Clinical Update and Treatment of Selected Infectious Gastrointestinal Diseases in Avian Species

TOPICS IN MEDICINE AND SURGERY CLINICAL UPDATE AND TREATMENT OF SELECTED INFECTIOUS GASTROINTESTINAL DISEASES IN AVIAN SPECIES João Brandão, LMV, and Hugues Beaufrère, DVM, PhD, Dip. ABVP (Avian), Dip. ECZM (Avian)

Abstract The anatomy of the avian gastrointestinal (GI) tract is unique and significantly different from that of other animals. The characteristics of the avian GI tract allow the different species to adapt and thrive in their habitats. Infectious diseases of bacterial, viral, fungal, and parasitic origin commonly affect avian species. The significance and the nature of these pathologies vary with species and if they live in the wild or a captive environment. This review compiles information available in the literature on specific infectious processes that were considered relevant and clinically significant by the authors. Clinicians should be knowledgeable and aware of the infectious agents, clinical signs associated with disease, diagnostic techniques, and treatment methodologies currently available regarding diseases that affect the avian GI tract. Recent information that provides new insight to these infectious processes is the focus of this article. Copyright 2013 Published by Elsevier Inc. Key words: avian; bacterial; viral; fungal; parasitic; disease

T

he Class Aves has one of the largest number of species of the terrestrial vertebrates.1 Among this group of animals, different characteristics allow the different species to adapt and thrive in their habitats. There are significant anatomical variations between the GI tracts of different avian orders and more so relative to other vertebrates. The avian digestive system may be divided into functional and anatomical regions that include the crop, proventriculus, and ventriculus, followed by the small and large intestine (⫾ceca). Some of these anatomical regions of the avian GI tract may be more developed, absent, or rudimentary depending on the species’ natural diet. The reason for this anatomical variability may remain unclear, but in most cases, it gives the species evolutionary advantages to procure and digest the food available within a particular ecological niche. As there is considerable information on avian gastroenterology, special attention is given to selected infectious diseases that were considered relevant and clinically significant by the authors.

BEAK _________________________________________

Bacterial

The first organ or structure associated with the digestive track is the beak. Although not related to the true digestive process, the beak allows the bird to grasp and crush food items. There is a wide range of beak types but their shape has a function according to the species, the food items that comprise the diet, and the feeding habits.

Bacterial infections of beak tissue have been reported in broiler chickens.2 After initial damage to the epidermis of the beak, bacterial contamination within the injury results in secondary infection and tissue necrosis.2 Bacterial infections affecting the infraorbital sinus may invade and secondarily cause beak deformities.

From the Louisiana State University School of Veterinary Medicine, Department Veterinary Clinical Sciences, Baton Rouge, LA USA; and University of Guelph Ontario Veterinary College, Health Sciences Centre, Ontario, Canada. Address correspondence to: João Brandão, LMV, LSU-School of Veterinary Medicine, Dept. VCS, Skip Bertman Dr, Baton Rouge, LA USA. E-mail: [email protected]. Ó 2013 Published by Elsevier Inc. 1557-5063/13/2101-$30.00 http://dx.doi.org/10.1053/j.jepm.2013.05.003

Journal of Exotic Pet Medicine 22 (2013), pp 101–117

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A 26-day-old Antipodes Island parakeet (Cyanoramphus unicolor) developed severe beak deformity that appeared to be related to infectious sinusitis caused by a mixed population of bacterial organisms, predominately Proteus spp.3 Mycotic Rhinosinusitis with secondary rhamphothecal destruction caused by Cryptococcus neoformans var gattii has been described in a Major Mitchell’s cockatoo (Cacatua leadbeateri).4 Fungal rhinosinusitis caused by Aspergillus spp. with secondary beak deformity has been reported in a yellow-napped Amazon parrot (Amazona ochrocephala auropalliata).5 A Penicillium cyclopium beak infection resulted in rhamphothecal necrosis and destruction in a blue and gold macaw (Ara ararauna).6 In other cases of penicilliosis, beak involvement has not been described.7 OROPHARYNGEAL CAVITY ___________________ The oropharyngeal cavity is considered the cranial aspect of the avian GI tract. In mammals, the mouth is responsible for the initiation of the digestive process both by mechanical processes (mastication) and enzymatic process (e.g., amylase). In birds, no true mastication occurs but the beak can fragment food items. Among different mouth structures, the tongue can provide a significant useful function. While some avian species rely on the beak to break the food, other species require the tongue to drag food into the mouth. Nectivorous species (e.g., hummingbirds and lorikeets) have villouslike projections that assist with the nectar collection.8-10 Damage to the

FIGURE 1. Oral Clinostomum sp. in a wild juvenile blackcrowned night heron (Nycticorax nycticorax).

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tongue can cause severe impairment of a bird’s ability to ingest food. Bacterial Bacteria are commonly found in the oral cavity of birds and other animals. The clinical importance of bacterial isolation from the oral cavity of an avian patient may be insignificant if not correlated to a disease process. The normal bacterial flora of the oral cavity of birds has not been properly described and only a few species have been assessed. In houbara (n = 19 [Chlamydotis undulata]), kori (n = 7 [Ardeotis kori]), and rufous-crested (n = 3 [Eupodotis ruficrista]) bustards, Klebsiella spp. were the only common bacteria found in the oropharyngeal samples of these 3 species.11 A study of the normal oropharyngeal flora of captive ostrich (Struthio camelus [n ¼ 50]) revealed the presence of a majority of Gram-negative and in particular, Escherichia coli (present in 74%), Bacillus spp. (38%), Staphylococcus coagulase-negative (32%), Klebsiella pneumoniae (32%), Rhodotorula spp. (8%), and Cryptococcus spp. (4%) bacteria.12 Bacterial cultures from the tongue of American black vulture (Coragyps atratus [n ¼ 6]) allowed identification of Actinomyces bovis, Lactobacillus cellobiosus, Micrococcus luteus, Neisseria sicca, Staphylococcus epidermidis, S. saprophyticus, and Streptococcus pyogenes.13 The authors hypothesize that an injury to the oral mucosa provides an avenue for common bacterial flora to colonize the compromised tissue. Although some of these studies may provide useful information of the normal bacterial flora, bacterial cultures are warranted in cases of suspected bacterial infection. Parasitic Trichomoniasis, also called “frounce” or “canker,” is a disease cause by Trichomonas gallinae. This flagellate protozoan is commonly diagnosed samples taken from the mouth, pharynx, esophagus, and crop of affected birds (Fig. 1). A disseminated trichomoniasis infection can also affect other organs such as the liver.14 Although Columbiformes are the most commonly affected species, birds of prey, Psittacines (e.g., budgerigars), Passerines, Galliformes, and other groups have been identified as being susceptible to T. gallinae.15 Prevalence studies in wild populations of pigeons have shown rates of 35% trichomoniasis-positive animals.16 The detection of these protozoa can be performed by direct smear of the mouth masses or culture.17 Culture has been reported to be more sensitive than direct

