Bioaccumulation, retention, and depuration of enteric viruses by Crassostrea virginica and Crassostrea ariakensis oysters

Applied and Environmental Microbiology

Volumn 74, Issue 22, 2008, Pages 6825-6831

  Nappier, Sharon P ^a   Graczyk, Thaddeus K ^a   Schwab, Kellogg J ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOACCUMULATION; BIOCHEMISTRY; COSMIC RAYS; CRUDE PETROLEUM; HEALTH RISKS; MICROORGANISMS; NUCLEIC ACIDS; OPERATING ROOMS; PATHOGENS; POROUS MATERIALS; RNA; SEAWATER; TANKS (CONTAINERS); TURBULENT FLOW;

CHESAPEAKE BAYS; CRASSOSTREA ARIAKENSIS; CRASSOSTREA VIRGINICA; DEPURATION; ENTERIC VIRUSES; HEPATITIS A VIRUSES; HUMAN HEALTHS; NOROVIRUS; ODDS RATIOS; POLIO VIRUSES; PROTEINASE K; REVERSE TRANSCRIPTIONS; SYNTHETIC SEAWATERS; VIRAL RNAS;

VIRUSES;

SEA WATER; VIRUS RNA;

BACTERIOPHAGE; BIOACCUMULATION; BIVALVE; FILTRATION; VIRAL DISEASE; VIRUS;

ARTICLE; BIOACCUMULATION; CRASSOSTREA ARIAKENSIS; CRASSOSTREA VIRGINICA; ENTERIC VIRUS; FOOD CONTAMINATION; FOOD INDUSTRY; FOOD INTAKE; HEALTH HAZARD; HEPATITIS A VIRUS; MORTALITY; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; OYSTER; POLIOMYELITIS VIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHELLFISH; VIRUS DETECTION;

ANIMALS; CRASSOSTREA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SEAWATER; SURVIVAL ANALYSIS; VIRUSES;

CRASSOSTREA ARIAKENSIS; CRASSOSTREA VIRGINICA; HEPATITIS A VIRUS; MURINE NOROVIRUS 1; NOROVIRUS; OSTREIDAE; POLIOVIRUS;

EID: 55949131128     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01000-08     Document Type: Article

References (33)

