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Epidemiology of Viral Foodborne Outbreaks: Role of Food Handlers, Irrigation Water, and Surfaces

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Viruses in Foods

Part of the book series: Food Microbiology and Food Safety ((RESDEV))

Abstract

Norovirus represents a considerable conundrum; although it is the leading cause of foodborne illness in the United States and other developed countries, most norovirus outbreaks are not attributable to food. The virus has a low infectious dose, is environmentally stable, and has a high degree of resistance to commercial sanitizers and disinfectants. Molecular characterization and sequencing of viruses associated with outbreaks has done much to deepen our understanding of the underlying epidemiology of norovirus. Foodborne norovirus outbreaks may be initiated from infected food handlers, contaminated foods, or contaminated environmental surfaces, in decreasing order of importance. Controlling foodborne norovirus requires a multifaceted approach.

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References

  • Anderson AD, Garrett VD, Sobel J, Monroe SS, Fankhauser RL, Schwab KJ, Bresee JS, Mead PS, Higgins C, Campana J, Glass RI, Outbreak Investigation Team (2001) Multistate outbreak of Norwalk-like virus gastroenteritis associated with a common caterer. Am J Epidemiol 154(11):1013–1019

    Article  CAS  PubMed  Google Scholar 

  • Baert L, Mattison K, Loisy-Hamon F, Harlow J, Martyres A, Lebeau B, Stals A, Van Coillie E, Herman L, Uyttendaele M (2011) Review: norovirus prevalence in Belgian, Canadian and French fresh produce: a threat to human health? Int J Food Microbiol 151(3):261–269

    Article  CAS  PubMed  Google Scholar 

  • Bidawid S, Malik N, Adegbunrin O, Sattar SA, Farber JM (2004) Norovirus cross-contamination during food handling and interruption of virus transfer by hand antisepsis: experiments with feline calicivirus as a surrogate. J Food Prot 67(1):103–109

    CAS  PubMed  Google Scholar 

  • Borchardt MA, Bradbury KR, Alexander EC Jr, Kolberg RJ, Alexander SC, Archer JR, Braatz LA, Forest BM, Green JA, Spencer SK (2011) Norovirus outbreak caused by a new septic system in a dolomite aquifer. Ground Water 49(1):85–97

    Article  CAS  PubMed  Google Scholar 

  • Boxman I, Dijkman R, Verhoef L, Maat A, van Dijk G, Vennema H, Koopmans M (2008) Norovirus on swabs taken from hands illustrate route of transmission: a case study. J Food Prot 72(8):1753–1755

    Google Scholar 

  • Boxman IL, Verhoef L, Dijkman R, Hägele G, Te Loeke NA, Koopmans M (2011) Year-round prevalence of norovirus in the environment of catering companies without a recently reported outbreak of gastroenteritis. Appl Environ Microbiol 77(9):2968–2974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brassard J, Gagné MJ, Généreux M, Côté C (2012) Detection of human food-borne and zoonotic viruses on irrigated, field-grown strawberries. Appl Environ Microbiol 78(10):3763–3766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Centers for Disease Control and Prevention (2011) Updated norovirus outbreak management and disease prevention guidelines. MMWR Recomm Rep 60(RR-3):1–18

    Google Scholar 

  • Centers for Disease Control and Prevention (CDC) (2007) Norovirus outbreak associated with ill food-service workers--Michigan, January-February 2006. MMWR Morb Mortal Wkly Rep 56(46):1212–1216

    Google Scholar 

  • Chancellor DD, Tyagi S, Bazaco MC, Bacvinskas S, Chancellor MB, Dato VM, de Miguel F (2006) Green onions: potential mechanism for hepatitis A contamination. J Food Prot 69(6):1468–1472

    PubMed  Google Scholar 

  • D’Souza DH, Sair A, Williams K, Papafragkou E, Jean J, Moore C, Jaykus L (2006) Persistence of caliciviruses on environmental surfaces and their transfer to food. Int J Food Microbiol 108(1):84–91

    Article  PubMed  Google Scholar 

  • Deneen VC, Hunt JM, Paule CR, James RI, Johnson RG, Raymond MJ, Hedberg CW (2000) The impact of foodborne calicivirus disease: the Minnesota experience. J Infect Dis 181(Suppl 2):S281–S283

