Anatomy of the proventriculus and ventriculus  The avian stomach consists of the proventriculus, the intermediate zone, the ventriculus, and the pylorus. The proventriculus and ventriculus are innervated by vagal and perivascular nerve fibers from the celiac and mesenteric plexii [1]. Cholinergic fibers innervate muscle cells and noradrenergic fibers innervate predominantly blood vessels [1]. The proventriculus is the glandular compartment, which is functionally equivalent to the mammalian stomach. The proventriculus is a fusiform organ that varies in size and shape among avian species, being relatively small in granivorous species and relatively large in carnivorous and piscivorous species (Fig. 1, Fig. 2) [2]. In all birds except carnivore and piscivore species, the mucosal surface of the proventriculus lacks the longitudinal folds characteristic of the mucosal surface of the esophagus and is lined by mucous secreting cells (Fig. 1, Fig. 2). The orifices of the gastric glands are visible to the naked eye at the extremity of the papillae that project into the lumen of the proventriculus. Mucous secreting cells also line the main duct of the gastric gland, and the alveoli of the glands are lined by oxynticopeptic cells, which secrete both hydrochloric acid (HCl) and pepsinogen [3]. The secretions of parietal and peptic cells are produced by a single cell type in birds. The distribution of the gastric glands is not consistent among avian species. Generally, they are distributed throughout the proventriculus, but sometimes are restricted to longitudinal tracts (owls), to a circular patch on the greater curvature (ratites), or to separate diverticula (Anhinga) [2]. The intermediate zone denotes the junction between the proventriculus and the ventriculus. It is the most common location of gastric neoplasms [4], [5], [6], [7]. In the domestic fowl, a constriction or isthmus marks the proximal aspect of the intermediate zone [2], [3]. The ventriculus, also known as gizzard, is the muscular compartment, which has no equivalent in the mammalian gastrointestinal tract. The development of the ventriculus varies among avian species and two basic types are recognized [2]. In granivores, insectivores, and herbivores, the ventriculus is well developed and distinct from the proventriculus (Fig. 1). The ventriculus in these species consists of four semiautonomous smooth muscle regions: the thinner caudoventral and craniodorsal regions, and the thicker caudodorsal and cranioventral regions [3]. Each region originates and terminates on a circular tendinous area. In carnivores and piscivores, the ventricular muscle is poorly developed and uniform in thickness (Fig. 2). The two pairs of semiautonomous muscles are lacking and no clear distinction exists between the proventriculus and the ventriculus in these species. In frugivores and testacivores, the development of the ventriculus is intermediate between these types and lean more towards the well-developed or poorly developed type according to the species [2]. Ratites have a unique stomach anatomy (Fig. 3). The gastric glands of ostriches and rheas are limited to a dorsally located patch [8]. The ostrich has a large, thin-walled proventriculus that passes dorsal to the ventriculus and empties into the ventriculus at its caudal aspect. The opening between the proventriculus and ventriculus is large, which makes removal of ventricular foreign bodies easier in this species. The ventriculus of the ostrich is similar to that of birds consuming a hard diet such as seeds and insects. In rheas, the proventriculus is much smaller than the ventriculus [8]. Their ventriculus is elongated, with a koilin layer also present in the proventriculus. Emus and cassowaries have a large proventriculus slightly smaller than their ventriculus. Their ventriculus is less muscular than other ratites. Cassowaries lack a cuticle [8]. The internal lining of the ventriculus of birds consists of a simple columnar epithelium with crypts containing the opening of tubular glands. The crypts and glands are lined primarily by chief cells, which produce a protein-rich secretion, but also contain endocrine cells. In species with a well-developed ventriculus, a cuticle or koilin layer is present on the surface of the epithelium (Fig. 4). The cuticle is a carbohydrate-protein complex with two distinct components: a scaffolding of interconnecting vertical rods and a horizontal matrix [3]. The vertical rods consist of a protein secretion produced by the chief cells, which hardens into the crypts, and protrude slightly beyond the surface of the ventricular epithelium. The horizontal matrix is formed primarily by secretions of the surface epithelium, but also desquamated epithelial cells. The secretions spread on the surface of the epithelium and around the rods before it hardens. This hardening process is thought to be due to a decrease in pH as hydrochloric acid diffuses through the cuticle [2]. The cuticle is water-resistant and usually brown, green, or yellow due to the reflux of bile pigments from the duodenum. The cuticle is asymmetrically developed and is thickest opposite to the thicker semiautonomous muscle masses. It acts as an abrasive surface to improve the grinding function of the ventriculus and is continuously renewed as it wears down. It also protects the underlying mucosa from the digestive action of enzymes [9]. The presence of grit in the ventriculus provides additional abrasive action. Grit is considered important mainly for species that do not remove the husk from seeds before swallowing them