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Processing Strategies to Inactivate Enteric Viruses in Shellfish

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Abstract

Noroviruses, hepatitis A and E viruses, sapovirus, astrovirus, rotavirus, Aichi virus, enteric adenoviruses, poliovirus, and other enteroviruses enter shellfish through contaminated seawater or by contamination during handling and processing, resulting in outbreaks ranging from isolated to epidemic. Processing and disinfection methods include shellfish depuration and relaying, cooking and heat pasteurization, freezing, irradiation, and high pressure processing. All the methods can improve shellfish safety; however, from a commercial standpoint, none of the methods can guarantee total virus inactivation without impacting the organoleptic qualities of the shellfish. Noroviruses cause the majority of foodborne viral illnesses, yet there is conflicting information on their susceptibility to inactivation by processing. The inability to propagate and quantitatively enumerate some viral pathogens in vitro or in animal models has led to the use of norovirus surrogates, such as feline calicivirus and murine norovirus. During processing, these surrogates may not mimic the inactivation of the viruses they represent and are, therefore, of limited value. Likewise, reverse transcription-PCR has limited usefulness in monitoring processing effectiveness due to its inability to identify infectious from inactivated viruses. This article (a) describes mechanisms of virus uptake and persistence in shellfish, (b) reviews the state-of-the-art in food processing strategies for the inactivation of enteric viruses in shellfish, (c) suggests the use of combined processing procedures to enhance shellfish safety, (d) highlights limitations in research data derived from virus surrogate studies and molecular assay procedures, and (e) recommends enhanced funding for human volunteer studies and the development of assays to detect viable viruses.

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References

  • Abad, F. X., Pintó, R. M., Gajardo, R., & Bosch, A. (1997). Viruses in mussels: Public health implications and depuration. Journal of Food Protection, 60, 677–681.

    Google Scholar 

  • Akin, E. W., Hamblet, F. E., & Hill, W. F. Jr. (1966). Accumulation and depuration of poliovirus by individual oysters (5 pp.). Gulf Coast Shellfish Sanitation Research Center, Dauphin Island, Alabama. Technical memorandum GCSSRC-FY66-5.

  • Ang, L. H. (1998). An outbreak of viral gastroenteritis associated with eating raw oysters. Communicable Disease and Public Health, 1, 38–40.

    CAS  PubMed  Google Scholar 

  • Anonymous. (1999). National Shellfish Sanitation Program Model Ordinance IV. Shellstock growing areas. Washington, DC: Department of Health and Human Services, U.S. Food and Drug Administration.

    Google Scholar 

  • Anonymous. (2004a). Regulation (EC) No 852/2004. On the Hygiene of Foodstuffs. Official Journal of the European Union, L139/1, 1–54.

    Google Scholar 

  • Anonymous. (2004b). Regulation (EC) No 853/2004. Laying down specific hygiene rules for food of animal origin. Official Journal of the European Union, L139/55, 55–151.

    Google Scholar 

  • Anonymous. (2004c). Regulation (EC) No 854/2004. Laying down specific rules for the organisation of official controls on products of animal origin intended for human consumption. Official Journal of the European Union, L155/206.

  • Bae, J., & Schwab, K. J. (2008). Evaluation of murine norovirus, feline calicivirus, poliovirus, and MS2 as surrogates for human norovirus in a model of viral persistence in surface water and groundwater. Applied and Environmental Microbiology, 74, 477–484.

    Article  CAS  PubMed  Google Scholar 

  • Baek, S. Y., Lim, S. Y., Lee, D. H., Min, K. H., & Kim, C. M. (2000). Incidence and characterization of Listeria monocytogenes from domestic and imported foods in Korea. Journal of Food Protection, 63, 186–189.

    CAS  PubMed  Google Scholar 

  • Belding, D. L., & Lane, F. C. (1909). The shellfisheries of Massachusetts: Their present condition and extent. In A report upon the mollusk shellfisheries of Massachusetts. Boston: Wright & Potter.

  • Beller, N. (1992). Hepatitis A outbreak in Anchorage, Alaska, traced to ice slush beverages. Western Journal of Medicine, 156, 624–627.

    CAS  PubMed  Google Scholar 

  • Belliot, G., Lavaux, A., Souihel, D., Agnello, D., & Pothier, P. (2008). Use of murine norovirus as a surrogate to evaluate resistance of human norovirus to disinfectants. Applied and Environmental Microbiology, 74, 3315–3318.

