Environmental conditions leading to shellfish contamination and related outbreaks

Food and Environmental Virology

Volumn 2, Issue 3, 2010, Pages 136-145

  Maalouf, Haifa ^a   Pommepuy, Monique ^a   Le Guyader, Françoise S ^a  

^a IFREMER   (France)

Author keywords

Environmental conditions; Norovirus; Outbreaks; Shellfish

Indexed keywords

RAIN;

ADENOVIRUS; AQUATIC ENVIRONMENT; ARTICLE; ASTROVIRUS; CALICIVIRUS; CLAM; CONSUMER; CONTAMINATED SHELLFISH; ENTERIC VIRUS; ENTEROVIRUS; EPIDEMIC; FECES; FOOD INTAKE; GASTROENTERITIS; HEPATITIS A; HEPATITIS A VIRUS; HUMAN; INCUBATION TIME; KOBUVIRUS; MUSSEL; NONHUMAN; NOROVIRUS; OYSTER; PRIORITY JOURNAL; ROTAVIRUS; SEWAGE TREATMENT PLANT; VIRAL CONTAMINATION; VIRUS LIKE AGENT; VIRUS STRAIN; VIRUS TRANSMISSION;

BIVALVIA; MOLLUSCA; NOROVIRUS;

EID: 77954762105     PISSN: 18670334     EISSN: 18670342     Source Type: Journal    
DOI: 10.1007/s12560-010-9043-4     Document Type: Article

References (89)