such as Columbiformes, Galliformes, and ratites [10]. Avian species with a less developed ventricular muscle, such as frugivores and nectarivores, also have a cuticle, but it is softer and more uniformly distributed. The components of the carbohydrate-protein complex indistinguishable [2]. Massive shedding of the cuticle occurs in some species such as the common magpie and the common starling [2]. Some male hornbills regurgitate the cuticle as a seed-filled sac to feed the nesting female [2]. The pylorus arises from the right face of the ventriculus and connects the ventriculus to the duodenum (Fig. 1, Fig. 2) [3]. It is poorly developed in some species, such as domestic fowl, and it forms a distinct chamber in aquatic species, such as the Great cormorant [2]. The pyloric fold regulates the rate of passage of food between the stomach and duodenum [9], slowing down the movement of large particles into the duodenum [11]. Physiology of the proventriculus and ventriculus Birds hatch from the egg with a sterile digestive tract. The microbial colonization of the digestive system in altricial birds occurs during parental feeding. Spontaneous sucking movement of the vent (cloacal drinking) also occurs and contributes to the uptake of microorganisms. These processes result in the establishment of normal gastrointestinal flora, predominantly consisting of Gram-positive bacteria (eg, Bacillus, Corynebacterium, Lactobacillus, Staphylococcus, and Streptococcus) in most passerine and psittacine species. Hydrochloric acid and pepsinogen are gastric secretions produced in the proventriculus. Pepsinogen is rapidly converted to pepsin by both acid and pepsin already present in the proventriculus. Lipase has been found in gastric secretions most likely due to duodenal reflux [1]. The pH of the proventriculus and ventriculus has been determined in many species (Table 1). The ventricular pH is generally lower than that of the proventriculus. As a result, gastric proteolysis takes place mainly in the ventriculus [3]. In carnivorous and piscivorous birds, the proventriculus acts as a site of food storage, made possible by folds allowing for extensibility. | | |  | | Proventriculus | Ventriculus | |
|---|
| Chicken | 4.8 | 2.5 | |
| Turkey | 4.7 | 2.2 | |
| Pigeon | 4.8 | 2.0 | |
| Duck | 3.4 | 2.3 | | | | |
In granivores, herbivores, and insectivores, the main function of the ventriculus is to triturate the ingesta to decrease the size of food particles and increase their surface area to promote gastric proteolysis. This is accomplished through the strong contractions of the asymmetrical ventricular muscle masses and abrasive action of the cuticle. The ventricular contractions result in rotary and crushing movements, which reduce the particle size of hard diets and mix the ingesta with the digestive enzymes [12]. In carnivorous and piscivorous species, the ventriculus is primarily a site of food storage rather than contributing to mechanical digestion, having evolved to digest relatively soft diets. In raptors, the ventriculus is also involved in the formation and regurgitation of pellets. There are three recognized phases to gastric secretion in mammals, which are also present in birds: the cephalic, gastric, and intestinal phases [13]. Vagal tone and multiple hormones are variably involved in each phase (Table 2). The cephalic phase is under vagal control and occurs when the birds see, smell, or expect food resulting in an increased production of HCl and pepsin [12]. In chickens, vagal stimulation results in greater pepsin secretion than HCl secretion, suggesting that their respective secretions may be under different control [13]. Denervation of the stomach had no significant effect on initiation and frequency of contractions in fed birds, but it uncoupled the coordination of contractions between the stomach and duodenum and it significantly delayed the onset of the cephalic phase [14]. These observations suggest that there is an endocrine component in the avian gastric response to the sight of food [14]. The gastric phase of secretion involves the action of gastrin, which stimulates HCl and pepsinogen secretion [1], [15]. Gastrin-releasing peptide, or bombesin, is another hormone that induces acid secretion, but its mechanism of action is still unknown [16]. The intestinal phase of secretion involves the action of cholecystokinin (CCK), secretin, and avian pancreatic polypeptide. CCK stimulates gastric secretion, but has no effect on pepsinogen secretion. Secretin and avian pancreatic polypeptide stimulate both acid and pepsinogen secretion [17], [18]. Avian pancreatic polypeptide is released from the pancreas; its effects are independent of'vagal stimulation [19]. As in mammals, histamine contributes to acid secretion [20]. Most species of birds kept in captivity rely almost exclusively on'autoenzymatic digestion, where their own genes code their digestive enzymes. Alloenzymatic digestion, which implies the action of enzymes of microbial origin, appears to be minimal [9]. | | | | | Hormones acting on the proventriculus and/or ventriculus | Functions | |
|---|
| Hormones produced in the proventriculus | Gastrin | -Stimulates HCl and pepsinogen secretion | |
| Gastrin-releasing peptide (bombesin) | -Stimulates HCl secretion | |
| Avian pancreatic polypeptide (APP) | -Stimulates HCl and pepsinogen secretion | |
| Hormones produced in the small intestine | Cholecystokinin (CCK) | -Stimulates HCl secretion | |
| | -Inhibits gastric emptying | |
| Secretin | -Stimulates HCl and pepsinogen secretion | | | | |
