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Food and Environmental Virology

, Volume 5, Issue 1, pp 13–23 | Cite as

Shellfish-Borne Viral Outbreaks: A Systematic Review

  • M. Bellou
  • P. Kokkinos
  • A. Vantarakis
Review Paper

Abstract

Investigations of disease outbreaks linked to shellfish consumption have been reported in the scientific literature; however, only few countries systematically collate and report such data through a disease surveillance system. We conducted a systematic review to investigate shellfish-borne viral outbreaks and to explore their distribution in different countries, and to determine if different types of shellfish and viruses are implicated. Six databases (Medline, Embase, Scopus, PubMed, Eurosurveillance Journal and Spingerlink electronic Journal) and a global electronic reporting system (ProMED) were searched from 1980 to July 2012. About 359 shellfish-borne viral outbreaks, alongside with nine ProMED reports, involving shellfish consumption, were identified. The majority of the reported outbreaks were located in East Asia, followed by Europe, America, Oceania, Australia and Africa. More than half of the outbreaks (63.6 %) were reported from Japan. The most common viral pathogens involved were norovirus (83.7 %) and hepatitis A virus (12.8 %). The most frequent type of consumed shellfish which was involved in outbreaks was oysters (58.4 %). Outbreaks following shellfish consumption were often attributed to water contamination by sewage and/or undercooking. Differences in reporting of outbreaks were seen between the scientific literature and ProMED. Consumption of contaminated shellfish represents a risk to public health in both developed and developing countries, but impact will be disproportionate and likely to compound existing health disparities.

