Processing strategies to inactivate enteric viruses in shellfish

Food and Environmental Virology

Volumn 2, Issue 3, 2010, Pages 183-193

  Richards, Gary P ^a   McLeod, Catherine ^b   Le Guyader, Françoise S ^c  

^a DELAWARE STATE UNIVERSITY   (United States)

^b SOUTH AUSTRALIAN RESEARCH AND DEVELOPMENT INSTITUTE   (Australia)

^c IFREMER   (France)

Author keywords

Depuration; Heat inactivation; Hepatitis A virus; High pressure; Norovirus; Processing; Shellfish

Indexed keywords

SEA WATER;

ACIDIFICATION; ADENOVIRUS; ARTICLE; ASTROVIRUS; COOKING; COOLING; DISINFECTION; ENTERIC VIRUS; EPIDEMIC; FOOD HANDLING; FOOD PROCESSING; FOOD QUALITY; FOOD SAFETY; FREEZING; HEPATITIS A; HEPATITIS A VIRUS; HEPATITIS E VIRUS; IRRADIATION; KOBUVIRUS; MARKET; NONHUMAN; NOROVIRUS; PASTEURIZATION; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAVIRUS; SAPOVIRUS; SHELLFISH; VESIVIRUS; VIRAL CONTAMINATION; VIRUS INACTIVATION; WATER CONTAMINATION;

AICHI VIRUS; ANIMALIA; ASTROVIRIDAE; ENTEROVIRUS; FELINE CALICIVIRUS; HEPATITIS A VIRUS; MURINE NOROVIRUS; NOROVIRUS; POLIOVIRUS; ROTAVIRUS; SAPOVIRUS;

EID: 77954761900     PISSN: 18670334     EISSN: 18670342     Source Type: Journal    
DOI: 10.1007/s12560-010-9045-2     Document Type: Article

References (90)

1. 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.
2. 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.
3. Ang, L. H. (1998). An outbreak of viral gastroenteritis associated with eating raw oysters. Communicable Disease and Public Health, 1, 38-40.
4. 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.
5. Anonymous. (2004a). Regulation (EC) No 852/2004. On the Hygiene of Foodstuffs. Official Journal of the European Union, L139/1, 1-54.
6. 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.
7. 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.
8. 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.
9. 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.
10. 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.
11. Beller, N. (1992). Hepatitis A outbreak in Anchorage, Alaska, traced to ice slush beverages. Western Journal of Medicine, 156, 624-627.
12. 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.
13. 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.
14. 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.
15. Brown, J. W. (1982). Economic analysis of "steam-shock" and "pasteurization" processes for oyster shucking. Marine Fisheries Review, 44, 21-25.
16. 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.
17. 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.
18. Canesi, L., Gallo, G., Gavioli, M., & Pruzzo, C. (2002). Bacteria-hemocyte interactions and phagocytosis in marine bivalves. Microscopy Research and Technique, 57, 469-476.
19. 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.
20. 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.
21. 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.
22. 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.
23. Cook, D. W., & Ellender, R. D. (1986). Relaying to decrease the concentration of oyster-associated pathogens. Journal of Food Protection, 49, 196-202.
24. 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.
25. 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.
26. 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.
27. 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.
28. Di Girolamo, R., Liston, J., & Matches, J. (1975). Uptake an elimination of poliovirus by West Coast oysters. Applied Microbiology, 29, 260-264.
29. DiGirolamo, R., Liston, J., & Matches, J. (1970). Survival of virus in chilled, frozen, and processed oysters. Applied Microbiology, 20, 58-63.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. 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.
51. 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.
52. Kingsley, D. H., Chen, H., & Hoover, D. G. (2004). Inactivation of selected picornaviruses by high hydrostatic pressure. Virus Research, 102, 221-224.
53. 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.
54. 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.
55. 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.
56. Kingsley, D. H., & Richards, G. P. (2003). Persistence of hepatitis A virus in oysters. Journal of Food Protection, 66, 331-334.
57. 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.
58. 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.
59. Lees, D. (2000). Viruses and bivalve shellfish. International Journal of Food Microbiology, 59, 81-116.
60. 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.
61. 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.
62. Liu, O. C., Seraichekas, H. R., & Murphy, B. L. (1967b). Viral depuration of the Northern quahaug. Applied Microbiology, 15, 307-315.
63. 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.
64. 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.
65. 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.
66. 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.
67. 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.
68. 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.
69. 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.
70. 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.
71. 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.
72. 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.
73. 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.
74. 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.
75. 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.
76. 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.
77. Richards, G. P. (1988). Microbial purification of shellfish: A review of depuration and relaying. Journal of Food Protection, 51(3), 218-251.
78. 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.
79. Richards, G. P. (1999). Limitations of molecular biological techniques for assessing the virological safety of foods. Journal of Food Protection, 62, 691-697.
80. 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.
81. 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.
82. 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.
83. 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.
84. 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.
85. 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.
86. 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.
87. Tomar, B. S. (1998). Hepatitis E in India. Zhonghua Min Guo Xiao Er Ke Yi Xue Hui Za Zhi, 39, 150-156.
88. 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.
89. Wang, D., Wu, Q., Kou, X., Yao, L., & Zhang, J. (2008). Distribution of norovirus in oyster tissues. Journal of Applied Microbiology, 105, 1966-1972.
90. 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.