1887

Abstract

Avian G18P[17] rotaviruses with similar complete genome constellation, including strains that showed pathogenicity in mammals, have been detected worldwide. However, it remains unclear how these strains spread geographically. In this study, to investigate the role of migratory birds in the dispersion of avian rotaviruses, we analysed whole genetic characters of the rotavirus strain RK1 that was isolated from a migratory species of birds [velvet scoter ()] in Japan in 1989. Genetic analyses revealed that the genotype constellation of the RK1 strain, G18-P[17]-I4-R4-C4-M4-A21-N4-T4-E4-H4, was highly consistent with those of other G18P[17] strains detected in various parts of the world, supporting the possibility that the G18P[17] strains spread via migratory birds that move over a wide area. Furthermore, the RK1 strain induced diarrhoea in suckling mice after oral gastric inoculation, indicating that at least some of the rotaviruses that originated from migratory birds are infectious to and pathogenic in mammals. In conclusion, it was demonstrated that migratory birds may contribute to the global spread of avian rotaviruses that are pathogenic in mammalian species.

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2022-02-17
2024-04-23
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References

  1. Estes MK, Greenberg HB. Rotaviruses. In Knipe DM, Howley PM. eds Fields Virology Philadelphia: 2013 pp 1347–1401
    [Google Scholar]
  2. Dhama K, Saminathan M, Karthik K, Tiwari R, Shabbir MZ et al. Avian rotavirus enteritis - an updated review. Vet Q 2015; 35:142–158 [View Article] [PubMed]
    [Google Scholar]
  3. Estes MK, Cohen J. Rotavirus gene structure and function. Microbiol Rev 1989; 53:410–449 [View Article] [PubMed]
    [Google Scholar]
  4. Martella V, Bányai K, Matthijnssens J, Buonavoglia C, Ciarlet M. Zoonotic aspects of rotaviruses. Vet Microbiol 2010; 140:246–255 [View Article] [PubMed]
    [Google Scholar]
  5. Santos N, Hoshino Y. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 2005; 15:29–56 [View Article] [PubMed]
    [Google Scholar]
  6. Bányai K, László B, Duque J, Steele AD, Nelson EAS et al. Systematic review of regional and temporal trends in global rotavirus strain diversity in the pre rotavirus vaccine era: insights for understanding the impact of rotavirus vaccination programs. Vaccine 2012; 30 Suppl 1:A122–30 [View Article] [PubMed]
    [Google Scholar]
  7. Dóró R, László B, Martella V, Leshem E, Gentsch J et al. Review of global rotavirus strain prevalence data from six years post vaccine licensure surveillance: is there evidence of strain selection from vaccine pressure?. Infect Genet Evol 2014; 28:446–461 [View Article] [PubMed]
    [Google Scholar]
  8. Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T et al. Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 2008; 82:3204–3219 [View Article] [PubMed]
    [Google Scholar]
  9. Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Bányai K et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 2008; 153:1621–1629 [View Article] [PubMed]
    [Google Scholar]
  10. Ghosh S, Kobayashi N. Exotic rotaviruses in animals and rotaviruses in exotic animals. Virusdisease 2014; 25:158–172 [View Article] [PubMed]
    [Google Scholar]
  11. Fujii Y, Mitake H, Yamada D, Nagai M, Okadera K et al. Genome Sequences of Rotavirus A Strains Ty-1 and Ty-3, Isolated from Turkeys in Ireland in 1979. Genome Announc 2016; 4:1–2 [View Article] [PubMed]
    [Google Scholar]
  12. Trojnar E, Sachsenröder J, Twardziok S, Reetz J, Otto PH et al. Identification of an avian group A rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotaviruses. J Gen Virol 2013; 94:136–142 [View Article] [PubMed]
    [Google Scholar]
  13. Gál J, Marton S, Ihász K, Papp H, Jakab F et al. Complete Genome Sequence of a Genotype G23P[37] Pheasant Rotavirus Strain Identified in Hungary. Genome Announc 2016; 4:4–5 [View Article] [PubMed]
    [Google Scholar]
  14. Patzina-Mehling C, Falkenhagen A, Gadicherla AK, Grützke J, Tausch SH et al. Whole genome sequence analysis of cell culture-adapted rotavirus A strains from chicken. Infect Genet Evol 2020; 81:104275 [View Article] [PubMed]
    [Google Scholar]
