Tracing enteric viruses in the European berry fruit supply chain

• Published in: International journal of food microbiology Vol. 167; no. 2; pp. 177 - 185
• Main Authors: Maunula, Leena, Kaupke, Agnieszka, Vasickova, Petra, Söderberg, Kirsi, Kozyra, Iwona, Lazic, Sava, van der Poel, Wim H.M., Bouwknegt, Martijn, Rutjes, Saskia, Willems, Kris A., Moloney, Rita, D'Agostino, Martin, de Roda Husman, Ana Maria, von Bonsdorff, Carl-Henrik, Rzeżutka, Artur, Pavlik, Ivo, Petrovic, Tamas, Cook, Nigel
• Format: Journal Article
• Language: English
• Published: Amsterdam Elsevier B.V 15.10.2013; Elsevier
• Subjects: a virus; Adenoviruses, Human - isolation & purification; Adenoviruses, Porcine - isolation & purification; Agricultural Irrigation; Animals; Berry fruit; Biological and medical sciences; Bovine polyomavirus; Cattle; Czech Republic; Disease Outbreaks; Enterovirus; Farms; Feces - virology; Finland; Food Contamination - analysis; Food Handling - methods; Food industries; Food microbiology; Food monitoring; food safety; Food Supply; Foodborne viruses; frozen raspberries; Fruit - virology; Fundamental and applied biological sciences. Psychology; hAdV; Hand - virology; Hepatitis A virus - isolation & purification; Hepatitis E virus - isolation & purification; hepatitis-e virus; Humans; infection; Norovirus - isolation & purification; norovirus outbreaks; NoV; Poland; Polyomavirus - isolation & purification; Real-time PCR; reverse transcription-pcr; Serbia; Swine; time rt-pcr; transmission; Viruses; waste-water; Water Microbiology; Poland; Czech Republic; Serbia; Finland; Food monitoring; hAdV; Real-time PCR; NoV; Foodborne viruses; Berry fruit; Small fruits; Real time; Polymerase chain reaction; Virus; Foodbome viruses; Molecular biology; Monitoring; Food
• ISSN: 0168-1605; 1879-3460
• DOI: 10.1016/j.ijfoodmicro.2013.09.003

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. •Berry fruit food chain was monitored for enteric viruses in European countries.•Contamination of irrigation water and food handlers' hands by viruses was observed.•Improved hygiene conditions are needed to control viruses at soft fruit farms.