Keywords

Shellfish Outbreak Viral infection Consumption Sewage 

References

  1. Alfano-Sobsey, E., Sweat, D., Hall, A., Breedlove, F., Rodriguez, R., Greene, S., et al. (2012). Norovirus outbreak associated with undercooked oysters and secondary household transmission. Epidemiology and Infection, 140, 276–282.PubMedCrossRefGoogle Scholar
  2. Anon. (1992). Shellfish-associated illness. Communicable Disease Report Weekly, 2, 39.Google Scholar
  3. Anon. (1993). Shellfish-associated illness. Communicable Disease Report Weekly, 3, 29.Google Scholar
  4. Anon. (1996). Small round structured viruses. Communicable Disease Report Weekly, 6, 207.Google Scholar
  5. Anon, (1998). Outbreaks of gastroenteritis in England and associated with shellfish: 1996 and 1997. Communicable Disease Report, 8, 21–24.Google Scholar
  6. Baker, K., Morris, J., McCarthy, N., Saldana, L., Lowther, J., Collinson, et al. (2010). An outbreak of norovirus infection linked to oyster consumption at a UK restaurant, February 2010. Journal of Public Health, 3(2), 205–211.Google Scholar
  7. Berg, D. E., Kohn, M. A., Farley, T. A., & McFarland, L. M. (2000). Multi-state outbreaks of acute gastroenteritis traced to fecal-contaminated oysters harvested in Louisiana. Journal of Infectious Diseases, 181(2), 381–386.CrossRefGoogle Scholar
  8. Beuret, C., Baumgarther, A., & Schluep, J. (2003). Virus-contaminated oysters: a three-month monitoring of oysters imported to Switzerland. Applied and Environmental Microbioly, 69(4), 2292–2297.CrossRefGoogle Scholar
  9. Bialek, S. R., Prethiba, A., Guo-Liang, X. G., Glatzer, M. B., Motes, M. L., Veazy, J. E., et al. (2007). Use of molecular epidemiology to confirm a multistate outbreak of hepatitis A caused by consumption of oysters. Clinical Infectious Diseases, 44, 838–840.PubMedCrossRefGoogle Scholar
  10. Bon, F., Ambert-Balay, K., Giraudon, H., Kaplon, J., Le Guyader, S., Pommepuy, M. et al. (2005). Molecular epidemiology of Caliciviruses detected in sporadic and outbreak cases of gastroenteritis in France from December 1998 to February 2004. Journal of Clinical Microbiology, 43(9), 4659–4664.Google Scholar
  11. Boxman, I. L., Tilburg, J. J., Te Loeke, N. A., et al. (2006). Detection of noroviruses in shellfish in the Netherlands. International Journal of Food Microbiology, 108, 391–396.PubMedGoogle Scholar
  12. Burkhardt, W., & Calci, K. R. (2000). Selective accumulation may account for shellfish-associated viral illness. Applied and Environmental Microbiology, 66, 1375–1378.PubMedCrossRefGoogle Scholar
  13. Cann, K. F., Thomas, D. R., Salmon, R. L., Wyn-Jones, A. P., & Kay, D. (2012). Extreme water-related weather events and waterborne disease. Epidemiology and Infection, 9, 1–16.Google Scholar
  14. Chalmers, J. W. T., & McMillan, J. H. (1995). An outbreak of viral gastroenteritis associated with adequately prepared oysters. Epidemiology and Infection, 115, 163–167.PubMedCrossRefGoogle Scholar
  15. Cheng, P. K., Wong, D. K., Chung, T. W., & Lim, W. W. (2005). Norovirus contamination found in oysters worldwide. Journal of Medical Virology, 76, 593–597.PubMedCrossRefGoogle Scholar
  16. Christensen, B. F., Lees, D., Henshilwood, K., Bjergskov, T., & Green, J. (1998). Human enteric viruses in oysters causing a large outbreak of human food borne infection in 1996/97. Journal of Shellfish Research, 17(5), 1633–1635.Google Scholar
  17. Chua, S. B., Lim, S., Ooi, P. L., Chew, S. K., & Goh, K. T. (2005). Oyster-associated outbreaks of norovirus gastroenteritis in Singapore. Journal of Infection, 51, 413–418.PubMedCrossRefGoogle Scholar
  18. 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.PubMedCrossRefGoogle Scholar
  19. David, S. T., McIntyre, L., MacDougall, L., Kelly, D., Liem, S., Schallié, K., et al. (2007). An outbreak of norovirus caused by consumption of oysters from geographically dispersed harvest sites, British Columbia, Canada, 2004. Foodborne Pathogens and Disease, 4(3), 349–358.Google Scholar
  20. Davis, C., Smith, A., Walden, R., et al. (1994). Viral gastroenteritis associated with consumption of raw oysters—Florida, 1993. The Journal of the American Medical Association, 272, 510–511.CrossRefGoogle Scholar
