Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-20T15:35:18.547Z Has data issue: false hasContentIssue false

The pathogenesis of proventricular dilatation disease

Published online by Cambridge University Press:  03 February 2017

Ian Tizard*
Affiliation:
Department of Veterinary Pathobiology and the Schubot Exotic Bird Health Center, Texas A&M University, College Station, TX 77843, USA
H. L. Shivaprasad
Affiliation:
University of California Animal Health and Food Safety Laboratory System-Tulare, University of California, Davis, Tulare, CA, USA
Jianhua Guo
Affiliation:
Department of Veterinary Pathobiology and the Schubot Exotic Bird Health Center, Texas A&M University, College Station, TX 77843, USA
Samer Hameed
Affiliation:
Department of Veterinary Pathobiology and the Schubot Exotic Bird Health Center, Texas A&M University, College Station, TX 77843, USA
Judith Ball
Affiliation:
Department of Veterinary Pathobiology and the Schubot Exotic Bird Health Center, Texas A&M University, College Station, TX 77843, USA
Susan Payne
Affiliation:
Department of Veterinary Pathobiology and the Schubot Exotic Bird Health Center, Texas A&M University, College Station, TX 77843, USA
*
*Corresponding author. E-mail: [email protected]

Abstract

Bornaviruses cause neurologic diseases in several species of birds, especially parrots, waterfowl and finches. The characteristic lesions observed in these birds include encephalitis and gross dilatation of the anterior stomach — the proventriculus. The disease is thus known as proventricular dilatation disease (PDD). PDD is characterized by extreme proventricular dilatation, blockage of the passage of digesta and consequent death by starvation. There are few clinical resemblances between this and the bornaviral encephalitides observed in mammals. Nevertheless, there are common virus-induced pathogenic pathways shared across this disease spectrum that are explored in this review. Additionally, a review of the literature relating to gastroparesis in humans and the control of gastric mobility in mammals and birds points to several plausible mechanisms by which bornaviral infection may result in extreme proventricular dilatation.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ackermann, A, Guelzow, T, Staeheli, P, Schneider, U and Heimrich, B (2010). Visualizing viral dissemination in the mouse nervous system, using a green fluorescent protein-expressing Borna disease virus vector. Journal of Virology 84: 54385442.Google Scholar
Aggestrup, S, Uddman, R, Sundler, F, Fahrenkrug, J, Hakanson, R, Sorensen, HR and Hambraeus, G (1983). Lack of vasoactive intestinal polypeptide nerves in esophageal achalasia. Gastroenterology 84: 924927.Google Scholar
Ang, CW, Dijkstra, JR, de Klerk, MA, Endtz, HP, van Doorn, PA, Jacobs, BC, Jeurissen, SH and Wagenaar, JA (2010). Host factors determine anti-GM1 response following oral challenge of chickens with Guillain–Barre syndrome derived Campylobacter jejuni strain GB11. PLoS ONE 5: e9820.Google Scholar
Aube, AC, Cabarrocas, J, Bauer, J, Philippe, D, Aubert, P, Doulay, F, Liblau, R, Galmiche, JP and Neunlist, M (2006). Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut 55: 630637.Google Scholar
Auteri, M, Zizzo, MG and Serio, R (2015). GABA and GABA receptors in the gastrointestinal tract: from motility to inflammation. Pharmacological Research 93: 1121.Google Scholar
Balaskas, C, Saffrey, MJ and Burnstock, G (1995). Distribution and colocalization of NADPH-diaphorase activity, nitric oxide synthase immunoreactivity, and VIP immunoreactivity in the newly hatched chicken gut. Anatomical Record 243: 1018.Google Scholar
Bashashati, M and Mccallum, RW (2015). Is interstitial cells of cajalopathy present in gastroparesis? Journal of Neurogastroenterology and Motility 21: 486493.CrossRefGoogle ScholarPubMed
Berg, M, Johansson, M, Montell, H and Berg, AL (2001). Wild birds as a possible natural reservoir of Borna disease virus. Epidemiology & Infection 127: 173178.Google Scholar
Berhane, Y, Smith, DA, Newman, S, Taylor, M, Nagy, E, Binnington, B and Hunter, B (2001). Peripheral neuritis in psittacine birds with proventricular dilatation disease. Avian Pathology 30: 563570.Google Scholar
Berthoud, HR (2008). Vagal and hormonal gut-brain communication: from satiation to satisfaction. Neurogastroenterology & Motility 20 (suppl. 1): 6472.CrossRefGoogle ScholarPubMed
Billaud, JN, Ly, C, Phillips, TR and de la Torre, JC (2000). Borna disease virus persistence causes inhibition of glutamate uptake by feline primary cortical astrocytes. Journal of Virology 74: 1043810446.Google Scholar