1. Anderson, E. J., & Weber, S. G. (2004). Rotavirus infection in adults. Lancet Infectious Disease, 4, 91-99.
2. Atmar, R. L., Opekum, A. R., Gilger, M. A., Estes, M. K., Crawford, S. E., Neill, F. H., et al. (2008). Norwalk virus shedding after experimental human infection. Emerging Infectious Disease, 14, 1553-1557.
3. Bedford, A. J., Williams, G., & Bellamy, A. R. (1978). Virus accumulation by the rock oyster Crassotrea glomerata. Applied Environmental Microbiology, 35, 1012-1018.
4. Blanton, L. H., Adams, S. M., Beard, R. S., Wei, G., Bulens, S. N., Widdowson, M.-A., et al. (2006). Molecular and epidemiologic trends of caliciviruses associated with outbreaks of acute gastroenteritis in the United States, 2000-2004. Journal of Infectious Disease, 193, 413-421.
5. Bosch, A., Lucena, F., Girones, R., & Jofre, J. (1988). Occurence of enteroviruses in marine sediment along the coast of Barcelona, Spain. Canadian Journal of Microbiology, 34, 921-924.
6. Burkhardt, W., & Calci, K. R. (2000). Selective accumulation may account for shellfish-associated viral illness. Applied Environmental Microbiology, 66, 1375-1378.
7. Chan, M. C. W., Sung, J. J. Y., Lam, R. K. Y., Chan, P. K. S., Lee, N. L. S., Lai, R. W. M., et al. (2006). Fecal viral load and norovirus associated gastroenteritis. Emerging Infectious Disease, 12, 1278-1280.
8. 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, 1633-1635.
9. Chung, H., & Sobsey, M. D. (1993). Comparative survival of indicator viruses and enteric viruses in seawater and sediment. Water Science Technology, 27, 425-428.
10. Costafreda, M. I., Bosch, A., & Pintó, R. M. (2006). Development, evaluation, and standardization of a real-time taqMan reverse transcription-PCR assay for quantification of hepatitis A virus in clinical and shellfish samples. Applied Environmental Microbiology, 72, 3846-3855.
11. da Silva, A., Le Saux, J.-C., Parnaudeau, S., Pommepuy, M., Elimelech, M., & Le Guyader, F. S. (2007). Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: Different behaviors of genogroups I and II. Applied Environmental Microbiology, 73, 7891-7897.
12. da Silva, A., Le Guyader, F. S., Le Saux, J.-C., Pommepuy, M., Montgomery, M. A., & Elimelech, M. (2008). Norovirus removal and particle association in a waste stabilisation pond. Environmental Science and Technology, 42, 9151-9157.
13. David, S. T., McIntyre, L., MacDougall, L., Kelly, D., Liem, S., Schallie, K., et al. (2007). An outbreak of norovirus caused by consumption of oysters from geographically dispersed harvest sites, British Columbia, Canada. Foodborne Pathogens and Disease, 4, 349-358.
14. 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.
15. Di Girolamo, R., Liston, J., & Matches, J. (1977). Ionic binding, the mechanism of viral uptake by shellfish mucus. Applied Environmental Microbiology, 33, 19-25.
16. Dowell, S. F. (2001). Seasonal variation in host susceptibility and cycles of certain infectious diseases. Emerging and Infectious Disease, 7, 369-374.
17. Dowell, S. F., Graves, 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 Disease, 171, 1497-1503.
18. Estes, M. K., & Kapikian, A. Z. (2007). Rotaviruses. In D. M. Knipe & P. M. Howley (Eds.), Fields virology (pp. 1917-1974). Baltimore, MD: Lippincot Williams and Wilkins.
19. Gallimore, C., Cheesbrough, J. S., Lamden, K., Bingham, C., & Gray, J. (2005). Multiple norovirus genotypes characterised from an oyster-associated outbreak of gastroenteritis. International Journal of Food Microbiology, 103, 323-330.
20. Gerba, C. P. (2000). Assessment of enteric pathogen shedding by bathers during recreational activity and its impact on water quality. Quantitative Microbiology, 2, 55-68.
21. Gerba, C. P. (2007). Virus occurence and survival in the environmental waters. Human viruses in water. Perspective in Medical Virology, 17, 91-108.
22. Gosling, E. (2003) How bivalves feed. In Bivalve molluscs: Biology, ecology and culture. Oxford, UK: Blackwell Publishing. ISBN 0-85238-234-01, 3987-123.
23. Halliday, M. L., Kang, L. Y., Zhou, T. R., 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 Shanghai, China. Journal of Infectious Disease, 164, 852-859.