    Article  CAS  PubMed  Google Scholar 

  • Bidawid, S., Farber, J. M., Satter, S. A., & Hayward, S. (2000). Heat inactivation of hepatitis A virus in dairy foods. Journal of Food Protection, 63, 522–528.

    CAS  PubMed  Google Scholar 

  • Brett, M. S., Short, P., & McLauchlin, J. (1998). A small outbreak of listeriosis associated with smoked mussels. International Journal of Food Microbiology, 43, 223–229.

    Article  CAS  PubMed  Google Scholar 

  • Brown, J. W. (1982). Economic analysis of “steam-shock” and “pasteurization” processes for oyster shucking. Marine Fisheries Review, 44, 21–25.

    Google Scholar 

  • Cacopardo, B., Russo, R., Preiser, W., Benanti, F., Brancati, F., & Nunnari, A. (1997). Acute hepatitis E in Catania (eastern Sicily) 1980–1994. The role of hepatitis E virus. Infection, 25, 313–316.

    Article  CAS  PubMed  Google Scholar 

  • Calci, K. R., Meade, G. K., Tezloff, R. C., & Kingsley, D. H. (2005). High-pressure inactivation of hepatitis A virus within oysters. Applied and Environmental Microbiology, 71, 339–343.

    Article  CAS  PubMed  Google Scholar 

  • Canesi, L., Gallo, G., Gavioli, M., & Pruzzo, C. (2002). Bacteria-hemocyte interactions and phagocytosis in marine bivalves. Microscopy Research and Technique, 57, 469–476.

    Article  PubMed  Google Scholar 

  • Cannon, J. L., Papafragkou, E., Park, G. W., Osborne, J., Jaykus, L. A., & Vinjé, J. (2006). Surrogates for the study of norovirus stability and inactivation in the environment: A comparison of murine norovirus and feline calicivirus. Journal of Food Protection, 69, 2761–2765.

    PubMed  Google Scholar 

  • Chai, T., Liang, K. T., Pace, J., & Schlimme, D. V. (1991). Effect of heat processing on quality of pasteurized oysters. Journal of Food Science, 56, 1292–1294.

    Article  Google Scholar 

  • Chironna, M., Germinario, C., De Medici, D., Fiore, A., Di Pasquale, S., Quarto, M., et al. (2002). Detection of hepatitis A virus in mussels from different sources marketed in Puglia region (South Italy). International Journal of Food Microbiology, 75, 11–18.

    Article  CAS  PubMed  Google Scholar 

  • Conaty, S., Bird, P., Bell, G., Kraa, E., Grohmann, G., & McAnulty, J. M. (2000). Hepatitis A in New South Wales, Australia from consumption of oysters: The first reported outbreak. Epidemiology and Infection, 124, 121–130.

    Article  CAS  PubMed  Google Scholar 

  • Cook, D. W., & Ellender, R. D. (1986). Relaying to decrease the concentration of oyster-associated pathogens. Journal of Food Protection, 49, 196–202.

    Google Scholar 

  • Dawson, D. J., Paish, A., Staffell, L. M., Seymour, I. J., & Appleton, H. (2005). Survival of viruses on fresh produce, using MS2 as a surrogate for norovirus. Journal of Applied Microbiology, 98, 203–209.

    Article  CAS  PubMed  Google Scholar 

  • De Medici, D., Ciccozzi, M., Foire, A., Di Pasquale, S., Parlato, A., Ricci-Bitti, P., et al. (2001). Closed-circuit system for the depuration of mussels experimentally contaminated with hepatitis A virus. Journal of Food Protection, 64, 877–880.

    PubMed  Google Scholar 

  • de Roda Husman, A. M., Bijkerk, P., Lodder, W., van den Berg, H., Pribil, W., Cabaj, A., et al. (2004). Calicivirus inactivation by nonionizing (253.7-nanometer-wavelength [UV]) and ionizing (gamma) radiation. Applied and Environmental Microbiology, 70, 5089–5093.

    Article  PubMed  Google Scholar 

  • Di Girolamo, R., Liston, J., & Matches, J. (1972). Effects of irradiation on the survival of virus in West Coast oysters. Applied Microbiology, 24, 1005–1006.

    CAS  PubMed  Google Scholar 

  • Di Girolamo, R., Liston, J., & Matches, J. (1975). Uptake an elimination of poliovirus by West Coast oysters. Applied Microbiology, 29, 260–264.

    PubMed  Google Scholar 

  • DiGirolamo, R., Liston, J., & Matches, J. (1970). Survival of virus in chilled, frozen, and processed oysters. Applied Microbiology, 20, 58–63.

