Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 18, Number 2—February 2012

Pathogenesis of Avian Bornavirus in Experimentally Infected Cockatiels

Anne K. PiepenbringComments to Author , Dirk Enderlein, Sibylle Herzog, Erhard F. Kaleta, Ursula Heffels-Redmann, Saskia Ressmeyer, Christiane Herden, and Michael Lierz
Author affiliations: Justus Liebig University Giessen, Giessen, Germany

Main Article

Table 1

Premortem findings in cockatiels experimentally infected with ABV*

Bird Age at inoculation,d/sex Antibodies against ABV
RNA‡, first detected, dpi Gastrointestinal signs
Neurologic signs
Died, dpi Euthanized, dpi
First detected, dpi Titer† First detected, dpi Titer† First detected, dpi Titer†
ic1 137/F 43 160 27 199 5,120 206
ic2 121/F 29 20 21 37 320 41 320 60
ic3 137/F 35 320 25 115
ic4 137/F 7 20 19 115
ic5 121/F 57 320 29 230
ic6 137/M 43 1,280 25 66
ic7 137/M 63 160 29 230
ic8 137/F 43 640 27 115
ic9 44/M 7 10 25 230
iv1 137/F 57 320 71 126 5,120 229
iv2 137/F 35 160 35 120
iv3 137/M 57 640 43 116 10,240 116
iv4 137/M 29 40 63 116
iv5 121/F 35 640 72 159 5,120 229
iv6 121/F 43 640 33 229
iv7 137/M 35 40 35 116
iv8 137/M 35 40 43 229
iv9 44/F 29 40 25 229
se1 137/M NA 76 230

*Investigation period was 230 d. ABV, avian bornavirus; dpi, days postinoculation; ic, intracerebrally inoculated; –, not detected or not applicable; iv, intravenously inoculated; se, sentinel.
†Antibodies detected by use of indirect immunofluorescence assay; titers <10.0 are considered negative.
‡Avian bornavirus RNA detected by real-time reverse transcription PCR as described by Honkavuori et al. (10); cycle thresholds >36.0 are negative.