Bode, L, Durrwald, R and Ludwig, H (1994). Borna virus infections in cattle associated with fatal neurological disease. Veterinary Record 135: 283284.Google Scholar
Bohorquez, DV, Shahid, RA, Erdmann, A, Kreger, AM, Wang, Y, Calakos, N, Wang, F and Liddle, RA (2015). Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells. Journal of Clinical Investigation 125: 782786.CrossRefGoogle ScholarPubMed
Boros, A, Timmermans, JP, Fekete, E, Adriaensen, D and Scheuermann, DW (1994). Appearance and some neurochemical features of nitrergic neurons in the developing quail digestive tract. Histochemistry 101: 365374.Google ScholarPubMed
Borre, YE, O'keeffe, GW, Clarke, G, Stanton, C, Dinan, TG and Cryan, JF (2014). Microbiota and neurodevelopmental windows: implications for brain disorders. Trends in Molecular Medicine 20: 509518.Google Scholar
Bravo, JA, Forsythe, P, Chew, MV, Escaravage, E, Savignac, HM, Dinan, TG, Bienenstock, J and Cryan, JF (2011). Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proceedings of the National Academy of Sciences of the United States of America 108: 1605016055.CrossRefGoogle Scholar
Brookes, S (2001a). Retrograde tracing of enteric neuronal pathways. Neurogastroenterology and Motility 13: 118.Google Scholar
Brookes, SJ (2001b). Classes of enteric nerve cells in the guinea-pig small intestine. Anatomical Record 262: 5870.Google Scholar
Buchholz, BM, Chanthaphavong, RS and Bauer, AJ (2009). Nonhemopoietic cell TLR4 signaling is critical in causing early lipopolysaccharide-induced ileus. Journal of Immunology 183: 67446753.Google Scholar
Cabarrocas, J, Savidge, TC and Liblau, RS (2003). Role of enteric glial cells in inflammatory bowel disease. Glia 41: 8193.Google Scholar
Carbone, KM, Duchala, CS and Narayan, O (1988). Borna disease. An immunopathologic response to viral infection in the CNS. Annals of the New York Academy of Sciences 540: 661662.CrossRefGoogle ScholarPubMed
Chaplin, SB and Duke, GE (1990). Effect of denervation of the myenteric plexus on gastroduodenal motility in turkeys. American Journal of Physiology 259: G481G489.Google Scholar
Christakos, S, Barletta, F, Huening, M, Dhawan, P, Liu, Y, Porta, A and Peng, X (2003). Vitamin D target proteins: function and regulation. Journal of Cellular Biochemistry 88: 238244.CrossRefGoogle ScholarPubMed
Clark, FD (1984). Proventricular dilatation syndrome in large psittacine birds. Avian Diseases 28: 813815.CrossRefGoogle ScholarPubMed
Curro, D, Ipavec, V and Preziosi, P (2008). Neurotransmitters of the non-adrenergic non-cholinergic relaxation of proximal stomach. European Review for Medical and Pharmacological Sciences 12 (suppl. 1): 5362.Google ScholarPubMed
Daoust, PY, Julian, RJ, Yason, CV and Artsob, H (1991). Proventricular impaction associated with nonsuppurative encephalomyelitis and ganglioneuritis in two Canada geese. Journal of Wildlife Diseases 27: 513517.CrossRefGoogle ScholarPubMed
De Giorgio, R, Di Simone, MP, Stanghellini, V, Barbara, G, Tonini, M, Salvioli, B, Mattioli, S and Corinaldesi, R (1999). Esophageal and gastric nitric oxide synthesizing innervation in primary achalasia. American Journal of Gastroenterology 94: 23572362.Google Scholar
Delnatte, P, Berkvens, C, Kummrow, M, Smith, DA, Campbell, D, Crawshaw, G, Ojkic, D and Delay, J (2011). New genotype of avian bornavirus in wild geese and trumpeter swans in Canada. Veterinary Record 169: 108.CrossRefGoogle ScholarPubMed
Delnatte, P, Ojkic, D, Delay, J, Campbell, D, Crawshaw, G and Smith, DA (2013). Pathology and diagnosis of avian bornavirus infection in wild Canada geese (Branta canadensis), trumpeter swans (Cygnus buccinator) and mute swans (Cygnus olor) in Canada: a retrospective study. Avian Pathology 42: 114128.CrossRefGoogle ScholarPubMed
Delnatte, P, Mak, M, Ojkic, D, Raghav, R, Delay, J and Smith, DA (2014a). Detection of Avian bornavirus in multiple tissues of infected psittacine birds using real-time reverse transcription polymerase chain reaction. Journal of Veterinary Diagnostic Investigation 26: 266271.Google Scholar
Delnatte, P, Nagy, E, Ojkic, D, Leishman, D, Crawshaw, G, Elias, K and Smith, DA (2014b). Avian bornavirus in free-ranging waterfowl: prevalence of antibodies and cloacal shedding of viral RNA. Journal of Wildlife Diseases 50: 512523.Google Scholar
Durrwald, R, Kolodziejek, J, Herzog, S and Nowotny, N (2007). Meta-analysis of putative human bornavirus sequences fails to provide evidence implicating Borna disease virus in mental illness. Reviews in Medical Virology 17: 181203.Google Scholar
