Detection of multiple noroviruses associated with an international gastroenteritis outbreak linked to oyster consumption

Journal of Clinical Microbiology

Volumn 44, Issue 11, 2006, Pages 3878-3882

  Le Guyader, Françoise S ^a   Bon, Fabienne ^b   DeMedici, Dario ^c   Parnaudeau, Sylvain ^a   Bertone, Alessandra ^d   Crudeli, Silvia ^e   Doyle, Aoife ^f   Zidane, Mohamed ^a   Suffredini, Elisabetta ^c   Kohli, Evelyne ^b   Maddalo, Francesco ^d   Monini, Marina ^e   Gallay, Anne ^f   Pommepuy, Monique ^a   Pothier, Pierre ^b   Ruggeri, Franco M ^e  

^a IFREMER   (France)

^b DIJON UNIVERSITY HOSPITAL   (France)

^c Centro Nazionale per la Qualità degli Alimenti e per i Rischi Alimentari   (Italy)

^d Ospedale Azienda Sanitaria Locale 5   (Italy)

^e ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^f INSTITUT DE VEILLE SANITAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

ACUTE GASTROENTERITIS; ARTICLE; FECES ANALYSIS; FOOD CONTAMINATION; FRANCE; GASTROENTERITIS; HUMAN; ITALY; MAJOR CLINICAL STUDY; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; OYSTER; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SHELLFISH; VIRUS DETECTION;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CHILD; CHILD, PRESCHOOL; DISEASE OUTBREAKS; FECES; FEMALE; FOOD POISONING; GASTROENTERITIS; HUMANS; MALE; MIDDLE AGED; NOROVIRUS; OSTREIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

NOROVIRUS; OSTREIDAE;

EID: 33750957829     PISSN: 00951137     EISSN: None     Source Type: Journal    
DOI: 10.1128/JCM.01327-06     Document Type: Article

References (36)