The proventriculus and ventriculus act as a unit, propelling the ingesta back and forth between the two components to optimize mechanical and enzymatic digestion (Fig. 5) [1], [2], [9]. There is also reflux of ingesta between the duodenum and ventriculus, which appears to be unique to birds [9], [21], [22]. In the turkey, the gastrointestinal cycle starts with the contraction of the thin muscles of the ventriculus, while the isthmus is closed, followed by opening of the pylorus, which propels the ingesta into the duodenum. The duodenum then initiates contraction while the isthmus relaxes and the pylorus closes. The contraction of the thick muscles of the ventriculus follows causing reflux of food from the ventriculus to the proventriculus [23]. The reflux of larger particles from the ventriculus to the proventriculus allows the addition of fresh pepsin and hydrochloric acid, which results in improved protein hydrolysis, emulsification of large lipid globules, and homogenization of the ingesta [9]. The cycle ends with contraction of the proventricular muscles followed by closure of the isthmus. The initiation of the gastrointestinal cycle appears to be dependent on a pacemaker located in the isthmus [24]. Destruction of the myenteric plexus of the isthmus results in the cessation of proventricular contractions and a 50% decrease in ventricular and duodenal contractions. The stomach of most granivorous birds lacks longitudinal muscle fibers, which may explains why slow migrating myoelectric complexes traveling aborad have not been recorded in birds [1], [23]. However, birds of prey do have longitudinal muscles, but slow waves have not been recorded in these species either [23]. Several factors influence the motility of the proventriculus and ventriculus. Ventricular contractions increase in frequency and amplitude during the day compared to the night in diurnal species [25]. Fasting decreases the frequency and amplitude of contractions during the day, resulting in a less pronounced diurnal variation [26]. The sight of food and the action of eating'increase the frequency of stomach contractions, whereas the entrance of'food into the duodenum slows the frequency of gastric contractions [1], [21], [25], [26]. Enterogastric reflexes control gastric emptying. It has been shown that an increase in duodenal pressure or the presence of HCl, hypertonic saline, amino acid solutions, or lipid solutions inhibit gastric motility [21], [27]. Hormonal regulation also appears to be involved. Cholecystokinin octapeptide (CCK-8) and cholecystokinin tetrapeptide (CCK-4) both inhibit gastric motility [28]. The inhibitory action of CCK-8 on the stomach appears to be mediated by the vagal nerve and involves the release of nitric oxide [29]. In addition, CCK-8 may have a direct action on the gastric muscles, because vagotomy in chickens resulted in increased contractions of the stomach [1]. In raptors, the sequence of contraction differs, starting with the proventriculus, then the isthmus, ventriculus, and the duodenum. Pellet formation and egestion allows expulsion of nondigestable material such as bone, fur, or feathers. Approximately 12 minutes prior to egestion, the contractions of the ventriculus increase in frequency and amplitude [1]. These contractions compact the material into a pellet and move it into the lower esophagus. A few seconds prior to the actual egestion, the pellet is moved toward the oral cavity by esophageal antiperistalsis. The abdominal muscles are not involved in egestion [1]. The proventriculus and ventriculus do not represent a major site for absorption of nutrients. The primary site of nutrient (carbohydrates, amino acids and peptides, fatty acids, electrolytes, vitamins) absorption is the small intestine, and to a lesser degree the large intestine. However, absorption of amino acids is reported to occur in the proventriculus and gizzard [1]. Diseases of the proventriculus and ventriculus The proventriculus and ventriculus can be affected by a variety of diseases, which are difficult to distinguish clinically. Clinical signs may include depression, regurgitation, delayed crop emptying, weight loss, increased or decreased appetite, passage of undigested seeds in the feces, diarrhea, and melena. Diagnosis of the disease process(es) involved may be difficult, and multiple diagnostic techniques including hematology, plasma biochemical analysis, blood lead/zinc levels, fecal/proventricular cytology and culture, fecal flotation, imaging (survey and contrast radiography, fluoroscopy, and endoscopy) and histopathology are useful to determine the cause of the symptoms. Knowledge of the diseases that commonly affect each avian species will allows an earlier diagnosis through prioritization of diagnostic tests. Fungal diseases Avian gastric yeast (megabacteria) There has been controversy surrounding the identity and role of megabacteria. They have been variously believed to be bacteria or fungi, normal or abnormal flora and primary or secondary invaders [4], [30], [31]. Recent research suggests that the organisms are fungi, and the term “avian gastric yeast” has been proposed [32], [33], [34]. These Gram-positive, periodic acid Schiff (PAS)-positive, acidophilic rod-shaped organisms have initially been described in budgerigars as the “going light syndrome,” which is characterized by high morbidity and low mortality [35]. Other species of birds diagnosed with avian gastric yeast include canaries, finches, lovebirds, cockatoos, chickens, turkeys, quails, ducks, geese, and ibises [32], [33], [36], [37], [38], [39]. The