1887

Abstract

Noroviruses are a major cause of acute gastroenteritis worldwide and are a genetically diverse group of viruses. Since 2002, an increasing number of norovirus outbreaks have been reported globally, but it is not clear whether this increase has been caused by a higher awareness or reflects the emergence of new genogroup II genotype 4 (GII.4) variants. The hypothesis that norovirus prevalence has increased post-2002 and is related to the emergence of GII.4 is tested in this study. Sera collected from children aged <5 years of three Dutch cross-sectional population based cohorts in 1963, 1983 and 2006/2007 (=143, =130 and =376, respectively) were tested for specific serum IgG by protein array using antigens to GII.4 and a range of other antigens representing norovirus GI, GII and GIV genotypes. The protein array was validated by paired sera of norovirus infected patients and supernatants of B-cell cultures with single epitope specificity. Evidence for norovirus infection was found to be common among Dutch children in each cohort, but the prevalence towards different genotypes changed over time. At the genogroup level, GI seroprevalence decreased significantly between 1963 and 2006/2007, while a significant increase of GII and, in particular, specific antibodies of the genotype GII.4 was detected in the 2006/2007 cohort. There were no children with only GII.4 antibodies in the 1963 cohort. This study shows that the high GII.4 norovirus incidence in very young children is a recent phenomenon. These findings are of importance for vaccine development and trials that are currently focusing mostly on GII.4 viruses.

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2016-09-01
2020-07-03
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References