Eisenman, LM, Brothers, R, Tran, MH, Kean, RB, Dickson, GM, Dietzschold, B and Hooper, DC (1999). Neonatal Borna disease virus infection in the rat causes a loss of Purkinje cells in the cerebellum. Journal of Neurovirology 5: 181189.Google Scholar
Endo, Y and Kobayashi, S (1987). A scanning electron microscope study on the autonomic groundplexus in the lamina propria mucosae of the guinea-pig small intestine. Archivum Histologicum Japonicum 50: 243250.Google Scholar
Fletcher, EL, Clark, MJ and Furness, JB (2002). Neuronal and glial localization of GABA transporter immunoreactivity in the myenteric plexus. Cell and Tissue Research 308: 339346.Google Scholar
Furness, JB (2008). The enteric nervous system: normal functions and enteric neuropathies. Neurogastroenterology and Motility 20 (suppl. 1): 3238.CrossRefGoogle ScholarPubMed
Gabella, G (1981). Ultrastructure of the nerve plexuses of the mammalian intestine: the enteric glial cells. Neuroscience 6: 425436.Google Scholar
Gabriel, R, Halasy, K, Fekete, E, Eckert, M and Benedeczky, I (1990). Distribution of GABA-like immunoreactivity in myenteric plexus of carp, frog and chicken. Histochemistry 94: 323328.Google Scholar
Gies, U, Bilzer, T, Stitz, L and Staiger, JF (1998). Disturbance of the cortical cholinergic innervation in Borna disease prior to encephalitis. Brain Pathology 8: 3948.Google Scholar
Gies, U, Gorcs, TJ, Mulder, J, Planz, O, Stitz, L, Bilzer, T, Luiten, PG and Harkany, T (2001). Cortical cholinergic decline parallels the progression of Borna virus encephalitis. Neuroreport 12: 37673772.Google Scholar
Goldstein, AM and Nagy, N (2008). A bird's eye view of enteric nervous system development: lessons from the avian embryo. Pediatric Research 64: 326333.CrossRefGoogle ScholarPubMed
Gonzalez-Dunia, D, Cubitt, B and de la Torre, JC (1998). Mechanism of Borna disease virus entry into cells. Journal of Virology 72: 783788.CrossRefGoogle ScholarPubMed
Gray, P, Hoppes, S, Suchodolski, P, Mirhosseini, N, Payne, S, Villanueva, I, Shivaprasad, HL, Honkavuori, KS, Lipkin, WI, Briese, T, Reddy, SM and Tizard, I (2010). Use of avian bornavirus isolates to induce proventricular dilatation disease in conures. Emerging Infectious Diseases 16: 473479.Google Scholar
Guo, J, Baroch, J, Randall, A and Tizard, I (2013). Complete genome sequence of an Avian Bornavirus isolated from a healthy Canadian Goose (Branta canadensis). Genome Announcements 1. pii: e0083913. doi:10.1128/genomeA.00839-13.Google Scholar
Guo, J, Shivaprasad, HL, Rech, RR, Heatley, JJ, Tizard, I and Payne, S (2014). Characterization of a new genotype of avian bornavirus from wild ducks. Virology Journal 11: 197.Google Scholar
Guo, J, Tizard, I, Baroch, J, Shivaprasad, HL and Payne, SL (2015). Avian bornaviruses in North American gulls. Journal of Wildlife Diseases 51: 754758.CrossRefGoogle ScholarPubMed
Hall, AJ and Duke, GE (2000). Effect of selective gastric intrinsic denervation on gastric motility in turkeys. Poultry Science 79: 240244.CrossRefGoogle ScholarPubMed
Hatalski, CG, Hickey, WF and Lipkin, WI (1998). Evolution of the immune response in the central nervous system following infection with Borna disease virus. Journal of Neuroimmunology 90: 137142.CrossRefGoogle ScholarPubMed
Heffels-Redmann, U, Enderlein, D, Herzog, S, Piepenbring, A, Burkle, M, Neumann, D, Herden, C and Lierz, M (2012). Follow-up investigations on different courses of natural avian bornavirus infections in psittacines. Avian Diseases 56: 153159.Google Scholar
Herden, C, Herzog, S, Richt, JA, Nesseler, A, Christ, M, Failing, K and Frese, K (2000). Distribution of Borna disease virus in the brain of rats infected with an obesity-inducing virus strain. Brain Pathology 10: 3948.CrossRefGoogle ScholarPubMed
Hernandez, LV, Gonzalo, S, Castro, M, Arruebo, MP, Plaza, MA, Murillo, MD and Grasa, L (2011). Nuclear factor kappaB is a key transcription factor in the duodenal contractility alterations induced by lipopolysaccharide. Experimental Physiology 96: 11511162.Google Scholar
Hoffmann, B, Tappe, D, Hoper, D, Herden, C, Boldt, A, Mawrin, C, Niederstrasser, O, Muller, T, Jenckel, M, Van der Grinten, E, Lutter, C, Abendroth, B, Teifke, JP, Cadar, D, Schmidt-Chanasit, J, Ulrich, RG and Beer, M (2015). A variegated squirrel bornavirus associated with fatal human encephalitis. New England Journal of Medicine 373: 154162.Google Scholar
Honda, T and Tomonaga, K (2013). Nucleocytoplasmic shuttling of viral proteins in borna disease virus infection. Viruses 5: 19781990.CrossRefGoogle ScholarPubMed