  21. Desenclos, J. C. A., Klontz, K. C., Wilder, M. H., Naiman, O. V., Margolis, H. S., & Gunn, R. A. (1991). A multistate outbreak of hepatitis A caused by the consumption of raw oysters. American Journal of Public Health, 81, 1268–1272.PubMedCrossRefGoogle Scholar
  22. Dore, B., Keaveneyl, S., Flannery, J., & Rajko-Nenow, P. (2010). Management of health risks associated with oysters harvested from a norovirus contaminated area, Ireland, 2010. Eurosurveillance, 15(19).Google Scholar
  23. Dowell, S. F., Groves, C., Kirkland, K. B., Cicirello, H. G., Ando, T., Jin, Q., et al. (1995). A multistate outbreak of oyster-associated gastroenteritis: Implications for interstate tracing of contaminated shellfish. Journal of Infectious Diseases, 171(6), 1497–1503.PubMedCrossRefGoogle Scholar
  24. Doyle, A., Barataud, D., Gallay, A., Thiolet, J. M., Le Guyader, S., Kohli, E., et al. (2004). Norovirus foodborne outbreaks associated with the consumption of oysters from the Etang de Thau, France, December 2002. Eurosurveillance, 9(3), 24–26.PubMedGoogle Scholar
  25. Farley, T. A., McFarland, L., Estes, M., & Schwab, K. (1998). Viral gastroenteritis associated with eating oysters—Louisiana, December 1996 to January 1997. The Journal of the American Medical Association, 279, 10–11.CrossRefGoogle Scholar
  26. Fleet, G. H., Heiskanen, P., Reid, I., & Buckle, K. A. (2000). Foodborne viral illness—status in Australia. International Journal of Food Microbiology, 59, 127–136.PubMedCrossRefGoogle Scholar
  27. Gail, E., & McCoubrey, D. J. (2010). Enteric viruses and management of shellfish production in New Zealand. Food and Environmental Virology, 2, 167–175.CrossRefGoogle Scholar
  28. Gallimore, C. I., Cheesbrough, J. S., Lamden, K., Bingham, C., & Gray, J. J. (2005). Multiple norovirus genotypes characterised from an oyster-associated outbreak of gastroenteritis. International Journal of Food Microbiology, 103, 323–330.PubMedCrossRefGoogle Scholar
  29. Galmés Truyols, A., Duran, J. G., Riutort, A. N., Cerdá, G. A., Isabel, C. B., Arbona, M. P., & Berga, J. V. (2011). Norovirus outbreak in Majorca (Spain) associated with oyster consumption. Gaceta Sanitaria, 25, 173–175.PubMedCrossRefGoogle Scholar
  30. Godoy, P., Torres, J., Guix, S., Prat, A., Alsedà, M., Domínguez, A., et al. (2000). Outbreak of food-borne associated with oysters consumption caused by norwalk-like virus. Medicina Clinica, 114(20), 765–768.PubMedGoogle Scholar
  31. Graczyk, T. K., & Schwab, K. J. (2000). Food borne infections vectored by molluscan shellfish. Current gastroenterology reports, 2, 305–309.PubMedCrossRefGoogle Scholar
  32. Guillois-Becel, 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(10).Google Scholar
  33. Hossen, V., Jourdan-da, N., Guillois-Bécel, Y., Marchal, J., & Krys, S. (2009). Food poisoning outbreaks linked to mussels contaminated with okadaic acid and ester dinophysistoxin-3 in France, June 2009. Eurosurveillance, 16(46).Google Scholar
  34. Iizuka, S., Oka, T., Tabara, K., Omura, T., Katayama, K., Takeda, N., et al. (2010). Detection of sapoviruses and noroviruses in an outbreak of gastroenteritis linked genetically to shellfish. Journal of Medical Virology, 82, 1247–1254.PubMedCrossRefGoogle Scholar
  35. Inouye, S., Yamashita, K., Yamadera, S., Yoshikawa, M., Kato, N., Okable, N. (2000). Surveillance of viral gastroenteritis in Japan: Pediatric cases and outbreak incidents. Infectious Disease Surveillance Center, 187(2), 270–274.Google Scholar
  36. Iritani, N., Kubo, H., Abe, N., Goto, K., Ogura, H., & Seto, Y. (2010). Molecular epidemiology of noroviruses detected in seasonal outbreaks of acute nonbacterial gastroenteritis in Osaka city, Japan, from 1996–1997 to 2008–2009. Journal of Medical Virology, 82, 2097–2105.PubMedCrossRefGoogle Scholar
  37. James, C. (Ed.). (2000). Control of communicable disease manual. Washington DC: American Public Health Association.Google Scholar
  38. Kaplan, J. E., Feldman, R., Campbell, D. S., Lookabaugh, C., & Gary, G. W. (1982). The frequency of a norwalk-like pattern of illness in outbreaks of acute gastro enteritis. American Journal of Public Health, 72, 1329–1332.PubMedCrossRefGoogle Scholar
  39. Karagiannis, I., Detsis, M., Gkolfinopoulou, K., Pervanidou, D., Panagiotopoulos, T., & Bonovas, S. (2010). An outbreak of gastroenteritis linked to seafood consumption in a remote Northern Aegean island, February-March 2010. Rural and Remote Health, 10, 1507.PubMedGoogle Scholar
