National survey of foodborne viruses in Australian oysters at production
Introduction
Human enteric viruses are increasingly recognised as important causes of foodborne disease globally, based on the incidence of reported foodborne disease and the severity of disease (including mortality) (FAO/WHO, 2008, FAO/WHO, 2012). International estimates of the proportion of enteric virus illnesses attributed to food are in the range of approximately 5% for hepatitis A virus (HAV) and 12–47% for norovirus (NoV). The virus-commodity combinations of greatest public health concern are NoV and HAV in bivalve molluscs, fresh produce and prepared (ready-to-eat) foods (FAO/WHO, 2008, FAO/WHO, 2012). A systematic review of global shellfish related viral foodborne outbreaks between 1980 and 2012 reported NoV (83.7%) and HAV (12.8%) as the most common viral pathogens and oysters (58.4%) as the most frequently consumed shellfish associated with outbreaks (Bellou et al., 2013). The majority of the reported outbreaks have been located in East Asia, followed by Europe, America, Oceania, Australia and Africa (Bellou et al., 2013). In Australia, between 2001 and 2010, seventeen suspected foodborne outbreaks of NoV or unknown aetiology were associated with consumption of bivalve shellfish, which included imported product (OzFoodNet Reports). A recent oyster related outbreak of NoV occurred in 2013 with 525 people affected nationally following consumption of contaminated oysters from Tasmania (Lodo et al., 2014).
As there are currently no effective control measures available to eliminate these viruses from food without changing the characteristics of the product, the most effective risk management strategy for NoV and HAV in bivalve shellfish is to prevent contamination in production areas. Freezing of shellfish does not deactivate foodborne viruses, but rather preserves them (EFSA, 2012). High-risk factors for contamination of oysters with enteric viruses include low water temperatures (allowing greater persistence of the viruses), elevated prevalence of enteric illness within the community and high rainfall leading to sewage system overflows (CEFAS, 2011).
In 2012, the Codex Alimentarius commission released guidelines on general principles of food hygiene to control viruses in food, with Annex I specifically focusing on control of HAV and NoV in bivalve molluscs (FAO/WHO, 2008). It recommended that countries monitor for NoV and HAV in bivalves following shellfish-related foodborne outbreaks and high-risk pollution events (heavy rainfall and overflow from sewage treatment plants). The EU legislation on the microbiological criteria for foodstuff has suggested that “criteria for pathogenic viruses in live bivalve molluscs should be established when the analytical methods are developed sufficiently” (EC, 2005). With the development of the ISO/TS 15216 method “Microbiology of food and animal feed - horizontal method for the determination of hepatitis A virus and norovirus in food using real-time RT-PCR” (ISO/CEN, 2013), virus methods have become available that may be considered suitable for use in legislation. Hence, consideration is being given to establishing virus limits for high-risk live bivalve molluscs. The EFSA Scientific Opinion on NoV in oysters recommended: the establishment of an acceptable limit for NoV in oysters to be harvested and placed on the market; NoV testing of oysters to verify compliance with the acceptable NoV limits established; and for food businesses to verify their Hazard Analysis and Critical Control Points plans and demonstrate compliance with acceptable levels (EFSA, 2012). In 2012, the EU Community Reference Laboratory recommended that if virus standards are introduced, then standards for NoV should be quantitative (i.e. a maximum acceptable level) and standards for HAV be qualitative (i.e. presence/absence) (CEFAS, 2013). It also considered and made recommendations on possible levels for a NoV standard in the context of both end-product and production area monitoring applications (CEFAS, 2013). The EU is current undertaking a two year survey to establish European prevalence of NoV contaminated oysters at the production area and dispatch centre levels (EFSA, 2016). Following this survey, the European Commission will appraise the results and decide whether microbiological criteria for NoV are appropriate.
The prevalence of NoV in oysters internationally has been reported to range from 2.4% to 76.2% (Lowther et al., 2012, Pavoni et al., 2013, Suffredini et al., 2014). Information on the prevalence of NoV in Australian oysters is limited, but suggests a low prevalence. A study of oysters from growing areas at risk of contamination, over a range of environmental conditions, found NoV in 1.7% of oysters sampled (Brake et al., 2014). As a response to the impending international regulations (noting that some nations already require NoV testing on imported products e.g. Singapore), the Australian oyster industry desired a more comprehensive evaluation of the prevalence of enteric foodborne viruses in Australian oysters at production. Similar surveys have been undertaken worldwide, and have found that the prevalence of foodborne viruses in oysters obtained in market products were comparable to those observed in commercial harvesting areas (EFSA, 2012). The current study aimed to estimate the national prevalence of NoV and HAV in Australian oysters suitable for harvest. The survey used the ISO/TS 15216 standard testing methodology for foodborne viruses in shellfish and a robust statistical sampling plan conducted over two rounds of sampling between July 2014 and August 2015.