    CAS  PubMed  Google Scholar 

  • Doultree, J. C., Druce, J. D., Birch, C. J., Bowden, D. S., & Marshall, J. A. (1999). Inactivation of feline calicivirus, a Norwalk virus surrogate. Journal of Hospital Infection, 41, 51–57.

    Article  CAS  PubMed  Google Scholar 

  • Enriquez, R., Frösner, G. G., Hochstein-Mintzel, V., Riedemann, S., & Reinhardt, G. (1992). Accumulation and persistence of hepatitis A virus in mussels. Journal of Medical Virology, 37, 174–179.

    Article  CAS  PubMed  Google Scholar 

  • Filppi, J. A., & Banwart, G. J. (1974). Effect of the fat content of ground beef on the heat inactivation of poliovirus. Journal of Food Science, 39, 865–868.

    Article  Google Scholar 

  • Goldmintz, D., Babinchak, J. A., Richards, G. P., & Graikoski, J. T. (1983). Bacteriological evaluation of steam pasteurized oysters, Crassostrea virginica. Developments in Industrial Microbiology, 24, 457–466.

    Google Scholar 

  • Greening, G., Hewitt, J., Hay, B. E., & Grant, C. M. (2003). Persistence of Norwalk-like viruses over time in Pacific oysters grown in the natural environment. In A. Villalba, B. Reguera, J. L. Romalde, & R. Beiras (Eds.), Proceedings of the 4th international conference on molluscan shellfish safety (pp. 367–377). Conselleria de Pesca e Asuntos Maritimos da Xunta de Galacia and Intergovernmental Oceanographic Commission of UNESCO, Santiago de Compostela, Spain.

  • Grohmann, G. S., Murphy, A. M., Christopher, P. J., Auty, G., & Greenberg, H. B. (1981). Norwalk virus gastroenteritis in volunteers consuming depurated oysters. Australian Journal of Experimental Biology and Medical Science, 59, 219–228.

    Article  CAS  PubMed  Google Scholar 

  • Grove, S. F., Lee, A., Stewart, C. M., & Ross, T. (2009). Development of a high pressure processing inactivation model for hepatitis A virus. Journal of Food Protection, 72, 1434–1442.

    PubMed  Google Scholar 

  • Guillois-Bécel, Y., Couturier, E., Le Saux, J. C., Roque-Afonso, A. M., Le Guyader, F. S., Le Goas, A., et al. (2009). An oyster-associated hepatitis A outbreak in France in 2007. Eurosurveillance, 14, 1–6.

    Google Scholar 

  • Halliday, M. L., Kang, L. Y., Zhou, T. K., Hu, M. D., Pan, Q. C., Fu, T. Y., et al. (1991). An epidemic of hepatitis A attributable to the ingestion of raw clams in Shanghi, China. Journal of Infectious Diseases, 164, 852–859.

    CAS  PubMed  Google Scholar 

  • Hamblet, F. E., Hill, W. F., Jr., Akin, E. W., & Benton, W. H. (1969). Oysters and human viruses: Effects of seawater turbidity, on poliovirus uptake and elimination. American Journal of Epidemiology, 89, 562–571.

    CAS  PubMed  Google Scholar 

  • Harewood, P., Rippey, S., & Montesalvo, M. (1994). Effect of gamma irradiation on shelf life and bacterial and viral loads in hard-shelled clams (Mercenaria mercenaria). Applied and Environmental Microbiology, 60, 2666–2670.

    CAS  PubMed  Google Scholar 

  • Hay, B. E., & Scotti, P. (1986). Evidence for intracellular absorption of virus by the Pacific oyster, Crassostrea gigas. New Zealand Journal of Marine and Freshwater Research, 20, 655–659.

    Article  Google Scholar 

  • Herdman, W. A., & Boyce, R. (1899). Oysters and disease. An account of certain observations upon the normal and pathological history and bacteriology of the oyster and other shellfish (pp. 35–40). Lancashire Sea-Fisheries Memoir No. 1, London.

  • Herdman, W. A., & Scott, A. (1896). Report on the investigations carried out in 1895 in connection with the Lancashire Sea-Fisheries Laboratory at the University College, Liverpool. Proceedings and Transactions of the Liverpool Biological Society, 10, 103–174.

    Google Scholar 

  • Hewitt, J., & Greening, G. E. (2004). Survival and persistence of norovirus, hepatitis A virus, and feline calicivirus in marinated mussels. Journal of Food Protection, 67, 1743–1750.