Main Article

  1. Daoust  PY, Julian  RJ, Yason  CV, Artsob  H. Proventricular impaction associated with nonsuppurative encephalomyelitis and ganglioneuritis in two Canada geese. J Wildl Dis. 1991;27:5137.PubMedGoogle Scholar
  2. Perpiñán  D, Fernández-Bellon  H, López  C, Ramis  A. Lymphoplasmacytic myenteric, subepicardial, and pulmonary ganglioneuritis in four nonpsittacine birds. J Avian Med Surg. 2007;21:2104. DOIPubMedGoogle Scholar
  3. Weissenböck  H, Sekulin  K, Bakonyi  T, Hogler  S, Nowotny  N. Novel avian Bornavirus in a nonpsittacine species (Canary; Serinus canaria) with enteric ganglioneuritis and encephalitis. J Virol. 2009;83:1136771. DOIPubMedGoogle Scholar
  4. Gregory  CR. Proventricular dilatation disease. In: Ritchie BW, editor. Avian viruses, function and control. Lake Worth (FL): Wingers Publishing Inc; 1995. p. 439–48.
  5. Dahlhausen  B, Aldred  S. Resolution of clinical proventricular dilatation disease by cycloogenase 2 inhibition. In: Proceedings of the 23rd Annual Conference and Expo of the Association of Avian Veterinarians, Monterey, CA, USA, Aug 26–30, 2002. Denver (CO): The Association; 2002. p. 9–12.
  6. Lierz  M. Proventricular dilatation disease. In: Harcourt-Brown N, Chitty J, editors. BSAVA manual of psittacine birds. 2nd ed. Gloucester (UK): British Small Animal Veterinary Association; 2005. p. 161–2.
  7. Berhane  Y, Smith  DA, Newman  S, Taylor  M, Nagy  E, Binnington  B, Peripheral neuritis in psittacine birds with proventricular dilatation disease. Avian Pathol. 2001;30:56370. DOIPubMedGoogle Scholar
  8. Lublin  A, Mechani  S, Farnoushi  I, Perl  S, Bendheim  U. An outbreak of proventricular dilatation disease in psittacine breeding farm in Israel. Israel Journal of Veterinary Medicine. 2006;61:169.
  9. Gregory  CR, Latimer  KS, Campagnoli  RP, Ritchie  BW. Histologic evaluation of the crop for diagnosis of proventricular dilatation syndrome in psittacine birds. J Vet Diagn Invest. 1996;8:7680. DOIPubMedGoogle Scholar
  10. Honkavuori  KS, Shivaprasad  HL, Williams  BL, Quan  PL, Hornig  M, Street  C, Novel borna virus in psittacine birds with proventricular dilatation disease. Emerg Infect Dis. 2008;14:18836. DOIPubMedGoogle Scholar
  11. Kistler  AL, Gancz  A, Clubb  S, Skewes-Cox  P, Fischer  K, Sorber  K, Recovery of divergent avian bornaviruses from cases of proventricular dilatation disease: identification of a candidate etiologic agent. Virol J. 2008;5:88. DOIPubMedGoogle Scholar
  12. Delnatte  P, Berkvens  C, Kummrow  M, Smith  DA, Campbell  D, Crawshaw  G, New genotype of avian bornavirus in wild geese and trumpeter swans in Canada. Vet Rec. 2011;169:108. DOIPubMedGoogle Scholar
  13. Ouyang  N, Storts  R, Tian  Y, Wigle  W, Villanueva  I, Mirhosseini  N, Histopathology and the detection of avian bornavirus in the nervous system of birds diagnosed with proventricular dilatation disease. Avian Pathol. 2009;38:393401. DOIPubMedGoogle Scholar
  14. 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;83:54017. DOIPubMedGoogle Scholar
  15. Weissenböck  H, Bakonyi  T, Sekulin  K, Ehrensperger  F, Doneley  RJ, Durrwald  R, Avian bornaviruses in psittacine birds from Europe and Australia with proventricular dilatation disease. Emerg Infect Dis. 2009;15:14539. DOIPubMedGoogle Scholar
  16. De Kloet  SR, Dorrestein  GM. Presence of avian bornavirus RNA and anti-avian bornavirus antibodies in apparently healthy macaws. Avian Dis. 2009;53:56873. DOIPubMedGoogle Scholar
  17. Heffels-Redmann  U, Enderlein  D, Herzog  S, Herden  C, Piepenbring  A, Neumann  D, Occurrence of avian bornavirus infection in captive psittacines in various European countries and its association to proventricular dilation disease. Avian Pathol. 2011;40:41926. DOIPubMedGoogle Scholar
  18. Lierz  M, Hafez  HM, Honkavuori  KS, Gruber  AD, Olias  P, Abdelwhab  EM, Anatomical distribution of avian bornavirus in parrots, its occurrence in clinically healthy birds and ABV-antibody detection. Avian Pathol. 2009;38:4916. DOIPubMedGoogle Scholar
  19. 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;84:21769. DOIPubMedGoogle Scholar
  20. Villanueva  I, Gray  P, Mirhosseini  N, Payne  S, Hoppes  S, Honkavuori  KS, The diagnosis of proventricular dilatation disease: use of a Western blot assay to detect antibodies against avian borna virus. Vet Microbiol. 2010;143:196201. DOIPubMedGoogle Scholar
