Meta-analysis of the reduction of norovirus and male-specific coliphage concentrations in wastewater treatment plants

Applied and Environmental Microbiology

Volumn 81, Issue 14, 2015, Pages 4669-4681

  Pouillot, Régis ^a   van Doren, Jane M ^a   Woods, Jacquelina ^a   Plante, Daniel ^b   Smith, Mark ^b   Goblick, Gregory ^a   Roberts, Christopher ^c   Locas, Annie ^d   Hajen, Walter ^c   Stobo, Jeffrey ^c   White, John ^d   Holtzman, Jennifer ^b   Buenaventura, Enrico ^b   Burkhardt, William ^a   Catford, Angela ^b   Edwards, Robyn ^d   DePaola, Angelo ^a   Calci, Kevin R ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b HEALTH CANADA   (Canada)

^c ENVIRONMENT CANADA   (Canada)

^d CANADIAN FOOD INSPECTION AGENCY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGES; CHLORINE; DISINFECTION; EFFLUENTS; FLOWCHARTING; MOLLUSCS; SEWAGE PUMPING PLANTS; TOXICITY; WATER TREATMENT PLANTS;

95% CREDIBLE INTERVALS; CHLORINE DISINFECTION; FOOD-BORNE ILLNESS; INFLUENT CONCENTRATIONS; MECHANICAL SYSTEMS; POTENTIAL SOURCES; SCIENTIFIC LITERATURE; WASTEWATER TREATMENT PLANTS;

WASTEWATER TREATMENT;

BIVALVE; DISINFECTION; EFFLUENT; GENOME; GENOTYPE; LAGOON; MALE; META-ANALYSIS; VIRUS; WASTE TREATMENT; WASTEWATER;

CANADA; UNITED STATES;

BIVALVIA; NOROVIRUS;

FRESH WATER; WASTE WATER;

CHEMISTRY; COLIPHAGE; DEVICES; DISINFECTION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; META ANALYSIS; MICROBIOLOGY; NOROVIRUS; VIROLOGY; WASTE WATER; WATER MANAGEMENT;

COLIPHAGES; DISINFECTION; FRESH WATER; GENOTYPE; NOROVIRUS; WASTE WATER; WATER PURIFICATION;

EID: 84931373696     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00509-15     Document Type: Article

References (69)

1. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17:7-12. http://dx.doi.org/10.3201/eid1701.P11101.
2. Thomas MK, Murray R, Flockhart L, Pintar K, Pollari F, Fazil A, Nesbitt A, Marshall B. 2013. Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006. Foodborne Pathog Dis 10:639-648. http://dx.doi.org/10.1089/fpd.2012.1389.
3. Hall AJ, Lopman BA, Payne DC, Patel MM, Gastanaduy PA, Vinje J, Parashar UD. 2013. Norovirus disease in the United States. Emerg Infect Dis 19:1198-1205. http://dx.doi.org/10.3201/eid1908.130465.
4. Patel MM, Hall AJ, Vinje J, Parashar UD. 2009. Noroviruses: a comprehensive review. J Clin Virol 44:1-8. http://dx.doi.org/10.1016/j.jcv.2008.10.009.
5. Mesquita JR, Costantini VP, Cannon JL, Lin SC, Nascimento MS, Vinje J. 2013. Presence of antibodies against genogroup VI norovirus in humans. Virol J 10:176. http://dx.doi.org/10.1186/1743-422X-10-176.
6. Atmar RL. 2010. Noroviruses-state of the art. Food Environ Virol 2:117-126. http://dx.doi.org/10.1007/s12560-010-9038-1.
7. Hall AJ, Eisenbart VG, Etingue AL, Gould LH, Lopman BA, Parashar UD. 2012. Epidemiology of foodborne norovirus outbreaks, United States, 2001-2008. Emerg Infect Dis 18:1566-1573. http://dx.doi.org/10.3201/eid1810.120833.
8. Shieh YC, Baric RS, Woods JW, Calci KR. 2003. Molecular surveillance of enterovirus and Norwalk-like virus in oysters relocated to a municipalsewage-impacted gulf estuary. Appl Environ Microbiol 69:7130-7136. http://dx.doi.org/10.1128/AEM.69.12.7130-7136.2003.
9. Maalouf H, Pommepuy M, Le Guyader FS. 2010. Environmental conditions leading to shellfish contamination and related outbreaks. Food Environ Virol 2:136-145. http://dx.doi.org/10.1007/s12560-010-9043-4.
10. Burkhardt W, III, Calci KR. 2000. Selective accumulation may account for shellfish-associated viral illness. Appl Environ Microbiol 66:1375-1378. http://dx.doi.org/10.1128/AEM.66.4.1375-1378.2000.
11. Flannery J, Keaveney S, Rajko-Nenow P, O'Flaherty V, Dore W. 2012. Concentration of norovirus during wastewater treatment and its impact on oyster contamination. Appl Environ Microbiol 78:3400-3406. http://dx.doi.org/10.1128/AEM.07569-11.
12. Biancani PJ, Carmichael RH, Daskin JH, Burkhardt W, Calci KR. 2012. Seasonal and spatial effects of wastewater effluent on growth, survival, and accumulation of microbial contaminants by oysters in Mobile Bay, Alabama. Estuar Coast 35:121-131. http://dx.doi.org/10.1007/s12237-011-9421-7.
13. Sobsey MD, Shields PA, Hauchman FS, Davis AL, Rullman VA, Bosch A. 1987. Survival and persistence of hepatitis A virus in environmental samples. J Med Virol 21:A23.
14. Dore WJ, Lees DN. 1995. Behavior of Escherichia coli and male-specific bacteriophage in environmentally contaminated bivalve mollusks before and after depuration. Appl Environ Microbiol 61:2830-2834.
15. National Shellfish Sanitation Program. 2011. Guide for the control of molluscan shellfish. National Shellfish Sanitation Program, U.S. Food and Drug Administration, Silver Spring, MD. http://www.fda.gov/downloads/Food/GuidanceRegulation/FederalStateFoodPrograms/UCM350344.pdf.
16. Canadian Shellfish Sanitation Program. 2012. Manual of operations. Canadian Shellfish Sanitation Program, Ottawa, Ontario, Canada. http://www.inspection.gc.ca/food/fish-and-seafood/manuals/canadian-shellfish-sanitation-program/eng/1351609988326/1351610579883.
17. Ottoson J, Hansen A, Westrell T, Johansen K, Norder H, Stenstrom TA. 2006. Removal of noro-and enteroviruses, Giardia cysts, Cryptosporidium oocysts, and fecal indicators at four secondary wastewater treatment plants in Sweden. Water Environ Res 78:828-834. http://dx.doi.org/10.2175/106143006X101719.
18. Baggi F, Demarta A, Peduzzi R. 2001. Persistence of viral pathogens and bacteriophages during sewage treatment: lack of correlation with indicator bacteria. Res Microbiol 152:743-751. http://dx.doi.org/10.1016/S0923-2508(01)01255-4.
