Quantitative farm-to-fork human norovirus exposure assessment of individually quick frozen raspberries and raspberry puree.

A quantitative human norovirus (NoV) exposure model describing transmission of NoV during pre-harvest, harvest and further processing of soft red fruits exemplified by raspberries is presented. The outcomes of the model demonstrate the presence of NoV in raspberry puree or individual quick frozen (IQF) raspberry fruits and were generated by Monte Carlo simulations by combining GoldSim® and @Risk® software. Input data were collected from scientific literature, observational studies and assumptions. NoV contamination of soft red fruits is assumed to take place at farms by application of contaminated water for pesticides dilution or by berries' pickers shedding NoV. The model was built simulating that a collection center received berries from ten farms with a total of 245 food handlers picking soft red fruits during a 10-hour day shift. Given 0, 5 and 20 out of 245 berries' pickers were shedding NoV, these conditions were calculated to result in a mean NoV contamination of respectively 0.47, 14.1 and 36.2 NoV particles per kg raspberries in case all raspberries are mixed to one day-batch of 11tons. The NoV contamination of the fruits was mainly driven by the route of NoV shedding food pickers (95.8%) rather than by spraying contaminated pesticide water (4.2%) (baseline scenario with 5 shedding pickers and contaminated pesticide water). Inclusion of appropriate hand washing procedures or hand washing followed by hand disinfection resulted in estimated reductions of the mean NoV levels from 14.1 to 0.16 and 0.17 NoV particles per kg raspberries, respectively, for the baseline scenario with 5 out of 245 food pickers shedding NoV. The use of a mild heat treatment (30s at 75°C) during further processing of berries to purees was noted to reduce mean NoV levels substantially from 14.1 to 0.2 NoV particles per kg raspberry puree. For IQF raspberries, the NoV contamination is heterogeneously distributed and resulted in a mean contamination of 3.1 NoV particles per 250g package containing approximately 115 berries. This farm-to-fork model is a useful tool for evaluating NoV mitigation strategies in the soft red fruit supply chain.

[1]  P. Teunis,et al.  Norwalk virus: How infectious is it? , 2008, Journal of medical virology.

[2]  Karin Leder,et al.  A probabilistic model of norovirus disease burden associated with greywater irrigation of home-produced lettuce in Melbourne, Australia. , 2013, Water research.

[3]  K. Hedlund,et al.  A foodborne norovirus outbreak at a manufacturing company , 2009, Epidemiology and Infection.

[4]  M. Hänninen,et al.  Campylobacter spp., Giardia spp., Cryptosporidium spp., Noroviruses, and Indicator Organisms in Surface Water in Southwestern Finland, 2000-2001 , 2004, Applied and Environmental Microbiology.

[5]  A P Wyn-Jones,et al.  Quantitative RT‐PCR for the enumeration of noroviruses (Norwalk‐like viruses) in water and sewage , 2004, Letters in applied microbiology.

[6]  Valentina Hlebec,et al.  Food safety knowledge and practices among food handlers in Slovenia , 2008 .

[7]  S. Sattar,et al.  Norovirus cross-contamination during food handling and interruption of virus transfer by hand antisepsis: experiments with feline calicivirus as a surrogate. , 2004, Journal of food protection.

[8]  A. M. de Roda Husman,et al.  Presence of Noroviruses and Other Enteric Viruses in Sewage and Surface Waters in The Netherlands , 2005, Applied and Environmental Microbiology.

[9]  A. Schultz,et al.  Separate norovirus outbreaks linked to one source of imported frozen raspberries by molecular analysis, Denmark, 2010–2011 , 2014, Epidemiology and Infection.

[10]  J. Vinjé,et al.  Updated norovirus outbreak management and disease prevention guidelines. , 2011, MMWR. Recommendations and reports : Morbidity and mortality weekly report. Recommendations and reports.

[11]  Harry Vennema,et al.  Genetic diversity of noroviruses in raw and treated sewage water. , 2005, Research in microbiology.

[12]  S. Temmam,et al.  A predictive microbiology approach for thermal inactivation of Hepatitis A virus in acidified berries. , 2010, Food microbiology.

[13]  Greg Paoli,et al.  Prevention of food worker transmission of foodborne pathogens: risk assessment and evaluation of effective hygiene intervention strategies , 2004 .