Honkavuori, KS, Shivaprasad, HL, Williams, BL, Quan, PL, Hornig, M, Street, C, Palacios, G, Hutchison, SK, Franca, M, Egholm, M, Briese, T and Lipkin, WI (2008). Novel borna virus in psittacine birds with proventricular dilatation disease. Emerging Infectious Diseases 14: 18831886.Google Scholar
Hoppes, S, Gray, PL, Payne, S, Shivaprasad, HL and Tizard, I (2010). The isolation, pathogenesis, diagnosis, transmission, and control of avian bornavirus and proventricular dilatation disease. Veterinary Clinics of North America: Exotic Animal Practice 13: 495508.Google Scholar
Hoppes, SM, Tizard, I and Shivaprasad, HL (2013). Avian bornavirus and proventricular dilatation disease: diagnostics, pathology, prevalence, and control. Veterinary Clinics of North America: Exotic Animal Practice 16: 339355.Google Scholar
Horie, M, Honda, T, Suzuki, Y, Kobayashi, Y, Daito, T, Oshida, T, Ikuta, K, Jern, P, Gojobori, T, Coffin, JM and Tomonaga, K (2010). Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463: 8487.Google Scholar
Horie, M, Kobayashi, Y, Suzuki, Y and Tomonaga, K (2013). Comprehensive analysis of endogenous bornavirus-like elements in eukaryote genomes. Philosophical transactions of the Royal Society of London. Series B, Biological Sciences 368: 20120499.CrossRefGoogle ScholarPubMed
Hornig, M, Weissenbock, H, Horscroft, N and Lipkin, WI (1999). An infection-based model of neurodevelopmental damage. Proceedings of the National Academy of Sciences of the United States of America 96: 1210212107.CrossRefGoogle ScholarPubMed
Hornig, M, Solbrig, M, Horscroft, N, Weissenbock, H and Lipkin, WI (2001). Borna disease virus infection of adult and neonatal rats: models for neuropsychiatric disease. Current Topics in Microbiology and Immunology 253: 157177.Google ScholarPubMed
Horvath, VJ, Izbeki, F, Lengyel, C, Kempler, P and Varkonyi, T (2014). Diabetic gastroparesis: functional/morphologic background, diagnosis, and treatment options. Current Diabetes Reports 14: 527.CrossRefGoogle ScholarPubMed
Huang, PL, Dawson, TM, Bredt, DS, Snyder, SH and Fishman, MC (1993). Targeted disruption of the neuronal nitric oxide synthase gene. Cell 75: 12731286.Google Scholar
Huizinga, JD and Chen, JH (2014). Interstitial cells of Cajal: update on basic and clinical science. Current Gastroenterology Reports 16: 363.CrossRefGoogle ScholarPubMed
Imaizumi, M and Hama, K (1969). An electron microscopic study on the interstitial cells of the gizzard in the love-bird (Uroloncha domestica). Zeitschrift fur Zellforschung und mikroskopische Anatomie 97: 351357.CrossRefGoogle ScholarPubMed
Jarius, S and Wildemann, B (2015). ‘Medusa head ataxia’: the expanding spectrum of Purkinje cell antibodies in autoimmune cerebellar ataxia. Part 3: anti-Yo/CDR2, anti-Nb/AP3B2, PCA-2, anti-Tr/DNER, other antibodies, diagnostic pitfalls, summary and outlook. Journal of Neuroinflammation 12: 168.CrossRefGoogle ScholarPubMed
Jessen, KR and Mirsky, R (1983). Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. Journal of Neuroscience 3: 22062218.Google Scholar
Jessen, KR, Hills, JM, Dennison, ME and Mirsky, R (1983). Gamma-aminobutyrate as an autonomic neurotransmitter: release and uptake of [3H]gamma-aminobutyrate in guinea pig large intestine and cultured enteric neurons using physiological methods and electron microscopic autoradiography. Neuroscience 10: 14271442.Google Scholar
Kao, M, Ludwig, H and Gosztonyi, G (1984). Adaptation of Borna disease virus to the mouse. Journal of General Virology 65 (Pt 10): 18451849.Google Scholar
Kistler, AL, Gancz, A, Clubb, S, Skewes-Cox, P, Fischer, K, Sorber, K, Chiu, CY, Lublin, A, Mechani, S, Farnoushi, Y, Greninger, A, Wen, CC, Karlene, SB, Ganem, D and Derisi, JL (2008). Recovery of divergent avian bornaviruses from cases of proventricular dilatation disease: identification of a candidate etiologic agent. Virology Journal 5: 88.CrossRefGoogle ScholarPubMed
Kistler, AL, Smith, JM, Greninger, AL, Derisi, JL and Ganem, D (2010). Analysis of naturally occurring avian bornavirus infection and transmission during an outbreak of proventricular dilatation disease among captive psittacine birds. Journal of Virology 84: 21762179.Google Scholar
Krey, H, Ludwig, H and Rott, R (1979). Spread of infectious virus along the optic nerve into the retina in Borna disease virus-infected rabbits. Archives of Virology 61: 283288.Google Scholar
Krey, H, Ludwig, H and Gierend, M (1981). Borna disease virus-induced retinouveitis treated with immunosuppressive drugs. Albrecht von Graefes Archiv für klinische und experimentelle Ophthalmologie 216: 111119.Google Scholar
