Sources and persistence of human noroviruses in fresh produce chains and associated public health risks

Abstract

Human norovirus is a frequent cause of gastroenteritis worldwide, and viewed as the most common cause of foodborne disease. Numerous norovirus outbreaks associated with fresh produce, especially soft-berries and lettuce are described. Risk management strategies need to be improved in order to reduce the foodborne norovirus disease burden from consumption of fresh produce. For this purpose, data on virus persistence, the relevance of norovirus contamination sources, and the efficacy of mitigation measures were obtained. Norovirus infectivity cannot be determined, and our results are based on the detection of norovirus genomes and infectivity estimates derived from murine norovirus (MNV-1), a commonly used surrogate to study human norovirus persistence. Norovirus GI.4 and GII.4, two strains commonly associated to foodborne norovirus disease, and MNV-1, were found to persist during post-harvest conditions of fresh raspberries and strawberries. Thus post-harvest contamination of berries and contamination during primary production, at least shortly before harvest, likely pose a public health risk. Avoiding norovirus contamination, rather than reducing the presence of persistent viruses on produce, is the preferred approach for ensuring food safety. Infected food handlers, contaminated surfaces and water, are considered to be relevant sources for norovirus contamination of fresh produce. To simulate the spread of noroviruses by food handler, quantitative data on virus transfer proportions from hands to fresh produce and vice versa were determined. The simulation showed that a single infected food handler picking raspberries may spread norovirus to up to 3 kg of raspberries, which may result in large number of infected consumers, given the model assumptions. In addition, the established farm-to-fork risk assessment confirmed food handlers not practicing good hand hygiene as one of the dominant sources of contamination, given the data and model used. To prevent norovirus cross-contamination between contaminated surfaces and fresh produce, the effect of wiping surfaces in reducing norovirus loads was studied. Cleaning wet spots with dry wipes was determined to efficiently reduce spot contamination on surfaces (removal of 104 noroviruses), however, spreading of noroviruses on surfaces by wiping may result in an increased public health risk at high initial virus loads. Noroviruses are found in various water sources. To investigate the potential of norovirus introduction by application of in water diluted pesticides, the persistence of noroviruses in such dilutions was studied. Noroviruses were found to frequently persist in pesticides, and their application may therefore pose a microbiological risk to public health if contaminated water is used for pesticides dilution. Current guidelines for fresh produce production fail to provide specific criteria on the required water quality. The established quantitative farm-to-fork risk assessment model provides a basis for food safety regulations, for example, by presenting a framework for deriving performance objectives for norovirus concentrations in water used to spray irrigate lettuce. A mean concentration of around 0.4 norovirus particles per liter was estimated to realize with 95% certainty an annual health target of less than 1 infection per 10,000 consumers of lettuce. These calculations are specific to the described lettuce chain and need to be reevaluated for other scenarios.