Reported behavior, knowledge and awareness toward the potential for norovirus transmission by food handlers in Dutch catering companies and institutional settings in relation to the prevalence of norovirus

Food Control

Volumn 34, Issue 2, 2013, Pages 420-427

  Verhoef, Linda ^a   Jaramillo Gutierrez, Giovanna ^a,b   Koopmans, Marion ^a,c   Boxman, Ingeborg L A ^d  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b EUROPEAN CENTRE FOR DISEASE PREVENTION AND CONTROL ECDC   (Sweden)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d Voedsel en Waren Autoriteit Netherlands   (Netherlands)

Author keywords

Environmental samples; Environmental swabs; Food safety knowledge; Foodborne; Questionnaires

Indexed keywords

NOROVIRUS;

EID: 84878891300     PISSN: 09567135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodcont.2013.05.015     Document Type: Article

References (33)

1. Bidawid S., Malik N., Adegbunrin O., Sattar S.A., Farber J.M. Norovirus cross-contamination during food handling and interruption of virus transfer by hand antisepsis: experiments with feline calicivirus as a surrogate. Journal of Food Protection 2004, 67(1):103-109.
2. Boxman I.L. Viral contamination by food handlers and recommended procedural controls. Viruses in food and water: Risks, surveillance and control 2013, 217-236. Woodhead Publishing Ltd. N. Cook (Ed.).
3. Boxman I.L., Verhoef L., Dijkman R., Hägele G., Te Loeke N.A., Koopmans M. Year-round prevalence of norovirus in the environment of catering companies without a recently reported outbreak of gastroenteritis. Applied and Environmental Microbiology 2011, 77(9):2968-2974.
4. de Wit M.A., Koopmans M.P., Kortbeek L.M., van Leeuwen N.J., Vinjé J., van Duynhoven Y.T. Etiology of gastroenteritis in sentinel general practices in the Netherlands. Clinical Infectious Diseases 2001, 33(3):280-288.
5. EFSA [European Food Safety Authority] Scientific opinion on an update on the present knowledge on the occurrence and control of foodborne viruses. EFSA Journal 2011, 9(2190):96. Available from, Accessed 17.02.12. http://www.efsa.europa.eu/en/efsajournal/doc/2190.pdf, 10.2903/j.efsa.2011.2190.
6. Egan M.B., Raats M.M., Grubb S.M., Eves A., Lumbers M.L., Dean M.S., et al. Areview of food safety and food hygiene training studies in the commercial sector. Food Control 2007, 18:180-190. 10.1016/j.foodcont.2006.08.001.
7. FAO/WHO [Food and Agriculture Organization of the United Nations/World Health Organization] Viruses in food: Scientific advice to support risk management activities: meeting report 2008, Microbiological Risk Assessment Series, No. 13. Available from, Accessed 17.02.12. http://www.who.int/foodsafety/publications/micro/mra13/en/index.html.
8. FAO/WHO [Food and Agriculture Organization of the United Nations/World Health Organization] Proposed draft guidelines on the application of general principles of food hygiene to the control of viruses in food 2012, CAC/GL-79-2012. REP12/FH. Appendix III. Available from, Accessed 27.02.12. http://www.codexalimentarius.org/meetings-reports/en/.
9. FDA [Food and Drug Administration] National Retail Food Team FDA report on the occurrence of foodborne illness risk factors in selected institutional foodservice, restaurant, and retail food store facility types 2009, Available from, Accessed 17.02.12. http://www.fda.gov/downloads/Food/FoodSafety/RetailFoodProtection/FoodborneIllnessandRiskFactorReduction/RetailFoodRiskFactorStudies/UCM224682.pdf.
10. Goodman E.R., Platt R., Bass R., Onderdonk A.B., Yokoe D.S., Huang S.S. Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms. Infection Control and Hospital Epidemiology 2008, 29(7):593-599.
11. Green L.R., Radke V., Mason R., Bushnell L., Reimann D.W., Mack J.C., et al. Factors related to food worker hand hygiene practices. Journal of Food Protection 2007, 70(3):661-666.
12. Green L., Selman C., Banerjee A., Marcus R., Medus C., Angulo F.J., et al. Food service workers' self-reported food preparation practices: an EHS-Net study. International Journal of Hygiene and Environmental Health 2005, 208(1-2):27-35.
13. Hedberg C.W., Smith S.J., Kirkland E., Radke V., Jones T.F., Selman C.A. Systematic environmental evaluations to identify food safety differences between outbreak and nonoutbreak restaurants. Journal of Food Protection 2006, 69(11):2697-2702.