Kubota, K, Ito, S, Ohta, T, Nakazato, Y and Ohga, A (1994). The inhibitory action of lead on mechanical responses of the proventricular smooth muscle in the chick. Japanese Journal of Veterinary Research 42: 109117.Google Scholar
Kuder, T, Nowak, E, Szczurkowski, A and Kuchinka, J (2003). The comparative analysis of the myenteric plexus in pigeon and hen. Anatomia Histolgia Embryologia 32: 15.CrossRefGoogle ScholarPubMed
Kuhn, J, Dürrwald, R, Bào, Y, Briese, T, Carbone, K, Clawson, A, Derisi, J, Garten, W, Jahrling, P, Kolodziejek, J, Rubbenstroth, D, Schwemmle, M, Stenglein, M, Tomonaga, K, Weissenböck, H and Nowotny, N (2015). Taxonomic reorganization of the family Bornaviridae. Archives of Virology 160: 621632.CrossRefGoogle ScholarPubMed
Langlois, I (2003). The anatomy, physiology, and diseases of the avian proventriculus and ventriculus. Veterinary Clinics of North America: Exotic Animal Practice 6: 85111.Google Scholar
Li, CY, Xue, P, Tian, WQ, Liu, RC and Yang, C (1996). Experimental Campylobacter jejuni infection in the chicken: an animal model of axonal Guillain–Barre syndrome. Journal of Neurology Neurosurgery and Psychiatry 61: 279284.CrossRefGoogle ScholarPubMed
Li, ZS, Young, HM and Furness, JB (1994). Nitric oxide synthase in neurons of the gastrointestinal tract of an avian species, Coturnix coturnix . Journal of Anatomy 184 (Pt 2): 261272.Google ScholarPubMed
Lierz, M, Hafez, HM, Honkavuori, KS, Gruber, AD, Olias, P, Abdelwhab, EM, Kohls, A, Lipkin, WI, Briese, T and Hauck, R (2009). Anatomical distribution of avian bornavirus in parrots, its occurrence in clinically healthy birds and ABV-antibody detection. Avian Pathology 38: 491496.CrossRefGoogle ScholarPubMed
Lies, B, Groneberg, D and Friebe, A (2014). Toward a better understanding of gastrointestinal nitrergic neuromuscular transmission. Neurogastroenterology and Motility 26: 901912.Google Scholar
Lin, CC, Wu, YJ, Heimrich, B and Schwemmle, M (2013). Absence of a robust innate immune response in rat neurons facilitates persistent infection of Borna disease virus in neuronal tissue. Cellular and Molecular Life Sciences 70: 43994410.Google Scholar
Lipkin, WI, Briese, T and Hornig, M (2011). Borna disease virus – fact and fantasy. Virus Research 162: 162172.CrossRefGoogle ScholarPubMed
Ludwig, H (2008). The biology of bornavirus. APMIS Supplment 124: 1420.Google Scholar
Ludwig, H and Bode, L (2000). Borna disease virus: new aspects on infection, disease, diagnosis and epidemiology. Revue Scientifique et Technique 19: 259288.Google Scholar
Lui, VC, Samy, ET, Sham, MH, Mulligan, LM and Tam, PK (2002). Glial cell line-derived neurotrophic factor family receptors are abnormally expressed in aganglionic bowel of a subpopulation of patients with Hirschsprung's disease. Laboratory Investigation 82: 703712.Google Scholar
Lundgren, AL, Johannisson, A, Zimmermann, W, Bode, L, Rozell, B, Muluneh, A, Lindberg, R and Ludwig, H (1997). Neurological disease and encephalitis in cats experimentally infected with Borna disease virus. Acta Neuropathology 93: 391401.Google Scholar
Makino, A, Fujino, K, Parrish, NF, Honda, T and Tomonaga, K (2015). Borna disease virus possesses an NF-kB inhibitory sequence in the nucleoprotein gene. Scientific Reports 5: 8696.Google Scholar
Malkinson, M, Weisman, Y, Ashash, E, Bode, L and Ludwig, H (1993). Borna disease in ostriches. Veterinary Record 133: 304.Google Scholar
Mannl, A, Gerlach, H and Leipold, R (1987). Neuropathic gastric dilatation in psittaciformes. Avian Diseases 31: 214221.Google Scholar
Martinez, A, Lopez, J and Sesma, P (2000). The nervous system of the chicken proventriculus: an immunocytochemical and ultrastructural study. Histochemical Journal 32: 6370.Google Scholar
Mayer, D, Fischer, H, Schneider, U, Heimrich, B and Schwemmle, M (2005). Borna disease virus replication in organotypic hippocampal slice cultures from rats results in selective damage of dentate granule cells. Journal of Virology 79: 1171611723.Google Scholar
Mcconalogue, K and Furness, JB (1994). Gastrointestinal neurotransmitters. Baillieres Clinical Endocrinology and Metabolism 8: 5176.Google Scholar
McVey Neufeld, KA, Perez-Burgos, A, Mao, YK, Bienenstock, J and Kunze, WA (2015). The gut microbiome restores intrinsic and extrinsic nerve function in germ-free mice accompanied by changes in calbindin. Neurogastroenterology and Motility 27: 627636.Google Scholar
Mearin, F, Mourelle, M, Guarner, F, Salas, A, Riveros-Moreno, V, Moncada, S and Malagelada, JR (1993). Patients with achalasia lack nitric oxide synthase in the gastro-oesophageal junction. European Journal of Clinical Investigation 23: 724728.Google Scholar
