Norovirus removal and particle association in a waste stabilization pond

Environmental Science and Technology

Volumn 42, Issue 24, 2008, Pages 9151-9157

  Da Silva, Allegra K ^a,c   Le Guyader, Françoise S ^b   Le Saux, Jean Claude ^b   Pommepuy, Monique ^b   Montgomery, Maggie A ^a   Elimelech, Menachem ^a  

^a YALE UNIVERSITY   (United States)

^b IFREMER   (France)

^c Berkeley   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLOIDAL PARTICLES; FINAL EFFLUENTS; M FILTERS; MEMBRANE FILTERS; NOROVIRUS; PARTICLE ASSOCIATIONS; PARTICLE SETTLING; POLYMERASE CHAIN REACTIONS; POSITIVELY CHARGED; POSITIVELY CHARGED MEMBRANES; SIZE RANGES; SUSPENDED PARTICLES; TIME REVERSES; VIRAL CONCENTRATIONS; VIRUS REMOVALS; WASTE STABILIZATION PONDS; WASTEWATER SAMPLES;

ASSOCIATION REACTIONS; FILTRATION; LAKES; MICROORGANISMS; SEWAGE TREATMENT PLANTS; STABILIZATION; STABILIZATION PONDS; VIRUSES; WASTEWATER;

EFFLUENTS;

COLLOID; MEMBRANE; POLLUTANT REMOVAL; POLYMERASE CHAIN REACTION; VIRUS; WASTEWATER;

ENVIRONMENTAL REMEDIATION; FILTRATION; NOROVIRUS; PARTICULATE MATTER; REFUSE DISPOSAL; WATER SUPPLY;

NOROVIRUS;

EID: 58149151403     PISSN: 0013936X     EISSN: None     Source Type: Journal    
DOI: 10.1021/es802787v     Document Type: Article

References (41)

