title: Virus transfer proportions between gloved fingertips, soft berries, and lettuce, and associated health risks.
abstract: Multiple outbreaks of human norovirus (hNoV) have been associated with fresh produce, such as soft berries and lettuce. Even though food handlers are considered an important source for the introduction of hNoV into food chains, their contribution to public health risks associated with hNoV remains unknown. To assess to which extent food handlers contribute to the introduction and spread of hNoV in fresh produce chains quantitative virus transfer data are needed. We estimated transfer proportions of hNoV GI.4, GII.4, murine norovirus (MNV-1), a culturable surrogate of hNoV, and human adenovirus (hAdV-2), a human pathogen proposed as an indicator for human faecal pollution, between gloved fingertips and raspberries, strawberries, and lettuce, by quantitative RT-PCR and cell culture if applicable. Virus transfer proportions were corrected for virus-matrix specific recoveries, and variability and uncertainty of the parameters were estimated. Virus transfer from gloves to soft berries was generally lower as compared to lettuce, with mean transfer proportions ranging between 0.1 to 2.3% and 9 to 10% for infectious MNV-1 and hAdV-2, respectively. Transfer from produce to glove was mostly greater than transfer from glove to produce, adding to the likelihood of virus transfer due to cross contamination from contaminated produce via food handlers. HNoV GI.4 and hNoV GII.4 showed no significant difference between their mean transfer proportions. Using the estimated transfer proportions, we studied the impact of low and high transfer proportions on the public health risk, based on a scenario in which a food handler picked raspberries with contaminated fingertips. Given the made assumptions, we could show that for a pathogen as infectious as hNoV, low transfer proportions may pose a greater public health risk than high transfer proportions, due to a greater viral spread. We demonstrated the potential of food handlers in spreading hNoV in food chains, showing that prevention of virus contamination on food handlers' hands is crucial for food safety. Nevertheless, complete prevention of virus contamination on fresh produce cannot be achieved in reality, and reliable and effective intervention measures are consequently required. We estimated that, especially for low transfer proportions, a robust one log10-unit reduction of infectious hNoV on contaminated produce, and on food handlers' hands, could lower the public health risk substantially. Using the obtained data in quantitative risk assessment will aid in elucidating the contribution of food handlers in hNoV transmission.
authors.affiliation: Centre for Zoonoses and Environmental Microbiology, Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), P.O. Box 1, NL-3720 BA Bilthoven, The Netherlands; Faculty of Veterinary Medicine, Institute for Risk Assessment Sciences (IRAS), Utrecht University, P.O. Box 80.178, NL-3508 TD Utrecht, The Netherlands. Electronic address: Verhaelen@gmail.com.
authors.forename: Katharina
authors.initials: K
authors.lastname: Verhaelen
authors.forename: Martijn
authors.initials: M
authors.lastname: Bouwknegt
authors.forename: Anna
authors.initials: A
authors.lastname: Carratalà
authors.forename: Froukje
authors.initials: F
authors.lastname: Lodder-Verschoor
authors.forename: Marta
authors.initials: M
authors.lastname: Diez-Valcarce
authors.forename: David
authors.initials: D
authors.lastname: Rodríguez-Lázaro
authors.forename: Ana Maria
authors.initials: AM
authors.lastname: de Roda Husman
authors.forename: Saskia A
authors.initials: SA
authors.lastname: Rutjes
mesh_terms: D005511:Food Handling / Q000592:standards*; D005516:Food Microbiology; D005638:Fruit / Q000821:virology*; D017575:Gloves, Protective / Q000821:virology*; D006801:Humans; D018545:Lactuca / Q000821:virology*; D020133:Reverse Transcriptase Polymerase Chain Reaction; D018570:Risk Assessment
keywords: Adenovirus; Food handlers; Fresh produce; Health risk; Norovirus; Virus transfer