  15. Beserra LAR, Barbosa CM, Berg M, Brandão PE, Soares RM et al. Genome constellations of rotavirus a isolated from avian species in Brazil, 2008-2015. Braz J Microbiol 2020; 51:1363–1375 [View Article] [PubMed]
    [Google Scholar]
  16. Brüssow H, Nakagomi O, Gerna G, Eichhorn W. Isolation of an avianlike group A rotavirus from a calf with diarrhea. J Clin Microbiol 1992; 30:67–73 [View Article]
    [Google Scholar]
  17. Mitake H, Ito N, Okadera K, Okada K, Nakagawa K et al. Detection of avian-like rotavirus A VP4 from a calf in Japan. J Vet Med Sci 2015; 77:221–224 [View Article] [PubMed]
    [Google Scholar]
  18. Busi C, Martella V, Papetti A, Sabelli C, Lelli D et al. Group A Rotavirus Associated with Encephalitis in Red Fox. Emerg Infect Dis 2017; 23:1535–1538 [View Article] [PubMed]
    [Google Scholar]
  19. Rohwedder A, Hotop H, Minamoto N, Ito H, Nakagomi O et al. Bovine rotavirus 993/83 shows a third subtype of avian VP7 protein. Virus Genes 1997; 14:147–151 [View Article]
    [Google Scholar]
  20. Brüssow H, Clark HF, Sidoti J. Prevalence of serum neutralizing antibody to serotype 9 rotavirus WI61 in children from South America and central Europe. J Clin Microbiol 1991; 29:208–211 [View Article]
    [Google Scholar]
  21. Mori Y, Sugiyama M, Takayama M, Atoji Y, Masegi T et al. Avian-to-mammal transmission of an avian rotavirus: analysis of its pathogenicity in a heterologous mouse model. Virology 2001; 288:63–70 [View Article] [PubMed]
    [Google Scholar]
  22. Brüssow H, Nakagomi O, Minamoto N, Eichhorn W. Rotavirus 993/83, isolated from calf faeces, closely resembles an avian rotavirus. J Gen Virol 1992; 73 (Pt 7):1873–1875 [View Article] [PubMed]
    [Google Scholar]
  23. Mori Y, Borgan MA, Takayama M, Ito N, Sugiyama M et al. Roles of outer capsid proteins as determinants of pathogenicity and host range restriction of avian rotaviruses in a suckling mouse model. Virology 2003; 316:126–134 [View Article] [PubMed]
    [Google Scholar]
  24. Minamoto N, Oki K, Tomita M, Kinjo T, Suzuki Y. Isolation and characterization of rotavirus from feral pigeon in mammalian cell cultures. Epidemiol Infect 2009; 100:481–492 [View Article] [PubMed]
    [Google Scholar]
  25. McCowan C, Crameri S, Kocak A, Shan S, Fegan M et al. A novel group A rotavirus associated with acute illness and hepatic necrosis in pigeons (Columba livia), in Australia. PLoS One 2018; 13:1–16 [View Article] [PubMed]
    [Google Scholar]
  26. Hunnam JC, Sloan S, McCowan CI, Glass E, Walker C. The racing pigeon (Columba livia domestica) industry in Victoria, Australia, and epidemiology of a novel Group A rotavirus outbreak. Transbound Emerg Dis 2019; 66:2058–2066 [View Article] [PubMed]
    [Google Scholar]
  27. Rubbenstroth D, Peus E, Schramm E, Kottmann D, Bartels H et al. Identification of a novel clade of group A rotaviruses in fatally diseased domestic pigeons in Europe. Transbound Emerg Dis 2019; 66:552–561 [View Article] [PubMed]
    [Google Scholar]
  28. Blakey J, Crossley B, Rosenberger JK, Rejmanek D, Markis M et al. Rotavirus A Associated with Clinical Disease and Hepatic Necrosis in California Pigeons (Columba livia domestica). Avian Dis 2019; 63:651–658 [View Article] [PubMed]
    [Google Scholar]
  29. Pauly M, Oni OO, Sausy A, Owoade AA, Adeyefa CAO et al. Molecular epidemiology of Avian Rotaviruses Group A and D shed by different bird species in Nigeria. Virol J 2017; 14:1–10 [View Article] [PubMed]
    [Google Scholar]
  30. Rubbenstroth D, Ulrich R, Wylezich C, Rautenschlein S, Beer M et al. First experimental proof of Rotavirus A (RVA) genotype G18P[17] inducing the clinical presentation of “young pigeon disease syndrome” (YPDS) in domestic pigeons (Columba livia). Transbound Emerg Dis 2020; 67:1507–1516 [View Article] [PubMed]
    [Google Scholar]
  31. Isegawa Y, Nakagomi O, Brüssow H, Minamoto N, Nakagomi T et al. A unique VP4 gene allele carried by an unusual bovine rotavirus strain, 993/83. Virology 1994; 198:366–369 [View Article] [PubMed]
    [Google Scholar]
  32. Rohwedder A, Schütz KI, Minamoto N, Brüssow H. Sequence analysis of pigeon, turkey, and chicken rotavirus VP8* identifies rotavirus 993/83, isolated from calf feces, as a pigeon rotavirus. Virology 1995; 210:231–235 [View Article] [PubMed]
    [Google Scholar]
