Skip to main content
Taylor & Francis - PMC COVID-19 Collection logoLink to Taylor & Francis - PMC COVID-19 Collection
. 2010 Jun 17;31(3):229–236. doi: 10.1080/03079450220136530

Molecular epizootiology of infectious bronchitis virus in Sweden indicating the involvement of a vaccine strain

Epizootiologie moléculaire du virus de la bronchite infectieuse en Suède: implication d'une souche vaccinale

Molekulare Epizootiologie des aviären Bronchitisvirus in Schweden, die auf die Beteiligung eines Vakzinestammes schließen lässt

Epizootiología molecular del virus de bronquitis infecciosa en Suecia que indica la participación de una cepa vacunal

A Farsang 1, C Ros 2, Lena H M Renström 3, Claudia Baule 3, T Soós 1, S Belák 3,*
PMCID: PMC7154300  PMID: 12396345

Abstract

To improve the detection and molecular identification of infectious bronchitis virus (avian coronavirus), two reverse transcriptase-polymerase chain reaction (PCR) assays were developed. As ‘diagnostic PCR’, a set of consensus nested primers was selected from highly conserved stretches of the nucleocapsid (N) gene. As ‘phylogeny’ PCR, a fragment of the spike protein gene (S1) was amplified and the PCR products were directly sequenced. To study the phylogenetic relationships of the viruses from various outbreaks, studies of molecular epizootiology were performed in Sweden, a Nordic region, where the occurrence of natural cases of the disease is relatively low and the occasional use of live vaccine(s) is well recorded and monitored. The disease appeared in the region in 1994, associated with production problems among layers of various ages. During outbreaks in 1995 and 1997, both layers and broilers were affected. To reduce losses, a live attenuated vaccine has been applied since 1997. By examining 12 cases between 1994 and 1998, molecular epizootiology revealed that, before 1997, the viruses had gene sequences very similar to strains of the Massachusetts serotype. However, comparative sequence analysis of the S1 gene revealed that the identity was not 100% to any of the strains of this serotype that we analysed. A virus related to the Dutch-type strain, D274, was also identified on one farm. Surprisingly, from 1997, the year that vaccination commenced with a live Massachusetts serotype vaccine, the majority of viruses detected had S1 sequences identical to the live Massachusetts vaccine strain. This genetic relation to the vaccine virus was also confirmed by N gene sequence analysis. The studies of molecular epizootiology reveal a strong probability that the vaccination had lead to the spread of the vaccine virus, causing various disease manifestations and a confusing epizootiological situation in the poultry population.

