Norovirus Genotype Profiles Associated with Foodborne Transmission, 1999–2012 - Volume 21, Number 4—April 2015 - Emerging Infectious Disease journal - CDC
Volume 21, Number 4—April 2015
Norovirus Genotype Profiles Associated with Foodborne Transmission, 1999–2012
Noroviruses are a leading cause of gastroenteritis worldwide. They belong to the family Caliciviridae and consist of an ≈7.5-kb genome in 3 open reading frames (ORFs). The first ORF (ORF1) encodes a polypeptide; ORF2 encodes the viral capsid protein (VP1); and ORF3 encodes a minor structural protein (VP2). Noroviruses are classified into at least 6 genogroups, GI–GVI (1). According to a recent unified proposal for nomenclature, genogroups are further subdivided into at least 38 genetic clusters (genotypes) (2). Noroviruses are environmentally stable (3) and can be transmitted by different routes (e.g., foodborne, personborne, waterborne, and environmental). Determining the transmission route during an outbreak investigation is complicated because transmission can occur by multiple routes in a single outbreak. After primary introduction of the virus through food, secondary person-to-person and environmental transmission can rapidly take over, making it hard to trace the disease back to contaminated food. Another complexity is that foodborne transmission can follow different routes as well; food can be contaminated during production (4) or during handling by an infected food handler (5).
Different exposure attribution methods (i.e., epidemiologic investigations, microbiological typing/subtyping, intervention studies, and expert elicitations) have been used to estimate the foodborne proportion of the overall disease incidence caused by a pathogen. Each approach has its advantages and disadvantages, and therefore the use of multiple methods has been recommended (6). Information about pathogen strain or subtypes may be of value for attribution but is dependent on substantial amounts of contextual data. For example, a method commonly used to attribute Salmonella spp. infections to a specific source uses strain collections representative of the pathogen in each of these sources (7).
For noroviruses, genogroup-specific differences have been reported with regard to environmental persistence (8), sensitivity to removal (9), and binding to receptors (10). These biological differences may underpin strain-specific epidemiologic patterns, suggesting a potentially useful approach for norovirus attribution. Such an approach was recently developed in a norovirus attribution study, which showed that the proportion of foodborne and person-to-person outbreaks differed between genotypes; the GI genotypes were more likely to be foodborne, and the II.4 genotype was more likely to be personborne (11). These findings indicate that genotype profiles may help distinguish which outbreaks are more likely to be foodborne than personborne. Also, a recent study on norovirus outbreaks in the United States showed that GI.3, GI.6, GI.7, GII.3, GII.6, and GII.12 were the norovirus genotypes most often associated with foodborne outbreaks and that, of the outbreaks with a known transmission route, 16% were foodborne (12). Norovirus infections, however, are a global problem, and efforts are under way to estimate the global social and economic costs of foodborne norovirus illness (13,14). To estimate the proportion of outbreaks attributed to foodborne transmission from a global perspective, we used aggregated norovirus outbreak data and genotyping information from different outbreak surveillance systems and from peer-reviewed literature.
Dr. Verhoef is an epidemiologist in the Center of Infectious Disease Control of the National Institute for Public Health and the Environment. Her work focuses on the epidemiology and surveillance of infectious diseases, particularly on the use of molecular typing information to facilitate source tracing activities.
We thank the World Health Organization's Foodborne Disease Burden Epidemiology Reference Group for financial support and critical review of this study, and we thank the FBVE and Noronet networks for collecting and sharing sequences.
The New Zealand Ministry of Health funded the work conducted by the ESR. This study was commissioned and paid for in part by the Foodborne Disease Burden Epidemiology Reference Group of the World Health Organization, the New Zealand Ministry of Health, and by the Government of the Netherlands on behalf of the Foodborne Disease Burden Epidemiology Reference Group.
- Fields BN, Knipe DM, Howley PM. Fields virology. 6th ed. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins Health; 2013.