19. Burkhardt W, III, Woods JW, Calci KR. 2005. Evaluation of wastewater treatment plant efficiency to reduce bacterial and viral loading using realtime RT-PCR. Abstr 105th Gen Meet Am Soc Microbiol. American Society for Microbiology, Washington, DC.
20. Harwood VJ, Levine AD, Scott TM, Chivukula V, Lukasik J, Farrah SR, Rose JB. 2005. Validity of the indicator organism paradigm for pathogen reduction in reclaimed water and public health protection. Appl Environ Microbiol 71:3163-3170. http://dx.doi.org/10.1128/AEM.71.6.3163-3170.2005.
21. Miescier JJ, Cabelli VJ. 1982. Enterococci and other microbial indicators in municipal wastewater effluents. J Water Pollut Control Fed 54:1599-1606.
22. Griffin DW, Lipp EK, McLaughlin MR, Rose JB. 2001. Marine recreation and public health microbiology: quest for the ideal indicator. Bioscience 51:817-825. http://dx.doi.org/10.1641/0006-3568(2001)051[0817:MRAPHM]2.0.CO;2.
23. LaBelle RL, Gerba CP, Goyal SM, Melnick JL, Cech I, Bogdan GF. 1980. Relationships between environmental factors, bacterial indicators, and the occurrence of enteric viruses in estuarine sediments. Appl Environ Microbiol 39:588-596.
24. da Silva AK, Le Guyader FS, Le Saux JC, Pommepuy M, Montgomery MA, Elimelech M. 2008. Norovirus removal and particle association in a waste stabilization pond. Environ Sci Technol 42:9151-9157. http://dx.doi.org/10.1021/es802787v.
25. da Silva AK, Le Saux JC, Parnaudeau S, Pommepuy M, Elimelech M, Le Guyader FS. 2007. Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: different behaviors of genogroups I and II. Appl Environ Microbiol 73:7891-7897. http://dx.doi.org/10.1128/AEM.01428-07.
26. Katayama H, Haramoto E, Oguma K, Yamashita H, Tajima A, Nakajima H, Ohgaki S. 2008. One-year monthly quantitative survey of noroviruses, enteroviruses, and adenoviruses in wastewater collected from six plants in Japan. Water Res 42:1441-1448. http://dx.doi.org/10.1016/j.watres.2007.10.029.
27. Simmons FJ, Kuo DHW, Xagoraraki I. 2011. Removal of human enteric viruses by a full-scale membrane bioreactor during municipal wastewater processing. Water Res 45:2739-2750. http://dx.doi.org/10.1016/j.watres.2011.02.001.
28. Lasobras J, Dellunde J, Jofre J, Lucena F. 1999. Occurrence and levels of phages proposed as surrogate indicators of enteric viruses in different types of sludges. J Appl Microbiol 86:723-729. http://dx.doi.org/10.1046/j.1365-2672.1999.00722.x.
29. Simpson D, Jacangelo J, Loughran P, McIlroy C. 2003. Investigation of potential surrogate organisms and public health risk in UV irradiated secondary effluent. Water Sci Technol 47:37-43.
30. Bustin SA, Nolan T. 2004. Pitfalls of quantitative real-time reversetranscription polymerase chain reaction. J Biomol Tech 15:155-166.
31. Woods JS. 2010. Determining the relationship of human enteric viruses in clinical, wastewater, and environmental samples utilizing molecular and cell culture techniques. Ph.D. dissertation. The University of Southern Mississippi, Hattiesburg, MS.
32. Formiga-Cruz M, Hundesa A, Clemente-Casares P, Albiñana-Gimenez N, Allard A, Girones R. 2005. Nested multiplex PCR assay for detection of human enteric viruses in shellfish and sewage. J Virol Methods 125:111-118. http://dx.doi.org/10.1016/j.jviromet.2005.01.009.
33. Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Takeda N, Katayama K. 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. http://dx.doi.org/10.1128/JCM.41.4.1548-1557.2003.
34. DePaola A, Jones JL, Woods J, Burkhardt W, III, Calci KR, Krantz JA, Bowers JC, Kasturi K, Byars RH, Jacobs E, Williams-Hill D, Nabe K. 2010. Bacterial and viral pathogens in live oysters: 2007 United States market survey. Appl Environ Microbiol 76:2754-2768. http://dx.doi.org/10.1128/AEM.02590-09.
35. Simard C, Houde A, Trottier Y-L. 2007. Concentration of hepatitis A virus and rotavirus in spring or mineral bottled water samples and their detection by the reverse-transcriptase polymerase chain reaction (OPFLP-04). In The compendium of analytical methods, vol 5. Health Canada, Ottawa, Ontario, Canada.