14. Kassa H., Silverman G.S., Baroudi K. Effect of a manager training and certification program on food safety and hygiene in food service operations. Environmental Health Insights 2010, 4:13-20. 10.4137/EHI.S4717.
15. Koopmans M., von Bonsdorff C.H., Vinjé J., de Medici D., Monroe S. Foodborne viruses. FEMS Microbiol Review 2002, 26(2):187-205.
16. Kroneman A., Verhoef L., Harris J., Vennema H., Duizer E., van Duynhoven Y., et al. 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. Journal of Clinical Microbiology 2008, 46(9):2959-2965.
17. Lopman B., Vennema H., Kohli E., Pothier P., Sanchez A., Negredo A., et al. Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet 2004, 363(9410):682-688.
18. Matlow A.G., Wray R., Richardson S.E. Attitudes and beliefs, not just knowledge, influence the effectiveness of environmental cleaning by environmental service workers. American Journal of Infection Control 2012, 40(3):260-262. [Epub 2011 Jul 13].
19. Meakins S.M., Adak G.K., Lopman B.A., O'Brien S.J. General outbreaks of infectious intestinal disease (IID) in hospitals, England and Wales, 1992-2000. Journal Hospital Infection 2003, 53(1):1-5.
20. Okabayashi T., Yokota S., Ohkoshi Y., Ohuchi H., Yoshida Y., Kikuchi M., et al. Occurrence of norovirus infections unrelated to norovirus outbreaks in an asymptomatic food handler population. Journal of Clinical Microbiology 2008, 46(6):1985-1988.
21. Ozawa K., Oka T., Takeda N., Hansman G.S. Norovirus infections in symptomatic and asymptomatic food handlers in Japan. Journal of Clinical Microbiology 2007, 45(12):3996-4005.
22. Phillips G., Tam C.C., Rodrigues L.C., Lopman B. Prevalence and characteristics of asymptomatic norovirus infection in the community in England. Epidemiology and Infection 2010, 138(10):1454-1458. [Epub 2010 Mar 3].
23. Pragle A.S., Harding A.K., Mack J.C. Food workers' perspectives on handwashing behaviors and barriers in the restaurant environment. Journal of Environmental Health 2007, 69(10):27-32.
24. Rockx B., De Wit M., Vennema H., Vinjé J., De Bruin E., Van Duynhoven Y., et al. Natural history of human calicivirus infection: a prospective cohort study. Clinical Infectious Diseases 2002, 35(3):246-253.
25. Schweon S.J., Edmonds S.L., Kirk J., Rowland D.Y., Acosta C. Effectiveness of a comprehensive hand hygiene program for reduction of infection rates in a long-term care facility. American Journal of Infection Control 2013, 41(1):39-44.
26. Strohbehn C., Sneed J., Paez P., Meyer J. Hand washing frequencies andprocedures used in retail food services. Journal of Food Protection 2008, 71(8):1641-1650.
27. Sumner S., Brown L.G., Frick R., Stone C., Carpenter L.R., Bushnell L., et al. Factors associated with food workers working while experiencing vomiting or diarrhea. Journal of Food Protection 2011, 74(2):215-220. 10.4315/0362-028X.JFP-10-108.
28. Teunis P.F., Moe C.L., Liu P., Miller S.E., Lindesmith L., Baric R.S., et al. Norwalk virus: how infectious is it?. Journal of Medical Virology 2008, 80(8):1468-1476.
29. Verhoef L., Depoortere E., Boxman I., Duizer E., van Duynhoven Y., Harris J., et al. Emergence of new norovirus variants on spring cruise ships and prediction of winter epidemics. Emerging Infectious Diseases 2008, 14(2):238-243.
30. Verhoef L., Koopmans M., Van Pelt W., Duizer E., Haagsma J., Werber D., et al. The estimated disease burden of norovirus in the Netherlands. Epidemiology and Infection 2012 May 17, 1-11. [Epub ahead of print]. 10.1017/S0950268812000799.
31. Vinjé J., Altena S.A., Koopmans M.P. The incidence and genetic variability of small round-structured viruses in outbreaks of gastroenteritis in The Netherlands. Journal of Infectious Diseases 1997, 176(5):1374-1378.
32. Widdowson M.A., Cramer E.H., Hadley L., Bresee J.S., Beard R.S., Bulens S.N., et al. Outbreaks of acute gastroenteritis on cruise ships and on land: identification of a predominant circulating strain of norovirus-United States, 2002. Journal of Infectious Diseases 2004, 190(1):27-36. [Epub 2004 Jun 8].
33. York V.K., Brannon L.A., Shanklin C.W., Roberts K.R., Howells A.D., Barrett E.B. Foodservice employees benefit from interventions targeting barriers to food safety. Journal of the American Dietetic Association 2009, 109(9):1576-1581.