  21. Gancz  AY, Kistler  AL, Greninger  AL, Farnoushi  Y, Mechani  S, Perl  S, Experimental induction of proventricular dilatation disease in cockatiels (Nymphicus hollandicus) inoculated with brain homogenates containing avian bornavirus 4. Virol J. 2009;6:100. DOIPubMedGoogle Scholar
  22. Gray  PL, Villanueva  I, Mirhosseini  N, Hoppes  S, Payne  S, Tizard  I. Experimental infection of birds with avian bornavirus. In: Proceedings of the Association of Avian Veterinarians 30th annual conference and expo, Milwaukee, WI, 2009, Aug 10–13, 2009. Denver (CO): The Association; 2009. p. 7–8.
  23. Gray  P, Hoppes  S, Suchodolski  P, Mirhosseini  N, Payne  S, Villanueva  I, Use of avian bornavirus isolates to induce proventricular dilatation disease in conures. Emerg Infect Dis. 2010;16:4739. DOIPubMedGoogle Scholar
  24. Zöller  B, Redman-Müller  I, Nanda  I, Guttenbach  M, Dosch  E, Schmid  M, Sequence comparison of avian interferon regulatory factors and identification of the avian CEC-32 cell as a quail cell line. J Interferon Cytokine Res. 2000;20:7117. DOIPubMedGoogle Scholar
  25. Herzog  S, Enderlein  D, Heffels-Redmann  U, Piepenbring  A, Neumann  D, Kaleta  EF, Indirect immunofluorescence assay for intra vitam diagnosis of avian bornavirus infection in psittacine birds. J Clin Microbiol. 2010;48:22824. DOIPubMedGoogle Scholar
  26. Herden  C, Herzog  S, Wehner  T, Zink  C, Richt  J, Frese  K. Comparison of different methods of diagnosing Borna disease in horses post mortem. In: Wernery U, Wade J, Mumford JA, Kaaden JR, editors. Equine infectious diseases VIII. Newmarket (UK): R&W Publications; 1999. p. 286–90.
  27. Narayan  O, Herzog  S, Frese  K, Scheefers  H, Rott  R. Pathogenesis of Borna disease in rats: immune-mediated viral ophthalmoencephalopathy causing blindness and behavioral abnormalities. J Infect Dis. 1983;148:30515. DOIPubMedGoogle Scholar
  28. Payne  S, Shivaprasad  HL, Mirhosseini  N, Gray  P, Hoppes  S, Weissenbock  H, 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 Pathol. 2011;40:1522. DOIPubMedGoogle Scholar
  29. Richt  JA, Pfeuffer  I, Christ  M, Frese  K, Bechter  K, Herzog  S. Borna disease virus infection in animals and humans. Emerg Infect Dis. 1997;3:34352. DOIPubMedGoogle Scholar
  30. Rott  R, Becht  H. Natural and experimental Borna disease in animals. Curr Top Microbiol Immunol. 1995;190:1730. DOIPubMedGoogle Scholar
  31. Herzog  S, Frese  K, Rott  R. Studies on the genetic control of resistance of black hooded rats to Borna disease. J Gen Virol. 1991;72:53540. DOIPubMedGoogle Scholar
  32. Herzog  S, Kompter  C, Frese  K, Rott  R. Replication of Borna disease virus in rats: age-dependent differences in tissue distribution. Med Microbiol Immunol (Berl). 1984;173:1717. DOIPubMedGoogle Scholar
  33. Heffels-Redmann  U, Enderlein  D, Herzog  S, Piepenbring  A, Bürkle  M, Neumann  D, Follow-up investigations on different courses of natural avian bornavirus infections in psittacines. Avian Dis. 2011. In press.
  34. Richt  JA, VandeWoude  S, Zink  MC, Clements  JE, Herzog  S, Stitz  L, Infection with Borna disease virus: molecular and immunobiological characterization of the agent. Clin Infect Dis. 1992;14:124050. DOIPubMedGoogle Scholar
  35. Richt  J, Herzog  S, Grabner  A, Garten  W, Herden  C. Borna disease in equines. In: Sellon DC, Long M, editors. Equine infectious diseases. St. Louis (MO): Elsevier; 2007. p. 201–16.
  36. Enderlein  D, Herzog  S, Herden  C, Neumann  D, Briese  T, Kaleta  EF, Avian bornavirus: detection of antibodies and RNA in PDD-affected birds [in German]. In: Krautwald-Junghanns ME, Kaleta EF, editors. First conference on diseases of birds and reptiles of the German Veterinary Medical Society; Giessen, Germany, Sept 25–27, 2009. Leipzig (Germany): The Society; 2009. p. 18–20.
  37. Richt  JA, Schmeel  A, Frese  K, Carbone  KM, Narayan  O, Rott  R. Borna disease virus-specific T cells protect against or cause immunopathological Borna disease. J Exp Med. 1994;179:146773. DOIPubMedGoogle Scholar

Main Article

Page created: January 17, 2012
Page updated: January 17, 2012
Page reviewed: January 17, 2012
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.