Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: Different behaviors of genogroups I and II

Applied and Environmental Microbiology

Volumn 73, Issue 24, 2007, Pages 7891-7897

  Da Silva, Allegra Kyria ^a   Le Saux, Jean Claude ^b   Parnaudeau, Sylvain ^b   Pommepuy, Monique ^b   Elimelech, Menachem ^a   Le Guyader, Françoise S ^b  

^a YALE UNIVERSITY   (United States)

^b IFREMER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED SLUDGE PROCESS; CONCENTRATION (PROCESS); GASTROENTEROLOGY; WASTEWATER TREATMENT;

EFFLUENT SAMPLES; SUBMERGED MEMBRANE BIOREACTORS; VIRUS EXTRACTION CONTROL;

VIRUSES;

ACTIVATED SLUDGE; BIOREACTOR; MEMBRANE; WASTEWATER; WATER TREATMENT;

ARTICLE; BIOREACTOR; CONCENTRATION (PARAMETERS); EFFLUENT; EXTRACTION; FRANCE; GASTROENTERITIS; GENE LOCATION; HUMAN; MENGO VIRUS; NONHUMAN; NOROVIRUS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SAMPLING; VIRAL CONTAMINATION; VIRUS LOAD; WASTE COMPONENT REMOVAL; WASTE WATER; WASTE WATER MANAGEMENT;

FRANCE; FRESH WATER; MENGOVIRUS; NOROVIRUS; REFERENCE STANDARDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; WATER PURIFICATION;

MENGO VIRUS; NOROVIRUS;

EID: 37349023992     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01428-07     Document Type: Article

References (42)

