title: Tracing enteric viruses in the European berry fruit supply chain.
abstract: In recent years, numerous foodborne outbreaks due to consumption of berry fruit contaminated by human enteric viruses have been reported. This European multinational study investigated possible contamination routes by monitoring the entire food chain for a panel of human and animal enteric viruses. A total of 785 samples were collected throughout the food production chain of four European countries (Czech Republic, Finland, Poland and Serbia) during two growing seasons. Samples were taken during the production phase, the processing phase, and at point-of-sale. Samples included irrigation water, animal faeces, food handlers' hand swabs, swabs from toilets on farms, from conveyor belts at processing plants, and of raspberries or strawberries at points-of-sale; all were subjected to virus analysis. The samples were analysed by real-time (reverse transcription, RT)-PCR, primarily for human adenoviruses (hAdV) to demonstrate that a route of contamination existed from infected persons to the food supply chain. The analyses also included testing for the presence of selected human (norovirus, NoV GI, NoV GII and hepatitis A virus, HAV), animal (porcine adenovirus, pAdV and bovine polyomavirus, bPyV) and zoonotic (hepatitis E virus, HEV) viruses. At berry production, hAdV was found in 9.5%, 5.8% and 9.1% of samples of irrigation water, food handlers' hands and toilets, respectively. At the processing plants, hAdV was detected in one (2.0%) swab from a food handler's hand. At point-of-sale, the prevalence of hAdV in fresh raspberries, frozen raspberries and fresh strawberries, was 0.7%, 3.2% and 2.0%, respectively. Of the human pathogenic viruses, NoV GII was detected in two (3.6%) water samples at berry production, but no HAV was detected in any of the samples. HEV-contaminated frozen raspberries were found once (2.6%). Animal faecal contamination was evidenced by positive pAdV and bPyV assay results. At berry production, one water sample contained both viruses, and at point-of-sale 5.7% and 1.3% of fresh and frozen berries tested positive for pAdV. At berry production hAdV was found both in irrigation water and on food handler's hands, which indicated that these may be important vehicles by which human pathogenic viruses enter the berry fruit chain. Moreover, both zoonotic and animal enteric viruses could be detected on the end products. This study gives insight into viral sources and transmission routes and emphasizes the necessity for thorough compliance with good agricultural and hygienic practice at the farms to help protect the public from viral infections.
authors.affiliation: Department of Food Hygiene and Environmental Health, Faculty of Veterinary Medicine, University of Helsinki, Finland. Electronic address: leena.maunula@helsinki.fi.
authors.forename: Leena
authors.initials: L
authors.lastname: Maunula
authors.forename: Agnieszka
authors.initials: A
authors.lastname: Kaupke
authors.forename: Petra
authors.initials: P
authors.lastname: Vasickova
authors.forename: Kirsi
authors.initials: K
authors.lastname: Söderberg
authors.forename: Iwona
authors.initials: I
authors.lastname: Kozyra
authors.forename: Sava
authors.initials: S
authors.lastname: Lazic
authors.forename: Wim H M
authors.initials: WH
authors.lastname: van der Poel
authors.forename: Martijn
authors.initials: M
authors.lastname: Bouwknegt
authors.forename: Saskia
authors.initials: S
authors.lastname: Rutjes
authors.forename: Kris A
authors.initials: KA
authors.lastname: Willems
authors.forename: Rita
authors.initials: R
authors.lastname: Moloney
authors.forename: Martin
authors.initials: M
authors.lastname: D'Agostino
authors.forename: Ana Maria
authors.initials: AM
authors.lastname: de Roda Husman
authors.forename: Carl-Henrik
authors.initials: CH
authors.lastname: von Bonsdorff
authors.forename: Artur
authors.initials: A
authors.lastname: Rzeżutka
authors.forename: Ivo
authors.initials: I
authors.lastname: Pavlik
authors.forename: Tamas
authors.initials: T
authors.lastname: Petrovic
authors.forename: Nigel
authors.initials: N
authors.lastname: Cook
mesh_terms: D000260:Adenoviruses, Human / Q000302:isolation & purification; D025662:Adenoviruses, Porcine / Q000302:isolation & purification; D057914:Agricultural Irrigation; D000818:Animals; D002417:Cattle; D018153:Czech Republic; D004196:Disease Outbreaks; D004770:Enterovirus; D005243:Feces / Q000821:virology; D005387:Finland; D005506:Food Contamination / Q000032:analysis*; D005511:Food Handling / Q000379:methods*; D005523:Food Supply; D005638:Fruit / Q000821:virology*; D006225:Hand / Q000821:virology; D030041:Hepatitis A virus / Q000302:isolation & purification; D016752:Hepatitis E virus / Q000302:isolation & purification; D006801:Humans; D029322:Norovirus / Q000302:isolation & purification; D011044:Poland; D011120:Polyomavirus / Q000302:isolation & purification; D055771:Serbia; D013552:Swine; D014780:Viruses; D014871:Water Microbiology
keywords: Berry fruit; Food monitoring; Foodborne viruses; NoV; Real-time PCR; hAdV