References

  1. Ballagi-Pord ány A. & Belák S. (1996). The use of mimic as internal standard to avoid false negative results in diagnostic PCR. Molecular and Cellular Probes, 10, 159–164. [DOI] [PubMed] [Google Scholar]
  2. Ballagi-Pord ány A., Klintevall K., Merza M., Klingeborn B. & Belák S. (1992). Direct detection of bovine leukemia virus infection: practical applicability of a double polymerase chain reaction. Journal of Veterinary Medicine B, 39, 69–77. [DOI] [PubMed] [Google Scholar]
  3. Belák S. & Ballagi-Pordány A. (1991). Bovine viral diarrhea virus infection: rapid diagnosis by the polymerase chain reaction. Archives of Virology, 3, 181–190. [DOI] [PubMed] [Google Scholar]
  4. Belák S. & Ballagi-Pordány A. (1993). Experiences on the applicability of the polymerase chain reaction in a diagnostic laboratory. Molecular and Cellular Probes, 7, 241–248. [DOI] [PubMed] [Google Scholar]
  5. Boursnell M.E.G., Brown T.D.K, Foulds I.J., Green P.F., Tomley F.M. & Binns M.M. (1987). Completion of the sequence of the genome of the coronavirus avian infectious bronchitis virus. Journal of General Virology, 68, 57–77. [DOI] [PubMed] [Google Scholar]
  6. Breslin J.J., Smith L.G., Fuller F.J. & Guy J.S. (1999a). Sequence analysis of the matrix/nucleocapsid gene region of turkey coronavirus. Intervirology, 42, 22–29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Breslin J.J., Smith L.G., Fuller F.J. & Guy J.S. (1999b). Sequence analysis of the turkey coronavirus nucleocapsid gene and 3' untranslated region identifies the virus as a close relative of infectious bronchitis virus. Virus Research, 65, 187–198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Capua I., Minta Z., Karpinska E., Mawditt K., Britton P., Cavanagh D. & Gough R.E. (1999). Co-circulation of four types of infectious bronchitis virus (793/B, 624/I, B1648 and Massachusetts). Avian Pathology, 28, 587–593. [DOI] [PubMed] [Google Scholar]
  9. Cavanagh D. (1983a). Coronavirus IBV: further evidence that the surface projections are associated with two glycopeptides. Journal of General Virology, 64, 1787–1791. [DOI] [PubMed] [Google Scholar]
  10. Cavanagh D. (1983b). Coronavirus IBV: structural characterisation of spike protein. Journal of General Virology, 64, 2577–2583. [DOI] [PubMed] [Google Scholar]
  11. Cavanagh D. (2001a). Commentary. A nomenclature for avian coronavirus isolates and the question of species status. Avian Pathology, 30, 109–115. [DOI] [PubMed] [Google Scholar]
  12. Cavanagh D. (2001b). Technical Review: innovation and discovery: the application of nucleic acid-based technology to avian virus detection and characterisation. Avian Pathology, 30, 581–598. [DOI] [PubMed] [Google Scholar]
  13. Cavanagh D., Davis P.J., Cook J.K.A., Li D., Kant A. & Koch G. (1992). Location of the amino acid differences in the S1 spike glycoprotein subunit of closely related serotypes of infectious bronchitis virus. Avian Pathology, 21, 33–43. [DOI] [PubMed] [Google Scholar]
  14. Cavanagh D., Ellis M.M. & Cook J.K.A. (1997). Relationship between sequence variation in the S1 spike protein of infectious bronchitis virus and the extent of cross-protection in vivo. Avian Pathology, 26, 63–74. [DOI] [PubMed] [Google Scholar]
  15. Cavanagh D., Mawditt K., Britton P. & Naylor C.J. (1999). Longitudinal field studies of infectious bronchitis virus and avian pneumovirus in broilers using type-specific polymerase chain reactions. Avian Pathology, 28, 593–605. [DOI] [PubMed] [Google Scholar]
  16. Cavanagh D., Mawditt K., Sharma M., Drury S.E., Ainsworth H.L., Britton P. & Gough R.E. (2001). Detection of a coronavirus from turkey poults in Europe genetically related to infectious bronchitis virus of chickens. Avian Pathology, 30, 365–378. [DOI] [PubMed] [Google Scholar]
  17. Cavanagh D., Mawditt K., Welchman D. de B., Britton P. & Gough R.E.. (2002). Coronaviruses from pheasants (Phasianus colchicus) are genetically closely related to coronaviruses of domestic fowl (infectious bronchitis virus) and turkeys. Avian Pathology, 31, 81–93. [DOI] [PubMed] [Google Scholar]
  18. Davelaar F.G., Kouwenhoven B. & Burger A.G. (1984). Occurrence and significance of infectious bronchitis virus variant strains in egg and broiler production in the Netherlands. Veterinary Quarterly, 6, 114–120. [DOI] [PubMed] [Google Scholar]
  19. de Wit J.J. (2000). Technical Review. Detection of infectious bronchitis virus. Avian Pathology, 29, 71–93 [DOI] [PubMed] [Google Scholar]
  20. Fabricant J. (1998). The early history of infectious bronchitis. Avian Disease, 42, 648–650. [PubMed] [Google Scholar]
  21. Guy J.S. (2000). Turkey coronavirus is more closely related to avian infectious bronchitis virus than to mammalian coronavirus. Avian Pathology, 29, 206–212. [DOI] [PubMed] [Google Scholar]
  22. Handberg K.J., Nielsen O.L., Pedersen M.W. & Jorgensen P.H. (1999). Detection and strain differentation of infectious bronchitis virus in tracheal tissues from experimentally infected chickens by reverse transcription-polymerase chain reaction. Comparison with an immunohistochemical technique. Avian Pathology, 28, 327–335. [DOI] [PubMed] [Google Scholar]