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microscopic examination of a wet mount slide.18 Birds that eat pigeons can become infected through diseased prey. T. gallinae (genotype A) has been suggested to be more prevalent in Columbiformes whereas T. gallinae (genotype B) is more often identified in raptor species.19 Several studies have been performed on the effect of trichomoniasis in raptors, which may have a significant negative effect on endangered populations like Bonelli’s eagle (Aquila fasciata).20 In Bonelli’s eagle, T. gallinae has been isolated in 36% (n ¼ 39) of nestlings and affected 41% (n ¼ 22) of the broods, leading to 22% single nestling mortality factor and responsible for 2% of the chick mortality.20 It has been shown that in urban populations of Cooper’s hawks (Accipiter cooperi) in Southeastern Arizona, trichomoniasis was the most prevalent cause of death of nestlings (79.9%).21 In a T. gallinae prevalence study involving goshawk nestlings (Ac. gentilis), a total of 65.1% of the nestlings showed positive results for the culture, but only 4.5% showed caseous plaques in the mouth and only 0.7% died with advanced stage of trichomoniasis.22 Higher prevalence of trichomonas (35% and 100%) has been reported in goshawk nestlings but mortality was not reported.23 It is suggested that owing to the high prevalence but low pathogenicity, a parasite-host evolutionary adaptation may have occurred.22 Populations of greenfinch (Carduelis chloris) and chaffinch (Fringilla coelebs) decreased by 35% and 21%, respectively, in areas with high incidence of trichomoniasis, representing a total mortality of half a million birds.24 Trichomoniasis caused by T. gallinae was identified as the cause of death of purple finches and American goldfinches in Canada.25 In a large retrospective study on morbidity causes in wild birds presented to a wildlife center, trichomoniasis was the most common infectious/parasitic cause of animal presentation.26 In the United States, a T. vaginalislike organism was detected in outbreaks of trichomoniasis.27,28 The most common treatment of trichomoniasis in birds is the nitroimidazole drugs (e.g., ronidazole, carnidazole, dimetridazole, ornidazole, and metronidazole). There have been several reports of nitroimidazole resistance by Trichomonas spp. in avian species. In one study with pigeon isolates, 6 out of 8 strains showed in vitro resistance to all the drugs that were previously effective in treating this protozoan parasite.29 In an in vivo study with racing pigeons, carnidazole and dimetridazole failed to eliminate the infection in 13 of 17 and 20 of 21 birds, respectively.30 The

same study revealed that in vitro effects of ronidazole were most effective against one specific captive racing pigeon resistant isolate, whereas for the other 3 wild pigeon isolates, all drugs were effective.30 Metronidazole and dimetridazole had better in vitro results than ornidazole and ronidazole on budgerigars isolates.31 In one study, ronidazole dosed at 60 mg/L in drinking water did not provide complete eradication based on in vitro results, thus a dose of 100 mg/L was recommended.18 Another study suggested that metronidazole, ornidazole, and secnidazole at 30 mg/kg had the best in vitro and in vivo results whereas nitazoxanide at 30 mg/kg had the lowest efficacy.32 With captive raptors, care should be taken to avoid their exposure to Trichomonas spp. organisms in prey. It has been shown that freezing prey items (e.g., pigeons) at 201C for at least 12 hours is enough to kill all Trichomonas spp. organisms.33 Among the common GI parasites of wild and captive birds, Capillaria spp. is the most commonly identified.34-39 Capillaria spp. eggs have been found in a raptor cast 6540 ⫾ 110 years before present.40 Although many Capillaria spp. cases remain subclinical, a disease process causing emaciation, depression, diarrhea, dysphagia, oral lesions (which can resemble trichomoniasis), and death may occur.41 Subclinical disease can be exacerbated by stress, concurrent disease, or injury.35 White plaques can be found in the mouth and pharynx, from which wet mount preparations may allow identification of the eggs.37 The most common treatment for Capillaria spp. infection is fenbendazole. In egg-laying broiler hens, fenbendazole dosed in the feed at 30 ppm for 5 days or 80 ppm for 3 days resulted in an effective parasite reduction of 92.3% and 99.3%, respectively.42 In pheasants (Phasianus colchicus) and quail (Perdix perdix), fenbendazole dosed in the feed at 100 ppm for 4 days reduced Syngamus trachea and Capillaria obsignata in more than 90% whereas feed dosages of 30 and 60 ppm for 5 days led to approximately 100% decline of Cap. obsignata in pullets.43 In another study, similar eggreduction effects were detected but adult worms were not as affected, which suggests that albendazole may have a limiting effect on the nematode reproduction but not on eliminating the infection.44 Treatment of pigeons with fenbendazole and albendazole dosed at 33 mg/kg in the drinking water for 3 consecutive days resulted in an overall efficacy of 71% and 66%, respectively.45 It is important to mention that fenbendazole toxicity has been reported in several

