Viral contamination by food handlers and recommended procedural controls

Viruses in Food and Water: Risks, Surveillance and Control

Volumn , Issue , 2013, Pages 217-236

  Boxman, I L A ^a  

^a Voedsel en Waren Autoriteit Netherlands   (Netherlands)

Author keywords

Food safety; HACCP; Hepatitis A virus; Norovirus; Virus transmission

Indexed keywords

EID: 84878866408     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1533/9780857098870.3.217     Document Type: Chapter

References (55)

1. Angelillo I.F., Viggiani N.M., Rizzo L., Bianco A. Food handlers and foodborne diseases: knowledge, attitudes, and reported behavior in Italy. J Food Prot 2000, 63:381-385.
2. Anonymous Microbiology of food and animal feed - Horizontal method for determination of hepatitis A virus and norovirus in food using real-time RT-PCR - part 1: method for quantification. CEN ISO/TS 15216-1 2013, draft.
3. Anonymous Microbiology of food and animal feed - horizontal method for determination of hepatitis A virus and norovirus in food using real-time RT-PCR - part 2: method for qualitative detection. CEN ISO/TS 15216-2 2013, (draft).
4. Atmar R.L., Opekun A.R., Gilger M.A., Estes M.K., Crawford S.E., Neill F.H., Graham D.Y. Norwalk virus shedding after experimental human infection. Emerg Infect Dis 2008, 14:1553-1557.
5. Barrabeig I., Rovira A., Buesa J., Bartolomé R., Pintó R., Prellezo H., Domínguez A. Foodborne norovirus outbreak: the role of an asymptomatic food handler. BMC Infect Dis 2010, 10:269. 10.1186/1471-2334-10-269.
6. Bidawid S., Farber J.M., Sattar S.A. Contamination of foods by food handlers: experiments on hepatitis A virus transfer to food and its interruption. Appl Environ Microbiol 2000, 66:2759-2763.
7. 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. J Food Prot 2004, 67:103-109.
8. Boone S.A., Gerba C.P. Significance of fomites in the spread of respiratory and enteric viral disease. Appl Environ Microbiol 2007, 73:1687-1696.
9. Boxman I.L., Tilburg J.J., Te Loeke N.A., Vennema H., De Boer E., Koopmans M. An efficient and rapid method for recovery of norovirus from food associated with outbreaks of gastroenteritis. J Food Prot 2007, 70:504-508.
10. Boxman I.L., Dijkman R., Te Loeke N.A., Hägele G., Tilburg J.J., Vennema H., Koopmans M. Environmental swabs as a tool in norovirus outbreak investigation, including outbreaks on cruise ships. J Food Prot 2009, 72:111-119.
11. Boxman I., Dijkman R., Verhoef L., Maat A., Van Dijk G., Vennema H., Koopmans M. Norovirus on swabs taken from hands illustrate route of transmission: a case study. J Food Prot 2009, 72:1753-1755.
12. 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. Appl Environ Microbiol 2011, 77:2968-2974.
13. Cates S.C., Muth M.K., Karns S.A., Penne M.A., Stone C.N., Harrison J.E., Radke V.J. Certified kitchen managers: do they improve restaurant inspection outcomes?. J Food Prot 2009, 72:384-391.
14. Dalling J. A review of environmental contamination during outbreaks of Norwalk-like virus. Br J Infect Contr 2004, 5:9-13.
15. Dancer S.J. The role of environmental cleaning in the control of hospital-acquired infection. J Hosp Infect 2009, 73:378-385.
16. Daniels N.A., Bergmire-Sweat D.A., Schwab K.J., Hendricks K.A., Reddy S., Rowe S.M., Fankhauser R.L., Monroe S.S., Atmar R.L., Glass R.I., Mead P. A food- borne outbreak of gastroenteritis associated with Norwalk-like viruses: first molecular traceback to deli sandwiches contaminated during preparation. J Infect Dis 2000, 181:1467-1470.
17. Debess E.E., Pippert E., Angulo F.J., Cieslak P.R. Food handler assessment in Oregon. Foodborne Pathog Dis 2009, 6:329-335.
18. D'souza D.H., Sair A., Williams K., Papafragkou E., Jean J., Moore C., Jaykus L. Persistence of caliciviruses on environmental surfaces and their transfer to food. Int J Food Microbiol 2006, 108:84-91.