    PubMed  Google Scholar 

  • Hewitt, J., & Greening, G. E. (2006). Effect of heat treatment on hepatitis A virus and norovirus in New Zealand greenshell mussels (Perna canaliculus) by quantitative real-time reverse transcription PCR and cell culture. Journal of Food Protection, 69, 2217–2223.

    PubMed  Google Scholar 

  • Hewitt, J., Rivera-Aban, M., & Greening, G. E. (2009). Evaluation of murine norovirus as a surrogate for human norovirus and hepatitis A virus in heat inactivation studies. Journal of Applied Microbiology, 107, 65–71.

    Article  CAS  PubMed  Google Scholar 

  • Hoff, J. C., & Becker, R. C. (1969). The accumulation and elimination of crude and clarified poliovirus suspensions by shellfish. American Journal of Epidemiology, 90, 53–61.

    CAS  PubMed  Google Scholar 

  • Jung, P.-M., Park, J. S., Park, J.-G., Park, J.-N., Han, I.-J., Song, B.-S., et al. (2009). Radiation sensitivity of poliovirus, a model for norovirus, inoculated in oyster (Crassostrea gigas) and culture broth under different conditions. Radiation Physics and Chemistry, 78, 597–599.

    Article  CAS  Google Scholar 

  • Khan, A. S., Moe, C. L., Glass, R. I., Monroe, S. S., Estes, M. K., Chapman, L. E., et al. (1994). Norwalk virus-associated gastroenteritis traced to ice consumption aboard a cruise ship in Hawaii: Comparison and application of molecular method-based assays. Journal of Clinical Microbiology, 32, 318–322.

    CAS  PubMed  Google Scholar 

  • Kingsley, D. H., & Chen, H. (2008). Aqueous matrix composition and pH influence feline calicivirus inactivation by high pressure processing. Journal of Food Protection, 71, 1598–1603.

    PubMed  Google Scholar 

  • Kingsley, D. H., & Chen, H. (2009). Influence of pH, salt, and temperature on pressure inactivation of hepatitis A virus. International Journal of Food Microbiology, 130, 61–64.

    Article  CAS  PubMed  Google Scholar 

  • Kingsley, D. H., Chen, H., & Hoover, D. G. (2004). Inactivation of selected picornaviruses by high hydrostatic pressure. Virus Research, 102, 221–224.

    Article  CAS  PubMed  Google Scholar 

  • Kingsley, D. H., Guan, D., Hoover, D. G., & Chen, H. (2006). Inactivation of hepatitis A virus by high-pressure processing: The role of temperature and pressure oscillation. Journal of Food Protection, 69, 2454–2459.

    PubMed  Google Scholar 

  • Kingsley, D. H., Holliman, D. R., Calci, K. R., Chen, H., & Flick, G. J. (2007). Inactivation of a norovirus by high-pressure processing. Applied and Environmental Microbiology, 73, 581–585.

    Article  CAS  PubMed  Google Scholar 

  • Kingsley, D. H., Hoover, D. G., Papafragkou, E., & Richards, G. P. (2002). Inactivation of hepatitis A virus and a calicivirus by high hydrostatic pressure. Journal of Food Protection, 65, 1605–1609.

    PubMed  Google Scholar 

  • Kingsley, D. H., & Richards, G. P. (2003). Persistence of hepatitis A virus in oysters. Journal of Food Protection, 66, 331–334.

    PubMed  Google Scholar 

  • Le Guyader, F. S., Le Saux, J. C., Ambert-Balay, K., Krol, J., Serais, O., Parnaudeau, S., et al. (2008). Aichi virus, norovirus, astrovirus, enterovirus, and rotavirus involved in clinical cases from a French oyster-related gastroenteritis outbreak. Journal of Clinical Microbiology, 46, 4011–4017.

    Article  PubMed  Google Scholar 

  • Le Guyader, F. S., Loisy, F., Atmar, R. L., Hutson, A. M., Estes, M. K., Ruvoen, N., et al. (2006). Norwalk virus-specific binding to oyster digestive tissues. Emerging Infectious Diseases, 12, 931–936.

    PubMed  Google Scholar 

  • Lees, D. (2000). Viruses and bivalve shellfish. International Journal of Food Microbiology, 59, 81–116.

    Article  CAS  PubMed  Google Scholar 

  • Liu, O. C. (1968). Appraisal and planning of virus research program (38 pp.). Northeast Shellfish Sanitation Research Center, U.S. Public Health Service, Narragansett, Rhode Island.

