A One-Year Survey of Norovirus in UK Oysters Collected at the Point of Sale

Food and Environmental Virology https://doi.org/10.1007/s12560-018-9338-4 ORIGINAL PAPER A One‑Year Survey of Norovirus in UK Oysters Collected at the Point of Sale J. A. Lowther1 · N. E. Gustar1 · A. L. Powell1 · S. O’Brien2 · D. N. Lees1 Received: 14 November 2017 / Accepted: 27 January 2018 © The Author(s) 2018 Abstract Contamination of bivalve shellfish, particularly oysters, with norovirus is recognised as a food safety risk and a potential contributor to the overall burden of gastroenteritis in the community. The United Kingdom (UK) has comprehensive national baseline data on the prevalence, levels, and seasonality of norovirus in oysters in production areas resulting from a previous two-year study (2009–2011). However, previously, data on final product as sold to the consumer have been lacking. As part of a wider project to establish the overall burden of foodborne norovirus in the UK, this study aimed to address this data gap. A one-year survey of oysters collected from the point-of-sale to the consumer was carried out from March 2015 to March 2016. A total of 630 samples, originating in five different European Union Member States, were collected from 21 regions across the UK using a randomised sampling plan, and tested for norovirus using a method compliant with ISO 15216-1, in addition to Escherichia coli as the statutory indicator of hygiene status. As in the previous production area study, norovirus RNA was detected in a high proportion of samples (68.7%), with a strong winter seasonality noted. Some statistically significant differences in prevalences and levels in oysters from different countries were noted, with samples originating in the Netherlands showing lower prevalences and levels than those from either the UK or Ireland. Overall, levels detected in positive samples were considerably lower than seen previously. Investigation of potential contributing factors to this pattern of results was carried out. Application of normalisation factors to the data from the two studies based on both the numbers of norovirus illness reports received by national surveillance systems, and the national average environmental temperatures during the two study periods resulted in a much closer agreement between the two data sets, with the notably different numbers of illness reports making the major contribution to the differences observed in norovirus levels in oysters. The large majority of samples (76.5%) contained no detectable E. coli; however, in a small number of samples (2.4%) levels above the statutory end product standard (230 MPN/100 g) were detected. This study both revealed the high prevalence of norovirus RNA in oysters directly available to the UK consumer, despite the high level of compliance with the existing E. coli-based health standards, while also highlighting the difficulty in comparing the results of surveys carried out in different time periods, due to variability in risk factors. Keywords Norovirus · Oysters · qRT-PCR · Survey Introduction Electronic supplementary material The online version of this article (https://doi.org/10.1007/s12560-018-9338-4) contains supplementary material, which is available to authorized users. * J. A. Lowther 1 Centre for Environment, Fisheries and Aquaculture Science, Weymouth DT4 8UB, UK 2 Institute of Psychology, Health & Society, University of Liverpool, Liverpool, England, UK Contamination of bivalve shellfish, particularly oysters, with norovirus is recognised as a food safety risk, with a considerable number of reports of outbreaks in the literature (reviewed in Bellou et al. 2013). In both the European Union and the United States, viral contamination in shellfish is regulated indirectly using enteric bacteria as an indicator of faecal pollution (Anonymous 2004, 2015b). However, this approach has been demonstrated to inadequately address the risk from human enteric viruses, with a number of viral outbreaks caused by batches compliant with the regulations 13 Vol.:(0123456789) Food and Environmental Virology (Chalmers and McMillan 1995; Le Guyader et al. 2008; Dore et al. 2010). Considerable progress has been made towards the development of detection methods for norovirus in molluscan shellfish and an ISO/CEN technical specification including such a method (ISO/TS 15216) was published in 2013 (Anonymous 2013), with a subsequent update to a fully validated standard in 2017 (Anonymous 2017). EU legislative texts foreshadow the adoption of virus controls in bivalve shellfish when the methods are sufficiently developed (Anonymous 2005) and the options for improvement of EU legislation to better address the virus risk have been actively discussed in recent years (EFSA Panel on Biological Hazards 2012). It has therefore become important to gain information about the application of the new methods, and the potential impact of possible legislative standards on bivalve shellfish production. Amongst current European Union Member States, the United Kingdom (UK) has some of the most comprehensive national baseline data on the prevalence, levels and seasonality of norovirus in oysters resulting from a two-year study carried out on samples taken directly from production areas in 2009–2011. (Lowther et al. 2012b). However, until recently, data on final product as sold to the consumer in the UK have been lacking, with to the best of our knowledge the only published study having tested oysters from a single dispatch centre only (Lowther et al. 2010). As part of a wider project to establish the overall burden of foodborne norovirus in the UK (“NoVAS: Assessing the contribution made by the food chain to the burden of UK-acquired norovirus infection”—UK Food Standards Agency Project reference: FS101040), this study aimed to address this data gap, as well as to compare results for final product with those obtained in the previous production area survey. Materials and Methods Sampling Plan The survey design was informed by a comprehensive practical evaluation of the purchase routes for oysters available to the UK consumer. This evaluation was undertaken by a specialist product retrieval company contracted to collect the survey samples (Stericycle ExpertSOLUTIONS, Reading, UK), through phone interviews with and physical visits to identified vendors. This market research was conducted in 21 selected cities/regions across the UK (selected to give a good geographical spread and including regions in each of the four constituent countries of England, Wales, Scotland and Northern Ireland). Vendors directly available to consumers of oysters were subdivided into the following types: supermarkets, fishmongers, restaurants, online sales and 13 wholesalers. A total of 373 vendors were identified across the 21 areas. A randomised sampling plan was drawn up aiming to obtain a total of 630 oyster samples over a 1-year period (16th March 2015–15th March 2016), with monthly targets of 26 samples in the truncated months of March 201 (...truncated)