pathogenicity of the organisms varies according to the species infected. In chickens in which gastric yeast was identified, no gastrointestinal lesions were observed, suggesting the organisms may not be pathogenic [33]. Most infected canaries and budgerigars had gastrointestinal lesions associated with a multifactorial disease process [33]. Multiple factors may contribute to the pathogenicity of the organisms such as the age, species, nutritional status, immunologic status, and the presence of concomitant infection. Significant losses have been reported in budgerigar aviaries also infected with Encephalitozoon hellem [40]. Most birds suffer from a chronic disease, and may present with weight loss, anorexia, weakness, regurgitation, and passage of undigested seeds in the feces. Birds gradually become debilitated and emaciated. They either die'or slowly recover, although recovery is unlikely in passerines once body'weight loss occurs [37]. An acute form has been reported only in budgerigars. Birds become suddenly depressed and usually die within 12–24 hours. Some may regurgitate blood and have melena [37]. Radiographs may reveal a dilated proventriculus, and contrast study may show an hourglass constriction of the contrast media secondary to mucous accumulation at the isthmus [41]. Contrast fluoroscopy can be helpful in differentiating avian gastric yeast from proventricular dilatation disease (PDD) [42]. In birds with gastric yeasts, an increase in rapid-phase contractions of the thick muscles of the ventriculus was observed, compared to dilatation and decreased motility with PDD. A definitive diagnosis is based on the demonstration of the organisms in a fecal sample (Fig. 6), a proventricular wash, a biopsy of the proventriculus, or at necropsy. Identification of avian gastric yeast should be initially attempted in a fecal sample or a proventricular wash, because taking a biopsy of the proventriculus carries a higher risk of complications. A proventricular wash may be obtained in an awake bird using a red rubber catheter passed orally. The difficulty of this technique resides in the ability to pass the catheter from the crop into the opening of the thoracic esophagus located on the caudodorsal midline of the crop. A proventricular wash may also be obtained in an anesthetized patient using a red rubber catheter or flexible endoscope passed orally, or through an ingluviotomy using a red rubber catheter or a rigid/flexible endoscope [43]. The ingluviotomy facilitates visualization of the entrance of the thoracic esophagus. When anesthetized, the patient should have an endotracheal tube in place as well as gauze sponges in the caudal oropharynx to decrease the likelyhood of aspiration. The organism's length varies between 20 to 90 nm, and they can be up to 5 μm wide [30], [33]. The absence of the organisms in the feces does not rule out infection. In one study, 15% of budgerigars with confirmed avian gastric yeast at necropsy did not have organisms in their droppings [44]. On gross examination, the proventriculus is usually empty except for the presence of thick white mucous. The wall is often thickened with small hemorrhages and ulcerations possibly present at the distal end as well as in the isthmus [32], [44]. On histopathologic examination, parallel layers of organisms are present on the surface of the mucosa and, in severe cases, within the glands of the lamina propria. Minimal inflammation is associated with the infection [32]. In most cases, the koilin layer of the ventriculus is irregular and softer; and some speculate this is secondary to reduced acidity resulting in poor precipitation of the protein–carbohydrate complexes [39]. A study involving canaries showed that the proventricular pH of affected birds ranged from 7.0–7.3, whereas a pH ranging from 0.7 to 2.4 was found in normal birds [39]. The alkalinization appears to be caused by the organisms themselves, because their passage in liquid media resulted in high increase in alkalinity [32]. Treatment includes acidification of the gastrointestinal tract by adding organic acids such as apple cider vinegar, white vinegar, or grapefruit juice to the drinking water, or using Lactobacillus sp. organisms that may act as competitive inhibitors of avian gastrointestinal pathogens [45]. The pH of the drinking water should remain above 2.5, and acids should be added for several weeks [32]. Amphotericin B given orally by crop gavage (0.15 to 0.3 mL of a 100 mg/mL suspension every 12 hours for 10 days for a budgerigar) is effective in many, but not all cases of avian gastric yeast [46], [47]. When added to the drinking water of budgerigars for 22 days at a concentration of 10 g/L, amphotericin B was effective at 98% [48]. Successful treatment with nystatin (5000 U/bird every 12 hours for 10 days) has been reported in goldfinches, but not in budgerigars [37], [46]. There is little to no absorption of amphotericin B and nystatin from the gastrointestinal tract when ulcerations are absent. The toxic effects of amphotericin B on the kidneys are restricted to parenteral administration. The recent confirmation of megabacteria as yeast explains why polyene macrolide antifungals such as amphotericin B and nystatin are effective. They bind ergosterols in fungal cell membranes, causing changes in permeability and resulting in death of the fungi. In severe cases, long-term treatment may be required. Candidiasis Ventricular candidiasis is uncommonly reported and usually seen in immunocompromised patients and neonates. A variety of psittacines, passerines, ratites, and