  40. Kingsley, D. H., Meade, G. K., & Richards, G. P. (2002). Detection of both hepatitis A virus and norwalklike virus in imported clams associated with food-borne illness. Applied and Environmental Microbiology, 68, 3914–3918.PubMedCrossRefGoogle Scholar
  41. Kohn, M. A., Farley, T. A., Ando, T., Curtis, M., Wilson, S. A., Jin, Q., et al. (1995). An outbreak of norwalk virus gastroenteritis associated with eating raw oysters: implications for maintaining safe oyster beds. Journal of the American Medical Association, 273(6), 466–471.PubMedCrossRefGoogle Scholar
  42. Koopmans, M., & Duizer, E. (2004). Foodborne viruses: an emerging problem. International Journal of Food Microbiology, 90, 23–41.PubMedCrossRefGoogle Scholar
  43. Le Guyader, F. S., Bon, F., DeMedici, D., et al. (2006). Detection of multiple noroviruses associated with an international gastroenteritis outbreak linked to oyster consumption. Journal of Clinical Microbiology, 44, 3878–3882.PubMedCrossRefGoogle Scholar
  44. Le Guyader, F. S., Le Saux, J. C., Ambert-Balay, K., 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(12), 4011–4017.PubMedCrossRefGoogle Scholar
  45. Le Guyader, F. S., Neill, F. H., Dubois, E., Bon, F., Loisy, F., Kohli, E., et al. (2003). A semi-quantitative approach to estimate norwalk-like virus contamination of oysters implicated in an outbreak. International Journal of Food Microbiology, 87, 107–112.PubMedCrossRefGoogle Scholar
  46. Le Guyader, F. S., Parnaudeau, S., Schaeffer, J., et al. (2009). Detection and quantification of noroviruses in shellfish. Applied and Environmental Microbiology, 75(3), 618–624.PubMedCrossRefGoogle Scholar
  47. Lee, H. C., Ang, L. W., Chiew, P. K. T., James, L., & Goh, T. K. (2011). Changing epidemiological patterns of hepatitis a infection in Singapore. Annals Academy of Medicine Singapore, 40, 439–447.Google Scholar
  48. Lee, T., Yam, W. C., Tam, T. Y., Ho, B. S. W., Ng, N. H., & Broom, M. J. (1999). Occurrence of hepatitis A virus in green-lipped mussels (Perna viridis). Water Research, 33, 885–889.CrossRefGoogle Scholar
  49. Lees, D. (2000). Viruses and bivalve shellfish. International Journal of Food Microbiology, 51, 81–116.CrossRefGoogle Scholar
  50. Leoni, E., Bevini, C., Degli Esposti, S., & Graziano, A. (1998). An outbreak of intrafamiliar hepatitis A associated with clam consumption: epidemic transmission to a school community. European Journal of Epidemiology, 14, 187–192.PubMedCrossRefGoogle Scholar
  51. Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P., Ioannidis, J. P. A., et al. (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Journal of Clinical Epidemiology, 62, e1–ee34.Google Scholar
  52. Lowther, J. A., Gustar, N. E., Hartnell, R. E., & Lees, D. N. (2012). Comparison of norovirus RNA levels in outbreak-related oysters with background environmental levels. Journal of Food Protection, 75(2), 389–393.PubMedCrossRefGoogle Scholar
  53. Maalouf, H., Pommepuy, M., & Le Guyader, F. S. (2010). Environmental conditions leading to shellfish contamination and related outbreaks. Food and Environmental Virology, 2(3), 136–145.CrossRefGoogle Scholar
  54. McDonnell, S., Kirkland, K. B., Hlady, W. G., Aristeguieta, C., Hopkins, R. S., Monroe, S. S., et al. (1997). Failure of cooking to prevent shellfish-associated viral gastroenteritis. Archives of Internal Medicine, 157, 111–116.PubMedCrossRefGoogle Scholar
  55. Morse, D. L., Guzewich, J. J., Hanrahan, J. P., Stricof, R., Shayegani, M., Deibel, R., et al. (1986). Widespread outbreaks of clam- and oyster- associated gastroenteritis. The New England Journal of Medicine, 314, 678–681.PubMedCrossRefGoogle Scholar
  56. Nenonen, N. P., Hannoun, C., Horal, P., Hernroth, B., & Bergstrom, T. (2008). Tracing of norovirus outbreak strains in mussels collected near sewage effluents. Applied and Environmental Microbiology, 74, 2544–2549.PubMedCrossRefGoogle Scholar
  57. Nenonen, N. P., Hannoun, C., Olsson, M. B., & Bergstrom, T. (2009). Molecular analysis of an oyster-related norovirus outbreak. Journal of Clinical Virology, 45(2), 105–108.PubMedCrossRefGoogle Scholar
  58. Ng, T. L., Chan, P. P., Phua, T. H., Loh, J. P., Yip, R., Wong, C., Liaw, C. W., Tan, B. H., Chiew, K. T., Chua, S. B., Lim, S., Ooi, P. L., Chew, S. K., Coh, K. T. (2005). Oyster-associated outbreaks of norovirus gastroenteritis in Singapore. Journal of Infection, 51, 413–418CrossRefGoogle Scholar