24. Haramoto, E., Katayama, H., Oguma, K., Yamashita, H., Tajima, A., Nakajima, H., et al. (2006). Seasonal profiles of human noroviruses and indicator bacteria in a wastewater treatment plant in Tokyo, Japan. Water Science and Technology, 54, 301-308.
25. Haramoto, E., Katayama, H., Oguma, K., & Ohgaki, S. (2008a). Development of sample storage methods for detecting enteric viruses in environmental water. Journal of Virological Methods, 151, 1-6.
26. Haramoto, E., Katayam, H., Phanuwan, C., & Ohgaki, S. (2008b). Quantitative detection of sapoviruses in wastewater and river water in Japan. Letters in Applied Microbiology, 46, 408-413.
27. Hernroth, B., & Allard, A. (2007). The persistence of infectious adenovirus (type 35) in mussels (Mytilus edulis) and oysters (Ostrea edulis). International Journal of Food Microbiology, 113, 296-302.
28. Iwai, M., Hasegawa, S., Obara, M., Nakamura, K., Horimoto, E., Takizawa, T., et al. (2009). Continuous presence of noroviruses and sapoviruses in raw sewage reflects infections among inhabitants of Toyoma, Japan (2006 to 2008). Applied Environmental Microbiology, 75, 1264-1270.
29. Kageyama, T., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., Kojima, S., et al. (2004). Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to norovirus in Japan. Journal of Clinical Microbiology, 42, 2988-2995.
30. Katayama, H., Haramoto, E., Oguma, K., Yamashita, H., Tajima, A., Nakajima, H., et al. (2008). One-year monthly quantitative survey of noroviruses, enteroviruses and adenoviruses in wastewater collected from six plants in Japan. Water Research, 42, 1441-1448.
31. Kingsley, D. H., & Richards, G. P. (2003). Persistence of hepatitis A virus in oysters. Journal of Food Protection, 66, 331-334.
32. Kingsley, D. H., Meade, G. K., & Richards, G. P. (2002). Detection of both hepatitis A virus and norwalk-like virus in imported clams associated with food-borne illness. Applied Environmental Microbiology, 68, 3914-3918.
33. Kohn, M. A., Farley, T. A., Ando, T., Curtis, M., WIilson, S. A., Monroe, S. S., et al. (1995). An outbreak of norwalk virus gastroenteritis associated with eating raw oysters. Journal of American Medical Association, 273, 466-471.
34. La Rosa, G., Fontana, S., Di Grazia, A., Iaconelli, M., Pourshaban, M., & Muscillo, M. (2007). Molecular identification and genetic analysis of norovirus genogroups I and II in water environments: Comparative analysis of different reverse transcription-PCR assays. Applied Environmental Microbiology, 73, 4152-4161.
35. Le Cann, P., Ranarijaona, S., Monpoeho, S., Le Guyader, F. S., & Ferré, V. (2004). Quantification of human astroviruses in sewage using real-time RT-PCR. Research in Microbiology, 155, 11-15.
36. 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.
37. Le Guyader, F. S., Bon, F., DeMedici, D., Parnaudeau, S., Bertone, A., Crudeli, S., et al. (2006a). Detection of multiple noroviruses associated with an international gastroenteritis outbreak linked to oyster consumption. Journal of Clinical Microbiology, 44, 3878-3882.
38. Le Guyader, F. S., Loisy, F., Atmar, R. L., Hutson, A. M., Estes, M. K., Ruvoen-Clouet, N., et al. (2006b). Norwalk virus specific binding to oyster digestive tissues. Emerging Infectious Disease, 12, 931-936.
39. 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.
40. Le Guyader, F. S., Krol, J., Ambert-Balay, K., Ruvoen-Clouet, N., Desaubliaux, B., Parnaudeau, S., et al. (2010). Comprehensive analysis of a norovirus-associated gastroenteritis outbreak, from the environment to the consumer. Journal of Clinical Microbiology, 48, 915-920.
41. Le Pendu, J., Ruvoen-Clouet, N., Kindberg, E., & Svensson, L. (2006). Mendelian resistance to human norovirus infections. Seminar in Immunology, 18, 375-386.
42. Leoni, E., Bevini, C., Espoti, S. D., & 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.
43. Lodder, W. J., & de Roda-Husman, A. M. (2005). Presence of noroviruses and other enteric viruses in sewage and surface waters in the Netherlands. Applied Environmental Microbiology, 71, 1453-1461.
44. Loisy, F., Atmar, R. L., 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 Environmental Microbiology, 71, 6049-6053.