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species. Treatment of pigeons and doves with 50 and 100 mg/kg of oral fenbendazole or albendazole resulted in mortality, with shorter survival time and higher weight loss when the high dosage was used.46 Eight of 12 pigeons that were treated with fenbendazole at 30 mg/kg orally for 5 consecutive days developed anorexia, lethargy, and dehydration and died 2 days after the onset of the clinical signs.47 Histopathology results of the birds that died from fenbendazole toxicity revealed acute hemorrhagic enteritis, diffuse lymphoplasmacytic enteritis, small intestinal crypt necrosis, periportal lymphoplasmacytic hepatitis, bile duct hyperplasia, and renal tubular necrosis.47 Whitebacked vultures (Gyps africanus), lappet-faced vultures (Torgos tracheliotus), and Marabou storks (Leptoptilos crumeniferus) treated with 47 to 60 mg/ kg of fenbendazole in the feed died due to suspected fenbendazole toxicity.48 Painted storks (Mycteria leucocephala) treated with 34 to 45 mg/kg orally once a day for 5 days (2 animals were medicated accidently twice daily on the first 2 days), develop bone marrow stem cell failure and enteritis with crypt cell degeneration and necrosis.49 It is hypothesized that the sensitivity to fenbendazole is due to species-specificity, dosagerelated response, or higher tubulin affinity to benzimidazoles in comparison to mammals.49 Side effects may be underreported because subclinical heteropenia and enteritis may not be detected by clinicians.49 It is also suggested that concurrent coccidial infection may cause enteritis and crypt epithelial necrosis.47,50 Consideration for possible adverse side effects is in order when treating birds with fenbendazole or albendazole. ESOPHAGUS/CROP ___________________________ The esophagus connects the mouth to the proventriculus and is divided into cervical and thoracic esophagus, and as opposed to mammals, no sphincters are present.51 In some species, the cervical esophagus expands to form a crop or ingluvies.51 The crop is the first digestive compartment of birds. The ingluvies is well developed in turkeys, poorly developed in most raptors, and absent in Strigiformes, Anseriformes, and Gruiformes; but it is very well developed in some species of vultures, which allows the bird to ingest up to 20% of its body weight in 1 meal.52 The hoatzin (Opisthocomus hoazin) has a well-developed crop that also serves as a major microbial fermentation site similar to the rumen of ruminants, a unique characteristic among avian species.53-55 The crop in some species of birds (e.g., pigeons, male 1 0 4

emperor penguins [Aptenodytes forsteri], and flamingos) allows for the production of “crop milk.”56 The secretion crop milk is a white caseous material formed by the desquamation of the epithelial cells that provides nutrition to the young.57 Crop milk, whose production is regulated by prolactin, is composed mainly of lipids and proteins, which allows for rapid growth of young birds.58,59 Mycotic In humans, Candida albicans is the most common Candida species found in the oral cavity. Can. albicans is pathogenic in immunocompromised individuals and it is considered normal flora of the avian GI tract and should not be confused with yeast found in some nutritional formulas and food items.12,60,61 In one study, Can. albicans was isolated from the mouth of 30 of 60 clinically healthy cockatiels.62 Other than affecting the oropharyngeal cavity and causing plaque formation, Candida spp. infections can also affect the crop. Some of the first reports of Can. albicans infections in a raptor cast, dating 6540.63 The identification of Can. albicans organisms in the GI tract of animals in the absence of candidiasis may be because of the presence of concurrent bacteria.64 Balish and Phillips65 have shown that inoculation of germ-free chicks resulted in large number of Candida spp. clusters, mainly in the crop, whereas conventional chicks that were also experimentally inoculated did not developed signs of infection. Furthermore, inoculation of germ-free chicks with E. coli appeared to protect these animals from candidiasis.64 In a recent study, Candida spp. organisms isolated from the crop of 23 debilitated wildcaught juvenile Amazon parrots (blue-fronted [A. aestiva] and orange-winged Amazon parrot [A. amazonica]), of which 13 were previously diagnosed with ingluvitis, revealed the following Candida species: Can. humicola (28%), Can. parapsilosis (24%), Can. guilliermondii (20%), Can. famata (20%), and Can. albicans (8%).66 Another study reported the presence of yeast in the GI tract of healthy cockatiels.62 The most common yeast found was Can. albicans (32.5%) but several other yeast were identified, including Can. tropicalis (20%), Trichosporon asteroides (12.5%), Can. famata (10%), Rhodotorula mucilaginosa (8.4%), Can. parapsilosis (6.7%), and Can. glabrata (4.2%).62 Crop isolates of prerelease wild Brazilian raptors identified Can. albicans (29.6%), Can. famata (29.6%), Can. parapsilosis (11.1%), Can. tropicalis (11.1%), R. mucilaginosa (11.1%), Can.