    Article  PubMed  Google Scholar 

  • El-Senousy WM, Costafreda MI, Pintó RM, Bosch A (2013) Method validation for norovirus detection in naturally contaminated irrigation water and fresh produce. Int J Food Microbiol 167(1):74–79

    Article  CAS  PubMed  Google Scholar 

  • Escudero BI, Rawsthorne H, Gensel C, Jaykus LA (2012) Persistence and transferability of noroviruses on and between common surfaces and foods. J Food Prot 75(5):927–935

    Article  CAS  PubMed  Google Scholar 

  • Ethelberg S, Lisby M, Bottiger B, Schultz AC, Villif A, Jensen T, Olsen KE, Scheutz F, Kjelso C, Muller L (2010) Outbreaks of gastroenteritis linked to lettuce, Denmark, January 2010. Euro Surveill 15(6):19484

    PubMed  Google Scholar 

  • Falkenhorst G, Krusell L, Lisby M, Madsen SB, Böttiger B, Mølbak K (2005) Imported frozen raspberries cause a series of norovirus outbreaks in Denmark, 2005. Euro Surveill 10(9), E050922.2

    PubMed  Google Scholar 

  • Fiore AE (2004) Hepatitis A transmitted by food. Clin Infect Dis 38(5):705–715

    Article  PubMed  Google Scholar 

  • Franck KT, Lisby M, Fonager J, Schultz AC, Böttiger B, Villif A, Absalonsen H, Ethelberg S (2015) Sources of calicivirus contamination in foodborne outbreaks in Denmark, 2005-2011-the role of the asymptomatic food handler. J Infect Dis 211(4):563–570

    Article  PubMed  Google Scholar 

  • Gallay A, De Valk H, Cournot M, Ladeuil B, Hemery C, Castor C, Bon F, Mégraud F, Le Cann P, Desenclos JC, Outbreak Investigation Team (2006) A large multi-pathogen waterborne community outbreak linked to fecal contamination of a groundwater system, France, 2000. Clin Microbiol Infect 12(6):561–570

    Article  CAS  PubMed  Google Scholar 

  • Gelting R, Sarisky J, Selman C, Otto C, Higgins C, Bohan PO, Buchanan SB, Meehan PJ (2005) Use of a systems-based approach to an environmental health assessment for a waterborne disease outbreak investigation at a snowmobile lodge in Wyoming. Int J Hyg Environ Health 208(1–2):67–73

    Article  PubMed  Google Scholar 

  • Gould LH, Walsh KA, Vieira AR, Herman K, Williams IT, Hall AJ, Cole D, Centers for Disease Control and Prevention (2013) Surveillance for foodborne disease outbreaks - United States, 1998-2008. MMWR Surveill Summ 62(2):1–34

    PubMed  Google Scholar 

  • Grove SF, Suriyanarayanan A, Puli B, Zhao H, Li M, Li D, Schaffner DW, Lee A (2015) Norovirus cross-contamination during preparation of fresh produce. Int J Food Microbiol 198C:43–49

    Article  Google Scholar 

  • Hall AJ, Eisenbart VG, Etingüe AL, Gould LH, Lopman BA, Parashar UD (2012) Epidemiology of foodborne norovirus outbreaks, United States, 2001-2008. Emerg Infect Dis 18(10):1566–1573

    Article  PubMed  PubMed Central  Google Scholar 

  • Hall AJ, Wikswo ME, Manikonda K, Roberts VA, Yoder JS, Gould LH (2013) Acute gastroenteritis surveillance through the National Outbreak Reporting System, United States. Emerg Infect Dis 19(8):1305–1309

    Article  PubMed  PubMed Central  Google Scholar 

  • Hall AJ, Wikswo ME, Pringle K, Gould LH, Parashar UD, National Center for Immunization and Respiratory Diseases, CDC (2014) Vital signs: foodborne norovirus outbreaks - United States, 2009-2012. MMWR Morb Mortal Wkly Rep 63(22):491–495

    PubMed  Google Scholar 

  • Hedberg CW, Palazzi-Churas KL, Radke VJ, Selman CA, Tauxe RV (2008) The use of clinical profiles in the investigation of foodborne outbreaks in restaurants: United States, 1982-1997. Epidemiol Infect 136(1):65–72