19. EFSA (European Food Safety Authority) Scientific Opinion on an update on the present knowledge on the occurrence and control of foodborne viruses EFSA J, 9, 2190 (96pp), (Accessed 17 February 2012). http://www.efsa.europa.eu/en/efsajournal/doc/2190.pdf, 10.2903/j.efsa.2011.2190.
20. EFSA (European Food Safety Authority) Panel on Biological Hazards (BIOHAZ), (2012), 'Scientific opinion on Norovirus (NoV) in oysters: methods, limits and control options' EFSA J, 10. 2500. (39pp), (Accessed 17 February 2012). http://www.efsa.europa.eu/en/efsajournal/pub/2500.htm, 10.2903/j.efsa.2012.2500.
21. FAO(Food and Agriculture Organization of the United Nations) Hazard analysis and critical control point (HACCP) system and guidelines for its application Annex to CAC/RCP 1-1969, (Accessed 17 February 2012). http://www.fao.org/docrep/005/y1579e/y1579e03.htm.
22. FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization) General Principles of Food Hygiene, CAC/RCP-1 (Accessed 17 February 2012)http://www.codexalimentarius.net/web/more_info.jsp?id_sta=23.
23. FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization) Understanding the Codex Alimentarius ISBN: 978-92-5-105614-1, Accessed 17 February 2012. ftp://www.ftp.fao.org/codex/Publications/understanding/Understanding_EN.pdf
24. 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 Microbiological Risk Assessment Series, No. 13., Accessed 17 February 2012. http://www.who.int/foodsafety/publications/micro/mra13/en/index.html.
25. FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization) FAO/WHO Food standards Codex Alimentarius Available from, (Accessed 17 February 2012). http://www.codexalimentarius.net/web/index_en.jsp.
26. FAO/WHO(Food and Agriculture Organization of the United Nations/World health organization) Available from, Accessed 3 May 2012. http://www.codexalimentarius.org/standards/list-of-standards.
27. FAO/WHO(Food and Agriculture Organization of the United Nations/World Health Organization) Guidelines on the Application of General Principles of Food Hygiene to the Control of Viruses in Food (CAC/GL 79-2012) 2012.
28. 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 Available from, Accessed 17 February 2012. http://www.fda.gov/downloads/Food/FoodSafety/RetailFoodProtection/FoodborneIllnessandRiskFactorReduction/RetailFoodRiskFactorStudies/UCM224682.pdf.
29. Fiore A. Hepatitis A transmitted by food. Clin Inf Dis 2004, 38:705-715.
30. FSA (food standards agency UK) Why are you focusing on handwashing after using the toilet? Available from, Accessed 17 February 2012. http://www.food.gov.uk/multimedia/faq/fhc-2qanda/.
31. Green L., Selman C., Banerjee A., Marcus R., Medus C., Fj Angulo, Radke V., Buchanan S., EHS-Net Working Group Food service workers' self-reported food preparation practices: an EHS-Net study. Int J Hyg Environ Health 2005, 208:27-35.
32. Green L.R., Selman C.A., Radke V., Ripley D., Mack J.C., Reimann D.W., Stigger T., Motsinger M., Bushnell L. Food worker hand washing practices: an observation study. J Food Prot 2006, 69:2417-2423.
33. Green L.R., Radke V., Mason R., Bushnell L., Reimann D.W., Mack J.C., Motsinger M.D., Stigger T., Selman C.A. Factors related to food worker hand hygiene practices. J Food Prot 2007, 70:661-666.
34. Hedberg C.W., Smith S.J., Kirkland E., Radke V., Jones T.F., Selman C.A., EHS-Net Working Group Systematic environmental evaluations to identify food safety differences between outbreak and nonoutbreak restaurants. J Food Prot 2006, 69:2697-2702.
35. Henke-Gendo C., Harste G., Juergens-Saathoff B., Mattner F., Deppe H., Heim A. New real-time PCR detects prolonged norovirus excretion in highly immunosuppressed patients and children. J Clin Microbiol 2009, 47:2855-2862.
36. Kassa H., Harrington B., Bisesi M., Khuder S. Comparison of microbiological evaluation of selected kitchen areas with visual inspection for preventing potential risk of food borne outbreaks in food service operations. J Food Prot 2001, 64:509-513.