1. Atmar, R. L., and M. K. Estes. 2001. Diagnosis of noncultivatable gastroenteritis viruses, the human caliciviruses. Clin. Microbiol. Rev. 14:15-37.
2. Atmar, R. L., and M. K. Estes. 2006. The epidemiologic and clinical importance of norovirus infection. Gastroenterol. Clin. N. Am. 35:275-290.
3. Atmar, R. L., F. H. Neill, J. I. Romalde, F. S. 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.
4. Blanton, L. H., S. M. Adams, R. S. Beard, G. Wei, S. N. Bulens, M. A. Widdowson, R. I. Glass, and S. S. Monroe. 2006. Molecular and epidemiologic trends of caliciviruses associated with outbreaks of acute gastroenteritis in the United States, 2000-2004. J. Infect. Dis. 193:413-421.
5. Bon, F., K. Ambert-Balay, H. Giraudon, J. Kaplon, S. Le Guyader, M. Pommepuy, A. Gallay, V. Vaillant, H. de Valk, R Chikhi-Brachet, A. Flahaut, P. Pothier, and E. Kohli. 2005. Molecular epidemiology of caliciviruses detected in sporadic and outbreak cases of gastroenteritis in France from December 1998 to February 2004. J. Clin. Microbiol. 43:4659-4664.
6. Chowdhary, R, A. Shukla, T. Datta, and T. N. Dhole. 2005. Rapid detection of sewage sample polioviruses by integrated cell culture polymerase chain reaction. Arch. Environ. Occup. Health 60:223-228.
7. Costafreda, M. I., A. Bosch, and R. M. Pinto. 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. Appl. Environ. Microbiol. 72:3846-3855.
8. Duizer, E., P. Bijkerk, B. Rockx, A. de Groot, F. Twisk, and M. Koopmans. 2004. Inactivation of caliciviruses. Appl. Environ. Microbiol. 70:4538-4543.
9. Garcia, C., H. L. DuPont, K. Z. Long, J. I. Santos, and G. P. Ko. 2006. Asymptomatic norovirus infection in Mexican children. J. Clin. Microbiol. 44:2997-3000.
10. Goodgame, R. W. 2001. Viral causes of diarrhea. Gastroenterol. Clin. N. Am. 30:779-795.
11. Gregory, J. B., R. W. Litaker, and R. T. Noble. 2006. Rapid one-step quantitative reverse transcriptase PCR assay with competitive internal positive control for detection of enteroviruses in environmental samples. Appl. Environ. Microbiol. 72:3960-3967.
12. Hovi, T. 2006. Surveillance for polioviruses. Biologicals 34:123-126.
13. Kageyama, T., S. Kojima, M. Shinohara, K. Uchida, S. Fukushi, F. B. Hoshino, N. Takeda, and K. Katayama. 2003. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J. Clin. Microbiol. 41:1548-1557.
14. Kageyama, T., M. Shinohara, K. Uchida, S. Fukushi, F. B. Hoshino, S. Kojima, R. Takai, T. Oka, N. Takeda, and K. Katayama. 2004. Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to norovirus in Japan. J. Clin. Microbiol. 42:2988-2995.
15. Kim, T. D., and H. Unno. 1996. The roles of microbes in the removal and inactivation of viruses in a biological wastewater treatment system. Water Sei. Technol. 33:243-250.
16. La Rosa, G., S. Fontana, A. Di Grazia, M. Iaconelli, M. Pourshaban, and M. Musculo. 2007. Molecular identification and genetic analysis of norovirus genogroups I and II in water environments: comparative analysis of different reverse transcription-PCR assays. Appl. Environ. Microbiol. 73:4152-4161.
17. Laverick, M. A., A. P. Wyn-Jones, and M. J. Carter. 2004. Quantitative RT-PCR for the enumeration of noroviruses (Norwalk-like viruses) in water and sewage. Lett. Appl. Microbiol. 39:127-136.
18. 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.
19. 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.
20. Lodder, W. J., and A. M. D. Husman. 2005. Presence of noroviruses and other enteric viruses in sewage and surface waters in The Netherlands. Appl. Environ. Microbiol. 71:1453-1461.
21. Loisy, F., R. L. Atmar, P. Guillen, 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.
22. Lopman, B., H. Vennema, E. Kohli, P. Pothier, A. Sanchez, A. Negredo, J. Buesa, E. Schreier, M. Reacher, D. Brown, J. Gray, M. Iturriza, C. Gallimore, B. Bottiger, K. O. Hedlund, M. Torven, C. H. von Bonsdorff, L. Maunula, M. Poljsak-Prijatelj, J. Zimsek, G. Reuter, G. Szucs, B. Melegh, L. Svennson, Y. van Duijnhoven, and M. Koopmans. 2004. Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet 363:682-688.
23. Lopman, B. A., D. W. Brown, and M. Koopmans. 2002. Human caliciviruses in Europe. J. Clin. Virol. 24:137-160.
24. Lopman, B. A., M. H. Reacher, I. B. Vipond, D. Hill, C. Perry, T. Halladay, D. W. Brown, W. J. Edmunds, and J. Sarangi. 2004. Epidemiology and cost of nosocomial gastroenteritis, Avon, England, 2002-2003. Emerg. Infect. Dis. 10:1827-1834.
25. Maunula, L., I. T. Miettinen, and C. H. von Bonsdorff. 2005. Norovirus outbreaks from drinking water. Emerg. Infect. Dis. 11:1716-1721.
26. Metcalf, T., J. Melnick, and M. K. Estes. 1995. Environmental virology: from detection of virus in sewage and water by isolation to identification by molecular biology-a trip of over 50 years. Annu. Rev. Microbiol. 49:461-487.
27. Mounts, A. W., T. Ando, M. Koopmans, J. S. Bresee, J. Noel, and R I. Glass. 2000. Cold weather seasonality of gastroenteritis associated with Norwalk-like viruses. J. Infect. Dis. 181:S284-S287.
28. Myrmel, M., E. M. M. Berg, B. Grinde, and E. Rimstad. 2006. Enteric viruses in inlet and outlet samples from sewage treatment plants. J. Water Health 4:197-209.
29. Okhuysen, P. C., X. Jiang, L. M. Ye, P. C. Johnson, and M. K. Estes. 1995. Viral shedding and fecal lga response after Norwalk virus-infection. J. Infect. Dis. 171:566-569.
30. Pusch, D., D. Y. Oh, S. Wolf, R. Dumke, U. Schroter-Bobsin, M. Hohne, I. Roske, and E. Schreier. 2005. Detection of enteric viruses and bacterial indicators in German environmental waters. Arch. Virol. 150:929-947.
31. Rutjes, S. A., R. Italiaander, H. van den Berg, W. J. Lodder, and A. M. D. Husman. 2005. Isolation and detection of enterovirus RNA from largevolume water samples by using the NucliSens miniMAG system and realtime nucleic acid sequence-based amplification. Appl. Environ. Microbiol. 71:3734-3740.
32. Schwab, K. J., M. K. Estes, F. H. Neill, and R. L. Atmar. 1997. Use of heat release and an internal RNA standard control in reverse transcription-PCR detection of Norwalk virus from stool samples. J. Clin. Microbiol. 35:511-514.
33. Svraka, S., E. Duizer, H. Vennema, E. de Bruin, B. van der Veer, B. Dorresteijn, and M. Koopmans. 2007. Etiological role of viruses in outbreaks of acute gastroenteritis in The Netherlands from 1994 through 2005. J. Clin. Microbiol. 45:1389-1394.
34. Tan, M., and X. Jiang. 2005. Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol. 13:285-293.
35. Trujillo, A. A., K. A. McCaustland, D. P. Zheng, L. A. Hadley, G. Vaughn, S. M. Adams, T. Ando, R. I. Glass, and S. S. Monroe. 2006. Use of TaqMan real-time reverse transcription-PCR for rapid detection, quantification, and typing of norovirus. J. Clin. Microbiol. 44:1405-1412.
36. Ueki, Y., D. Sano, T. Watanabe, 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.
37. Vainio, K., and M. Myrmel. 2006. Molecular epidemiology of norovirus outbreaks in Norway during 2000 to 2005 and comparison of four norovirus real-time reverse transcriptase PCR assays. J. Clin. Microbiol. 44:3695-3702.
38. van den Berg, H., W. Lodder, W. van der Poel, H. Vennema, and A. M. D. Husman. 2005. Genetic diversity of noroviruses in raw and treated sewage water. Res. Microbiol. 156:532-540.
39. Westrell, T., P. Teunis, H. van den Berg, W. Lodder, H. Ketelaars, T. A. Stenstrom, and A. M. D. Husman. 2006. Short- and long-term variations of norovirus concentrations in the Meuse River during a 2-year study period. Water Res. 40:2613-2620.
40. Whiley, D. A., and T. P. Sloots. 2005. Sequence variation in primer targets affects the accuracy of viral quantitative PCR. J. Clin. Virol. 34:104-107.
41. 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.
42. Zheng, D. P., T. Ando, R. L. Fankhauser, R. S. Beard, R. I. Glass, and S. S. Monroe. 2006. Norovirus classification and proposed strain nomenclature. Virology 346:312-323.