45. Lopalco, P. L., Malfait, P., Salmaso, S., Germinario, C., Quarto, M., & Barbuti, S. (1997). A persisting outbreak of hepatitis A in Puglia, Italy, 1996: Epidemiological follow up. Eurosurveillance, 2, 31-32.
46. Lopman, B. A., Vennema, H., Kohli, E., Pothier, P., Sanchez, A., Negredo, A., et al. (2004). Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet, 363, 682-688.
47. Lopman, B., Zambon, M., & Brown, D. W. (2008). The evolution of norovirus, the gastric flu. PLoS Medicine, 5, e42.
48. Lysen, M., Thorhagen, M., Brytting, M., Hjertqvist, M., Andersson, Y., & Hedlund, K.-O. (2009). Genetic diversity among food-borne and waterborne norovirus strains causing outbreak in Sweden. Journal of Clinical Microbiology, 47, 2411-2418.
49. Maalouf, H., Zakhour, M., Le Pendu, J., Le Saux, J.-C., Atmar, R. L., Le Guyader, F. S. (accepted). Norovirus genogroup I and II ligands in oysters: Tissue distribution and seasonal variations. Applied Environmental Microbiology.
50. Mackowiak, P. A., Caraway, T., & Portnoy, B. L. (1976). Oyster-associated hepatitis: Lessons from the Louisiana experience. American Journal of Epidemiology, 103, 181-191.
51. McLeod, C., Hay, B., Grant, C., Greening, G., & Day, D. (2009). Localization of norovirus and poliovirus in Pacific oysters. Journal of Applied Microbiology, 106, 1220-1230.
52. Metcalf, T. G. (1982). Viruses in shellfish growing waters. Environmental International, 7, 21-27.
53. Metcalf, T. G., & Melnick, J. L. (1983). Simple apparatus for collecting estuarine sediments and suspended solids to detect solids associated virus. Applied Environmental Microbiology, 45, 323-327.
54. Miagostovich, M. P., Ferreira, F. F. M., Guimaraes, F. R., Fumian, T. M., Dniz-Mendes, L., Luz, S. L. B., et al. (2008). Molecular detection and characterization of gastroenteritis viruses occurring naturally in the stream waters of Manaus, central Amazonia, Brazil. Applied Environmental Microbiology, 74, 375-382.
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. Role of norwalk virus. New England Journal of Medicine, 314, 678-681.
56. Mounts, A. W., Ando, T., Koopmans, M., Bresee, J. S., Noel, J., & Glass, R. I. (2000). Cold weather seasonality of gastroenteritis associated with norwalk-like viruses. Journal of Infectious Disease, 181(Suppl), S284-S287.
57. Murphy, A. M., Grohmann, G. S., Christopher, P. J., Lopez, W. A., Davey, G. R., & Millsom, R. H. (1979). An Australian wide outbreak of gastroenteritis from oysters caused by norwalk virus. The Medical Journal of Australia, 2, 329-333.
58. Myrmel, M., Berg, E. M. M., Grinde, B., & Rimstad, E. (2006). Enteric viruses in inlet and outlet samples from sewage treatment plants. Journal of Water Health, 4, 197-209.
59. Nenonen, N. P., Hannoun, C., Olsson, M. B., & Bergstrom, T. (2009). Molecular analysis of an oyster-related norovirus outbreak. Journal of Clinical Virology, 45, 105-108.
60. Ng, T. L., Chan, P. P., Phua, T. H., Loh, J. P., Yip, R., Wong, C., et al. (2005). Oyster-associated outbreaks of norovirus gastroenteritis in Singapore. Journal of Infection, 51, 413-418.
61. Noda, M., Fukuda, S., & Nishio, O. (2008). Statistical analysis of attack rate in norovirus foodborne outbreaks. International Journal of Food Microbiology, 122, 216-220.
62. Pallansch, M., & Roos, R. (2007). Enteroviruses: Polioviruses, coxsackievirus, echoviruses and newer enteroviruses. In D. M. Knipe & P. M. Howley (Eds.), Fields virology (pp. 839-893). Baltimore, MD: Lippincot Williams and Wilkins.
63. Patel, M. N., Widdowson, M.-A., Glass, R. I., Akazawa, K., Vinje, J., & Parashar, U. D. (2008). Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerging Infectious Disease, 14, 1224-1231.
64. Pintó, R. M., & Saiz, J.-C. (2007). Enteric hepatitis viruses. Human viruses in water. Perspective in Medical Virology, 17, 39-68.
65. 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.
66. Pommepuy, M., Dumas, F., Caprais, M. P., Camus, P., Le Mennec, C., Parnaudeau, S., et al. (2004). Sewage impact on shellfish microbial contamination. Water Science and Technology, 50, 117-124.
67. Pommepuy, M., Hervio-Heath, D., Caprais, M.-P., Gourmelon, M., Le Saux, J.-C., & Le Guyader, F. S. (2005). Fecal contamination in coastal areas: An engineering approach. In S. Belkin & R. R. Colwell (Eds.), Oceans and health, pathogens in the marine environment (pp. 331-360). New York, NY: Springer.