Section snippets
Survey design
The design called for a total of 300 oyster samples to be collected over 13 months between July 2014 and August 2015 in two sampling periods, representing a winter/spring (round 1) and a summer/autumn (round 2) period. A sample size of 150 for each of the two sampling rounds would provide a statistical probability of 0.95 of detecting at least one sample with detectable levels of viruses if ≥2% of the samples were contaminated. The sample size calculation was based on the binomial distribution:
National oyster sampling
Between 2007–08 and 2011–12, the annual average production of oysters per state was valued at AU $40.7 million, AU $0.5 million, AU $34.6 million and AU $21.8 million for NSW, Qld, SA and Tas, respectively (ABARES, 2012). Production in other Australian states is insignificant by value and not captured in the statistics. The proportion of state oyster production to the overall national annual production (by value) was used to allocate sample numbers for collection from each state. For NSW, 63
Discussion
This is the first Australian survey of foodborne viruses in commercially produced oysters where the sampling plan has been statistically designed to estimate prevalence based on production by region. This survey only sampled mature shellfish taken from harvest areas which were open for harvest. For Tas, SA and Qld this represented oysters that were considered to be fit for direct harvest and consumption. For NSW, this represented either oysters fit for direct harvest and consumption, or fit for
Conclusions
This national survey of Australian oysters destined for market resulted in an estimated prevalence of NoV and HAV of <2%, with no virus positive samples detected and no related foodborne illnesses reported. Although, there will always be a risk of foodborne viral illness associated with oysters when product is eaten raw, especially if grown in water that can be impacted by sewage and environmental run-off; the results of this study suggest that the viral contamination risk was low for the
Acknowledgments
We acknowledge the financial support of the Fisheries Research and Development Corporation (grant number: FRDC 2013/234), Oysters Australia, Tasmanian Oyster Research Council, Tasmanian Shellfish Executive Committee, South Australian Oyster Research Council, South Australian Shellfish Quality Assurance Program and New South Wales Food Authority. We acknowledge the Australian oyster industries and state Shellfish Quality Assurance Programs for their in principle support of the project and
References (44)
- et al.
A survey of Australian oysters for the presence of human noroviruses
Food Microbiol.
(2014) - et al.
Use of FRNA bacteriophages to indicate the risk of norovirus contamination in Irish oysters
J. Food Prot.
(2009) - et al.
Depuration dynamics of viruses in shellfish
Int. J. Food Microbiol.
(2002) - et al.
Viral elimination during commercial depuration of shellfish
Food Control
(2014) - et al.
Detection and quantification of hepatitis A virus and norovirus in Spanish authorized shellfish harvesting areas
Int. J. Food Microbiol.
(2015) - et al.
Norovirus contamination on French marketed oysters
Int. J. Food Microbiol.
(2013) - et al.
Seasonal and regional prevalence of norovirus, hepatitis A virus, hepatitis E virus, and rotavirus in shellfish harvested from South Korea
Food Control
(2014) - et al.
Qualitative and quantitative assessment of viral contamination in bivalve molluscs harvested in Italy
Int. J. Food Microbiol.
(2014) Table 1: Gross Value of Fisheries Production
(2012)- et al.
The Annual Cost of Foodborne Illness in Australia
(2006)
Australian Shellfish Quality Assurance Program, Operations Manual
Shellfish-borne viral outbreaks: a systematic review
Food Environ. Virol.
Norovirus and other human enteric viruses in Moroccan shellfish
Food Environ. Virol.
Investigation into the Prevalence, Distribution and Levels of Norovirus Titre in Oyster Harvesting Areas in the UK
Discussion Paper on Live Bivalve Molluscs (LBM) and Human Enteric Virus Contamination: Options for Improving Risk Management in EU Food Hygiene Package
Hepatitis A in New South Wales, Australia from consumption of oysters: the first reported outbreak
Epidemiol. Infect.
Human and animal enteric caliciviruses in oysters from different coastal regions of the United States
Appl. Environ. Microbiol.
Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: different behaviors of genogroups I and II
Appl. Environ. Microbiol.
Bacterial and viral pathogens in live oysters: 2007 United States market survey
Appl. Environ. Microbiol.
Management of health risks associated with oysters harvested from a norovirus contaminated area, Ireland, February-March 2010
Eurosurveillance
Annex II of Commission Regulation (EC) No 854/2004 on Laying Down Specific Rules for the Organisation of Official Controls on Products of Animal Origin Intended for Human Consumption
Commission Regulation (EC) No 2073/2005 on Microbiological Criteria for Foodstuffs
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