JPC SYSTEMIC PATHOLOGY
Signalment, Slide A (JPC #2389731): 1 1/2-year-old male cockatoo
HISTORY: The bird was lethargic and anorexic for some time. It seemed to be wasting away and had been regurgitating food off and on for several weeks. Grossly, the proventriculus and ventriculus were dilated.
- Small intestine and mesentery: Multifocally there is an infiltrate composed of moderate numbers of lymphocytes and plasma cells that centers on the myenteric plexuses and extends into the adjacent tunica muscularis. Within affected myenteric ganglia, there are decreased numbers of ganglion cells. Similar inflammatory cells are also present within nerve bundles of the adjacent mesentery. There is diffuse mesenteric fat atrophy with reduced adipocyte cytoplasm containing one or more varisized intracytoplasmic lipid vacuoles, prominence of nuclei, and blood vessels in close proximity to one another.
- Cerebrum: Multifocally there are perivascular infiltrates of low numbers of lymphocytes and plasma cells within the gray and white matter and the leptomeninges.
- Peripheral nerve: Multifocally within the nerve and surrounding epineurium, there are perivascular aggregates of lymphocytes and plasma cells.
- Small intestine and mesentery: Ganglioneuritis and leiomyositis, lymphoplasmacytic, subacute, multifocal, mild, with ganglion cell loss, cockatoo, avian.
- Cerebrum: Meningoencephalitis, lymphoplasmacytic, subacute, multifocal, mild.
- Peripheral nerve: Epineuritis, lymphoplasmacytic, subacute, multifocal, mild.
- Adipose tissue, mesentery: Fat atrophy, diffuse, moderate.
- Kidney: No significant findings.
Signalment, Slide B (JPC #2820183): Female psittacine
HISTORY: Chronic weight loss
- Heart: Diffusely, nerves subjacent to the epicardium contain an infiltrate of low numbers of lymphocytes and plasma cells that occasionally extend into the surrounding connective tissue.
- Liver: Multifocally within portal areas, there is an infiltrate composed of low numbers of lymphocytes and plasma cells, and rare heterophils.
- Heart, epicardial nerves: Neuritis, lymphoplasmacytic, subacute, diffuse, moderate.
- Liver: Hepatitis, portal, lymphoplasmacytic and heterophilic, subacute, multifocal, mild.
ETIOLOGIC DIAGNOSIS: Bornaviral ganglioneuritis, leiomyositis, meningoencephalitis, neuritis, and hepatitis
CAUSE: Avian bornavirus (ABV)
CONDITION: Proventricular dilatation disease (PDD)
CONDITION SYNONYMS: Psittacine proventricular dilatation syndrome (PDDS), neuropathic gastric dilatation (NGD), macaw wasting disease, lymphoplasmacytic ganglioneuritis and encephalomyelitis
- Proventricular dilatation disease (PDD) was first identified in the 1970s, and is a progressive neurologic, often fatal, disease of psittacine birds (worldwide) characterized by lymphoplasmacytic myenteric ganglioneuritis and encephalomyelitis
- PDD primarily affects the autonomic nerves of the upper and middle digestive tract, including the esophagus, crop, proventriculus, ventriculus, and duodenum
- Infection is common and widespread among captive psittacines; asymptomatic carriers are an important factor in spread of the disease
- Caused by an 80 nm diameter RNA virus, ABV, that replicates in the nucleus of cells
- Unlike borna disease virus (BDV), ABV has a wide tissue tropism (not limited to neurotropism)
- Virus can be detected in feces, cloacal swabs, swabs from the nares and choana, and feathers of the axilla
- Fecal-oral transmission likely (widely accepted, but not definitively proven); it is assumed that respiratory transmission can occur
- Pathogenesis has not been completely determined, but it is likely similar to mammalian borna disease
- Infection is common and widespread in North America with healthy or subclinical carriers documented in several species; asymptomatic birds shed viral particles in oral, nasal, and fecal secretions, and from feathers in the axilla
- There may be an autoimmune component to PDD
TYPICAL CLINICAL FINDINGS:
- Clinical signs are related to dysfunction of digestive or central nervous systems, or both
- Weight loss, crop stasis, proventricular and ventricular dilatation, intermittent regurgitation, maldigestion (passage of undigested seeds in the feces), starvation, and ultimately death
- Depression, seizures, ataxia, blindness, and tremors
- Clinically affected animals die after a protracted clinical course
- Many birds with PDD develop microbial overgrowth in the dilated and nonmotile proventriculus and can succumb to sepsis
TYPICAL GROSS FINDINGS:
- Dilation and impaction of the proventriculus and ventriculus
- The proventriculus and ventriculus may be thin walled, flaccid, and distended
- The proximal duodenum may be similarly affected
- The right ventricle of the heart may be thin walled and dilated
TYPICAL LIGHT MICROSCOPIC FINDINGS:
- Characterized by lymphoplasmacytic infiltrates within myenteric plexuses, ganglia, and nerves
- Similar infiltrates are often present in the brain, spinal cord, peripheral nerves, conductive tissue of the heart, and adrenal glands
- Lymphoplasmacytic infiltrates may extend perivascularly and perineurally into surrounding connective tissue