    Article  CAS  PubMed  Google Scholar 

  • Hirneisen KA, Kniel KE (2013) Comparative uptake of enteric viruses into spinach and green onions. Food Environ Virol 5(1):24–34

    Article  PubMed  Google Scholar 

  • Kokkinos P, Kozyra I, Lazic S, Bouwknegt M, Rutjes S, Willems K, Moloney R, de Roda Husman AM, Kaupke A, Legaki E, D’Agostino M, Cook N, Rzeżutka A, Petrovic T, Vantarakis A (2012) Harmonized investigation of the occurrence of human enteric viruses in the leafy green vegetable supply chain in three European countries. Food Environ Virol 4(4):179–191

    Article  CAS  PubMed  Google Scholar 

  • Kroneman A, Verhoef L, Harris J, Vennema H, Duizer E, van Duynhoven Y, Gray J, Iturriza M, Böttiger B, Falkenhorst G, Johnsen C, von Bonsdorff CH, Maunula L, Kuusi M, Pothier P, Gallay A, Schreier E, Höhne M, Koch J, Szücs G, Reuter G, Krisztalovics K, Lynch M, McKeown P, Foley B, Coughlan S, Ruggeri FM, Di Bartolo I, Vainio K, Isakbaeva E, Poljsak-Prijatelj M, Grom AH, Leshem E, Barclay L, Wikswo M, Vega E, Gregoricus N, Parashar UD, Vinjé J, Hall AJ (2013) Genotype GI.6 norovirus, United States, 2010-2012. Emerg Infect Dis 19(8):1317–1320

    Article  Google Scholar 

  • Li J, Smith K, Kaehler D, Everstine K, Rounds J, Hedberg C (2010) Evaluation of a statewide foodborne illness complaint surveillance system in Minnesota, 2000 through 2006. J Food Prot 73(11):2059–2064

    PubMed  Google Scholar 

  • Lopman B, Gastañaduy P, Park GW, Hall AJ, Parashar UD, Vinjé J (2012) Environmental transmission of norovirus gastroenteritis. Curr Opin Virol 2(1):96–102

    Article  PubMed  Google Scholar 

  • Lysén M, Thorhagen M, Brytting M, Hjertqvist M, Andersson Y, Hedlund KO (2009) Genetic diversity among food-borne and waterborne norovirus strains causing outbreaks in Sweden. J Clin Microbiol 47(8):2411–2418

    Article  PubMed  PubMed Central  Google Scholar 

  • Mäde D, Trübner K, Neubert E, Höhne M, Johne R (2013) Detection and typing of norovirus from frozen strawberries involved in a large-scale gastroenteritis outbreak in Germany. Food Environ Virol 5(3):162–168

    Article  PubMed Central  Google Scholar 

  • Mathijs E, Stals A, Baert L, Botteldoorn N, Denayer S, Mauroy A, Scipioni A, Daube G, Dierick K, Herman L, Van Coillie E, Uyttendaele M, Thiry E (2012) A review of known and hypothetical transmission routes for noroviruses. Food Environ Virol 4(4):131–152

    Article  PubMed  Google Scholar 

  • Mattison K, Harlow J, Morton V, Cook A, Pollari F, Bidawid S, Farber JM (2010) Enteric viruses in ready-to-eat packaged leafy greens. Emerg Infect Dis 16(11):1815–1817

    Article  PubMed  PubMed Central  Google Scholar 

  • Maunula L, Roivainen M, Keränen M, Mäkela S, Söderberg K, Summa M, von Bonsdorff CH, Lappalainen M, Korhonen T, Kuusi M, Niskanen T (2009) Detection of human norovirus from frozen raspberries in a cluster of gastroenteritis outbreaks. Euro Surveill 14(49):19435

    PubMed  Google Scholar 

  • Maunula L, Kaupke A, Vasickova P, Söderberg K, Kozyra I, Lazic S, van der Poel WH, Bouwknegt M, Rutjes S, Willems KA, Moloney R, D’Agostino M, de Roda Husman AM, von Bonsdorff CH, Rzeżutka A, Pavlik I, Petrovic T, Cook N (2013) Tracing enteric viruses in the European berry fruit supply chain. Int J Food Microbiol 167(2):177–185