miscellaneous other avian species have been diagnosed with endoventricular mycosis, but finches appear to be predisposed with an incidence of 14% at necropsy [49]. Histologic identification of the organism is necessary for a diagnosis. Fungal organisms are found in the koilin layer and occasionally in the mucosa [7]. Supportive care and oral antifungal therapy are indicated. Proventricular candidiasis has also been diagnosed in a cockatoo with concomitant avian gastric yeast [36]. Diagnosis was based on cytologic examination of a proventricular mucous sample, and the bird responded to treatment with ketoconazole and Lactobacillus sp. No underlying condition causing immunosuppression was identified. Zygomycete Infection with zygomycete fungi is occasionally reported and usually associated with gross hemorrhage and necrosis of the proventriculus [7], [49]. Diagnosis may be made by evaluation of a cytologic or biopsy sample collected from the proventriculus. Histologically, zygomycete fungi are seen throughout the proventricular wall and within the blood vessels [7]. Supportive care and combination antifungal therapy administered orally may be successful in mild to moderate cases, but prognosis is generally poor to guarded. Bacterial diseases Bacterial proventriculitis can be primary or secondary to the overgrowth of opportunistic pathogens. Gram-negative organisms such as Escherichia coli, Klebsiella sp., Salmonella sp., and Enterobacter sp. are most commonly implicated [15]. The infection is rarely limited to the proventriculus and ventriculus, and often affects the intestines as well. Clinical signs, as for other gastrointestinal diseases, may include anorexia, weight loss, regurgitation, diarrhea, and presence of undigested seeds in the feces. Poor hygiene, young or old age, immunosuppression, or concurrent illnesses are predisposing factors. Diagnosis is based on fecal cytology and culture, and treatment should be based on sensitivity results. Mycobacteriosis most commonly affects the intestines, but has been reported in the proventriculus of passerines and psittacines [7], [50]. Antemortem diagnosis is difficult, and may include hematology, plasma biochemistry, whole-body radiographs, cytologic and histopathologic evaluation of samples collected using endoscopy, acid-fast stains of feces or tissue (eg, liver), culture and mycobacterial DNA, or RNA probes on culture or biopsy specimens. Treatment of mycobacteriosis is controversial, because this disease is potentially zoonotic. Therapy involves the long-term concurrent administration of a combination of three or more drugs to limit the development of resistant strains [51]. Length of treatment range from 1 to 18 months. Therapy can be initiated with rifabutin (15 mg/kg orally every 24 hours), ethambutol (30 mg/kg orally every 24 hours), and azithromycin (43 mg/kg orally every 24 hours) or clarithromycin (85 mg/kg every 24 hours). If the patient responds poorly or relapse occurs, a fluoroquinolone or an aminoglycoside should be added to the regimen. Multiple other therapeutic regimens have been used [52]. Treatment should be continued several months past the last positive biopsy or culture. Exposed birds should be isolated, quarantined for 2 years, and evaluated every 2 to 3 months to determine if they are infected [53]. Viral diseases Proventricular dilatation disease Several different terms have been used to describe this condition, including neuropathic gastric dilatation, proventricular dilatation syndrome, psittacine wasting syndrome, and more recently, lymphoplasmacytic ganglioneuritis and encephalomyelitis, which describes the histologic changes in affected birds [10], [54]. This condition has been reported in spoonbills, Canada geese, toucans, weaver finches, and more than 50 species of psittacines [54]. The etiology of this condition appears to be viral, because an 80-nm, enveloped virus has been identified in affected birds and could induce the disease in experimentally infected birds [55]. The virus causes lymphoplasmacytic infiltration of the nerve ganglia supplying the musculature of the gastrointestinal tract, and the central nervous system (Fig. 7). Birds may present with gastrointestinal signs only, neurologic signs only, or a combination of both. Progressive weight loss despite an increased appetite, delayed crop emptying, regurgitation, and presence of undigested seeds in the feces may be observed clinically. Ataxia and proprioceptive and motor deficits are often present with central nervous system involvement. Radiography and contrast studies are useful diagnostic tools (Fig. 8, Fig. 9). Dilatation of the proventriculus and ventriculus associated with increased gastrointestinal transit time may be observed. Mildly affected birds or birds with only neurologic signs may not have any radiographic abnormalities. Fruit and nectar eaters, baby birds on feeding formula, and anorectic birds tube fed a critical care diet may have a normally slightly dilated proventriculus. A dilated proventriculus and ventriculus are not diagnostic for PDD because other infectious diseases, heavy metal toxicosis, gastric foreign body, and other metabolic disorders may also result in dilatation of the gastrointestinal tract (Fig. 10) [10], [50], [54]. Definitive diagnosis is based on a biopsy of the crop, proventriculus, or ventriculus showing lymphoplasmacytic ganglioneuritis. It is important to take a large biopsy (0.5×0.5 cm) containing at least one visible vessel to ensure the presence of a nerve. According to one study, evaluation of an adequate crop