Metzler, A, Frei, U and Danner, K (1976). Virologically confirmed outbreak of Borna's disease in a Swiss herd of sheep. Schweizer Archiv Fur Tierheilkunde 118: 483492.Google Scholar
Mirabella, N, Squillacioti, C, Genovese, A, Germano, G and Paino, G (2003). Topography and neurochemistry of the enteric ganglia in the proventriculus of the duck (Anas platyrhynchos). Anatomy and Embryology (Berline) 207: 101108.Google Scholar
Mirhosseini, N, Gray, PL, Hoppes, S, Tizard, I, Shivaprasad, HL and Payne, S (2011). Proventricular dilatation disease in cockatiels (Nymphicus hollandicus) after infection with a genotype 2 avian bornavirus. Journal of Avian Medicine and Surgery 25: 199204.Google Scholar
Moses, PL, Ellis, LM, Anees, MR, Ho, W, Rothstein, RI, Meddings, JB, Sharkey, KA and Mawe, GM (2003). Antineuronal antibodies in idiopathic achalasia and gastro-oesophageal reflux disease. Gut 52: 629636.CrossRefGoogle ScholarPubMed
Narayan, O, Herzog, S, Frese, K, Scheefers, H and Rott, R (1983a). Behavioral disease in rats caused by immunopathological responses to persistent borna virus in the brain. Science 220: 14011403.Google Scholar
Narayan, O, Herzog, S, Frese, K, Scheefers, H and Rott, R (1983b). Pathogenesis of Borna disease in rats: immune-mediated viral ophthalmoencephalopathy causing blindness and behavioral abnormalities. Journal of Infectious Diseases 148: 305315.Google Scholar
Nascimento, RD, Martins, PR, De Souza Lisboa, A, Adad, SJ, Morais da Silveira, AB and Reis, D (2013). An imbalance between substance P and vasoactive intestinal polypeptide might contribute to the immunopathology of megaesophagus after Trypanosoma cruzi infection. Human Pathology 44: 269276.Google Scholar
Nilsson, S (2011). Comparative anatomy of the autonomic nervous system. Autonomic Neuroscience 165: 39.Google Scholar
Nouri, M, Bredberg, A, Westrom, B and Lavasani, S (2014). Intestinal barrier dysfunction develops at the onset of experimental autoimmune encephalomyelitis, and can be induced by adoptive transfer of auto-reactive T cells. PLoS ONE 9: e106335.Google Scholar
O'grady, G, Wang, TH, Du, P, Angeli, T, Lammers, WJ and Cheng, LK (2014). Recent progress in gastric arrhythmia: pathophysiology, clinical significance and future horizons. Clinical and Experimental Pharmacology and Physiology 41: 854862.Google Scholar
Olsson, C and Holmgren, S (2011). Autonomic control of gut motility: a comparative view. Autonomic Neuroscience 165: 80101.CrossRefGoogle ScholarPubMed
Ouyang, N, Storts, R, Tian, Y, Wigle, W, Villanueva, I, Mirhosseini, N, Payne, S, Gray, P and Tizard, I (2009). Histopathology and the detection of avian bornavirus in the nervous system of birds diagnosed with proventricular dilatation disease. Avian Pathology 38: 393401.Google Scholar
Ovanesov, MV, Vogel, MW, Moran, TH and Pletnikov, MV (2007). Neonatal Borna disease virus infection in rats is associated with increased extracellular levels of glutamate and neurodegeneration in the striatum. Journal of Neurovirology 13: 185194.Google Scholar
Park, W and Vaezi, MF (2005). Etiology and pathogenesis of achalasia: the current understanding. American Journal of Gastroenterology 100: 14041414.Google Scholar
Paterson, WG (2001). Etiology and pathogenesis of achalasia. Gastrointestinal Endoscopy Clinics of North America 11: 249266, vi.Google Scholar
Payne, S, Shivaprasad, HL, Mirhosseini, N, Gray, P, Hoppes, S, Weissenbock, H and Tizard, I (2011). Unusual and severe lesions of proventricular dilatation disease in cockatiels (Nymphicus hollandicus) acting as healthy carriers of avian bornavirus (ABV) and subsequently infected with a virulent strain of ABV. Avian Pathology 40: 1522.Google Scholar
Payne, SL, Delnatte, P, Guo, J, Heatley, JJ, Tizard, I and Smith, DA (2012). Birds and bornaviruses. Animal Health Research Reviews 13: 145156.CrossRefGoogle ScholarPubMed
Perez-Burgos, A, Wang, B, Mao, YK, Mistry, B, McVey, Ne ufeld, KA, Bienenstock, J and Kunze, W (2013). Psychoactive bacteria Lactobacillus rhamnosus (JB-1) elicits rapid frequency facilitation in vagal afferents. American Journal of Physiology – Gastrointestinal and Liver Physiology 304: G211G220.Google Scholar
Pfannkuche, H, Konrath, A, Buchholz, I, Richt, JA, Seeger, J, Muller, H and Gabel, G (2008). Infection of the enteric nervous system by Borna disease virus (BDV) upregulates expression of Calbindin D-28k. Veterinary Microbiology 127: 275285.CrossRefGoogle ScholarPubMed
Piepenbring, AK, Enderlein, D, Herzog, S, Kaleta, EF, Heffels-Redmann, U, Ressmeyer, S, Herden, C and Lierz, M (2012). Pathogenesis of avian bornavirus in experimentally infected cockatiels. Emerging Infectious Diseases 18: 234241.CrossRefGoogle ScholarPubMed