    Article  PubMed  Google Scholar 

  • Medus C, Smith KE, Bender JB, Besser JM, Hedberg CW (2006) Salmonella outbreaks in restaurants in Minnesota, 1995 through 2003: evaluation of the role of infected food workers. J Food Prot 69(8):1870–1878

    PubMed  Google Scholar 

  • Mijovski JZ, Bosch A, Buesa J, Fauquier AS, Hernandéz-Pezzi G, Hedlund KO, Koopmans M (2008) 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 46(9):2959–2965

    Article  PubMed  PubMed Central  Google Scholar 

  • Müller L, Schultz AC, Fonager J, Jensen T, Lisby M, Hindsdal K, Krusell L, Eshøj A, Møller LT, Porsbo LJ, Böttiger BE, Kuhn K, Engberg J, Ethelberg S (2014) Separate norovirus outbreaks linked to one source of imported frozen raspberries by molecular analysis, Denmark, 2010-2011. Epidemiol Infect 22:1–9

    Google Scholar 

  • Naimi TS, Wicklund JH, Olsen SJ, Krause G, Wells JG, Bartkus JM, Boxrud DJ, Sullivan M, Kassenborg H, Besser JM, Mintz ED, Osterholm MT, Hedberg CW (2003) Concurrent outbreaks of Shigella sonnei and enterotoxigenic Escherichia coli infections associated with parsley: implications for surveillance and control of foodborne illness. J Food Prot 66(4):535–541

    PubMed  Google Scholar 

  • National Restaurant Association (2015) Facts at a glance. http://www.restaurant.org/News-Research/Research/Facts-at-a-Glance. Accessed 15 February 2015

  • Nicolay N, McDermott R, Kelly M, Gorby M, Prendergast T, Tuite G, Coughlan S, McKeown P, Sayers G (2011) Potential role of asymptomatic kitchen food handlers during a food-borne outbreak of norovirus infection, Dublin, Ireland, March 2009. Euro Surveill 16(30):19931

    PubMed  Google Scholar 

  • Olsen SJ, MacKinnon LC, Goulding JS, Bean NH, Slutsker L (2000) Surveillance for foodborne-disease outbreaks--United States, 1993-1997. MMWR CDC Surveill Summ 49(1):1–62

    CAS  PubMed  Google Scholar 

  • Ozawa K, Oka T, Takeda N, Hansman GS (2007) Norovirus infections in symptomatic and asymptomatic food handlers in Japan. J Clin Microbiol 45(12):3996–4005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parashar UD, Dow L, Fankhauser RL, Humphrey CD, Miller J, Ando T, Williams KS, Eddy CR, Noel JS, Ingram T, Bresee JS, Monroe SS, Glass RI (1998) An outbreak of viral gastroenteritis associated with consumption of sandwiches: implications for the control of transmission by food handlers. Epidemiol Infect 121(3):615–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrignani M, Verhoef L, Vennema H, van Hunen R, Baas D, van Steenbergen JE, Koopmans MP (2014) Underdiagnosis of foodborne hepatitis A, The Netherlands, 2008-2010. Emerg Infect Dis 20(4):596–602

    Article  PubMed  PubMed Central  Google Scholar 

  • Petrignani M, van Beek J, Borsboom G, Richardus JH, Koopmans M (2015) Norovirus introduction routes into nursing homes and risk factors for spread: a systematic review and meta-analysis of observational studies. J Hosp Infect 89(3):163–178

    Article  CAS  PubMed  Google Scholar 

  • Repp KK, Keene WE (2012) A point-source norovirus outbreak caused by exposure to fomites. J Infect Dis 205(11):1639–1641

    Article  PubMed  PubMed Central  Google Scholar 

  • Repp KK, Hostetler TP, Keene WE (2013) A norovirus outbreak related to contaminated surfaces. J Infect Dis 208(2):295–298

    Article  CAS  PubMed  Google Scholar 

  • Rönnqvist M, Aho E, Mikkelä A, Ranta J, Tuominen P, Rättö M, Maunula L (2014) Norovirus transmission between hands, gloves, utensils, and fresh produce during simulated food handling. Appl Environ Microbiol 80(17):5403–5410

