1887

Abstract

Norovirus (NoV) is one of the major causes of diarrhoeal disease with epidemic, outbreak and sporadic patterns in humans of all ages worldwide. NoVs of genotype GII.4 cause nearly 80–90 % of all NoV infections in humans. Periodically, some GII.4 strains become predominant, generating major pandemic variants. Retrospective analysis of the GII.4 NoV strains detected in Italy between 2007 and 2013 indicated that the pandemic variant New Orleans 2009 emerged in Italy in the late 2009, became predominant in 2010–2011 and continued to circulate in a sporadic fashion until April 2013. Upon phylogenetic analysis based on the small diagnostic regions A and C, the late New Orleans 2009 NoVs circulating during 2011–2013 appeared to be genetically different from the early New Orleans 2009 strains that circulated in 2010. For a selection of strains, a 3.2 kb genome portion at the 3′ end was sequenced. In the partial ORF1 and in the full-length ORF2 and ORF3, the 2011–2013 New Orleans NoVs comprised at least three distinct genetic subclusters. By comparison with sequences retrieved from the databases, these subclusters were also found to circulate globally, suggesting that the local circulation reflected repeated introductions of different strains, rather than local selection of novel viruses. Phylogenetic subclustering did not correlate with changes in residues located in predicted putative capsid epitopes, although several changes affected the P2 domain in epitopes A, C, D and E.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.000204
2015-09-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/9/2919.html?itemId=/content/journal/jgv/10.1099/vir.0.000204&mimeType=html&fmt=ahah

References

  1. Allen D.J., Gray J.J., Gallimore C.I., Xerry J., Iturriza-Gómara M. 2008; Analysis of amino acid variation in the P2 domain of the GII-4 norovirus VP1 protein reveals putative variant-specific epitopes. PLoS One 3:e1485 [View Article][PubMed]
    [Google Scholar]
  2. Bok K., Abente E.J., Realpe-Quintero M., Mitra T., Sosnovtsev S.V., Kapikian A.Z., Green K.Y. 2009; Evolutionary dynamics of GII.4 noroviruses over a 34-year period. J Virol 83:11890–11901 [View Article][PubMed]
    [Google Scholar]
  3. Bruggink L.D., Dunbar N.L., Marshall J.A. 2014; Emergence of GII.e as a major ORF 1 norovirus genotype and its associated ORF 2 GII.4 variant forms. Infect Genet Evol 22:157–163 [View Article][PubMed]
    [Google Scholar]
  4. Bull R.A., Eden J.S., Rawlinson W.D., White P.A. 2010; Rapid evolution of pandemic noroviruses of the GII.4 lineage. PLoS Pathog 6:e1000831 [View Article][PubMed]
    [Google Scholar]
  5. Chan M.C., Lee N., Ho W.S., Law C.O., Lau T.C., Tsui S.K., Sung J.J. 2012; Covariation of major and minor viral capsid proteins in norovirus genogroup II genotype 4 strains. J Virol 86:1227–1232 [View Article][PubMed]
    [Google Scholar]
  6. Clark B., McKendrick M. 2004; A review of viral gastroenteritis. Curr Opin Infect Dis 17:461–469 [View Article][PubMed]
    [Google Scholar]
  7. De Grazia S., Medici M.C., Pinto P., Moschidou P., Tummolo F., Calderaro A., Bonura F., Bànyai K., Giammanco G.M., Martella V. 2012; Genetic heterogeneity and recombination in human type 2 astroviruses. J Clin Microbiol 50:3760–3764 [View Article][PubMed]
    [Google Scholar]
  8. De Grazia S., Martella V., Chironna M., Bonura F., Tummolo F., Calderaro A., Moschidou P., Giammanco G.M., Medici M.C. 2013; Nationwide surveillance study of human astrovirus infections in an Italian paediatric population. Epidemiol Infect 141:524–528 [View Article][PubMed]
    [Google Scholar]
  9. Debbink K., Lindesmith L.C., Donaldson E.F., Costantini V., Beltramello M., Corti D., Swanstrom J., Lanzavecchia A., Vinjé J., Baric R.S. 2013; Emergence of new pandemic GII.4 Sydney norovirus strain correlates with escape from herd immunity. J Infect Dis 208:1877–1887 [View Article][PubMed]
    [Google Scholar]
  10. Eden J.S., Bull R.A., Tu E., McIver C.J., Lyon M.J., Marshall J.A., Smith D.W., Musto J., Rawlinson W.D., White P.A. 2010; Norovirus GII.4 variant 2006b caused epidemics of acute gastroenteritis in Australia during 2007 and 2008. J Clin Virol 49:265–271 [View Article][PubMed]
    [Google Scholar]
  11. Eden J.S., Tanaka M.M., Boni M.F., Rawlinson W.D., White P.A. 2013; Recombination within the pandemic norovirus GII.4 lineage. J Virol 87:6270–6282 [View Article][PubMed]