  59. Nishida, T., et al. (2003). Detection, quantitation, and phylogenetic analysis of noroviruses in Japanese oysters. Applied and Environmental Microbiology, 69, 5782–5786.PubMedCrossRefGoogle Scholar
  60. Nishida, T., et al. (2007). Genotyping and quantitation of noroviruses in oysters from two distinct sea areas in Japan. Microbiology and Immunology, 51, 177–184.PubMedGoogle Scholar
  61. Otsu, R. (1999). Outbreaks of gastroenteritis caused by SRSVs from 1987 to 1992 in Kyushu, Japan: Four outbreaks associated with oyster consumption. European Journal of Epidemiology, 15, 175–180.PubMedCrossRefGoogle Scholar
  62. Parashar, U. D., & Monroe, S. S. (2001). Norwalk-like viruses as a cause of foodborne disease outbreaks. Reviews in Medical Virology, 11(4), 243–252.Google Scholar
  63. PHLS Viral Gastroenteritis Sub-Committee. (1993). Outbreaks of gastroenteritis associated with SRSVs. PHLS Microbiology Digest, 10, 2–8.Google Scholar
  64. Pinto, R. M., Costafreda, M. I., & Bosch, A. (2009). Risk assessment in shellfish-borne outbreaks of Hepatitis A. Applied and Environmental Microbiology, 75, 7350–7355.PubMedCrossRefGoogle Scholar
  65. Pontrelli, G., Boccia, D., Di Renzi, M., Massari, M., Giugliano, F., Celentano, L. P., et al. (2008). Epidemiological and virological characterization of a large community-wide outbreak of hepatitis A in southern Italy. Epidemiology and Infection, 136, 1027–1034.PubMedCrossRefGoogle Scholar
  66. Potasman, I., Paz, A., & Odeh, M. (2002). Infectious outbreaks associated with bivalve shellfish consumption: A worldwide perspective. Clinical Infectious Diseases, 35, 921–928.PubMedCrossRefGoogle Scholar
  67. Prato, R., Lopalco, P., Chironna, M., Barbuti, G., Germinario, C., & Quarto, M. (2004). Norovirus gasteroenteritis general outbreak associated with raw shellfish consumption in south Italy. BMC Infectious Diseases, 4, 37.PubMedCrossRefGoogle Scholar
  68. Richards, G. P. (1985). Outbreaks of shellfish-associated enteric virus illness in the United States: Requisite for development of viral guidelines. Journal of Food Protection, 48, 815–823.Google Scholar
  69. Rippey, S. R. (1994). Infectious diseases associated with molluscan shellfish consumption. Clinical Microbiology Reviews, 7(4), 419–425.PubMedGoogle Scholar
  70. Rodríguez-Lázaro, D., Cook, N., Ruggeri, F. M., Sellwood, J., Nasser, A., Nascimento, M. S., et al. (2011). Virus hazards from food, water and other contaminated environments. Federation of European Microbiological Societies, 1–29.Google Scholar
  71. Said, B., Ijaz, S., Kafatos, G., Booth, L., Thomas, H. L., Walsh, A., et al. (2009). Hepatitis E outbreak on cruise ship. Emerging Infectious Diseases, 15(11).Google Scholar
  72. Saito, K., Sato, N., Takahashi, A., Tsutsumi, R., & Sato, S. (2006). Study on pollutant pathway of norovirus contamination in oysters. Kansenshogaku Zasshi, The Journal of the Japanese Association for Infectious Diseases, 80, 399–404. (in Japanese).Google Scholar
  73. Sanchez, G., Pinto, R. M., Vanaclocha, H., & Bosch, A. (2002). Molecular characterization of hepatitis A virus isolates from a transcontinental shellfish-borne outbreak. Journal of Clinical Microbiology, 40, 4148–4155.PubMedCrossRefGoogle Scholar
  74. Sarna, M., Stafford, R., Patel, M., & Hall, G. (2007). Internationally distribud frozen oysters’ meat causing multiple outbreaks of norovirus infection in Australia. Clinical Infectious Diseases, 44, 1026–1031.PubMedCrossRefGoogle Scholar
  75. Sekine, S., Okada, S., Hayashi, Y., Ando, T., Terayama, T., Yabuuchi, K., et al. (1989). Prevalence of small round structured virus infections in acute gastroenteritis outbreaks in Tokyo. Microbiology and Immunology, 33(3), 207–221.PubMedGoogle Scholar
  76. Shieh, Y. C., Khudyakov, Y., Xia, G., et al. (2007). Molecular confirmation of oysters as the vector for hepatitis A in a 2005 multi-state outbreak. Journal of Food Protection, 70, 145–150.PubMedGoogle Scholar
  77. Simmons, G., Greening, G., Gao, W., & Campbell, D. (2001). Raw oyster consumption and outbreaks of viral gastroenteritis in New Zealand: evidence for risk to the public’s health. Australian and New Zealand Journal of Public Health, 25, 234–240.PubMedCrossRefGoogle Scholar