  • Liu, O. C., Seraichekas, H. R., & Murphy, B. L. (1967a). Viral pollution and self-cleansing mechanisms of hard clams. In G. Berg (Ed.), Transmission of viruses by the water route (pp. 419–437). New York: Interscience Publishers.

    Google Scholar 

  • Liu, O. C., Seraichekas, H. R., & Murphy, B. L. (1967b). Viral depuration of the Northern quahaug. Applied Microbiology, 15, 307–315.

    CAS  PubMed  Google Scholar 

  • Loisy, F., Atmar, R. L., Le Le Saux, J. C., Cohen, J., Caprais, M. P., Pommepuy, M., et al. (2005). Use of rotavirus virus-like particles as surrogates to evaluate virus persistence in shellfish. Applied and Environmental Microbiology, 71, 6049–6053.

    Article  CAS  PubMed  Google Scholar 

  • Mallet, J. C., Beghian, L. E., Metcalf, T. G., & Kaylor, J. D. (1991). Potential of irradiation technology for improved shellfish sanitation. Journal of Food Safety, 11, 231–245.

    Article  Google Scholar 

  • McLeod, C., Hay, B., Grant, C., Greening, G., & Day, D. (2009a). Localization of norovirus and poliovirus in Pacific oysters. Journal of Applied Microbiology, 106, 1220–1230.

    Article  CAS  PubMed  Google Scholar 

  • McLeod, C., Hay, B., Grant, C., Greening, G., & Day, D. (2009b). Inactivation and elimination of human enteric viruses by Pacific oysters. Journal of Applied Microbiology, 107, 1809–1818.

    Article  CAS  PubMed  Google Scholar 

  • Meinhold, A. F., & Sobsey, M. D. (1982). The uptake, elimination and tissue distribution of poliovirus in the American oyster, Crassostrea virginica (p. 181). Abstracts of the Annual Meeting of the American Society for Microbiology.

  • Metcalf, T. G., Mullin, B., Eckerson, D., Moulton, E., & Larkin, E. P. (1979). Bioaccumulation and depuration of enteroviruses by the soft-shelled clam, Mya arenaria. Applied and Environmental Microbiology, 38, 275–282.

    CAS  PubMed  Google Scholar 

  • Millard, J., Appleton, H., & Parry, J. V. (1987). Studies on heat inactivation of hepatitis A virus with special reference to shellfish. Part 1. Procedures for infection and recovery of virus from laboratory-maintained cockles. Epidemiology and Infection, 98, 397–414.

    Article  CAS  PubMed  Google Scholar 

  • Mitchell, J. R., Presnell, M. W., Akin, E. W., Cummings, J. M., & Liu, O. C. (1966). Accumulation and elimination of poliovirus by the Eastern oyster. American Journal of Epidemiology, 84, 40–50.

    CAS  PubMed  Google Scholar 

  • Mokhtari, A., & Jaykus, L. A. (2009). Quantitative exposure model for the transmission of norovirus in retail food preparation. International Journal of Food Microbiology, 133, 38–47.

    Article  PubMed  Google Scholar 

  • Mormann, S., Dabisch, M., & Becker, B. (2010). Effects of technological processes on the tenacity and inactivation of norovirus GGII in experimentally contaminated foods. Applied and Environmental Microbiology, 76, 536–545.

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa-Okamoto, R., Arita-Nishida, T., Todo, S., Kato, H., Iwata, H., Akiyama, M., et al. (2009). Detection of multiple sapovirus genotypes and genogroups in oyster-associated outbreaks. Japanese Journal of Infectious Diseases, 62, 63–66.

    CAS  PubMed  Google Scholar 

  • Nuanualsuwan, S., Mariam, T., Himathongkham, S., & Cliver, D. O. (2002). Ultraviolet inactivation of feline calicivirus, human enteric viruses and coliphages. Photochemistry and Photobiology, 76, 406–410.

    Article  CAS  PubMed  Google Scholar 

  • Power, U. F., & Collins, J. K. (1989). Differential depuration of poliovirus, Escherichia coli, and a coliphage by the common mussel, Mytilus edulis. Applied and Environmental Microbiology, 55, 1386–1390.

    CAS  PubMed  Google Scholar 

  • Power, U. F., & Collins, J. K. (1990). Tissue distribution of a coliphage and Escherichia coli in mussels after contamination and depuration. Applied and Environmental Microbiology, 56, 803–807.

    CAS  PubMed  Google Scholar 

  • Richards, G. P. (1988). Microbial purification of shellfish: A review of depuration and relaying. Journal of Food Protection, 51(3), 218–251.