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catenulata (3.7%), and Trichos. asteroides (3.7%).67 Several yeast species were also isolated from the crop of nonreleasable European Accipitriformes, Falconiformes, and Strigiformes; C. neoformans, C. laurentii, Can. albicans, Can. inconspicua, Can. pelliculosa, Can. tropicalis, Can. famata, and R. rubra.68 Can. albicans was isolated in 38% of wild stitchbird nestlings, but no relation between the presence of yeast and survival success was detected.69 Interestingly, these studies showed different prevalence of Can. albicans as well as the presence of other Candida spp. that can cause clinical candidiasis, at least in Amazon parrots. Although the clinical significance remains unclear, some of these yeasts can be disease causing for humans. It has been shown that a close genetic relation exists between a chicken Can. albicans isolate and isolates from humans.70 The most common therapy for avian oral and crop candidiasis is nystatin. Nystatin is a polyene macrolide antibiotic that inhibits sterol synthesis in the cytoplasmic membrane.72 Nystatin is not absorbed across intact skin or mucosa and is therefore only useful for topical treatment of oral and pharyngeal candidiasis.71,72 In vitro sensitivity of Candida spp. to several antifungal drugs (amphotericin B, fluconazole, and itraconazole) has been reported. Three out of 21 isolates (2 Can. albicans and 1 Can. tropicalis) were simultaneously resistant to itraconazole and fluconazole.67 Can. albicans isolates from cockatiels revealed minimum inhibitory concentration for amphotericin B of 0.25 to 1 mg/mL, itraconazole 0.03125 to Z16 mg/mL and 14 isolates Z1 mg/mL, and fluconazole 0.25 to Z64 mg/mL and 4 isolates Z64 mg/mL. Fluconazole can be considered a treatment option for severe cases of candidiasis. GASTRIC COMPARTMENTS (PROVENTRICULUS AND VENTRICULUS) _________________________ The avian stomach is different from mammals in that it is composed of several compartments including the proventriculus (pars glandularis), the intermediate zone, the ventriculus (pars muscularis), and the pylorus.73 For more in-depth information on anatomy and physiology, a review on proventriculus and ventriculus has been published by Langlois.73 Bacterial Some authors suggest that the GI tract of birds is sterile at birth and that the bacterial colonization of the avian GI tract occurs during feeding by the parents (in altricial birds) or by spontaneous

cloacal suckling movement, also known as cloacal drinking.73 In a recent study, cultures of the cecal content of 18-day-old chicken embryos revealed Enterococcus spp., Staphyloccus spp. and Micrococcus spp.74 As the embryo develops, a more differentiated microbial population was detected and it is suggested that bacteria cross the eggshell exposing the embryo.74 The normal bacterial flora of most Passerine and Psittacine species is usually composed of Gram-positive bacteria such as Bacillus spp., Corynebacterium spp., Lactobacillus spp., Staphylococcus spp., and Streptococcus spp.73 In raptors, Proteus spp. is also listed as a normal bacterial flora.75 True bacterial infections rarely affect the proventriculus and ventriculus, but are commonly diagnosed above and below this area in the GI tract. Viral Among viral diseases affecting pet birds, proventriculus dilation disease or proventriculus dilatation disease (PDD) may be the most investigated. Since the first reports of PDD in the 70s, several names have been associated with this condition: psittacine proventricular dilatation syndrome, 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, proventricular dilatation disease, proventricular dilatation syndrome, or macaw fading syndrome.76 This condition has been reported in more than 70 Psittacine species, mainly Psittacidae and Cacatuidae species.77 It is suggested that budgerigars may be resistant to this disease.77 Besides Psittacines, this condition has also been reported in canaries, greenfinches, long-wattled (Cephalopterus penduliger) umbrellabirds, Canada geese (Branta canadensis), roseate spoonbills (Platalea ajaja), peregrine falcons (Falco peregrinus), toucans, and bearded barbets (Lybius dubius).77 Until recently, the causative agent of this condition was unknown but, in 2008, 2 research groups identified a novel bornavirus from PDD-positive birds.78,79 Strong evidence suggests that bornavirus is associated with the PDD disease process.80 Bornaviruses are negative-encoded, single-stranded nonsegmented RNA viruses.77 To date, 7 different genotypes of bornavirus have been identified in Psittacine species whereas 2 other genotypes has been identified in a canary and a wild Canada goose.81-83

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Experimental inoculation with bornavirus has been performed in cockatiels, conures, and mallard ducks.83-88 Questions have been raised regarding the conclusions of a number of the psittacine bornavirus studies because of the presence of other viruses either in the inoculated isolate or affecting the study animals.84 Proventricular dilatation disease is caused by nonpurulent inflammation of the autonomic nervous system of the upper GI tract, nervous tissue, and cardiac tissue but concurrent clinical neurological signs and GI disease may not be present.84 Histologically, severe lymphoplasmacytic ganglioneuritis of the GI tract can be detected.81 As the disease name suggests, one of the most common signs is dilation of the proventriculus, which causes abnormal digestion. The typical clinical signs include weight loss although the food intake may remain unchanged, regurgitation, proventricular impaction, and undigested seeds in the feces.81 In some cases, neurological deficits (e.g., seizure, ataxia, abnormal head movement, and proprioceptive and motor deficits) may be present.81 In a suspected PDD case, diagnostic tests include imaging (radiography/fluoroscopy/ultrasonography) with or without contrast studies, crop biopsy, and molecular testing for bornavirus.77 Imaging is a useful tool but it should not be considered definitive for PDD. In PDD cases, a moderate to severely dilated proventriculus can sometimes be detected when diagnostic imaging is used.77 The normal fluoroscopic GI cycle has been described in Amazon parrots along with proventricular measurements.89-91 The proventriculus:keel ratio has been determined and it is said that ratio values o0.48 are suggestive of normal diameter and absence of PDD whereas ratio 40.52 was detected in all PDD-positive animals.92,93 Crop biopsy is considered the gold standard for the diagnosis of PDD although a relevant number of false negatives may occur.77,88 The rate of false negatives may be decreased by using proper biopsy collection methods. Immunohistochemistry may also increase the sensitivity of histopathology in diagnosing PDD. Polymerase chain reaction (PCR) can be performed using frozen tissue samples collected from clinically ill birds. Although proventriculus and ventriculus biopsies may be more rewarding, the collection of these tissues is more invasive, thereby resulting in more risk to an already debilitated patient.77 Molecular diagnosis and serology for PDD have recently become available. The use of PCR, western blot, indirect immunofluorescence assay, and enzyme-linked 1 0 6