37. Kassa H., Silverman G.S., Baroudi K. Effect of a manager training and certification program on food safety and hygiene in food service operations. Environ Health Insights 2010, 4:13-20.
38. Kirkwood C.D., Streitberg R. Calicivirus shedding in children after recovery from diarrhoeal disease. J Clin Virol 2008, 43:346-348.
39. Koopmans M., Von Bonsdorff C.H., Vinjé J., De Medici D., Monroe S. Foodborne viruses. FEMS Microbiol Rev 2002, 26:187-205.
40. Lopman B., Gastañaduy P., Woo Park G., Hall A.J., Parashar U.D., Vinjé J. Environmental transmission of norovirus gastroenteritis. Curr Opin Virol 2011, 2:1-7. 10.1016/j.coviro.2011.11.005.
41. Lubran M.B., Pouillot R., Bohm S., Calvey E.M., Meng J., Dennis S. Observational study of food safety practices in retail deli departments. J Food Prot 2010, 73:1849-1857.
42. Moe C.L. Preventing norovirus transmission: how should we handle food handlers?. Clin Infect Dis 2009, 48:38-40.
43. Murata T., Katsushima N., Mizuta K., Muraki Y., Hongo S., Matsuzaki Y. Prolonged norovirus shedding in infants < or=6months of age with gastroenteritis. Pediatr Infect Dis J 2007, 26:46-49.
44. Nicolay N., Mcdermott R., Kelly M., Gorby M., Prendergast T., Tuite G., Coughlan S., Mckeown P., Sayers G. Potential role of asymptomatic kitchen food handlers during a food-borne outbreak of norovirus infection, Dublin, Ireland, march 2009. Euro Surveill 2011, 16(30). pii=19931.
45. Okabayashi T., Yokota S., Ohkoshi Y., Ohuchi H., Yoshida Y., Kikuchi M., Yano K., Fujii N. Occurrence of norovirus infections unrelated to norovirus outbreaks in an asymptomatic food handler population. J Clin Microbiol 2008, 46:1985-1988.
46. Ozawa K., Oka T., Takeda N., Hansman G.S. Norovirus infections in symptomatic and asymptomatic food handlers in Japan. J Clin Microbiol 2007, 45:3996-4005.
47. Phillips G., Tam C.C., Rodrigues L.C., Lopman B. Risk factors for symptomatic and asymptomatic norovirus infection in the community. Epidemiol Infect 2010, 139:1676-1686.
48. Pragle A.S., Harding A.K., Mack J.C. Food workers' perspectives on handwashing behaviors and barriers in the restaurant environment. J Environ Health 2007, 69:27-32.
49. Schwab K.J., Neill F.H., Fankhauser R.L., Daniels N.A., Monroe S.S., Bergmire-Sweat D.A., Estes M.K., Atmar R.L. Development of methods to detect "Norwalk-like viruses" (NLVs) and hepatitis A virus in delicatessen foods: application to a food-borne NLV outbreak. Appl Environ Microbiol 2000, 66:213-218.
50. Strohbehn C., Sneed J., Paez P., Meyer J. Hand washing frequencies and procedures used in retail food services. J Food Prot 2008, 71:1641-1650.
51. Teunis P.F., Moe C.L., Liu P., Miller S.E., Lindesmith L., Baric R.S., Le Pendu J., Calderon R.L. Norwalk virus: how infectious is it?. J Med Virol 2008, 80:1468-1476.
52. Todd E.C., Greig J.D., Bartleson C.A., Michaels B.S. Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 3. Factors contributing to outbreaks and description of outbreak categories. J Food Prot 2007, 70:2199-2217.
53. Todd E.C., Michaels B.S., Smith D., Greig J.D., Bartleson C.A. Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 9. Washing and drying of hands to reduce microbial contamination. J Food Prot 2010, 73:1937-1955.
54. Todd E.C., Greig J.D., Michaels B.S., Bartleson C.A., Smith D., Holah J. Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 11. Use of antiseptics and sanitizers in community settings and issues of hand hygiene compliance in health care and food industries. J Food Prot 2010, 73:2306-2320.
55. Wu H.M., Fornek M., Schwab K.J., Chapin A.R., Gibson K., Schwab E., Spencer C., Henning K. A norovirus outbreak at a long-term care facility: the role of environmental surface contamination. Infect Control Hosp Epidemiol 2005, 26:802-810.