  23. Jia W., Karaca K., Parrish C.R. & Naqi S.A. (1995). A novel variant of avian bronchitis virus resulting from recombination among three different strains. Archives of Virology, 140, 259–271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. King D.J. (1988). Identification of recent infectious bronchitis virus isolates that are serologically different from current vaccine strains. Avian Disease, 32, 362–364. [PubMed] [Google Scholar]
  25. King D.J. & Cavanagh D. (1991). Infectious bronchitis, In Calnek B.W., Barnes H.J., Beard C.W., Reid W.M. & Yoder H.W. Jr. (Eds.), Diseases of Poultry 9th edn (pp. 471–484). Ames, IA: Iowa State University Press. [Google Scholar]
  26. Kingsham B.E., Keeler C.L. Jr., Nix W.A., Landman B.S. & Gelb J. Jr. (2000). Identification of avian infectious bronchitis virus by direct automated cycle sequencing of the S-1 gene. Avian Disease, 44, 325–335. [PubMed] [Google Scholar]
  27. Kottier S.A., Cavanagh D. & Britton P. (1995). Experimental evidence of recombination in coronavirus infectious bronchitis virus. Virology, 213, 569–580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kusters J.G., Niester H.G.M., Lenstra J.A., Horzinek M.C. & Van Der Zeijst B.A.M. (1989). Phylogeny of antigenic variants of avian coronavirus IBV. Virology, 169, 217–221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kwon H.M., Jackwood M.W. & Gelb J. Jr. (1993). Differentiation of infectious bronchitis virus serotype using polymerase chain reaction and restriction fragment length polymorphism analysis. Avian Disease, 37, 194–202. [PubMed] [Google Scholar]
  30. Lai M.M.C. & Cavanagh D. (1997). The molecular biology of coronaviruses. Advances in Virus Research, 48, 1–100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lee C-W. & Jackwood M.W. (2000). Evidence of genetic diversity generated by recombination among avian coronavirus IBV. Archives of Virology, 145, 2135–2148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lee C. & Jackwood M.W. (2001). Origin and evolution of Georgia 98 (GA98), a new serotype of avian infectious bronchitis virus. Virus Research, 80, 33–39. [DOI] [PubMed] [Google Scholar]
  33. Li H. & Yang H. (2001). Sequence analysis of nephropathogenic infectious bronchitis virus strains of the Massachusetts genotype in Beijing. Avian Pathology, 30, 535–541. [DOI] [PubMed] [Google Scholar]
  34. Lin Z., Kato A., Kudou Y. & Ueda S. (1991). A new typing method for the avian infectious bronchitis virus using polymerase chain reaction and restriction enzyme fragment length polymorphism. Archives in Virology, 116, 19–31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Meulemans G., Boschmanns M., Decaesstecker M., van der Berg T.P., Denis P. & Cavanagh D. (2001). Epidemiology of infectious bronchitis virus in Belgian broilers: a retrospective study, 1986 to 1995. Avian Pathology, 30, 411–421. [DOI] [PubMed] [Google Scholar]
  36. Schalk A.F. & Hawn M.C. (1931). An apparently new respiratory disease of chicks. Journal of American Veterinary Medical Association, 78, 413–422. [Google Scholar]
  37. Saif L.J. (1993). Coronavirus immunogens. Veterinary Microbiology, 34, 285–297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sapats S.I., Ashton F., Wright P.J. & Ignjatovic J. (1996). Sequence analysis of the S1 glycoprotein of infectious bronchitis viruses: identification of a novel genotypic group in Australia. Journal of General Virology, 77, 413–418. [DOI] [PubMed] [Google Scholar]
  39. Sharma J.M. (1999). Introduction to poultry vaccines and immunity. Advances in Veterinary Medicine, 41, 481–494. [DOI] [PubMed] [Google Scholar]
  40. Verhofstede C., Fransen K., Marissens D., Verhelst R., van der Groen G., Lauwers S., Zissis G. & Plum J. (1996). Isolation of HIV-1 RNA from plasma: evaluation of eight different extraction methods. Journal of Virological Methods, 60, 155–159. [DOI] [PubMed] [Google Scholar]
  41. Vilcek S., Elvander M., Ballagi-Pordány A. & Belák S. (1994). Development of nested PCR assays for detection of bovine respiratory syncytial virus in clinical samples. Journal of Clinical Microbiology, 32, 2225–2231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wang L., Junker D., Hock L. Ebiary E. & Collison E.W. (1994). Evolutionary implications of genetic variations in the S1 gene of infectious bronchitis virus. Virus Research, 34, 327–338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wang L., Xu Y. & Collisson E.W. (1997). Experimental confirmation of recombination upstream of the S1 hypervariable region of infectious bronchitis virus. Virus Research, 49, 139–145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Williams A.K., Wang L., Sneed L.W. & Collison E.W. (1992). Comparative analyses of the nucleocapsid genes of several of infectious bronchitis virus and other coronaviruses. Virus Research, 25, 213–222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zwaagstra K.A., Zeijst B.A.M. & Kusters J.G. (1992). Rapid detection and identification of avian infectious bronchitis virus. Journal of Clinical Microbiology, 30, 79–84. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Avian Pathology are provided here courtesy of Taylor & Francis

RESOURCES