immunosorbent assay has been reported.77,94,95 Avian bornavirus has also been reported to be detectable in the urine of parrots by reverse transcriptase-PCR.96 It is important to mention that not all birds that shed bornavirus have clinical disease associated with PDD.97,98 Currently, there is no curative treatment available for PDD. The use of anti-inflammatory drugs (celecoxib, tepoxalin, and meloxicam) with the objective of reducing the inflammation of the central and peripheral nervous system has been reported as a treatment option for PDD.77 Parasitic A large number of parasites have been reported in the avian GI tract but few actually cause clinical signs. Clinically important parasitic helminths in several bird groups are summarized in Table 1. The prevalence of these important helminths may reach 50% to 100% in certain avian populations and some helminthic diseases are among the principal cause of disease in some bird species. Mycotic Macrorhabdus (formerly megabacteriosis) is a disease process caused by Macrorhabdus ornithogaster (Fig. 2).99 Since its first clinical reports, this organism was classified as a yeast and bacteria but its current classification based on molecular, morphological, and antifungal susceptibility is indicative of a yeast.99 These mycotic organisms specifically colonize the isthmus of the GI tract.100,101 M. ornithogaster appears to be a significant disease in some pet bird species (e.g., budgerigar, parrotlets, and Gouldian finches [Erythrura gouldiae]) and has been reported in several continents.102 M. ornithogaster has also been reported to naturally infect, ostrich, rhea, canary, zebra finch (Taeniopygia guttata), free-range chicken, turkey, guinea-fowl, pigeon, toucan, chucker partridge (Alectoris chukar), and crested screamers (Chauna torquata).100,103,104 A similar organism has also been detected in gray partridges.105 A recent study assessed the prevalence of M. ornithogaster in exotic and wild birds in Poland by fecal smears (live birds) and histopathology (dead birds).106 Among 399 birds of 45 species, 28.7% (exotic birds) and 26.1% (wild birds) tested positive for this organism with high rates reported in macaws (41.6%), African gray parrots (33.3%), cockatiels (26.9%), and lovebirds (16.7%).106 In most cases, the presence of M. ornithogaster was not correlated to clinical disease.106 In another study, among 178 canaries

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TABLE 1. Selected gastrointestinal helminths of clinical importance in birds165-167 Helminth

Bird Species

GI Site

Comments

Libyostrongylus Ostrich douglassi

Proventriculus

High mortality rate in young ostriches Diphtheric proventriculitis

Amidostomum spp.

Anseriformes

Ventriculus

High prevalence Impaired ventricular function and nutritional deprivation

Eustrongylides ignotus

Herons and egrets

Proventriculus

High prevalence Stomach perforation, peritonitis High mortality rate in young Ardeidae in North America

Ascarids

Wide range, raptors

Various

Clinical signs most common in young captive raptors

Capillarids

Wide range, raptors, Various, upper and lower GI pigeons

Dispharynx nasuta

Wild game birds, chicken, and passerines

Proventriculus

Worms penetrate proventricular mucosa and cause thickening and functional obstruction Mucosal papillomatous proliferation

Tetrameres spp.

Duck, chicken, pigeons, and aquatic birds

Proventriculus

Females in proventicular glands

Buccal cavity, esophagus (heron and stork), intestines (others)

Severity depends on bird species large-scale epizootics in ducks in the US Echinostomiasis: significant cause of mortality in domestic ducks in Europe and Asia

Digenetic Water birds, trematodes especially anseriformes

and 40 budgerigars, 28% and 22.5%, respectively, were diagnosed postmortem with megabacteriosis.107 Prevalence of megabacteriosis in 2 Australian colonies of captive budgerigars was

White lesions in oropharynx and tongue, enteritis

92 of 340 and 197 of 487, with an overall predisposition of males but no age predilection.108 Megabacteriois tends to present as a chronic wasting disease and animals commonly presents

FIGURE 2. Macrorhabdus ornithogaster in a fecal smear of a budgerigar (Melopsittacus undulatus) stained with Romanowsky stain (1000). Brandão and Beaufrère/Journal of Exotic Pet Medicine 22 (2013), pp 101–117

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with dysphagia, diarrhea, vomiting, unthriftiness, weight loss, and death.109 An acute form of megabacteriosis has also been suggested and appears to be more common in parrolets but is rarely noted in budgerigars.110 Apparently healthy animals develop an acute anorexia and regurgitation with occasional bloodstaining followed by death in 1 to 2 days.110 The most common diagnostic tests performed are microscopic identification of the organism in the feces (stained and wet mount) and an upper GI tract swab or histopathological examination of a tissue sample.111 PCR is also available through commercial laboratories. The Calcofluor staining method has been reported to be a rapid and inexpensive method to visualize the organism in both fecal smears and histopathology but it requires one to use a fluorescent microscope.112 Culture and isolation of this organism is considered to be difficult although the use of Basal Medium Eagle, pH 3 to 4, containing 20% fetal bovine serum and 5% glucose or sucrose under microaerophilic conditions at 421C allowed repeated passages of M. ornithogaster without loss of viability.100 Phylogenetic analysis was achieved using 18s recombinant deoxyribonucleic acid (DNA).99 It is important to note that the simple presence of this yeast is not indicative of pathogenicity and that other predisposing factors, like genetic, management/husbandry, and/or pathogenic strains, may be necessary to cause clinical disease.110 The detection of proventricular ulceration is generally required to confirm pathogenicity. Different treatments have been reported. The use of nystatin at 3,500,000 IU per liter of drinking water for 48 hours followed by 2,000,000 IU per liter for 28 days was considered an effective treatment for megabacteriosis in a flock of 500 budgerigars.113 The treatment of 1 canary with nystatin (0.1 mL once daily, orally) for 7 days was also reported to be curative.101 The use of amphotericin B and ketoconazole (no dosage or route of administration reported) in an outbreak of megabacteriosis in canaries has been suggested to be efficient for the reduction of mortality but not for the treatment of advanced cases of megabacteriosis.103 Amphotericin B is considered the treatment of choice for M. ornithogaster infections and it has shown efficacy at a very high dose of 100 mg/kg twice a day by gavage for 30 days but not if used for only 14 days.110 Under in vitro conditions, M. ornithogaster has been shown to be susceptible to amphotericin B.114 Moore et al.112 suggest that animals that have been 1 0 8