[14]  T. Oka,et al.  Norovirus Infections in Symptomatic and Asymptomatic Food Handlers in Japan , 2007, Journal of Clinical Microbiology.

[15]  Marion Koopmans,et al.  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 , 2013 .

[16]  M. Höhle,et al.  Large multistate outbreak of norovirus gastroenteritis associated with frozen strawberries, Germany, 2012. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[17]  D. Graham,et al.  Norwalk virus infection of volunteers: new insights based on improved assays. , 1994, The Journal of infectious diseases.

[18]  S. Sattar,et al.  Comparative in vivo efficiencies of hand-washing agents against hepatitis A virus (HM-175) and poliovirus type 1 (Sabin) , 1993, Applied and environmental microbiology.

[19]  Saskia A Rutjes,et al.  Virus transfer proportions between gloved fingertips, soft berries, and lettuce, and associated health risks. , 2013, International journal of food microbiology.

[20]  M. Bouwknegt,et al.  Persistence of human norovirus GII.4 and GI.4, murine norovirus, and human adenovirus on soft berries as compared with PBS at commonly applied storage conditions. , 2012, International journal of food microbiology.

[21]  Sang-Jong Kim,et al.  The genetic diversity of human noroviruses detected in river water in Korea. , 2008, Water research.

[22]  G. Wells,et al.  In vivo protocol for testing efficacy of hand-washing agents against viruses and bacteria: experiments with rotavirus and Escherichia coli , 1989, Applied and environmental microbiology.

[23]  J Debevere,et al.  The efficacy of preservation methods to inactivate foodborne viruses. , 2009, International journal of food microbiology.

[24]  M. Uyttendaele,et al.  Batch testing for noroviruses in frozen raspberries. , 2015, International journal of food microbiology.

[25]  D. D'Souza,et al.  Efficacy of chemical treatments against murine norovirus, feline calicivirus, and MS2 bacteriophage. , 2010, Foodborne pathogens and disease.

[26]  Larissa B. Thackray,et al.  Detection of Murine Norovirus 1 by Using Plaque Assay, Transfection Assay, and Real-Time Reverse Transcription-PCR before and after Heat Exposure , 2007, Applied and Environmental Microbiology.

[27]  L. Jacxsens,et al.  A quantitative exposure model simulating human norovirus transmission during preparation of deli sandwiches. , 2015, International journal of food microbiology.

[28]  S. Coughlan,et al.  Potential role of asymptomatic kitchen food handlers during a food-borne outbreak of norovirus infection, Dublin, Ireland, March 2009. , 2011, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[29]  N. Kishida,et al.  One-year weekly survey of noroviruses and enteric adenoviruses in the Tone River water in Tokyo metropolitan area, Japan. , 2012, Water research.

[30]  A. Steyer,et al.  High prevalence of enteric viruses in untreated individual drinking water sources and surface water in Slovenia. , 2011, International journal of hygiene and environmental health.

[31]  A. Rzeżutka,et al.  Seasonal Occurrence of Human Enteric Viruses in River Water Samples Collected from Rural Areas of South-East Poland , 2011, Food and Environmental Virology.

[32]  M. Bouwknegt,et al.  Persistence of human norovirus in reconstituted pesticides--pesticide application as a possible source of viruses in fresh produce chains. , 2013, International journal of food microbiology.

[33]  Jianrong Li,et al.  Evidence of the Internalization of Animal Caliciviruses via the Roots of Growing Strawberry Plants and Dissemination to the Fruit , 2015, Applied and Environmental Microbiology.

[34]  D. Schaffner,et al.  Norovirus cross-contamination during preparation of fresh produce. , 2015, International journal of food microbiology.

[35]  S. Sattar,et al.  Improved Inactivation of Nonenveloped Enteric Viruses and Their Surrogates by a Novel Alcohol-Based Hand Sanitizer , 2008, Applied and Environmental Microbiology.

[36]  D. Cheon,et al.  Occurrence of Norovirus Infections in Asymptomatic Food Handlers in South Korea , 2012, Journal of Clinical Microbiology.

[37]  P. Teunis,et al.  Short- and long-term variations of norovirus concentrations in the Meuse river during a 2-year study period. , 2006, Water research.