Piepenbring, AK, Enderlein, D, Herzog, S, Al-Ibadi, B, Heffels-Redmann, U, Heckmann, J, Lange-Herbst, H, Herden, C and Lierz, M (2016). Parrot Bornavirus (PaBV)-2 isolate causes different disease patterns in cockatiels than PaBV-4. Avian Pathology 45: 156168.Google Scholar
Planz, O, Dumrese, T, Hulpusch, S, Schirle, M, Stevanovic, S and Stitz, L (2001). A naturally processed rat major histocompatibility complex class I-associated viral peptide as target structure of borna disease virus-specific CD8+ T cells. Journal of Biological Chemistry 276: 1368913694.Google Scholar
Raghav, R, Taylor, M, Delay, J, Ojkic, D, Pearl, DL, Kistler, AL, Derisi, JL, Ganem, D and Smith, DA (2010). Avian bornavirus is present in many tissues of psittacine birds with histopathologic evidence of proventricular dilatation disease. Journal of Veterinary Diagnostic Investigation 22: 495508.Google Scholar
Raymond, L, Lach, B and Shamji, FM (1999). Inflammatory aetiology of primary oesophageal achalasia: an immunohistochemical and ultrastructural study of Auerbach's plexus. Histopathology 35: 445453.Google Scholar
Reynhout, JK and Duke, GE (1999). Identification of interstitial cells of Cajal in the digestive tract of turkeys (Meleagris gallopavo). Journal of Experimental Zoology 283: 426440.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Richt, JA, Grabner, A and Herzog, S (2000). Borna disease in horses. Veterinary Clinics of North America: Equine Practice 16: 579595, xi.Google Scholar
Rinder, M, Ackermann, A, Kempf, H, Kaspers, B, Korbel, R and Staeheli, P (2009). Broad tissue and cell tropism of avian bornavirus in parrots with proventricular dilatation disease. Journal of Virology 83: 54015407.Google Scholar
Rosas-Ballina, M and Tracey, KJ (2009). The neurology of the immune system: neural reflexes regulate immunity. Neuron 64: 2832.CrossRefGoogle ScholarPubMed
Rosas-Ballina, M, Olofsson, PS, Ochani, M, Valdes-Ferrer, SI, Levine, YA, Reardon, C, Tusche, MW, Pavlov, VA, Andersson, U, Chavan, S, Mak, TW and Tracey, KJ (2011). Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 334: 98101.Google Scholar
Rossi, G, Crosta, L and Pesaro, S (2008). Parrot proventricular dilation disease. Veterinary Record 163: 310.Google Scholar
Rotondo, A, Serio, R and Mule, F (2010). Functional evidence for different roles of GABAA and GABAB receptors in modulating mouse gastric tone. Neuropharmacology 58: 10331037.Google Scholar
Rubbenstroth, D, Rinder, M, Stein, M, Hoper, D, Kaspers, B, Brosinski, K, Horie, M, Schmidt, V, Legler, M, Korbel, R and Staeheli, P (2013). Avian bornaviruses are widely distributed in canary birds (Serinus canaria f. domestica). Veterinary Microbiology 165: 287295.Google Scholar
Rubbenstroth, D, Brosinski, K, Rinder, M, Olbert, M, Kaspers, B, Korbel, R and Staeheli, P (2014a). No contact transmission of avian bornavirus in experimentally infected cockatiels (Nymphicus hollandicus) and domestic canaries (Serinus canaria forma domestica). Veterinary Microbiology 172: 146156.Google Scholar
Rubbenstroth, D, Schmidt, V, Rinder, M, Legler, M, Corman, VM and Staeheli, P (2014b). Discovery of a new avian bornavirus genotype in estrildid finches (Estrildidae) in Germany. Veterinary Microbiology 168: 318323.CrossRefGoogle ScholarPubMed
Ruhl, A (2005). Glial cells in the gut. Neurogastroenterology and Motility 17: 777790.Google Scholar
Saffrey, MJ, Marcus, N, Jessen, KR and Burnstock, G (1983). Distribution of neurons with high-affinity uptake sites for GABA in the myenteric plexus of the guniea-pig, rat and chicken. Cell and Tissue Research 234: 231235.Google Scholar
Sampson, TR and Mazmanian, SK (2015). Control of brain development, function, and behavior by the microbiome. Cell Host & Microbe 17: 565576.Google Scholar
Sanders, KM, Koh, SD and Ward, SM (2006). Interstitial cells of Cajal as pacemakers in the gastrointestinal tract. Annual Review of Physiology 68: 307343.Google Scholar
Sauder, C and de la Torre, JC (1999). Cytokine expression in the rat central nervous system following perinatal Borna disease virus infection. Journal of Neuroimmunology 96: 2945.Google Scholar
Savory, CJ and Hodgkiss, JP (1984). Influence of vagotomy in domestic fowls on feeding activity, food passage, digestibility and satiety effects of two peptides. Physiology & Behavior 33: 937944.Google Scholar
Scordel, C, Huttin, A, Cochet-Bernoin, M, Szelechowski, M, Poulet, A, Richardson, J, Benchoua, A, Gonzalez-Dunia, D, Eloit, M and Coulpier, M (2015). Borna disease virus phosphoprotein impairs the developmental program controlling neurogenesis and reduces human GABAergic neurogenesis. PLoS Pathogens 11: e1004859.Google Scholar