treated with amphotericin B may be susceptible to future shedding of the organism. Fluconazole has promising results for the treatment of experimentally infected chickens but it is suspected to be toxic for budgerigars at a daily dose of 10 mg/ kg.110 Iodine preparations, lufenuron, ketoconazole, terbinafine, and itraconazole have been shown to be ineffective when treating megabacteriosis.110 Addition of dietary probiotic supplements (e.g., Lactobaccillus spp.) has been suggested as a means to decrease the shedding rate of M. ornithogaster, possibly due to decreasing the pH of the GI tract.110 Acidification of the gastric content has been anecdotically reported as a treatment option but it has also been reported that M. ornithogaster is able to grow in very acidic environment.109,115 In another study, optimal in vitro growth of this organism was achieved at a pH of 3 to 4.100 To prevent the propagation of this condition, it has been shown that raising specific pathogen-free animals by removing the eggs from pathogen-positive nests, followed by cleaning with warm 5% povidone-iodine solution and hand raising the chicks eliminated the presence of M. ornithogaster in the offspring.112 This study also revealed that vertical in ovo transmission does not occur, and that feeding and fecal contamination are the most likely routes of transmission.112 Culling of positive individuals did not appear to affect the progression of the disease but culling positive individuals after amphotericin treatment may be advisable to decrease the number of amphotericin B-resistant strains.108 Treatment with sodium benzoate in drinking water at 1 tbs/L ( 5 mL/L) for 5 weeks was successful in managing an outbreak in nonbreeding budgerigars but caused neurological signs and death in breeding budgerigars at the dose of half tbs/L ( 5 mL/L) because of increased water intake.116 No report of zoonotic risk associated with M. ornithogaster has been reported.117 Experimental infection of Balb/c mice with 107 cfu/0.1 mL intraperitoneal caused 100% mortality.103 To our knowledge, no naturally occurring transmission from birds to mammals or reptiles has been reported. INTESTINE ____________________________________ Following the gastric compartments, the small and large intestines are present. The development of the different intestinal sections varies among species. The intestinal portion of carnivore, insectivore, and frugivore species is shorter than granivore and herbivore species because of differences in food

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digestion.56 The large intestine usually consists of a paired ceca and rectum, although the size and relevance of the ceca is variable.76 For example, the ceca is either absent or rudimentary in parrots, passerines, swifts, pigeons, and toucans.56 Conversely, galliformes and ostriches have large ceca.76 In the past, correlation between diet (high cellulose) and size of the ceca was suggested but currently, some authors do not support this theory.56 Bacterial Mycobacteriosis primarily affects the GI tract of avian species. The most common route of transmission is fecal-oral, but ingestion of infected prey, inhalation, and wound contamination is also possible.118,119 After ingestion of Mycobacterium avium, the liver and intestines are the first organs to be affected, and by the hematogenous route, other organs can also become infected.119 Mycobacteriosis among captive birds may be more prevalent owing to greater density of birds and long-term use and exposure to contaminated areas.120 The most common clinical signs of mycobacteriosis include weight loss, polyphagia, poor feather condition, polyuria, diarrhea, and abdominal distention.119 As for humans, the true diagnosis of mycobacteriosis is difficult and clinicians tend to diagnose this condition based on clinical data but definitive diagnosis should be based on laboratorial isolation and identification of the pathogen.121 Hematology results showing moderate to marked leukocytosis with heterophilia and monocytosis, with or without reactive lymphocytes and decrease packed cell volume, may be suggestive of mycobacteriosis but does not provide a definitive diagnosis.119 Diagnosis can be based on fecal acid-fast staining cytology, radiographs, lesion biopsy, endoscopy, fecal culture, or lesion culture.118 Recently, a comparative study of the different diagnostic methods for mycobacteriois in ring-necked doves was performed showing that no single test allowed definitive diagnosis of all infected birds; liver and bone marrow biopsy and culture had the highest sensitivity whereas PCR and Ziehl-Neelsen staining had poor results.122 In another study using My. avium–inoculated Japanese quails, LowesteinJensen culture medium yielded better results and as the disease progressed, the rate of positive fecal cultures was higher.123 When comparing other diagnostic tests (PCR and acid-fast staining with Ziehl-Nielsen and Truant stains) with culture, all had 100% specificity for tissue and 495% for fecal

material.123 Sensitivity for fecal samples was higher with Truant stain (30.4%) whereas tissue sample PCR had the highest results (100%).123 Mycobacterium spp. often are slow-growing bacteria, which makes laboratory identification fastidious and difficult.124 Intradermal tuberculin test has been used for several decades in poultry and it was considered a useful tool.125 This test, besides being impractical in noncaptive birds (it requires capture for administration and assessment of the local reaction at 48 to 72 hours), had a high incidence of false negatives in raptors, pigeons, geese, quail, and several exotic species.118 The use of fecal cytology as a diagnostic tool is questionable owing to the low fecal shedding rate of bacteria and the random excretion, therefore, a negative fecal cytology result should not be considered a result to rule out the possibility of this disease affecting the patient.126 Although the presumptive diagnosis of mycobacteriosis may be based on patient presentation, clinical signs, and minor diagnostic tests as mentioned earlier, definitive identification of the pathogen is rarely obtained.127 In human medicine, PCR-based sequencing identification by PCR amplification of mycobacterial DNA with genus-specific primers and sequencing of amplicons is the gold standard.121 In birds, culture is said to be the gold standard, although, due to the fastidious growth of some species, special culture techniques and DNA probes may be needed.125 Culture and tissue sample PCR is the most sensitive and specific laboratory testing available.123 Until recently, My. avium-intracellulare complex was considered the most common avian mycobacteria but recent molecular techniques allowed the identification of My. genavense, a slow-growing mycobacterium, in several avian mycobacteriosis cases.127-129 Among 5345 necropsies, 204 were diagnosed as mycobacteriosis based on histopathology, of which a total of 48 were cultured and analyzed using 16s ribosomal RNA (rRNA) allowing for identification of 34 My. genavense, 8 My. avium, 2 My. fortuitum, 2 My. tuberculosis, 1 My. gordonae, and 1 My. nonchromogenicum.128 In a recent study, out of 24 mycobacteriosis cases, 23 were My. genavense whereas only 1 case was My. avium, which were identified by PCR and rRNA hypervariable region (16s rRNA) with similarity percentages ranging from 99.4% to 100%.127 The 16s sRNA gene has been sequenced for several species and it is a useful tool to differentiate between Mycobacterium species but some have similar 16s rRNA sequences (e.g., My. kansasii and My. gastri).121 Nevertheless, molecular techniques were revolutionary and have