    Article  PubMed  PubMed Central  Google Scholar 

  • Sarvikivi E, Roivainen M, Maunula L, Niskanen T, Korhonen T, Lappalainen M, Kuusi M (2012) Multiple norovirus outbreaks linked to imported frozen raspberries. Epidemiol Infect 140(2):260–267

    Article  CAS  PubMed  Google Scholar 

  • Saupe AA, Kaehler D, Cebelinski EA, Nefzger B, Hall AJ, Smith KE (2013) Norovirus surveillance among callers to foodborne illness complaint hotline, Minnesota, USA, 2011-2013. Emerg Infect Dis 19(8):1293–1296

    Article  PubMed  PubMed Central  Google Scholar 

  • Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis 17(1):7–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharps CP, Kotwal G, Cannon JL (2012) Human norovirus transfer to stainless steel and small fruits during handling. J Food Prot 75(8):1437–1446

    Article  PubMed  Google Scholar 

  • Shieh YC, Tortorello ML, Fleischman GJ, Li D, Schaffner DW (2014) Tracking and modeling norovirus transmission during mechanical slicing of globe tomatoes. Int J Food Microbiol 180:13–18

    Article  PubMed  Google Scholar 

  • Steele M, Odumeru J (2004) Irrigation water as source of foodborne pathogens on fruit and vegetables. J Food Prot 67(12):2839–2849

    PubMed  Google Scholar 

  • Sumner S, Brown LG, Frick R, Stone C, Carpenter LR, Bushnell L, Nicholas D, Mack J, Blade H, Tobin-D’Angelo M, Everstine K, Environmental Health Specialists Network Working Group (2011) Factors associated with food workers working while experiencing vomiting or diarrhea. J Food Prot 74(2):215–220

    Article  PubMed  Google Scholar 

  • Turcios RM, Widdowson MA, Sulka AC, Mead PS, Glass RI (2006) Reevaluation of epidemiological criteria for identifying outbreaks of acute gastroenteritis due to norovirus: United States, 1998-2000. Clin Infect Dis 42(7):964–969

    Article  PubMed  Google Scholar 

  • Vega E, Barclay L, Gregoricus N, Shirley SH, Lee D, Vinjé J (2014) Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013. J Clin Microbiol 52(1):147–155

    Article  PubMed  PubMed Central  Google Scholar 

  • Verhaelen K, Bouwknegt M, Rutjes SA, de Roda Husman AM (2013) Persistence of human norovirus in reconstituted pesticides--pesticide application as a possible source of viruses in fresh produce chains. Int J Food Microbiol 160(3):323–328

    Article  CAS  PubMed  Google Scholar 

  • Verhoef L, Vennema H, van Pelt W, Lees D, Boshuizen H, Henshilwood K, Koopmans M, Food-Borne Viruses in Europe Network (2010) Use of norovirus genotype profiles to differentiate origins of foodborne outbreaks. Emerg Infect Dis 16(4):617–624

    Article  PubMed  PubMed Central  Google Scholar 

  • Verhoef L, Kouyos RD, Vennema H, Kroneman A, Siebenga J, van Pelt W, Koopmans M, Foodborne Viruses in Europe Network (2011) An integrated approach to identifying international foodborne norovirus outbreaks. Emerg Infect Dis 17(3):412–418

    Article  PubMed  PubMed Central  Google Scholar 

  • White KE, Osterholm MT, Mariotti JA, Korlath JA, Lawrence DH, Ristinen TL, Greenberg HB (1986) A foodborne outbreak of Norwalk virus gastroenteritis. Evidence for post-recovery transmission. Am J Epidemiol 124(1):120–126

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Division of Environmental Health Sciences, University of Minnesota, 1214 Mayo Building, MMC 8807, 420 Delaware Street SE, Minneapolis, MN, 55455, USA

    Craig Hedberg

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  1. Craig Hedberg
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Editors and Affiliations

  1. University of Minnesota, St. Paul, Minnesota, USA

    Sagar M. Goyal

  2. University of Georgia, Griffin, Georgia, USA

    Jennifer L. Cannon

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Hedberg, C. (2016). Epidemiology of Viral Foodborne Outbreaks: Role of Food Handlers, Irrigation Water, and Surfaces. In: Goyal, S., Cannon, J. (eds) Viruses in Foods. Food Microbiology and Food Safety(). Springer, Cham. https://doi.org/10.1007/978-3-319-30723-7_5

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