68. 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.
69. Prato, R., Lopalco, P. L., Chironna, M., Barbuti, G., Germinario, C., & Quarto, M. (2004). Norovirus gastroenteritis general outbreak associated with raw shellfish consumption in south Italy. BMC Infectious Diseases, 4, 1-6.
70. Pusch, D., Oh, D. Y., Wolf, S., Dumke, R., Schroter-Bobsin, U., Hohne, M., et al. (2005). Detection of enteric viruses and bacterial indicators in German environmental waters. Archive of Virology, 150, 929-947.
71. Rohayem, J. (2009). Norovirus seasonality and the potential impact of climate change. European Society of Clinical Microbiology and Infectious Diseases, 15, 524-527.
72. Rose, M. A., Dhar, A. K., Brooks, H. A., Zecchini, F., & Gersberg, R. M. (2006). Quantitation of hepatitis A virus and enterovirus levels in the lagoon canals and Lido beach of Venice, Italy, using real-time RT-PCR. Water Research, 40, 2387-2396.
73. Sanchez, G., Pintó, R., 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.
74. Sansonetti, P. (2009). Framing a concept and an agenda for infectious diseases in EMBO molecular medicine. EMBO Molecular Medicine, 1, 193-194.
75. Schijven, J. F., Hassanizadeh, S. M., & de Roda Husman, A. M. (2010). Vulnerability of unconfined aquifers to virus contamination. Water Research, 44, 1170-1181.
76. 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.
77. Shieh, Y. S. C., Monroe, S. S., Fankhauser, R. L., Langlois, G. W., Burkhardt, W., & Baris, R. S. (2000). Detection of norwalk-like virus in shellfish implicated in illness. Journal of Infectious Disease, 181, 360-366.
78. Shieh, Y. C., Khudyakov, Y. E., Ganova-Raeva, L. M., Khambaty, F. M., Woods, J. W., Veazey, J. E., et al. (2007). Molecular confirmation of oysters as the vector for hepatitis A in a 2005 multistate outbreak. Journal of Food Protection, 70, 145-150.
79. Shumway, S. E., Cucci, T. L., Newell, R. C., & Yentsch, C. M. (1985). Particles selection, ingestion and absorption in filter feeding bivalves. Journal of Experimental Marine Biology and Ecology, 91, 77-92.
80. Siebenga, J. J., Vennema, H., Zheng, D.-P., Vinje, J., et al. (2009). Norovirus illness is a global problem: Emergence and spread of norovirus GII. 4 variants, 2001-2007. Journal of Infectious Disease, 200, 802-812.
81. Simmons, G., Garbutt, C., Hewitt, J., & Greening, G. (2007). A New Zealand outbreak of norovirus gastroenteritis linked to the consumption of imported raw Korean oysters. New Zealand Medical Journal, 120, U2773.
82. 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.
83. Tan, M., & Jiang, X. (2007). Norovirus-host interaction: Implications for disease control and prevention. Expert Review in Molecular Medicine, 9, 1-22.
84. Tan, M., Xia, M., Chen, Y., Bu, W., Hegde, R. S., Meller, J., et al. (2009). Conservation of carbohydrate binding interfaces-evidence of human HBGA selection in norovirus evolution. PLoS One, 4, e5058.
85. Teunis, P. F. M., Moe, C. L., Liu, P., Miller, S. E., Lindesmith, L., Baric, R. S., et al. (2008). Norwalk virus: How infectious is it? Journal of Medical Virology, 80, 1468-1476.
86. Tian, P., Engelbrektson, A. L., Jiang, X., Zhong, W., & Mandrell, R. E. (2007). Norovirus recognizes histo-blood group antigens on gastrointestinal cells of clams, mussels, and oysters: A possible mechanism of bioaccumulation. Journal of Food Protection, 70, 2140-2147.
87. van der Berg, H., Lodder, W., van der Poel, W., Vennema, H., & de Roda Husman, A.-M. (2005). Genetic diversity of noroviruses in raw and treated sewage water. Research in Microbiology, 156, 532-540.
88. Webby, R. J., Carville, K. S., Kirk, M. D., Greening, G., Ratcliff, R. M., Creara, S. K., et al. (2007). Internationally distributed frozen oyster meat causing multiple outbreaks of norovirus infection in Australia. Clinical and Infectious Disease, 44, 1026-1031.
89. Westrell, T., Teunis, P., van den Berg, H., Lodder, W., Ketelaars, H., Stenstrom, T. A., et al. (2006). Short- and long-term variations of norovirus concentrations in the Meuse river during a 2-year study period. Water Research, 40, 2613-2620.