    [Google Scholar]
  12. Eden J.S., Hewitt J., Lim K.L., Boni M.F., Merif J., Greening G., Ratcliff R.M., Holmes E.C., Tanaka M.M., other authors. 2014; The emergence and evolution of the novel epidemic norovirus GII.4 variant Sydney 2012. Virology 450-451:106–113 [View Article][PubMed]
    [Google Scholar]
  13. Fonager J., Hindbæk L.S., Fischer T.K. 2013; Rapid emergence and antigenic diversification of the norovirus 2012 Sydney variant in Denmark, October to December, 2012. Euro Surveill 18:20413[PubMed] [CrossRef]
    [Google Scholar]
  14. Giammanco G.M., Rotolo V., Medici M.C., Tummolo F., Bonura F., Chezzi C., Martella V., De Grazia S. 2012; Recombinant norovirus GII.g/GII.12 gastroenteritis in children. Infect Genet Evol 12:169–174 [View Article][PubMed]
    [Google Scholar]
  15. Giammanco G.M., De Grazia S., Tummolo F., Bonura F., Calderaro A., Buonavoglia A., Martella V., Medici M.C. 2013; Norovirus GII.4/Sydney/2012 in Italy, winter 2012-2013. Emerg Infect Dis 19:1348–1349 [View Article][PubMed]
    [Google Scholar]
  16. Giammanco G.M., De Grazia S., Terio V., Lanave G., Catella C., Bonura F., Saporito L., Medici M.C., Tummolo F., other authors. 2014; Analysis of early strains of the norovirus pandemic variant GII.4 Sydney 2012 identifies mutations in adaptive sites of the capsid protein. Virology 450-451:355–358 [View Article][PubMed]
    [Google Scholar]
  17. Green K.Y. 2013; Caliciviridae: the noroviruses. In Fields Virology, 6th edn. pp. 949–979 Edited by Knipe D. M., Howley P. M. Philadelphia: Wolters Kluwer Health/Lippincott Williams and Wilkins;
    [Google Scholar]
  18. Hall A.J., Lopman B.A., Payne D.C., Patel M.M., Gastañaduy P.A., Vinjé J., Parashar U.D. 2013; Norovirus disease in the United States. Emerg Infect Dis 19:1198–1205 [View Article][PubMed]
    [Google Scholar]
  19. Hasing M.E., Lee B.E., Preiksaitis J.K., Tellier R., Honish L., Senthilselvan A., Pang X.L. 2013; Emergence of a new norovirus GII.4 variant and changes in the historical biennial pattern of norovirus outbreak activity in Alberta, Canada, from 2008 to 2013. J Clin Microbiol 51:2204–2211 [View Article][PubMed]
    [Google Scholar]
  20. Kamel A.H., Ali M.A., El-Nady H.G., de Rougemont A., Pothier P., Belliot G. 2009; Predominance and circulation of enteric viruses in the region of Greater Cairo, Egypt. J Clin Microbiol 47:1037–1045 [View Article][PubMed]
    [Google Scholar]
  21. Kroneman A., Vega E., Vennema H., Vinjé J., White P.A., Hansman G., Green K., Martella V., Katayama K., Koopmans M. 2013; Proposal for a unified norovirus nomenclature and genotyping. Arch Virol 158:2059–2068 [View Article][PubMed]
    [Google Scholar]
  22. Lindesmith L.C., Donaldson E.F., Lobue A.D., Cannon J.L., Zheng D.P., Vinjé J., Baric R.S. 2008; Mechanisms of GII.4 norovirus persistence in human populations. PLoS Med 5:e31 [View Article][PubMed]
    [Google Scholar]
  23. Lindesmith L.C., Beltramello M., Donaldson E.F., Corti D., Swanstrom J., Debbink K., Lanzavecchia A., Baric R.S. 2012; Immunogenetic mechanisms driving norovirus GII.4 antigenic variation. PLoS Pathog 8:e1002705 [View Article][PubMed]
    [Google Scholar]
  24. Lindesmith L.C., Costantini V., Swanstrom J., Debbink K., Donaldson E.F., Vinjé J., Baric R.S. 2013; Emergence of a norovirus GII.4 strain correlates with changes in evolving blockade epitopes. J Virol 87:2803–2813 [View Article][PubMed]
    [Google Scholar]
  25. Lole K.S., Bollinger R.C., Paranjape R.S., Gadkari D., Kulkarni S.S., Novak N.G., Ingersoll R., Sheppard H.W., Ray S.C. 1999; Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152–160[PubMed]
    [Google Scholar]
  26. Mans J., Murray T.Y., Taylor M.B. 2014; Novel norovirus recombinants detected in South Africa. Virol J 11:168 [View Article][PubMed]
    [Google Scholar]
  27. Martella V., Medici M.C., De Grazia S., Tummolo F., Calderaro A., Bonura F., Saporito L., Terio V., Catella C., other authors. 2013a; Evidence for recombination between pandemic GII.4 norovirus strains New Orleans 2009 and Sydney 2012. J Clin Microbiol 51:3855–3857 [View Article][PubMed]
    [Google Scholar]
  28. Martella V., Medici M.C., Terio V., Catella C., Bozzo G., Tummolo F., Calderaro A., Bonura F., Di Franco M., other authors. 2013b; Lineage diversification and recombination in type-4 human astroviruses. Infect Genet Evol 20:330–335 [View Article][PubMed]
    [Google Scholar]