- Kroneman A, Vega E, Vennema H, Vinje J, White PA, Hansman G, Proposal for a unified norovirus nomenclature and genotyping. Arch Virol.2013;158:2059–68. DOIPubMed
- Cannon JL, Papafragkou E, Park GW, Osborne J, Jaykus LA, Vinje J. Surrogates for the study of norovirus stability and inactivation in the environment: a comparison of murine norovirus and feline calicivirus. J Food Prot. 2006;69:2761–5 .PubMed
- Lees D. Viruses and bivalve shellfish. Int J Food Microbiol. 2000;59:81–116. DOIPubMed
- Thornley CN, Hewitt J, Perumal L, Van Gessel SM, Wong J, David SA, Multiple outbreaks of a novel norovirus GII.4 linked to an infected post-symptomatic food handler. Epidemiol Infect. 2013;141:1585–97. DOIPubMed
- Pires SM. Assessing the applicability of currently available methods for attributing foodborne disease to sources, including food and food commodities. Foodborne Pathog Dis. 2013;10:206–13. DOIPubMed
- Hald T, Vose D, Wegener HC, Koupeev T. A Bayesian approach to quantify the contribution of animal-food sources to human salmonellosis. Risk Anal. 2004;24:255–69. DOIPubMed
- Gentry J, Vinje J, Guadagnoli D, Lipp EK. Norovirus distribution within an estuarine environment. Appl Environ Microbiol. 2009;75:5474–80.DOIPubMed
- Tuladhar E, Hazeleger WC, Koopmans M, Zwietering MH, Beumer RR, Duizer E. Residual viral and bacterial contamination of surfaces after cleaning and disinfection. Appl Environ Microbiol. 2012;78:7769–75 . DOIPubMed
- Maalouf H, Zakhour M, Le Pendu J, Le Saux JC, Atmar RL, Le Guyader FS. Distribution in tissue and seasonal variation of norovirus genogroup I and II ligands in oysters. Appl Environ Microbiol. 2010;76:5621–30 . DOIPubMed
- Verhoef L, Vennema H, van Pelt W, Lees D, Boshuizen H, Henshilwood K, Use of norovirus genotype profiles to differentiate origins of foodborne outbreaks. Emerg Infect Dis. 2010;16:617–24. DOIPubMed
- Vega E, Barclay L, Gregoricus N, Shirley SH, Lee D, Vinje J. Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013. J Clin Microbiol. 2014;52:147–55. DOIPubMed
- Siebenga JJ, Vennema H, Zheng DP, Vinje J, Lee BE, Pang XL, Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001–2007. J Infect Dis. 2009;200:802–12. DOIPubMed
- Stein C, Kuchenmuller T, Hendrickx S, Pruss-Ustun A, Wolfson L, Engels D, The Global Burden of Disease assessments–WHO is responsible? PLoS Negl Trop Dis. 2007;1:e161. DOIPubMed
- Kroneman A, Harris J, Vennema H, Duizer E, van Duynhoven Y, Gray J, Data quality of 5 years of central norovirus outbreak reporting in the European Network for food-borne viruses. J Public Health (Oxf). 2008;30:82–90. DOIPubMed
- Vega E, Barclay L, Gregoricus N, Williams K, Lee D, Vinje J. Novel surveillance network for norovirus gastroenteritis outbreaks, United States. Emerg Infect Dis. 2011;17:1389–95 .PubMed
- Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol. 2003;41:1548–57. DOIPubMed
- Greening GE, Hewitt J, Rivera-Aban M, Croucher D. Molecular epidemiology of norovirus gastroenteritis outbreaks in New Zealand from 2002–2009. J Med Virol. 2012;84:1449–58. DOIPubMed
- Matthews JE, Dickey BW, Miller RD, Felzer JR, Dawson BP, Lee AS, The epidemiology of published norovirus outbreaks: a review of risk factors associated with attack rate and genogroup. Epidemiol Infect. 2012;140:1161–72. DOIPubMed
- Brown LD, Cai TT, DasGupta A. Interval estimation for a binomial proportion. Stat Sci. 2001;16:101–33. DOI
- Lindesmith LC, Beltramello M, Donaldson EF, Corti D, Swanstrom J, Debbink K, Immunogenetic mechanisms driving norovirus GII.4 antigenic variation. PLoS Pathog. 2012;8:e1002705. DOIPubMed