Shillabeer, G and Davison, JS (1987). Proglumide, a cholecystokinin antagonist, increases gastric emptying in rats. American Journal of Physiology 252: R353R360.Google ScholarPubMed
Smalley, SG, Barrow, PA and Foster, N (2009). Immunomodulation of innate immune responses by vasoactive intestinal peptide (VIP): its therapeutic potential in inflammatory disease. Clinical & Experimental Immunology 157: 225234.Google Scholar
Spicer, RD (1982). Infantile hypertrophic pyloric stenosis: a review. British Journal of Surgery 69: 128135.Google Scholar
Stahl, T, Mohr, C, Kacza, J, Reimers, C, Pannicke, T, Sauder, C, Reichenbach, A and Seeger, J (2003). Characterization of the acute immune response in the retina of Borna disease virus infected Lewis rats. Journal of Neuroimmunology 137: 6778.Google Scholar
Steinmetz, A, Pees, M, Schmidt, V, Weber, M, Krautwald-Junghanns, ME and Oechtering, G (2008). Blindness as a sign of proventricular dilatation disease in a grey parrot (Psittacus erithacus erithacus). Journal of Small Animal Practice 49: 660662.Google Scholar
Stenglein, MD, Leavitt, EB, Abramovitch, MA, Mcguire, JA and Derisi, JL (2014). Genome sequence of a bornavirus recovered from an African Garter snake (Elapsoidea loveridgei). Genome Announcements 2. pii: e0077914. doi:10.1128/genomeA.00779-14.Google Scholar
Stitz, L, Sobbe, M and Bilzer, T (1992). Preventive effects of early anti-CD4 or anti-CD8 treatment on Borna disease in rats. Journal of Virology 66: 33163323.Google Scholar
Stitz, L, Bilzer, T and Planz, O (2002). The immunopathogenesis of Borna disease virus infection. Frontiers in Bioscience 7: d541d555.Google Scholar
Storch, WB, Eckardt, VF, Wienbeck, M, Eberl, T, Auer, PG, Hecker, A, Junginger, T and Bosseckert, H (1995). Autoantibodies to Auerbach's plexus in achalasia. Cellular and Molecular Biology (Noisy-le-grand) 41: 10331038.Google Scholar
Thomas, PA, Akwari, OE and Kelly, KA (1979). Hormonal control of gastrointestinal motility. World Journal of Surgery 3: 545552.Google Scholar
Thomsen, AF, Nielsen, JB, Hjulsager, CK, Chriel, M, Smith, DA and Bertelsen, MF (2015). Aquatic bird bornavirus 1 in wild geese, Denmark. Emerging Infectious Diseases 21: 22012203.Google Scholar
Thomsen, L, Robinson, TL, Lee, JC, Farraway, LA, Hughes, MJ, Andrews, DW and Huizinga, JD (1998). Interstitial cells of Cajal generate a rhythmic pacemaker current. Nature Medicine 4: 848851.Google Scholar
Thomson, RM and Parry, GJ (2006). Neuropathies associated with excessive exposure to lead. Muscle & Nerve 33: 732741.Google Scholar
Tizard, I, Ball, J, Stoica, G and Payne, S (2016). The pathogenesis of bornaviral diseases in mammals. Animal Health Research Reviews 17: 118.Google Scholar
Tome, D, Schwarz, J, Darcel, N and Fromentin, G (2009). Protein, amino acids, vagus nerve signaling, and the brain. American Journal of Clinical Nutrition 90: 838s843s.Google Scholar
Tomonaga, K, Kobayashi, T and Ikuta, K (2002). Molecular and cellular biology of Borna disease virus infection. Microbes and Infectection 4: 491500.CrossRefGoogle ScholarPubMed
Tracey, KJ (2016). Reflexes in immunity. Cell 164: 343344.Google Scholar
Vanderwinden, JM, Mailleux, P, Schiffmann, SN, Vanderhaeghen, JJ and De Laet, MH (1992). Nitric oxide synthase activity in infantile hypertrophic pyloric stenosis. New England Journal of Medicine 327: 511515.Google Scholar
Vice, CA (1992). Myocarditis as a component of psittacine proventricular dilatation syndrome in a Patagonian conure. Avian Diseases 36: 11171119.Google Scholar
Weissenbock, H, Sekulin, K, Bakonyi, T, Hogler, S and Nowotny, N (2009). Novel avian bornavirus in a nonpsittacine species (Canary; Serinus canaria) with enteric ganglioneuritis and encephalitis. Journal of Virology 83: 1136711371.Google Scholar
Wood, JD (2008). Enteric nervous system: reflexes, pattern generators and motility. Current Opinion in Gastroenterology 24: 149158.Google Scholar
Wunschmann, A, Honkavuori, K, Briese, T, Lipkin, WI, Shivers, J and Armien, AG (2011). Antigen tissue distribution of Avian bornavirus (ABV) in psittacine birds with natural spontaneous proventricular dilatation disease and ABV genotype 1 infection. Journal of Veterinary Diagnostic Investigation 23: 716726.Google Scholar
Zhang, L, Lei, Y, Liu, X, Wang, X, Liu, Z, Li, D, Zheng, P, Zhang, L, Chen, S and Xie, P (2014). Glutamate and lipid metabolic perturbation in the hippocampi of asymptomatic Borna disease virus-infected horses. PLoS ONE 9: e99752.CrossRefGoogle ScholarPubMed