  29. Medici M.C., Tummolo F., Martella V., Giammanco G.M., De Grazia S., Arcangeletti M.C., De Conto F., Chezzi C., Calderaro A. 2014; Novel recombinant GII.P16_GII.13 and GII.P16_GII.3 norovirus strains in Italy. Virus Res 188:142–145 [View Article][PubMed]
    [Google Scholar]
  30. Motomura K., Yokoyama M., Ode H., Nakamura H., Mori H., Kanda T., Oka T., Katayama K., Noda M., other authors. 2010; Divergent evolution of norovirus GII/4 by genome recombination from May 2006 to February 2009 in Japan. J Virol 84:8085–8097 [View Article][PubMed]
    [Google Scholar]
  31. Okada M., Tanaka T., Oseto M., Takeda N., Shinozaki K. 2006; Genetic analysis of noroviruses associated with fatalities in healthcare facilities. Arch Virol 151:1635–1641 [View Article][PubMed]
    [Google Scholar]
  32. Patel M.M., Widdowson M.A., Glass R.I., Akazawa K., Vinjé J., Parashar U.D. 2008; Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14:1224–1231 [View Article][PubMed]
    [Google Scholar]
  33. Ruvoën-Clouet N., Belliot G., Le Pendu J. 2013; Noroviruses and histo-blood groups: the impact of common host genetic polymorphisms on virus transmission and evolution. Rev Med Virol 23:355–366 [View Article][PubMed]
    [Google Scholar]
  34. Seah E.L., Gunesekere I.C., Marshall J.A., Wright P.J. 1999; Variation in ORF3 of genogroup 2 Norwalk-like viruses. Arch Virol 144:1007–1014 [View Article][PubMed]
    [Google Scholar]
  35. Shanker S., Choi J.M., Sankaran B., Atmar R.L., Estes M.K., Prasad B.V. 2011; Structural analysis of histo-blood group antigen binding specificity in a norovirus GII.4 epidemic variant: implications for epochal evolution. J Virol 85:8635–8645 [View Article][PubMed]
    [Google Scholar]
  36. Siebenga J.J., Vennema H., Renckens B., de Bruin E., van der Veer B., Siezen R.J., Koopmans M. 2007; Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J Virol 81:9932–9941 [View Article][PubMed]
    [Google Scholar]
  37. Siebenga J.J, Vennema H., Zheng D.P., Vinjé J., Lee B.E., Pang X.L., Ho E.C., Lim W., Choudekar A., other authors. 2009; Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001-2007. J Infect Dis 200:802–812 [View Article][PubMed]
    [Google Scholar]
  38. Tam C.C., Rodrigues L.C., Viviani L., Dodds J.P., Evans M.R., Hunter P.R., Gray J.J., Letley L.H., Rait G., other authors. 2012; Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut 61:69–77 [View Article][PubMed]
    [Google Scholar]
  39. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013; mega6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  40. Thornley C.N., Hewitt J., Perumal L., Van Gessel S.M., Wong J., David S.A., Rapana J.P., Li S., Marshall J.C., Greening G.E. 2013; Multiple outbreaks of a novel norovirus GII.4 linked to an infected post-symptomatic food handler. Epidemiol Infect 141:1585–1597 [View Article][PubMed]
    [Google Scholar]
  41. van Beek J., Ambert-Balay K., Botteldoorn N., Eden J.S., Fonager J., Hewitt J., Iritani N., Kroneman A., Vennema H., other authors. 2013; Indications for worldwide increased norovirus activity associated with emergence of a new variant of genotype II.4, late 2012. Euro Surveill 18:8–9[PubMed]
    [Google Scholar]
  42. Vennema H., de Bruin E., Koopmans M. 2002; Rational optimization of generic primers used for Norwalk-like virus detection by reverse transcriptase polymerase chain reaction. J Clin Virol 25:233–235 [View Article][PubMed]
    [Google Scholar]
  43. Vinjé J., Green J., Lewis D.C., Gallimore C.I., Brown D.W., Koopmans M.P. 2000; Genetic polymorphism across regions of the three open reading frames of Norwalk-like viruses. Arch Virol 145:223–241 [View Article][PubMed]
    [Google Scholar]
  44. Wang Q.H., Han M.G., Cheetham S., Souza M., Funk J.A., Saif L.J. 2005; Porcine noroviruses related to human noroviruses. Emerg Infect Dis 11:1874–1881 [View Article][PubMed]
    [Google Scholar]
  45. Yen C., Wikswo M.E., Lopman B.A., Vinjé J., Parashar U.D., Hall A.J. 2011; Impact of an emergent norovirus variant in 2009 on norovirus outbreak activity in the United States. Clin Infect Dis 53:568–571 [View Article][PubMed]
    [Google Scholar]
  46. Zakikhany K., Allen D.J., Brown D., Iturriza-Gómara M. 2012; Molecular evolution of GII-4 Norovirus strains. PLoS One 7:e41625 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.000204
Loading
/content/journal/jgv/10.1099/vir.0.000204
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error