  78. Smith, A. J., McCartey, A. J., Saldana, N., Ihekweazu, C., McPhedran, K., Adak, et al. (2011). A large foodborne outbreak of norovirus in diners at a restaurant in England between January and February 2009. Epidemiology and Infection, 1–6.Google Scholar
  79. Sockett, P. N., Cowden, J. M., LeBaigue, S., Ross, D., Adak, G., & Evans, H. (1993). Foodborne disease surveillance in England and Wales: 1989–1991. Communicable Disease Report, 3, 159–174.Google Scholar
  80. Sockett, P. N., West, P. A., & Jacob, M. (1985). Shellfish and public health. PHLS Microbiology Digest, 2, 29–35.Google Scholar
  81. Stafford, R., Strain, D., Heymer, M., Smith, C., Trent, M., & Beard, J. (1997). An outbreak of norwalk virus gastroenteritis following consumption of oysters. Communicable Diseases Intelligence, 21(21), 317–320.PubMedGoogle Scholar
  82. Statistical Database. (2000). Statistical database (Vol. 2000). Rome: Food and Agriculture Organization of the United Nations.Google Scholar
  83. Stone, S. P., Cooper, B. S., Kibbler, C. C., Cookson, B. D., Roberts, J. A., Medley, G. F., et al. (2007). The ORION statement: Guidelines for transparent reporting of outbreak reports and intervention studies of Nosocomial infection. Journal of Antimicrobial Chemotherapy, 59, 833–840.Google Scholar
  84. Sugieda, M., Nakajima, K., & Nakajima, S. (1996). Outbreaks of norwalk-like virus-associated gastroenteritis traced to shellfish: Coexistence of two genotypes in one specimen. Epidemiology and Infection, 116, 339–346.PubMedCrossRefGoogle Scholar
  85. Symes, S. J., Gunesekere, I. C., Marshall, J. A., & Wright, P. J. (2007). Norovirus mixed infection in an oyster-associated outbreak: an opportunity for recombination. Archives of Virology, 152(6), 1075–1086.PubMedCrossRefGoogle Scholar
  86. Tang, Y. W., Wang, J. X., Xu, Z. Y., Guo, Y. F., Qian, W. H., & Xu, J. X. (1991). A serologically confirmed, case-control study, of a large outbreak of hepatitis A in China, associated with consumption of clams. Epidemiology and Infection, 107, 651–657.PubMedCrossRefGoogle Scholar
  87. Ueki, Y., Akiyama, K., Watanabe, T., & Omura, T. (2004). Genetic analysis of noroviruses taken from gastroenteritis patients, river water and oysters. Water Science and Technology, 50, 51–56.PubMedGoogle Scholar
  88. Ueki, Y., Sano, D., Watanabe, T., Akiyama, K., & Omura, T. (2005). Norovirus pathway in water environment estimated by genetic analysis of strains from patients of gastroenteritis, sewage, treated wastewater, river water and oysters. Water Research, 39, 4271–4280.PubMedCrossRefGoogle Scholar
  89. Umesh, D., Parashar, & Monroe, S. (2001). Norwalk-like viruses’ as a cause of foodborne disease outbreaks. Reviews in Medical Virology, 11, 243–252.CrossRefGoogle Scholar
  90. Verhoef, L., Vennema, H., Pelt, W. V., Lees, D., Boshuizen, H., Henshilwood, K., et al. (2010). Use of norovirus genotype profiles to different origins of foodborne outbreaks. Emerging Infectious Diseases, 16(4).Google Scholar
  91. Wall, R., Dymond, N., Bell, A., Thornley, C., Buik, H., Cumming, D., et al. (2011). Two New Zealand outbreaks of norovirus gastroenteritis linked to commercially farmed oysters. New Zealand Medicine Journal, 124(1347), 63–71.Google Scholar
  92. Wallance, B. J., Guzewich, J., Cambridge, M., Altektuse, S., & Morse, D. L. (1999). Seafood-associated disease outbreaks in New York, 1980–1994. American Journal of Preventive Medicine, 17(1), 48–54.CrossRefGoogle Scholar
  93. Webby, R. J., Carville, C. S., Kirk, M. D., Greening, G., Ratcliff, R. M., Creras, S. K., et al. (2007). Internationally distributed frozen oyster meat causing multiple outbreaks of norovirus infection in Australia. Clinical Infectious Diseases, 44, 1026–1031.PubMedCrossRefGoogle Scholar
  94. Westrel, T., Dusch, V., Ethelberg, S., Harris, J., Hjertqvist, M., Jourdanoda Silva, N., et al. (2010). Norovirus outbreaks linked to oyster consumption in the United Kingdom, Norway, France and Denmark, 2010. Eurosurveillance, 15(12), 19524.Google Scholar

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© Springer Science+Business Media New York 2012

Authors and Affiliations

  1. 1.Environmental Microbiology Unit, Department of Public Health, School of MedicineUniversity of PatrasRio PatrasGreece

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