- There may be focal to diffuse myocardial necrosis
- Within the brain, there are nonsuppurative perivascular cuffs with mild glial cell activation, demyelination, and Purkinje cell necrosis
- There are perivascular cuffs in the spinal cord and lymphoplasmacytic infiltrates within associated ganglia and dorsal nerve roots
ADDITIONAL DIAGNOSTIC TESTS:
- Clinically, a tentative diagnosis is made based on history, clinical signs, and radiographic evidence of proventricular dilatation
- Antemortem crop biopsy is used to look for classical histopathologic findings but results in approximately 25% false negatives
- Plucked feathers are the most reliable non-invasive source of DNA and RNA for ID of virus via RT-PCR
- Postmortem histopathology is confirmatory
- More rapid tests have been recently developed:
- IHC - is 100% sensitive and 100% sensitive for ABV using histopathology as the gold standard
- Western blot
For gross finding of proventricular dilation:
- Proventricular impaction is common in psittacine chicks that consume bedding material
- Proventricular dilation is common in chickens fed low fiber diets
- Proventricular dilaton is common in geese with lead poisoning
For lymphoplasmacytic meningoencephalitis in birds:
- Avian paramyxovirus type 1 (Newcastle disease virus)
- EEE/WEE/VEE (alphavirus)
- Avian encephalomyelitis virus (picornavirus)
- Avian adenovirus
- Influenza A virus
- West Nile virus (flavivirus)
Intestinal poxvirus infection and Pacheco’s disease can lead to proventricular lesions grossly and histologically similar to PPD
- Proventricular dilation is common in chickens fed low fiber diets
- Dysautonomia (Key-Gaskell syndrome): combination of gastrointestinal dysfunction, ocular signs, dysuria, and aspiration pneumonia secondary to megaesophagus; chromatolytic degeneration of the neurons of autonomic ganglia, without evidence of inflammation
- Horses (“grass sickness”)
- May be associated with infection by Clostridium botulinum type C
- Dogs, particularly in Kansas
- A waterfowl genotype of ABV similar to PDD has been reported in Canada Geese and trumpeter swans in Canada and is associated with encephalitis
- Borna disease virus (BDV) – causes neurologic staggering disease in horses, cats, sheep, and ostriches most often in Europe; equids and sheep are most susceptible
- Caines D, Pinard CL, et al. Autonomic dysfunction in a Jack Russell terrier. Can Vet J. 2011; 52:297-299.
- Cantile C, Youssef S. Nervous system. Maxie MG ed. In: Jubb Kennedy and Palmer's Pathology of Domestic Animals. Vol 1. 6th ed. Philadelphia, PA: Elsevier Saunders; 2016:377-378..
- Collette SA, McManamon R, Rech RR, Howerth EW. Pathology in practice. Proventricular dilatation disease. J Am Vet Med Assoc. 2010;236(5):519-521.
- De Kloet SR, Dorrestein GM. Presence of avian bornavirus RNA and anti-avian bornavirus antibodies in apparently healthy macaws. Avian Dis. 2009;53(4):568-573.
- Donatti RV, Resende M, et al. Fatal proventricular disease in captive native psittacines in Brazil. Avian Dis. 2014; 58(1):187-193.
- Gray P, Hoppes S, Suchodolski P, et al. Use of avian bornavirus isolates to induce proventricular dilatation disease in conures. Emerg Infect Dis. 2010;16(3):473-479.
- Guo J, Tizard I, Baroch J, et al. Avian bornaviruses in North American gulls. J Wildl Dis. 2015; 51(3):754-758.
- Honkavuori KS, Shivaprasad HL, Williams BL, et al. Novel borna virus in psittacine birds with proventricular dilatation disease. Emerg Infect Dis. 2008;14(12):1883-1886.
- Hoppes S, Gray PL, Payne S, Shivaprasad HL, Tizard I. The isolation, pathogenesis, diagnosis, transmission, and control of avian bornavirus and proventricular dilatation disease. Vet Clin North Am Exot Anim Pract. 2010;13(3):495-508.
- Keller DL, Honkavuori KS, Briese T. Proventricular dilatation disease associated with avian bornavirus in a scarlet macaw (Ara macao). J Vet Diagn Invest. 2010;22(6):961-965.
- Kistler AL, Smith JM, Greninger AL, Derisi JL, Ganem D. Analysis of naturally occurring avian bornavirus infection and transmission during an outbreak of proventricular dilatation disease among captive psittacine birds. J Virol. 2010;84(4):2176-2179.
- Raghav R, Taylor M, Delay J, et al. Avian bornavirus is present in many tissues of psittacine birds with histopathologic evidence of proventricular dilatation disease. J Vet Diagn Invest. 2010;22(4):495-508.
- Rinder M, Ackermann A, Kempf H, Kaspers B, Korbel R, Staeheli P. Broad tissue and cell tropism of avian bornavirus in parrots with proventricular dilatation disease. J Virol. 2009;83(11):5401-5407.
- Rossi G, Crosta L, Pesaro S. Parrot proventricular dilation disease. Vet Rec. 2008;163(10):310.
- Schmidt RE, Reavill DR, Phalen DN. Gastrointestinal system and pancreas. In: Pathology of Pet and Aviary 2nd ed. Ames, IA: Wiley Blackwell; 2015:69-70.
- Shivapradsad HL. Miscellaneous diseases. In: Boulianne M, ed. Avian Disease Manual. 7th Jacksonville, FL: AAAP; 2013:199.
- Swayne DE, Barnes JH, Abdul-Aziz T, Fletcher OJ. Nervous system. In: Avian Histopathology. 4th Jacksonville, FL: AAAP; 2016:476,510