1. Lopman, B. A.; Reacher, M. H.; Vipond, I. B.; Hill, D.; Perry, C.; Halladay, T.; Brown, D. W.; Edmunds, W. J.; Sarangi, J. Epidemiology and cost of nosocomial gastroenteritis, Avon, England, 2002-2003. Emerging Infect. Dis. 2004, 10, 1827-1834.
2. Pruss-Ustun, A.; Bos, R.; Gore, F.; Bartram, J. Safer water, better health: cost, benefits, and sustainability interventions to protect and promote health; World Health Organization, 2008.
3. Atmar, R. L.; Estes, M. K. The epidemiologic and clinical importance of norovirus infection. Gastroenterol. Clin. North Am. 2006, 35, 275-290.
4. Fankhauser, R. L.; Noel, J. S.; Monroe, S. S. Molecular epidemiology of "Norwalk-like viruses" in outbreaks of gastroenteritis in the United States. J. Infect. Dis. 1998, 178, 1571-1578.
5. Le Guyader, F. S.; Atmar, R. L. Viruses in shellfish. In Human Viruses in Water; Bosch, A., Ed.; Elsevier: Amsterdam, The Netherlands, 2007; Vol17, pp 205-226.
6. Zheng, D. P.; Ando, T.; Fankhauser, R. L.; Beard, R. S.; Glass, R. I.; Monroe, S. S. Norovirus classification and proposed strain nomenclature. Virology 2006, 346, 312-323.
7. Laverick, M. A.; Wyn-Jones, A. P.; Carter, M. J. Quantitative RT-PCR for the enumeration of noroviruses (Norwalk-like viruses) in water and sewage. Lett. Appl. Microbiol. 2004, 39, 127-136.
8. Le Guyader, F. S.; Haugarreau, L.; Miossec, L.; Dubois, E.; Pommepuy, M. Three-year study to assess human enteric viruses in shellfish. Appl. Environ. Microbiol. 2000, 66, 3241-3248.
9. Lodder, W. J.; Husman, A. M. D. Presence of noroviruses and other enteric viruses in sewage and surface waters in The Netherlands. Appl. Environ. Microbiol. 2005, 71, 1453-1461.
10. Metcalf, T.; Melnick, J.; Estes, M. K. 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. 1995, 49, 461-487.
11. Myrmel, M.; Berg, E. M. M.; Grinde, B.; Rimstad, E. Enteric viruses in inlet and outlet samples from sewage treatment plants. J. Water Health 2006, 4, 197-209.
12. Pusch, D.; Oh, D. Y.; Wolf, S.; Dumke, R.; Schroter-Bobsin, U.; Hohne, M.; Roske, I.; Schreier, E. Detection of enteric viruses and bacterial indicators in German environmental waters. Arch. Virol. 2005, 150, 929-947.
13. Ueki, Y.; Sano, D.; Watanabe, T.; Akiyama, K.; Omura, T. Norovirus pathway in water environment estimated by genetic analysis of strains from patients of gastroenteritis, sewage, treated wastewater, river water and oysters. Water Res. 2005, 39, 4271-4280.
14. van den Berg, H.; Lodder, W.; van der Poel, W.; Vennema, H.; Husman, A. M. D. Genetic diversity of noroviruses in raw and treated sewage water. Res. Microbiol. 2005, 156, 532-540.
15. Westrell, T.; Teunis, P.; van den Berg, H.; Lodder, W.; Ketelaars, H.; Stenstrom, T. A.; Husman, A. M. D. Short- and long-term variations of norovirus concentrations in the Meuse river during a 2-year study period. Water Res. 2006, 40, 2613-2620.
16. Goodgame, R. W. Viral causes of diarrhea. Gastroenterol. Clin. North Am. 2001, 30, 779-795.
17. Svraka, S.; Duizer, E.; Vennema, H.; de Bruin, E.; van der Veer, B.; Dorresteijn, B.; Koopmans, M. Etiological role of viruses in outbreaks of acute gastroenteritis in The Netherlands from 1994 through 2005. J. Clin. Microbiol. 2007, 45, 1389-1394.
18. Widdowson, M. A.; Sulka, A.; Bulens, S. N.; Beard, R. S.; Chaves, S. S.; Hammond, R.; Salehi, E. D. P.; Swanson, E.; Totaro, J.; Woron, R.; Mead, P. S.; Bresee, J. S.; Monroe, S. S.; Glass, R. I. Norovirus and foodborne disease, United States, 1991-2000. Emerging Infect. Dis. 2005, 11, 95-102.
19. da Silva, A. K.; Le Saux, J.-C.; Parnaudeau, S.; Pommepuy, M.; Elimelech, M.; Le Guyader, F. S. Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: Different behaviors of genogroups I and II. Appl. Environ. Microbiol. 2007, 73, 7891-7897.
20. Huffman, D. E.; Nelson, K. L.; Rose, J. B. Calicivirus - an emerging contaminant in water: state of the art. Environ. Eng. Sci. 2003, 20, 503-515.