  33. Ito H, Sugiyama M, Masubuchi K, Mori Y, Minamoto N. Complete nucleotide sequence of a group A avian rotavirus genome and a comparison with its counterparts of mammalian rotaviruses. Virus Res 2001; 75:123–138 [View Article] [PubMed]
    [Google Scholar]
  34. Hubálek Z. An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 2004; 40:639–659 [View Article] [PubMed]
    [Google Scholar]
  35. Dhama K, Mahendran M, Tomar S. Pathogens transmitted by migratory birds: threat perceptions to poultry health and production. International J of Poultry Science 2008; 7:516–525 [View Article]
    [Google Scholar]
  36. Fuller T, Bensch S, Müller I, Novembre J, Pérez-Tris J et al. The ecology of emerging infectious diseases in migratory birds: an assessment of the role of climate change and priorities for future research. Ecohealth 2012; 9:80–88 [View Article] [PubMed]
    [Google Scholar]
  37. Jourdain E, Gauthier-Clerc M, Bicout DJ, Sabatier P. Bird migration routes and risk for pathogen dispersion into western Mediterranean wetlands. Emerg Infect Dis 2007; 13:365–372 [View Article] [PubMed]
    [Google Scholar]
  38. Takehara K, Kiuchi H, Kuwahara M, Yanagisawa F, Mizukami M et al. Identification and characterization of a plaque forming avian rotavirus isolated from a wild bird in Japan. J Vet Med Sci 1991; 53:479–486 [View Article] [PubMed]
    [Google Scholar]
  39. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
    [Google Scholar]
  40. Maes P, Matthijnssens J, Rahman M, Van Ranst M. RotaC: a web-based tool for the complete genome classification of group A rotaviruses. BMC Microbiol 2009; 9:238 [View Article] [PubMed]
    [Google Scholar]
  41. Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Bányai K et al. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 2011; 156:1397–1413 [View Article] [PubMed]
    [Google Scholar]
  42. Okadera K, Abe M, Ito N, Mitake H, Okada K et al. Isolation and characterization of a novel type of rotavirus species A in sugar gliders (Petaurus breviceps). J Gen Virol 2016; 97:1158–1167 [View Article] [PubMed]
    [Google Scholar]
  43. Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints12. Am J Epidemiol 1938; 27:493–497 [View Article]
    [Google Scholar]
  44. Minamoto N, Sugimoto O, Yokota M, Tomita M, Goto H et al. Antigenic analysis of avian rotavirus VP6 using monoclonal antibodies. Arch Virol 1993; 131:293–305 [View Article] [PubMed]
    [Google Scholar]
  45. Offit PA, Blavat G, Greenberg HB, Clark HF. Molecular basis of rotavirus virulence: role of gene segment 4. J Virol 1986; 57:46–49 [View Article]
    [Google Scholar]
  46. Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus ADME et al. Global patterns of influenza a virus in wild birds. Science 2006; 312:384–388 [View Article] [PubMed]
    [Google Scholar]
  47. Ursu K, Papp H, Kisfali P, Rigó D, Melegh B et al. Monitoring of group A rotaviruses in wild-living birds in Hungary. Avian Dis 2011; 55:123–127 [View Article] [PubMed]
    [Google Scholar]
  48. Pihl S, Fox T. Velvet scoter. In Kear J. eds Ducks, Geese and Swans: Species Accounts Oxford: Oxford University Press; 2005 pp 715–719
    [Google Scholar]
  49. Schumann T, Hotzel H, Otto P, Johne R. Evidence of interspecies transmission and reassortment among avian group A rotaviruses. Virology 2009; 386:334–343 [View Article] [PubMed]
    [Google Scholar]
  50. Morelli M, Ogden KM, Patton JT. Silencing the alarms: Innate immune antagonism by rotavirus NSP1 and VP3. Virology 2015; 479–480:75–84 [View Article] [PubMed]
    [Google Scholar]
  51. Kojima K, Taniguchi K, Kobayashi N. Species-specific and interspecies relatedness of NSP1 sequences in human, porcine, bovine, feline, and equine rotavirus strains. Arch Virol 1996; 141:1–12 [View Article] [PubMed]
    [Google Scholar]
  52. Dunn SJ, Cross TL, Greenberg HB. Comparison of the rotavirus nonstructural protein NSP1 (NS53) from different species by sequence analysis and northern blot hybridization. Virology 1994; 203:178–183 [View Article] [PubMed]
    [Google Scholar]
  53. Hua J, Chen X, Patton JT. Deletion mapping of the rotavirus metalloprotein NS53 (NSP1): the conserved cysteine-rich region is essential for virus-specific RNA binding. J Virol 1994; 68:3990–4000 [View Article] [PubMed]
    [Google Scholar]
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