[38]  P. White,et al.  Norovirus Excretion in an Aged-Care Setting , 2008, Journal of Clinical Microbiology.

[39]  K. Gin,et al.  Prevalence and Genotypes of Human Noroviruses in Tropical Urban Surface Waters and Clinical Samples in Singapore , 2009, Applied and Environmental Microbiology.

[40]  S. Rutjes,et al.  Presence of Enteric Viruses in Source Waters for Drinking Water Production in the Netherlands , 2010, Applied and Environmental Microbiology.

[41]  Jianrong Li,et al.  Attachment and localization of human norovirus and animal caliciviruses in fresh produce. , 2015, International journal of food microbiology.

[42]  Amirhossein Mokhtari,et al.  Quantitative exposure model for the transmission of norovirus in retail food preparation. , 2009, International journal of food microbiology.

[43]  D. Mara,et al.  Estimation of norovirus infection risks to consumers of wastewater-irrigated food crops eaten raw. , 2010, Journal of water and health.

[44]  Wen-Hwa Ko.  The relationship among food safety knowledge, attitudes and self-reported HACCP practices in restaurant employees , 2013 .

[45]  Zijian Wang,et al.  Molecular detection of three gastroenteritis viruses in urban surface waters in Beijing and correlation with levels of fecal indicator bacteria , 2012, Environmental Monitoring and Assessment.

[46]  A. Hamilton,et al.  Exposure Factors for Wastewater‐Irrigated Asian Vegetables and a Probabilistic Rotavirus Disease Burden Model for Their Consumption , 2014, Risk analysis : an official publication of the Society for Risk Analysis.

[47]  I. Seymour,et al.  Survival of viruses on fresh produce, using MS2 as a surrogate for norovirus , 2005, Journal of applied microbiology.

[48]  Ivo Pavlik,et al.  Quantitative farm-to-fork risk assessment model for norovirus and hepatitis A virus in European leafy green vegetable and berry fruit supply chains. , 2015, International journal of food microbiology.

[49]  J. Schijven,et al.  Monitoring of Waterborne Pathogens in Surface Waters in Amsterdam, The Netherlands, and the Potential Health Risk Associated with Exposure to Cryptosporidium and Giardia in These Waters , 2008, Applied and Environmental Microbiology.

[50]  D. Graham,et al.  Norwalk Virus Shedding after Experimental Human Infection , 2008, Emerging infectious diseases.

[51]  P. Pothier,et al.  Adhesion of human pathogenic enteric viruses and surrogate viruses to inert and vegetal food surfaces. , 2012, Food microbiology.

[52]  L. Jacxsens,et al.  Zero Risk Does Not Exist: Lessons Learned from Microbial Risk Assessment Related to Use of Water and Safety of Fresh Produce , 2015 .

[53]  M. Wilhelm,et al.  Detection of human viruses in rivers of a densly-populated area in Germany using a virus adsorption elution method optimized for PCR analyses. , 2009, Water research.

[54]  R. Girones,et al.  Detection and quantification of classic and emerging viruses by skimmed-milk flocculation and PCR in river water from two geographical areas. , 2013, Water research.

[55]  S. Fontana,et al.  Molecular Identification and Genetic Analysis of Norovirus Genogroups I and II in Water Environments: Comparative Analysis of Different Reverse Transcription-PCR Assays , 2007, Applied and Environmental Microbiology.

[56]  R. Johne,et al.  Detection and Typing of Norovirus from Frozen Strawberries Involved in a Large-Scale Gastroenteritis Outbreak in Germany , 2013, Food and Environmental Virology.

[57]  Aron J. Hall,et al.  Vital Signs: Foodborne Norovirus Outbreaks — United States, 2009–2012 , 2014, MMWR. Morbidity and mortality weekly report.

[58]  G. Kampf,et al.  Efficacy of three ethanol-based hand rubs against feline calicivirus, a surrogate virus for norovirus. , 2005, The Journal of hospital infection.

[59]  C. Gantzer,et al.  Comparison of Coliforms and Coliphages as Tools for Assessment of Viral Contamination in River Water , 2004, Applied and Environmental Microbiology.

[60]  J. Cannon,et al.  Human norovirus transfer to stainless steel and small fruits during handling. , 2012, Journal of food protection.