1. Atmar, R. L., and M. K. Estes. 2001. Diagnosis of noncultivatable gastroenteritis viruses, the human caliciviruses. Clin. Microbiol. Rev. 14:15-37.
2. Bae, J., and K. J. Schwab. 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. Appl. Environ. Microbiol. 74:477-484.
3. Calvo, G. W., M. W. Luckenbach, S. K. Allen, and E. M. Burreson. 2001. Comparative field study of Crassostrea ariakensis and Crassostrea virginica in relation to salinity in Virginia. J. Shellfish Res. 20:221-229.
4. Di Girolamo, R., J. Liston, and J. Matches. 1977. Ionic bonding, the mechanism of viral uptake by shellfish mucus. Appl. Environ. Microbiol. 33:19-25.
5. Di Girolamo, R., J. Liston, and J. Matches. 1975. Uptake and elimination of poliovirus by West Coast oysters. Appl. Environ. Microbiol. 29:260-264.
6. Duizer, E., K. J. Schwab, F. H. Neill, R. L. Atmar, M. P. Koopmans, and M. K. Estes. 2004. Laboratory efforts to cultivate noroviruses. J. Gen. Virol. 85:79-87.
7. Gallimore, C. I., J. S. Cheesbrough, K. Lamden, C. Bingham, and J. J. Gray. 2005. Multiple norovirus genotypes characterized from an oyster-associated outbreak of gastroenteritis. Int. J. Food Microbiol. 103:323-330.
8. Graczyk, T. K., A. S. Girouard, L. Tamang, S. P. Nappier, and K. J. Schwab. 2006. Recovery, bioaccumulation, and inactivation of human waterborne pathogens by the Chesapeake Bay nonnative oyster, Crassostrea ariakensis. Appl. Environ. Microbiol. 72:3390-3395.
9. Hoff, J. C., and R. C. Becker. 1969. The accumulation and elimination of crude and clarified poliovirus suspensions by shellfish. Am. J. Epidemiol. 90:53-61.
10. Hudson, K. L., A. Kozlowski, and S. K. Allen. 2004. Biosecurity and comparison field trials of triploid Crassostrea ariakensis with C. virginica. NOAA Chesapeake Bay Office of Integrated Research Program Symposium report no. 103-114. NOAA Chesapeake Bay Office, Annapolis, MD.
11. Kennedy, V., R. I. E. Newell, and A. F. Eble. 2007. The eastern oyster Crassostrea virginica. Maryland Sea Grant College, College Park.
12. Koopmans, M., and E. Duizer. 2004. Foodborne viruses: an emerging problem. Int. J. Food Microbiol. 90:23-41.
13. Lees, D. 2000. Viruses and bivalve shellfish. Int. J. Food Microbiol. 59:81-116.
14. Le Guyader, F., F. Loisy, R. L. Atmar, A. M. Hutson, M. K. Estes, N. Ruvoen-Clouet, M. Pommepuy, and J. Le Pendu. 2006. Norwalk virus-specific binding to oyster digestive tissues. Emerg. Infect. Dis. 12:931-936.
15. Le Guyader, F. S., F. Bon, D. DeMedici, S. Parnaudeau, A. Bertone, S. Crudeli, A. Doyle, M. Zidane, E. Suffredini, E. Kohli, F. Maddalo, M. Monini, A. Gallay, M. Pommepuy, P. Pothier, and F. M. Ruggeri. 2006. Detection of multiple noroviruses associated with an international gastroenteritis outbreak linked to oyster consumption. J. Clin. Microbiol. 44:3878-3882.
16. Le Guyader, F. S., F. H. Neill, E. Dubois, F. Bon, F. Loisy, E. Kohli, M. Pommepuy, and R. L. Atmar. 2003. A semiquantitative approach to estimate Norwalk-like virus contamination of oysters implicated in an outbreak. Int. J. Food Microbiol. 87:107-112.
17. Loisy, F., R. L. Atmar, J. C. Le Saux, J. Cohen, M. P. Caprais, M. Pommepuy, and F. S. Le Guyader. 2005. Use of rotavirus virus-like particles as surrogates to evaluate virus persistence in shellfish. Appl. Environ. Microbiol. 71:6049-6053.
18. Mitchell, J. R., M. W. Presenell, E. W. Akin, J. M. Cummins, and O. C. Liu. 1966. Accumulation and elimination of poliovirus by the eastern oyster. Am. J. Epidemiol. 84:40-50.
19. Nappier, S. P., and K. J. Schwab. 2006. Murine norovirus-1: a novel surrogate for human norovirus in shellfish, abstr. P-080. Abstr. 106th Gen. Meet. Am. Soc. Microbiol. American Society for Microbiology, Washington, DC.
20. National Research Council of the National Academies. 2005. Nonnative oysters in the Chesapeake Bay. The National Academies Press, Washington, DC.
21. Parashar, U. D., and S. S. Monroe. 2001. "Norwalk-like viruses" as a cause of foodborne disease outbreaks. Rev. Med. Virol. 11:243-252.
22. Schwab, K. J., R. De Leon, and M. D. Sobsey. 1995. Concentration and purification of beef extract mock eluates from water samples for the detection of enteroviruses, hepatitis A virus, and Norwalk virus by reverse transcription-PCR. Appl. Environ. Microbiol. 61:531-537.
23. Schwab, K. J., F. H. Neill, M. K. Estes, T. G. Metcalf, and R. L. Atmar. 1998. Distribution of Norwalk virus within shellfish following bioaccumulation and subsequent depuration by detection using RT-PCR. J. Food Prot. 61:1674-1680.
24. Schwab, K. J., F. H. Neill, R. L. Fankhauser, N. A. Daniels, S. S. Monroe, D. A. Bergmire-Sweat, M. K. Estes, and R. L. Atmar. 2000. Development of methods to detect "Norwalk-like viruses" (NLVs) and hepatitis A virus in delicatessen foods: application to a food-borne NLV outbreak. Appl. Environ. Microbiol. 66:213-218.
25. Sobsey, M. D., and L. A. Jaykus. 1991. Human enteric viruses and depuration of bivalve mollusks, p. 71-114. In W. S. Otwell, G. E. Rodrick, and R. E. Martin (ed.), Molluscan shellfish depuration. CRC Press, Boston, MA.
26. Sobsey, M. D., C. Wallis, and J. L. Melnick. 1975. Development of a simple method for concentrating enteroviruses from oysters. Appl. Microbiol. 29:21-26.
27. Symes, S. J., I. C. Gunesekere, J. A. Marshall, and P. J. Wright. 2007. Norovirus mixed infection in an oyster-associated outbreak: an opportunity for recombination. Arch. Virol. 152:1075-1086.
28. Tian, P., A. H. Bates, H. M. Jensen, and R. E. Mandrell. 2006. Norovirus binds to blood group A-like antigens in oyster gastrointestinal cells. Lett. Appl. Microbiol. 43:645-651.
29. Tian, P., A. L. Engelbrektson, X. Jiang, W. Zhong, and R. E. Mandrell. 2007. Norovirus recognizes histo-blood group antigens on gastrointestinal cells of clams, mussels, and oysters: a possible mechanism of bioaccumulation. J. Food Prot. 70:2140-2147.
30. Ueki, Y., M. Shoji, A. Suto, T. Tanabe, Y. Okimura, Y. Kikuchi, N. Saito, D. Sano, and T. Omura. 2007. Persistence of caliciviruses in artificially contaminated oysters during depuration. Appl. Environ. Microbiol. 73:5698-5701.
31. Wait, D. A., and M. D. Sobsey. 2001. Comparative survival of enteric viruses and bacteria in Atlantic Ocean seawater. Water Sci. Technol. 43:139-142.
32. Wobus, C. E., S. M. Karst, L. B. Thackray, K. O. Chang, S. V. Sosnovtsev, G. Belliot, A. Krug, J. M. Mackenzie, K. Y. Green, and H. W. Virgin. 2004. Replication of norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol. 2:e432.
33. Wobus, C. E., L. B. Thackray, and H. W. Virgin. 2006. Murine norovirus: a model system to study norovirus biology and pathogenesis. J. Virol. 80:5104-5112.