    Google Scholar 

  • Richards, G. P. (1991). Shellfish depuration, Chap. 16. In D. R. Ward & C. R. Hackney (Eds.), Microbiology of marine food products (pp. 395–428). New York: Van Nostrand Reinhold.

    Google Scholar 

  • Richards, G. P. (1999). Limitations of molecular biological techniques for assessing the virological safety of foods. Journal of Food Protection, 62, 691–697.

    CAS  PubMed  Google Scholar 

  • Richards, G. P., Watson, M. A., & Kingsley, D. H. (2004). A SYBR green, real-time RT-PCR method to detect and quantitate Norwalk virus in stools. Journal of Virological Methods, 116, 63–70.

    Article  CAS  PubMed  Google Scholar 

  • Romalde, J. L., Estes, M. K., Szücs, G., Atmar, R. L., Woodley, C. M., & Metcalf, T. G. (1994). In situ detection of hepatitis A virus in cell cultures and shellfish tissues. Applied and Environmental Microbiology, 60, 1921–1926.

    CAS  PubMed  Google Scholar 

  • Schwab, K. J., Neill, F. H., Estes, M. K., Metcalf, T. G., & Atmar, R. L. (1998). Distribution of Norwalk virus within shellfish following bioaccumulation and subsequent depuration by detection using RT-PCR. Journal of Food Protection, 61, 1674–1680.

    CAS  PubMed  Google Scholar 

  • Seamer, C. (2007). The biology of virus uptake and elimination by Pacific oysters (Crassostrea gigas) (pp. 239). School of Biological Sciences. Wellington, Victoria University of Wellington. PhD Thesis.

  • Seraichekas, H. R., Brashear, D. A., Barnick, J. A., Carey, P. F., & Liu, O. C. (1968). Viral depuration by assaying individual shellfish. Applied Microbiology, 16, 1865–1871.

    CAS  PubMed  Google Scholar 

  • Shimasaki, N., Kiyohara, T., Totsuka, A., Nojima, K., Okada, Y., Kajioka, J., et al. (2009). Inactivation of hepatitis A virus by heat and high hydrostatic pressure: Variation among laboratory strains. Vox Sanguinis, 96, 14–19.

    Article  CAS  PubMed  Google Scholar 

  • Sobsey, M. D., Davis, A. L., & Rullman, V. A. (1987). Persistence of hepatitis A virus and other viruses in depurated Eastern oysters. Proceedings Oceans, 87(5), 1740–1745.

    Google Scholar 

  • Tomar, B. S. (1998). Hepatitis E in India. Zhonghua Min Guo Xiao Er Ke Yi Xue Hui Za Zhi, 39, 150–156.

    CAS  PubMed  Google Scholar 

  • Ueki, Y., Shoji, M., Suto, A., Tanabe, T., Okimura, Y., Kikuchi, Y., et al. (2007). Persistence of calicivirus in artificially contaminated oysters during depuration. Applied and Environmental Microbiology, 73, 5698–5701.

    Article  CAS  PubMed  Google Scholar 

  • Wang, D., Wu, Q., Kou, X., Yao, L., & Zhang, J. (2008). Distribution of norovirus in oyster tissues. Journal of Applied Microbiology, 105, 1966–1972.

    Article  CAS  PubMed  Google Scholar 

  • Wolf, S., Rivera-Aban, M., & Greening, G. E. (2009). Long-range reverse transcription as a useful tool to assess the genomic integrity of norovirus. Food and Environmental Virology, 1, 129–136.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. U.S. Department of Agriculture, Agricultural Research Service, Microbial Food Safety Research Unit, Delaware State University, Dover, DE, 19901, USA

    Gary P. Richards

  2. South Australian Research and Development Institute, GPO Box 397, Adelaide, South Australia, 5001, Australia

    Catherine McLeod

  3. Laboratoire de Microbiologie, Centre de Nantes, IFREMER, Rue de L’lle O’yeu, B.P. 21105, 44311, Nantes Cedex 03, France

    Françoise S. Le Guyader

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  1. Gary P. Richards
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  2. Catherine McLeod
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  3. Françoise S. Le Guyader
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Correspondence to Gary P. Richards.

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Richards, G.P., McLeod, C. & Le Guyader, F.S. Processing Strategies to Inactivate Enteric Viruses in Shellfish. Food Environ Virol 2, 183–193 (2010). https://doi.org/10.1007/s12560-010-9045-2

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