biopsy sample reliably diagnosed proventricular dilatation disease in 76% of affected birds [56], while others reported that crop biopsy is 66% accurate in diagnosing PDD [57]. A normal crop biopsy does not rule out PDD. A review of confirmed cases showed the presence of crop lesions in 30–35% of the cases, whereas the proventriculus and ventriculus had lesions in over 98% of the cases [58]. This suggests that a proventricular biopsy may be a more appropriate diagnostic technique; however, the procedure is more invasive and associated with a higher risk of complications in an already debilitated patient. Treatment of birds with PDD is palliative at best, and the disease has been reported to be invariably fatal. However, recent clinical reports give some hope to improve the clinical status of these patients. The administration of cyclooxygenase-2 (COX-2) inhibitors such as celecoxib (Celebrex, Pfizer) resulted in clinical improvement within 1 week of therapy, followed by gradual resolution of clinical signs and return to a normal diet after 6–12 weeks of treatment. No adverse side effects were observed during and after cessation of treatment [18]. Further research is warranted on the use of selective COX-2 inhibitors in the treatment of PDD. Supportive care is also indicated, and can include small frequent meals, liquid diet, gastrointestinal promotility drugs (metoclopramide, cisapride), parenteral vitamins, and treatment of secondary bacterial and/or fungal infections. It has been suggested to avoid using metoclopramide in patients with neurologic signs, because extrapyramidal signs consistent with acute dystonic-dyskinetic reaction were observed in a macaw following its use [59]. Some clinicians reported temporary improvement with the use of alpha interferon (30 units every 24 hours for 5 days, then 30 units twice a week for 2 weeks, then 30 units once a week for 2 weeks), but no scientific data support these clinical observations [54]. Until the route of transmission of the virus, a dependable screening test and an effective way to control infection (eg, vaccine) are determined, it would be prudent to keep affected and exposed birds in single-bird households, where they have no direct or indirect contact with other' birds. Other viral diseases Poxvirus and herpesvirus (Pacheco's disease) can also lead to changes in the proventriculus similar to those seen with myenteric ganglioneuritis. However, these lesions are infrequently observed [7]. Parasitic diseases Cryptosporidia Infection of the proventriculus with Cryptosporidium sp. is seen in a variety of psittacine species [60], but is uncommon. The organisms develop intracellularly but extracytoplasmically just under the surface of mucosal epithelial cells [61]. Sporulated oocysts are infective when shed in the feces, and transmission occurs directly by ingestion or inhalation. The infection is usually self-limiting, but chronic or severe clinical disease may be seen in juvenile cockatiels in association with other infectious agents [61]. Avian cryptosporidium appear to be temperature- and species-adapted, and do not represent a risk to humans [61]. Diagnosis is made after concentration of the oocysts by sugar flotation. Oocysts are small, measuring 4–6 μm, and can be easily overlooked. On postmortem examination, there are often no gross lesions, but mucosal hypertrophy/hyperplasia may be seen [7]. No effective treatment is known. Paromomycin (Humatin, Parke-Davis) at 165 mg/kg every 12 hours for 5 days successfully eliminated oocyte shedding in a cat [62]. In reptiles, 100 mg/kg of paromomycin for 7 days followed by twice a week administration for 3 months reduced or eliminated oocyte shedding, but the organisms were still present in the gastric mucosa [63]. Hyperimmune bovine colostrum has also been used with variable results in reptiles [64], [65]. Supportive care and limiting reexposure through diligent hygiene may help to control infection. Disinfection of the environment with 50% bleach or 50% ammonia (v/v) prevents oocyst development [66]. Nematodes Nematodes are seen infrequently in companion and aviary birds. Infection occurs most frequently in birds kept on a dirt-floored enclosure, because most infections require access to intermediate host or larvated eggs. Proventricular nematodes include Echinura sp., Gongylonema sp., Procyrnea sp., Streptocara sp., Dyspharynx sp., and Tetrameres sp. [4], [67], [68]. Streptocara sp. and Dyspharynx sp. have been reported to cause thickening of the proventricular mucosa. These parasites burrow into the mucosa, causing ulcers and formation of inflammatory nodules [68]. Nematodes affecting the ventriculus include Amidostonum sp., Epomidiostomum sp., Cheilospirura sp., and Acuaria sp. [4], [67]. Acuaria skrjabini caused significant mortalities of passerines in Australian aviaries, secondary to ventricular mucosal necrosis, but psittacine species were not affected [69], [70]. Diagnosis of nematode infection is usually made by examination of feces fixed in a saturated salt flotation, but identification of the adults following endoscopic removal is also possible. Treatment with anthelmintics such as fenbendazole (20–50 mg/kg orally every 24 hours for 3–5 days), pyrantel pamoate (7 mg/kg orally, repeat in 2 weeks) or ivermectin usually results in successful elimination of the parasites. Acuaria sp. are resistant to many anthelmintics, but therapy with 80 mg of levamisole or 50 mg of fenbendazole/L of drinking water was successful [70]. Ivermectin can be administered orally or topically at a dose of 0.2 mg/kg [61]. Toxicity has been observed in small birds treated with ivermectin intramuscularly; thus, this route is not recommended for patients weighing less than 500 g. Dosages exceeding 0.2 mg/kg are probably unnecessary in birds, but may be required if a lower dose is not efficacious [61], [71]. Treatment of small patients often requires dilution of ivermectin to 0.1% with propylene glycol. Diluted ivermectin should be used immediately because stability of the diluted form has not been established [61]. Application of diluted ivermectin on the apteric cervical area over the jugular vein appears to be clinically effective in small species [61]. Gastric foreign body or impaction Gastric impaction or foreign body is a common problem in neonates kept on crushed walnut shell, ground corn cob, styrofoam packing, kitty litter, grit, and shredded paper pulp [4]. Wooden and metallic foreign bodies have been associated with proventricular dilatation in a cockatoo, and metallic foreign bodies may lead to perforation of the stomach [72]. The ventriculus is most commonly affected because of its capacity for strong contractions. Gastric perforation can result in an acute, generalized peritonitis, a local peritonitis with abscess formation on the serosa, or an acute fatal hemorrhage from trauma to a hepatic vessel [4]. The clinical signs associated with gastric foreign body are nonspecific. Birds may present with a clinical history of intermittent lethargy, inappetence, recurrent bacterial enteritis, tenesmus, and vomiting. Some foreign materials, such as heavy metals, plastic, or rubber are potentially toxic, and birds often present with clinical symptoms of toxicosis [73]. Radiography, contrast studies, and endoscopy are useful diagnostic aids. Medical management should always be attempted prior to surgical removal of the object. Foreign bodies may be removed using proventricular or ventricular flushing, endoscopy, or laxative administration (mineral oil, psyllium fiber) [43], [47], [74]. Appropriate supportive care, including fluid therapy, antimicrobial therapy, and analgesia should be provided as needed. Proventricular or ventricular flushing to expel a foreign body from the gastrointestinal tract should be performed under general anesthesia as opposed to when a proventricular wash is used to collect a sample (eg, avian gastric yeast diagnostic). The same techniques described to perform a proventricular wash can be used, and copious amount of saline is flushed to reflux food and other material into the crop. Then, the content of the crop is aspirated through the mouth or ingluviotomy site with a suction device. During this procedure, it is helpful to keep the head of the patient lower than the proventriculus and ventriculus to ease the flow of material into the crop. Endoscopic removal of foreign body can be accomplished via the mouth or an ingluviotomy using grasping forceps or a basket [43]. Surgical removal of proventricular and ventricular foreign bodies is best performed through a proventriculotomy. Generally, a left lateral celiotomy is used but in some cases where the proventriculus and ventriculus are displaced, a ventral midline celiotomy may be more appropriate. Endoscopy may be useful in assisting visualization and removal of the foreign body and documenting that all material has been removed. It often allows foreign body removal using a smaller proventricular incision thereby decreasing surgery time. Intoxication Heavy metal (lead, zinc, copper) and vitamin D toxicosis have been involved in the pathology of the proventriculus and ventriculus [4], [74]. Birds may present with gastrointestinal signs, but often show clinical signs associated with other organ systems such as the neurologic and urinary systems. Ingestion of a lead foreign body resulting in toxicosis is frequently encountered in avian patients. Lead toxicosis is associated with demyelination of the vagus and other nerves, which results in decreased gastrointestinal motility secondary to blockage of nerve conduction [75]. Radiographs may show dilatation of the proventriculus and other parts of the gastrointestinal tract. The presence and quantity of metallic material can also be evaluated (Fig. 11, Fig. 12). Radiographic identification of a metallic foreign body with clinical signs of lead toxicosis is suggestive of lead poisoning. However, the absence of metallic density does not rule out lead toxicosis, because a bird may reach toxic blood lead levels by chewing without swallowing material containing lead. Whole blood lead levels greater than 0.2 ppm (20 μg/dL) are suggestive and levels greater than 0.4 to 0.6 ppm (40–60 μg/dL) are diagnostic for lead toxicosis [74]. Treatment for lead toxicosis has four different aspects: supportive care, chelation therapy, removal of the foreign bodies, and elimination of the source of lead from the bird's environment. Supportive care may include fluid therapy, parenteral multivitamins, and tube feeding. Chelation agents include edetate calcium disodium (CaEDTA) (calcium disodium versanate, 3M Riker, Northridge, CA), D-penicillamine (Cuprimine, Merck Inc., Rahway, NJ), and dimercaptosuccinic acid (Chermet, McNeil Consumer Products Co, Fort Washington, PA). CaEDTA is an injectable chelator, whereas D-penicillamine and dimercaptosuccinic acid are administered orally. CaEDTA is the agent of choice to initiate therapy, because birds often have decreased gastric motility or are regurgitating. Combination therapy can be used in severe cases. CaEDTA (35 mg/kg every 12 hours) should be given for 3–5 consecutive