  1. Ahmed S. M., Hall A. J., Robinson A. E., Verhoef L., Premkumar P., Parashar U. D., Koopmans M., Lopman B. A.. 2014; Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis14:725–730 [CrossRef][PubMed]
    [Google Scholar]
  2. Baas D. C., Koopmans M. P., de Bruin E., ten Hulscher H., Buisman A. M., Hendrikx L. H., van Beek J., Godeke G. J., Reimerink J., van Binnendijk R. S.. 2013; Detection of influenza A virus homo- and heterosubtype-specific memory B-cells using a novel protein microarray-based analysis tool. J Med Virol85:899–909 [CrossRef][PubMed]
    [Google Scholar]
  3. Bernstein D., Atmar R. L., Lyon G. M., Treanor J. J., Chen W. H., Jiang X., Vinjé J., Gregoricus N., Frenck R. W., Jr. et al. 2015; Norovirus vaccine against experimental human GII.4 virus illness: a challenge study in healthy adults. J Infect Dis211:870–878 [CrossRef][PubMed]
    [Google Scholar]
  4. Boon D., Mahar J. E., Abente E. J., Kirkwood C. D., Purcell R. H., Kapikian A. Z., Green K. Y., Bok K.. 2011; Comparative evolution of GII.3 and GII.4 norovirus over a 31-year period. J Virol85:8656–8666 [CrossRef][PubMed]
    [Google Scholar]
  5. Carmona-Vicente N., Fernández-Jiménez M., Ribes J. M., Téllez-Castillo C. J., Khodayar-Pardo P., Rodríguez-Diaz J., Buesa J.. 2015; Norovirus infections and seroprevalence of genotype GII.4-specific antibodies in a Spanish population. J Med Virol87:675–682 [CrossRef][PubMed]
    [Google Scholar]
  6. de Graaf M., van Beek J., Vennema H., Podkolzin A. T., Hewitt J., Bucardo F., Templeton K., Mans J., Nordgren J. et al. 2015; Emergence of a novel GII.17 norovirus – end of the GII.4 era?. Euro Surveill20:21178 [CrossRef][PubMed]
    [Google Scholar]
  7. Desai R., Hembree C. D., Handel A., Matthews J. E., Dickey B. W., McDonald S., Hall A. J., Parashar U. D., Leon J. S., Lopman B.. 2012; Severe outcomes are associated with genogroup 2 genotype 4 norovirus outbreaks: a systematic literature review. Clin Infect Dis55:189–193 [CrossRef][PubMed]
    [Google Scholar]
  8. 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 Virol87:6270–6282 [CrossRef][PubMed]
    [Google Scholar]
  9. Harrington P. R., Lindesmith L., Yount B., Moe C. L., Baric R. S.. 2002; Binding of Norwalk virus-like particles to ABH histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J Virol76:12335–12343 [CrossRef][PubMed]
    [Google Scholar]
  10. Jiang X., Wang M., Graham D. Y., Estes M. K.. 1992; Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J Virol66:6527–6532[PubMed]
    [Google Scholar]
  11. Kobayashi S., Fujiwara N., Takeda N., Minagawa H.. 2009; Seroepidemiological study of norovirus infection in Aichi Prefecture, Japan. Microbiol Immunol53:356–359 [CrossRef][PubMed]
    [Google Scholar]
  12. Koopmans M., de Bruin E., Godeke G. J., Friesema I., van Gageldonk R., Schipper M., Meijer A., van Binnendijk R., Rimmelzwaan G. F. et al. 2012; Profiling of humoral immune responses to influenza viruses by using protein microarray. Clin Microbiol Infect18:797–807 [CrossRef][PubMed]
    [Google Scholar]
  13. 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 Virol158:2059–2068 [CrossRef][PubMed]
    [Google Scholar]
  14. 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 Pathog8:e1002705 [CrossRef][PubMed]
    [Google Scholar]
  15. Lopman B., Vennema H., Kohli E., Pothier P., Sanchez A., Negredo A., Buesa J., Schreier E., Reacher M. et al. 2004; Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet363:682–688 [CrossRef][PubMed]
    [Google Scholar]
  16. Masurel N., Mulder J.. 1966; Studies on the content of antibodies for equine influenza viruses in human sera. Bull World Health Organ34:885–893[PubMed]
    [Google Scholar]
  17. Menon V. K., George S., Aladin F., Nawaz S., Sarkar R., Lopman B., Gray J. J., Gomara M., Kang G.. 2013; Comparison of age-stratified seroprevalence of antibodies against norovirus GII in India and the United Kingdom. PLoS One8:e56239 [CrossRef][PubMed]
    [Google Scholar]
  18. Nurminen K., Blazevic V., Huhti L., Räsänen S., Koho T., Hytönen V. P., Vesikari T.. 2011; Prevalence of norovirus GII-4 antibodies in Finnish children. J Med Virol83:525–531 [CrossRef][PubMed]
    [Google Scholar]
  19. Pinna D., Corti D., Jarrossay D., Sallusto F., Lanzavecchia A.. 2009; Clonal dissection of the human memory B-cell repertoire following infection and vaccination. Eur J Immunol39:1260–1270 [CrossRef][PubMed]
    [Google Scholar]
  20. Rockx B., Baric R. S., de Grijs I., Duizer E., Koopmans M. P.. 2005; Characterization of the homo- and heterotypic immune responses after natural norovirus infection. J Med Virol77:439–446 [CrossRef][PubMed]
    [Google Scholar]
  21. Shiota T., Okame M., Takanashi S., Khamrin P., Takagi M., Satou K., Masuoka Y., Yagyu F., Shimizu Y. et al. 2007; Characterization of a broadly reactive monoclonal antibody against norovirus genogroups I and II: recognition of a novel conformational epitope. J Virol81:12298–12306 [CrossRef][PubMed]
    [Google Scholar]
  22. Siebenga J. J., Vennema H., Duizer E., Koopmans M. P.. 2007a; Gastroenteritis caused by norovirus GGII.4, The Netherlands, 1994–2005. Emerg Infect Dis13:144–146 [CrossRef]
    [Google Scholar]
  23. Siebenga J. J., Vennema H., Renckens B., de Bruin E., van der Veer B., Siezen R. J., Koopmans M.. 2007b; Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J Virol81:9932–9941 [CrossRef]
    [Google Scholar]
  24. Siebenga J. J., Vennema H., Zheng D. P., Vinjé J., Lee B. E., Pang X. L., Ho E. C., Lim W., Choudekar A. et al. 2009; Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001–2007. J Infect Dis200:802–812 [CrossRef][PubMed]
    [Google Scholar]
  25. Siebenga J. J., Lemey P., Kosakovsky Pond S. L., Rambaut A., Vennema H., Koopmans M.. 2010; Phylodynamic reconstruction reveals norovirus GII.4 epidemic expansions and their molecular determinants. PLoS Pathog6:e1000884 [CrossRef][PubMed]
    [Google Scholar]
  26. Son H., Jeong H. S., Cho M., Lee J., Lee H., Yoon K., Jeong A. Y., Jung S., Kim K., Cheon D. S.. 2013; Seroepidemiology of predominant norovirus strains circulating in Korea by using recombinant virus-like particle antigens. Foodborne Pathog Dis10:461–466 [CrossRef][PubMed]
    [Google Scholar]
  27. Tamminen K., Huhti L., Koho T., Lappalainen S., Hytönen V. P., Vesikari T., Blazevic V.. 2012; A comparison of immunogenicity of norovirus GII-4 virus-like particles and P-particles. Immunology135:89–99 [CrossRef][PubMed]
    [Google Scholar]
  28. Tan M., Zhong W., Song D., Thornton S., Jiang X.. 2004; E. coli-expressed recombinant norovirus capsid proteins maintain authentic antigenicity and receptor binding capability. J Med Virol74:641–649 [CrossRef][PubMed]
    [Google Scholar]
  29. Tan M., Jiang X.. 2005; The P domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. J Virol79:14017–14030 [CrossRef][PubMed]
    [Google Scholar]
  30. van Beek J., Ambert-Balay K., Botteldoorn N., Eden J. S., Fonager J., Hewitt J., Iritani N., Kroneman A., Vennema H. et al. 2013; Indications for worldwide increased norovirus activity associated with emergence of a new variant of genotype II.4, late 2012. Euro Surveill18:8–9[PubMed]
    [Google Scholar]
  31. van der Klis F. R., Mollema L., Berbers G. A., de Melker H. E., Coutinho R. A.. 2009; Second national serum bank for population-based seroprevalence studies in the Netherlands. Neth J Med67:301–308[PubMed]
    [Google Scholar]
  32. Verhoef L., Hewitt J., Barclay L., Ahmed S. M., Lake R., Hall A. J., Lopman B., Kroneman A., Vennema H. et al. 2015; Norovirus genotype profiles associated with foodborne transmission, 1999–2012. Emerg Infect Dis21:592–599 [CrossRef][PubMed]
    [Google Scholar]
  33. Vinjé J.. 2015; Advances in laboratory methods for detection and typing of norovirus. J Clin Microbiol53:373–381 [CrossRef][PubMed]
    [Google Scholar]
  34. Wrammert J., Koutsonanos D., Li G. M., Edupuganti S., Sui J., Morrissey M., McCausland M., Skountzou I., Hornig M. et al. 2011; Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med208:181–193 [CrossRef][PubMed]
    [Google Scholar]
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