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provided new methodologies for the identification of Mycobacterium spp. as well as other bacteria. The most commonly affected organs include, but are not limited to, the liver, spleen, and intestines.125 For the purpose of this review, we focus on the intestinal lesions; the reader should refer to Tell et al. and Converse120,125 for further information of avian mycobacteriosis. On necropsy, gross findings in the intestines appear like paratuberculosislike lesions that include very prominent thickening or clubbed villi, and multiple, variably sized, gray, tan, or yellow nodules that protrude from the serosal surface of the intestine and occasional disseminated granulomas in the intestinal wall.120,125 Postmortem diagnosis is based on the identification of mycobacteria in the blood or tissues, but without the use of acid-fast stain the bacteria will not be identified.120 Similar lesions between experimentally infected and naturally occurring disease have been reported.130 Several treatment protocols have been reported for avian mycobacteriosis. A whooping crane (Grus americana) diagnosed with My. avium complex was treated with rifampin (45 mg/kg orally, once a day), ethambutol (30 mg/kg orally, once a day), and 2 doses of My. vaccae antigen for 1 year until suspected reoccurrence of clinical signs was noted at which time, azithromycin (40 mg/kg orally, once a day) to which ethambutol (30 mg/kg orally, once a day) was added 16 weeks later.131 The animal died 3 weeks after introduction of ethambutol with severe hepatopathy and chronic fibrosing cardiomyopathy, which was suspected to be related to drug interactions.131 Regardless, at the time of necropsy, no My. avium was possible to be isolated, which suggests that azithromycin may be an adequate medication for the treatment of mycobacteriosis in this individual.131 In 2007, Lennox compiled a list of treatment protocols and outcomes. The most common protocol used was isoniazid (30 mg/kg orally, once a day), ethambutol (30 mg/kg orally, once a day), and rifampin (45 mg/kg orally, once a day) with a treatment period varying from 6 to 19 months.119 My. marinum was isolated from the proximal rhinotheca and sinus of a blue-fronted Amazon parrot which was treated with clarithromycin (85 mg/kg orally, once a day), ethambutol (30 mg/ kg orally, once a day), and rifampin (45 mg/kg orally, once a day), but died 4 months after antimicrobial therapy.132 In the case of little blue penguins (Eudyptula minor) with My. intracellulare treated with rifampin (15 mg/kg orally, once a day), ethambutol (15 mg/kg orally, once a day), 1 1 0

and clarithromycin (10 mg/kg orally, once a day) for several years lead to resistance and the protocol was changed to minocycline (10 mg/kg orally, once a day) and clarithromycin (10 mg/kg orally, once a day).133 Other bacteria can cause significant enteritis in avian species, including Clostridium perfringens, which is the suspected causative agent of necrotic enteritis and cholangiohepatitis.134 Necrotic enteritis in chickens has been described since 1961 and it manifests as an acute or chronic enterotoxemia.135 Necrotic enteritis is a reemerging disease, in part, owing to banning of antimicrobial use as growth promoters in poultry.136 Five types of Cl. perfringens have been identified (A, B, C, D, and E) which are responsible for the production of 6 major toxins; alpha (α), beta (β), epsilon (ε), iota (ι), enterotoxin, and Cl. perfringens beta2 toxin (cpb-2).134 In a recent study, Cl. perfringens type A isolates from 31 cases of avian necrotic or ulcerative enteritis and 19 from nonclostridial enteritis were evaluated for the production of toxins.134 The results did not support the theory of beta2 toxin being the cause of necrotic enteritis.134 A novel toxin, NetB has been suggested to be a virulence factor of avian Cl. perfringens strains capable of causing necrotic enteritis in chickens.135 Similar studies, to the authors’ knowledge, have not been performed in other avian species outside of chickens. Some studies have assessed the development of a vaccine for necrotic enteritis in chickens.136-138 Peracute and acute death is usually encountered in birds of prey with Clostridium spp. infections.139 Among other species of birds, reports of Clostridium spp. infections are scarce and the significance of this disease remains unclear although it appears to be problematic in some species.140-143 Cl. colinum is the agent of ulcerative enteritis of quail. Among the reported cases, lorikeets and lories appear to be overrepresented.144,145 Cl. tertium has been isolated from apparently healthy newly hatched chicks.74 Presence of clostridium has also been reported in wild birds.146,147 The most common clinical signs of clostridium infection in birds include diarrhea, fetid stool, megacolon, megacloaca, vomiting, and melena.140,142,148 Culture and sensitivity is advisable to determine appropriate antimicrobial therapy. Fecal cytology and tissue biopsy can be suggestive of the presence of Gram-positive rods but culture is necessary for definitive identification. The reported treatments of Clostridium spp. infections include clindamycin and piperacillin.144,148 An in vitro sensitivity study of