days, alternating with 3–5 days without treatment [76]. More than one course of treatment may be necessary, as lead concentrations equilibrate from the soft tissue into the bone and blood. CaEDTA chelates lead in the bone and the blood, but not in the soft tissue. Removal of the foreign material can be achieved with administration of cathartics such as mineral oil, peanut butter, and magnesium sulfate (Epsom salt), which may facilitate the passage of small metallic particles through the digestive system. Endoscopy may also be used to retrieve metallic particles, but endoscopic removal of small particles may be difficult and sometimes impossible if ingesta are present in the proventriculus and ventriculus. Proventricular and ventricular flushing assisted with fluoroscopy is another means to remove foreign material. During this procedure, the patient should be intubated and preferably placed in right lateral recumbency with its head lowered at a 30–45 degree angle. Surgical removal of foreign material should be performed as a last resort. If the bird is on chelation therapy and stable or steadily improving, the risks of surgery probably outweigh its benefits. Zinc is another frequently encountered heavy metal that can result in toxicosis when ingested by birds. Zinc toxicosis is associated with ileus and necrotizing ventriculitis in waterfowl and psittacines [76], [77], [78]. Necrosis of the ventricular mucosa may lead to koilin exfoliation and secondary obstruction. The diagnostic approach is similar to that for lead toxicosis. Serum zinc levels greater than 2 ppm (200 μg/dL) are suggestive of zinc toxicosis [76]. Blood should be collected in nonrubber stopper containers to avoid contamination of zinc from leaching into the sample. Therapeutic approach for zinc toxicosis follows the same principles as treatment of lead toxicosis. CaEDTA and D-penicillamine have been recommended to treat zinc toxicosis, but dimercaptosuccinic acid has proven effective in a Hyacinth macaw [74], [79]. Usually one course of treatment is sufficient to return and maintain zinc concentrations within normal limits, because zinc is not stored in the bone. Clinical abnormalities associated with copper poisoning are rarely reported in birds. Chronic consumption of a diet with excessive copper may lead to roughening and thickening of the cuticle, resulting in a wart-like appearance. Hemorrhages under the koilin layer have also been observed [4]. Hypervitaminosis D3 may result in mineralization of the ventriculus and other organs. Mineralization can also be secondary to renal disease. Usually, no gross lesions are present, and the mineral deposit is demonstrated histologically in the superficial mucosa and cuticle [7]. Neoplasia Neoplastic diseases of the avian stomach are most commonly located at the isthmus [10]. Carcinomas and less commonly leiomyosarcomas have been reported [7]. There appears to be a higher incidence of proventricular adenocarcinoma in gray-cheeked parakeets [4], [5], [10], [80]. Primary malignant gastric neoplasms are uncommon in psittacine birds. A carcinoma of the ventriculus with metastasis to the lungs has been reported in a sulphur-crested cockatoo (Cacatua galerita) [81]. Clinical signs may include vomiting, melena, anemia, hypoproteinemia, and passage of undigested seeds in the feces. Histopathology is necessary to distinguish neoplasia from inflammation or ulceration due to other causes [5]. PAS staining may help to determine if the tumor originates from the proventriculus or the ventriculus. Internal papillomatosis of parrots may be associated with lesions in the proventriculus and the ventriculus. However, lesions more commonly involve, in order of decreasing frequency, the cloaca, glottis, choanal slit, esophagus, and oropharynx [82]. This condition is most common in New World Psittacines including macaws, hawk-headed parrots, Amazon parrots and conures, but is also reported in Old World species such as budgerigars, pionus parrots, caiques, and African gray parrots [83]. The etiology has not been identified, and DNA in situ hybridization and DNA in situ polymerase chain reaction failed to demonstrate papillomavirus in psittacines with internal papillomas [84]. Herpesvirus-like particles were observed in one conure, but their presence was considered incidental [85]. Clinical signs resemble those associated with other diseases of the proventriculus and ventriculus. The presence of papillomatous lesions in locations other than the proventriculus and ventriculus in a patient with gastrointestinal signs should alert the practitioner. Radiography, contrast studies, and endoscopic examination of the stomach compartments may assist diagnosis of this condition, but definitive diagnosis requires histopathologic examination of biopsies from a lesion. Summary Diseases affecting the proventriculus and ventriculus often present with similar clinical signs. It is important for the avian practitioner to be familiar with these diseases, their prevalence, and the species most commonly affected to judiciously prioritize the appropriate diagnostic techniques. A basic understanding of the anatomy and physiology of the proventriculus and ventriculus is useful in integrating the pathophysiology and clinical signs associated with variable disease processes. It is also essential to evaluate radiographs and endoscopic images, perform diagnostic techniques, make a diagnosis, and provide appropriate therapy. Acknowledgements The author thanks Dr. Cheryl Greenacre, DVM, Dipl. 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