21. Pommepuy, M.; Dominique, H.-H.; Caprais, M. P.; Gourmelon, M.; Le Guyader, F. S. Fecal contamination in coastal area: an engineering approach. In Oceans and Health: Pathogens in the marine environment; Belkin, S. S., Colwell, R., Eds.; Kluwer Academic and Plenum Publishers: New York, 2005; pp331-360.
22. The United Nations, 2000. http://www.un.org/millenniumgoals/.
23. Toutes-les-villes.com.
24. Standard Methods for the Examination of Water and Wastewater, 20th ed.; American Public Health Association: Washington, DC, 1998.
25. Atmar, R. L.; Neill, F. H.; Romalde, J. I.; Le Guyader, F. S.; Woodley, C. M.; Metcalf, T. G.; Estes, M. K. Detection of Norwalk virus and hepatitis A virus in shellfish tissues with the PCR. Appl. Environ. Microbiol. 1995, 61, 3014-3018.
26. Costafreda, M. I.; Bosch, A.; Pinto, R. M. Development, evaluation, and standardization of a real-time TaqMan reverse transcription-PCR assay for quantificiation of hepatitis A virus in clinical and shellfish samples. Appl. Environ. Microbiol. 2006, 72, 3846-3855.
27. Loisy, F.; Atmar, R. L.; Guillon, P.; Le Cann, P.; Pommepuy, M.; Le Guyader, F. S. Real-time RT-PCR for norovirus screening in shellfish. J. Virol. Methods 2005, 123, 1-7.
28. Chalapati, R. V.; Lakhe, S. B.; Waghmare, S. V. Virus removal in waste stabilization ponds in India. Water Res. 1981, 15, 773-778.
29. Feachem, R. G.; Bradley, D. J.; Garelick, H.; Mara, D. D. Sanitation and Disease: Health Aspects of Excreta and Wastewater Management; John Wiley & Sons: Chichester, U.K., 1983.
30. Maynard, H. E.; Ouki, S. K.; Williams, S. C. Tertiary lagoons: A review of removal mechanisms and performance. Water Res. 1999, 33, 1-13.
31. Ohgaki, S.; Ketratanakul, A.; Prasertsom, U. Effect of sunlight on coliphages in an oxidation pond. Water Sci. Technol. 1986, 18, 37-46.
32. Templeton, M. R.; Andrews, R. C.; Hofmann, R. Particle-associated viruses in water: Impacts on disinfection processes. Crit. Rev. Environ. Sci. Technol. 2008, 38, 137-164.
33. Gerba, C. P.; Stagg, C. H.; Abadie, M. G. Characterization of sewage solid-associated viruses and behavior in natural waters. Water Res. 1978, 12, 805-812.
34. Hejkal, T. W.; Wellings, F. M.; Lewis, A. L.; LaRock, P. A. Distribution of viruses associated with particles in wastewater. Appl. Environ. Microbiol. 1981, 41, 628-634.
35. Davies-Colley, R. J.; Craggs, R. J.; Park, J.; Sukias, J. P. S.; Nagels, J. W.; Stott, R. Virus removal in a pilot-scale 'advanced' pond system as indicated by somatic and F-RNA bacteriophages. Water Sci. Technol. 2005, 51, 107-110.
36. Davies-Colley, R. J.; Donnison, A. M.; Speed, D. J. Towards a mechanistic understanding of pond disinfection. Water Sci. Technol. 2000, 42, 149-158.
37. Davies-Colley, R. J.; Donnison, A. M.; Speed, D. J. Sunlight wavelengths inactivating faecal indicator microorganisms in waste stabilisation ponds. Water Sci. Technol. 1997, 35, 219-225.
38. Davies-Colley, R. J.; Donnison, A. M.; Speed, D. J.; Ross, C. M.; Nagels, J. W. Inactivation of faecal indicator microorganisms in waste stabilisation ponds: Interactions of environmental factors with sunlight. Water Res. 1999, 33, 1220-1230.
39. Sinton, L. W.; Hall, C. H.; Lynch, P. A.; Davies-Colley, R. J. Sunlight inactivation of fecal indicator bacteria and bacteriophages from waste stabilization pond effluent in fresh and saline waters. Appl. Environ. Microbiol. 2002, 68, 1122-1131.
40. Kohn, T.; Grandbois, M.; McNeill, K.; Nelson, K. L. Association with natural organic matter enhances the sunlight-mediated inactivation of MS2 coliphage by singlet oxygen. Environ. Sci. Technol. 2007, 41, 4626-4632.
41. Kohn, T.; Nelson, K. L. Sunlight-mediated inactivation of MS2 coliphage via exogenous singlet oxygen produced by sensitizers in natural waters. Environ. Sci. Technol. 2007, 41, 192-197.