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Cl. perfringens isolates from chickens showed that penicillins and cefazolin had excellent activity and no resistance whereas tetracycline and streptomycin were not recommended.149 An in vivo study of tylosin phosphate in feed suggested that this medication at 100 ppm was effective for the treatment of clinical outbreaks of necrotic enteritis in chickens.150 Amoxicillin, tylosin, and lincomycin were considered curative treatments in a subclinical experimental infection model that used coccidia as the predisposing factor in broilers. Parasitic Clinically important helminths are summarized in Table 1 and clinically important protozoa in Table 2. CLOACA ______________________________________ The cloaca is the final anatomical section of the avian and reptile digestive tract and is formed by 3 compartments: the coprodeum (communicates with the rectum), the urodeum (opening of the ureters and genital tract), and the proctodeum (connects to the outside through the vent lips).76 Viral The presence of internal papillomas is a common disease condition diagnosed in Psittacine species (Fig. 3).151 Papillomas commonly develop in the cloaca although it has also been reported in the oropharynx, larynx, esophagus, crop, ventriculus, proventriculus, and commissure of the beak.151 A strong association has been shown between the Psittacid herpesvirus (PsHV) and internal papillomas. Prevalence of PsHV in parrots with mucosal papillomas is higher than in the general population or animals without mucosal papillomas.152 PsHV persist as latent infection in the oral and cloacal mucosa of psittacine birds. Pacheco's disease is also caused by PsHV which causes a acute fatal disease if the animals have not been evolutionarily adapted to that specific viral genotype.153 Two different herpesvirus have been identified and both appear to be able to cause internal papilloma formation.153 Although in mammals the formation of mucosal papillomas is commonly associated with papillomavirus, this has not been identified in Psittacine species, either naturally occurring or experimentally induced ones.154,155 One report has not been able to identify either PsHV or papillomavirus from a

cloacal papilloma of a sulfur-crested cockatoo (Ca. galerita).155 Animals with GI papillomas commonly manifest blood in the droppings (feces, urine, or urates), straining to defecate, papilloma and/or cloacal prolapse, cloacal stricture (possibly secondary to surgical debulking or cloacitis), and possible bile duct or pancreatic duct carcinomas.155-157 If considered necessary, debulking the tissue mass using cryotherapy, electrocautery, chemical cauterization, or surgical excision are commonly used techniques; care should be taken to prevent strictures at the surgical site. The use of purse-string sutures to reduce cloacal prolapse associated with papillomas is contraindicated as it can block the cloaca.158 Application of acetic acid to affected cloacal tissue will cause the diseased mucosal tissue to turn white.76 Molecular testing and histopathology are the only definitive tests to diagnose internal papillomas and confirm a possible viral component. ZOONOTIC RISKS ____________________________ Some disease pathogens of avian species may pose a zoonotic risk, independently of being pathogenic to the individual bird. Several studies assessing the presence of pathogenic bacteria and yeasts in the fecal material or cloaca of birds have been published. It is said that pigeon droppings are the main source of pathogenic yeast exposure to humans.159 Among migratory European wild bird species, several potential zoonotic pathogenic yeasts were isolated from the cloaca.159 Of the 421 animals sampled, 15.7% positive yeast isolates were identified, of which R. rubra (28.2%), C. albidus (18.4%), Can. albicans (9.2%), Trichos. cutaneum (8.4%), Can. guilliermondii (6.1%), Can. tropicalis (6.1%), Can. humicola (5.3%), C. laurentii (5.3%), Trichos. beigelii (5.3%), Hansenula anomala (3.1%), Can. famata (1.5%), Can. lusitaniae (0.8%), Can. pelliculosa (0.8%), R. glutinis (0.8%), Saccharomyces cerevisiae (0.8%).159 There are also reports of the prevalence of potential pathogenic yeasts isolated from captive pigeons.160,161 Although not reported in the scientific literature, there is an hypothetical zoonotic risk associated with a Mycobacterium spp. positive pet bird; owners should be informed of such hypothetical risk and humane euthanasia should be discussed.125,162 A case of My. tuberculosis in a green-winged macaw (Ar. chloroptera), multiple small white nodules were detected on the tongue,

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TABLE 2. Selected gastrointestinal protozoa of clinical importance in birds165,167 Protozoa

Bird Species

GI Site

Comment

Trichomonas gallinae

Raptors, passerines, budgerigars, poultry, Oropharynx pigeons, and doves

Caseous lesions

Giardia psittaci

Budgerigars, cockatiels, and lovebirds

Diarrhea and enteritis

Spironucleus columbae

Pigeon

Eimeria spp.

Wide range, mainly poultry, ducks, and pigeons

Small and large intestines

Depends on Eimeria species Higher morbidity in young birds Systemic form in cranes Significant disease of poultry

Isospora spp.

Passerines, wide range except poultry

Intestines

Young canaries infected with I. canaria

Caryospora spp. Falcons and owls

Intestines

Important disease of young captive falcons Not reported in Accipitriformes

Histomonas meleagridis

Ceca and liver

Caseous typhlitis and hepatic necrosis

Proventriculus, intestines and ceca

Cr. baileyi is a respiratory pathogen Enteritis, diarrhea and zoonosis

Intestines

Mortality in young pigeons

Chicken and turkey

Cryptosporidium Galliformes mainly spp.

choana, and glottis as well as systemic disease.163 In the case of an African gray parrot (Psittacus erithacus) with lingual masses and poor body condition, My. tuberculosis infection was

diagnosed.164 It is suggested that this infection was caused by transmission from the humans whom were previously diagnosis with tuberculosis (reverse zoonosis).163 In cases of ocular, sinus, oral, or cutaneous nodular lesions, My. tuberculosis infection should be considered and public health policies followed.163 A recent report detailed an outbreak of mycobacteriosis in pigeons during which a rabbit housed in the same area tested positive for My. avium as did several pigeons.168

REFERENCES

FIGURE 3. Cloacal papilloma in a green-winged macaw (Ara. chloropterus) visualized by cloacoscopy.

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