1. Atmar, R. L., F. H. Neill, J. L. Romalde, F. Le Guyader, C. M. Woodley, T. G. Metcalf, and M. K. Estes. 1995. Detection of Norwalk virus and Hepatitis A virus in shellfish tissues with the PCR. Appl. Environ. Microbiol. 61:3014-3018.
2. Atmar, R. L., and Estes, M. K. 2001. Diagnosis of nonculturable gastroenteritis viruses, the human caliciviruses. Clin. Microbiol. Rev. 14:15-37.
3. Bon, F., P. Fascia, M. Dauvergne, D. Tenenbaum, H. Planson, A. M. Petion, P. Pothier, and E. Kohli. 1999. Prevalence of group A rotavirus, human calicivirus, astrovirus, and adenovirus type 40 and 41 infections among children with acute gastroenteritis in Dijon, France. J. Clin. Microbiol. 37:3055-3058.
4. Bon, F., H. Giraudon, C. Sancey, C. Barranger, M. Joannes, P. Pothier, and E. Kohli. 2004. Development and evaluation of a new commercial test allowing the simultaneous detection of noroviruses and sapoviruses by reverse transcription and microplate hybridization. J. Clin. Microbiol. 42:2218-2220.
5. Bosch, A., G. Sanchez, F. S. Le Guyader, H. Vanaclocha, L. Haugarreau, and R. M. Pinto. 2001. Human enteric viruses in coquina clams associated with a large hepatitis A outbreak. Water Sci. Tech. 43:61-65.
6. Boxman, I. L. A., J. J. H. C. Tilburg, N. A. J. M. Loeke, H. Vennema, K. Jonker, E. de Boer E., and M. Koopmans, M. 2006. Detection of noroviruses in shellfish in The Netherlands. Int. J. Food Microbiol. 108:391-396.
7. Burkhardt, W., and K. R. Calci. 2000. Selective accumulation may account for shellfish-associated viral illness. Appl. Environ. Microbiol. 66:1375-1378.
8. Butt, A. A., K. E. Aldridge, and C. V. Sanders. 2004. Infections related to the ingestion of seafood. I. Viral and bacterial infections. Lancet Infect. Dis. 4:201-212.
9. De Medici, D., M. Ciccozzi, A. Fiore, S. Di Pasquale, A. Parlato, P. Ricci-Bitti, and L. Croci. 2001. Closed-circuit system for the depuration of mussels experimentally contaminated with hepatitis A virus. J. Food Prot. 64:877-880.
10. De Medici, D., L. Croci, S. Di Pasquale, A. Fiore, and L. Too, L. 2001. Detecting the presence of infectious hepatitis A virus in molluscs positive to RT-nested-PCR. Lett. Appl. Microbiol. 33:362-366.
11. De Medici, D., L. Croci, E. Suffredini, and L. Toti. 2004. Reverse transcription booster PCR for detection of noroviruses in shellfish. Appl. Environ. Microbiol. 70:6329-6332.
12. Gallimore, C., J. S. Cheesbrough, K. Lamden, C. Bingham, and J. Gray. 2005. Multiple norovirus genotypes characterized from an oyster-associated outbreak of gastroenteritis. Int. J. Food Microbiol. 103:323-330.
13. Hafliger, D., M. Gilgen, J. Luthy, and P. H. Hubner. 1997. Seminested RT-PCR systems for small round structured viruses and detection of enteric viruses in seafood. Int. J. Food Microbiol. 37:27-36.
14. Hutson, A. M., R. L. Atmar, and M. K. Estes. 2004. Norovirus disease: changing epidemiology and host susceptibility factors. Trends Microbiol. 12:279-287.
15. Kageyama, T., M. Shinohara, K. Uchida, S. Fukhusi, F. B. Hoshino, S. Kojima, R. Takai, T. Oka, N. Takeda, and K. Katayama, K. 2004. Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to Norovirus in Japan. J. Clin. Microbiol. 42:2988-2995.
16. Kojima, S., T. Kageyama, S. Fukushi, F. B. Hoshino, M. Shinihara, K. Uchida, K. Natori, N. Takeda, and K. Kageyama. 2002. Genogroup specific PCR primers for detection of Norwalk-like viruses. J. Virol. Methods 100:107-114.
17. Koopmans, M., and E. Duizer. 2004. Foodborne viruses: an emerging problem. Int. J. Food Microbiol. 90:23-41.
18. Le Guyader, F. S., L. Haugarreau, L. Miossec, E. Dubois, and M. Pommepuy. 2000. Three-year study to assess human enteric viruses in shellfish. Appl. Environ. Microbiol. 66:3241-3248.
19. Le Guyader, F. S., F. H. Neill, E. Dubois, F. Bon, F. Loisy, E. Kohli, M. Pommepuy, and R. L. Atmar. 2003. A semi-quantitative approach to estimate Norwalk-like virus contamination of oysters implicated in an outbreak. Int. J. Food Microbiol. 87:107-112.
20. Le Guyader, F. S., C. Mittelhozer, L. Haugarreau, K.-O. Hedlund, R. Alsterlund, M. Pommepuy, and L. Svensson. 2004. Detection of noroviruses in raspberries associated with a gastroenteritis outbreak. Int. J. Food Microbiol. 97:179-186.
21. Le Guyader, F. S., 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.
22. Loisy, F., R. L. Atmar, P. Guillon, P. Le Cann, M. Pommepuy, and F. S. Le Guyader. 2005. Real-time RT-PCR for norovirus screening in shellfish. J. Virol. Methods 123:1-7.
23. 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.
24. Lopman, B., H. Vennema, E. Kohli, P. Pothier, A. Sanchez, A. Negredo, et al. 2004. Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet 363:682-688.
25. Mackowiak, P. A., C. T. Caraway, and B. L. Portnoy. 1976. Oyster-associated hepatitis: lessons from the Louisiana experience. Am. J. Epidemiol. 103:181-191.
26. Maunula, L., I. T. Miettinen, and C.-H. von Bonsdorff. 2005. Norovirus outbreaks from drinking water. Emerg. Infect. Dis. 11:1716-1721.
27. Metcalf, T. G. 1982. Viruses in shellfish growing waters. Environ. Int. 7:21-27.
28. Pommepuy, M., M. P. Caprais, J.-C. Le Saux, C. Le Mennec, S. Parnaudeau, Y. Madec, M. Monier, G. Brest, and F. S. Le Guyader. 2003. Evaluation of viral shellfish depuration in a semi-professional size tank, p. 485-499. In B. Villalba, B. Reguera, J. L. Romalde, and R. Beiras (ed.), Molluscan shellfish safety. Conseillaria de Pesca e Assuntos Maritimos da Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Santiago de Compostela, Spain.
29. Pommepuy, M., D. Hervio-Heath, M.-P. Caprais, M. Gournielon, and F. S. Le Guyader. 2005. Fecal contamination in coastal area: an engineering approach, p. 331-360. In S. Belkin (ed.), Oceans and health: pathogens in the marine environment. Kluwer Academic/Plenum Publishers, Dordrecht, The Netherlands.
30. 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.
31. Ueki, Y., D. Sano, T. Watnabe, K. Akiyama, and T. Omura. 2005. Norovirus pathway in water environment estimated by genetic analysis of strains from patients of gastroenteritis, sewage, treated wastewater, river water and oysters. Water Res. 39:4271-4280.
32. Vinje, J., and M. Koopmans. 1996. Molecular detection and epidemiology of small round structured viruses in outbreaks of gastroenteritis in The Netherlands. J. Infect. Dis. 174:610-615.
33. Vinje, J., H. Vennema, L. Maunula, C.-H. von Bonsdorff, M. Hoehne, E. Shreier, A. Richards, J. Green, D. Brown, S. Beard, S. Monroe, E. De Bruin, L. Svensson, and M. P. G. Koopmans. 2003. International collaborative study to compare reverse transcriptase PCR assays for detection and genotyping of noroviruses. J. Clin. Microbiol. 41:4023-4033.
34. Widdowson, M. A., A. Sulka, S. N. Bulens, R. S. Beard, S. S. Chaves, R. Hammond, E. D. P. Salehi, E. Swanson, J. Totaro, R. Woron, P. S. Mead, J. S. Bresee, S. S. Monroe, and R. I. Glass. 2005. Norovirus and foodborne disease, United States, 1991-2000. Emerg. Infect. Dis. 11:95-102.
35. Yuen, L. K., M. G. Catton, B. J. Cox, P. Wright, and J. A. Marshall. 2001. Heminested multiplex reverse-transcription-PCR for detection and differentiation of Norwalk-like virus genogroups 1 and 2 in fecal samples. J. Clin. Microbiol. 39:2690-2694.
36. Zheng, D. P., T. Ando, R. L. Fankhauser, R. S. Beard, R. Glass, and S. S. Monroe. 2006. Norovirus classification and proposed strain nomenclature. Virology 346:312-323.