- Verhoef L, Depoortere E, Boxman I, Duizer E, van Duynhoven Y, Harris J, Emergence of new norovirus variants on spring cruise ships and prediction of winter epidemics. Emerg Infect Dis. 2008;14:238–43. DOIPubMed
- Bernard H, Hohne M, Niendorf S, Altmann D, Stark K. Epidemiology of norovirus gastroenteritis in Germany 2001–2009: eight seasons of routine surveillance. Epidemiol Infect. 2014;142:63–74.PubMed
- Lopman BA, Adak GK, Reacher MH, Brown DW. Two epidemiologic patterns of norovirus outbreaks: surveillance in England and Wales, 1992–2000.Emerg Infect Dis. 2003;9:71–7. DOIPubMed
- Gallimore CI, Pipkin C, Shrimpton H, Green AD, Pickford Y, McCartney C, Detection of multiple enteric virus strains within a foodborne outbreak of gastroenteritis: an indication of the source of contamination. Epidemiol Infect. 2005;133:41–7 . DOIPubMed
- O'Brien SJ, Gillespie IA, Sivanesan MA, Elson R, Hughes C, Adak GK. Publication bias in foodborne outbreaks of infectious intestinal disease and its implications for evidence-based food policy. England and Wales 1992–2003. Epidemiol Infect. 2006;134:667–74. DOIPubMed
- Kroneman A, Verhoef L, Harris J, Vennema H, Duizer E, van Duynhoven Y, Analysis of integrated virological and epidemiological reports of norovirus outbreaks collected within the Foodborne Viruses in Europe network from 1 July 2001 to 30 June 2006. J Clin Microbiol. 2008;46:2959–65.DOIPubMed
- Verhoef LP, Kroneman A, Van Duijnhoven Y, Boshuizen H, van Pelt W, Koopmans M. Selection tool for foodborne norovirus outbreaks. Emerg Infect Dis. 2009;15:31–8. DOIPubMed
- Rondy M, Koopmans M, Rotsaert C, Van Loon T, Beljaars B, Van Dijk G, Norovirus disease associated with excess mortality and use of statins: a retrospective cohort study of an outbreak following a pilgrimage to Lourdes. Epidemiol Infect. 2011;139:453–63. DOIPubMed
- Sukhrie FH, Beersma MF, Wong A, van der Veer B, Vennema H, Bogerman J, Using molecular epidemiology to trace transmission of nosocomial norovirus infection. J Clin Microbiol. 2011;49:602–6. DOIPubMed
- Symes SJ, Gunesekere IC, Marshall JA, Wright PJ. Norovirus mixed infection in an oyster-associated outbreak: an opportunity for recombination.Arch Virol. 2007;152:1075–86. DOIPubMed
- van Beek J, Ambert-Balay K, Botteldoorn N, Eden JS, Fonager J, Hewitt J, Indications for worldwide increased norovirus activity associated with emergence of a new variant of genotype II.4, late 2012. Euro Surveill. 2013;18:8–9 .PubMed
- Eden JS, Tanaka MM, Boni MF, Rawlinson WD, White PA. Recombination within the pandemic norovirus GII.4 lineage. J Virol. 2013;87:6270–82.DOIPubMed
- Fonager J, Barzinci S, Fischer TK. Emergence of a new recombinant Sydney 2012 norovirus variant in Denmark, 26 December 2012 to 22 March 2013. Euro Surveill. 2013;18:••• .PubMed
- Havelaar AH, Galindo AV, Kurowicka D, Cooke RM. Attribution of foodborne pathogens using structured expert elicitation. Foodborne Pathog Dis.2008;5:649–59. DOIPubMed
- Adak GK, Long SM, O'Brien SJ. Trends in indigenous foodborne disease and deaths, England and Wales: 1992 to 2000. Gut. 2002;51:832–41.DOIPubMed
- Tam CC, Rodrigues LC, Viviani L, Dodds JP, Evans MR, Hunter PR, Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut. 2012;61:69–77 . DOIPubMed
- Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD, Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14:725–30. DOIPubMed
Suggested citation for this article: Verhoef L, Hewitt J, Barclay L, Ahmed S, Lake R, Hall AJ, et al. Norovirus genotype profiles associated with foodborne transmission, 1999–2012. Emerg Infect Dis. 2015 Apr [date cited]. http://dx.doi.org/10.3201/eid2104.141073
1These authors contributed equally to this article.
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