36. Houde A, Leblanc D, Poitras E, Ward P, Brassard J, Trottier Y-L, Mueller P, Simard C. 2010. Detection of norovirus genogroups I and II using the conventional and real-time reverse-transcriptase polymerase chain reaction (OPFLP-10). In The compendium of analytical methods, vol 5. Health Canada, Ottawa, Ontario, Canada.
37. Vega E, Barclay L, Gregoricus N, Williams K, Lee D, Vinje J. 2011. Novel surveillance network for norovirus gastroenteritis outbreaks, United States. Emerg Infect Dis 17:1389-1395.
38. Mattison K, Plante M, Bidawid S, Bin Kingombe C, Houde A, Ward P. 2010. Detection of feline caliciviruses using the conventional and realtime reverse-transcriptase polymerase chain reaction (OPFLP-06). In The compendium of analytical methods, vol 5. Health Canada, Ottawa, Ontario, Canada.
39. Kojima S, Kageyama T, Fukushi S, Hoshino FB, Shinohara M, Uchida K, Natori K, Takeda N, Katayama K. 2002. Genogroup-specific PCR primers for detection of Norwalk-like viruses. J Virol Methods 100:107-114. http://dx.doi.org/10.1016/S0166-0934(01)00404-9.
40. Turnbull B. 1974. Nonparametric estimation of a survivorship function with doubly censored data. J Am Stat Assoc 69:169-173. http://dx.doi.org/10.1080/01621459.1974.10480146.
41. R Development Core Team. 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
42. Therneau TM, Grambsch PM. 2000. Modeling survival data: extending the Cox model. Springer, New York, NY.
43. Gilks WR, Richardson S, Spiegelhalter D. 1996. Markov chain Monte Carlo in practice. Chapman & Hall/CRC, London, United Kingdom.
44. Whitaker J. 1990. Graphical models in applied multivariate analysis. John Wiley & Sons, Ltd, Chichester, United Kingdom.
45. Thomas A, O'Hara B, Ligges U, Sturtz S. 2006. Making BUGS open. R News 6:12-17.
46. Plummer M, Best N, Cowles K, Vines K. 2006. CODA: convergence diagnosis and output analysis for MCMC. R News 6:7-11.
47. Albert I, Grenier E, Denis JB, Rousseau J. 2008. Quantitative risk assessment from farm to fork and beyond: a global Bayesian approach concerning food-borne diseases. Risk Anal 28:557-571. http://dx.doi.org/10.1111/j.1539-6924.2008.01000.x.
48. Gelman A, Rubin D. 1992. Inference from iterative simulation using multiple sequences. Stat Sci 7:457-511. http://dx.doi.org/10.1214/ss/1177011136.
49. Haramoto E, Katayama H, Oguma K, Yamashita H, Tajima A, Nakajima H, Ohgaki S. 2006. Seasonal profiles of human noroviruses and indicator bacteria in a wastewater treatment plant in Tokyo, Japan. Water Sci Technol 54:301-308. http://dx.doi.org/10.2166/wst.2006.888.
50. Francy DS, Stelzer EA, Bushon RN, Brady AM, Williston AG, Riddell KR, Borchardt MA, Spencer SK, Gellner TM. 2012. Comparative effectiveness of membrane bioreactors, conventional secondary treatment, and chlorine and UV disinfection to remove microorganisms from municipal wastewaters. Water Res 46:4164-4178. http://dx.doi.org/10.1016/j.watres.2012.04.044.
51. Fumian TM, Vieira CB, Leite JP, Miagostovich MP. 2013. Assessment of burden of virus agents in an urban sewage treatment plant in Rio de Janeiro, Brazil. J Water Health 11:110-119. http://dx.doi.org/10.2166/wh.2012.123.
52. Nordgren J, Matussek A, Mattsson A, Svensson L, Lindgren P-E. 2009. Prevalence of norovirus and factors influencing virus concentrations during one year in a full-scale wastewater treatment plant. Water Res 43: 1117-1125. http://dx.doi.org/10.1016/j.watres.2008.11.053.
53. Sima LC, Schaeffer J, Le Saux JC, Parnaudeau S, Elimelech M, Le Guyader FS. 2011. Calicivirus removal in a membrane bioreactor wastewater treatment plant. Appl Environ Microbiol 77:5170-5177. http://dx.doi.org/10.1128/AEM.00583-11.
54. Tian P, Yang D, Pan L, Mandrell R. 2012. Application of a receptorbinding capture quantitative reverse transcription-PCR assay to concentrate human norovirus from sewage and to study the distribution and stability of the virus. Appl Environ Microbiol 78:429-436. http://dx.doi.org/10.1128/AEM.06875-11.
55. Victoria M, Guimaraes FR, Fumian TM, Ferreira FF, Vieira CB, Shubo T, Leite JP, Miagostovich MP. 2010. One year monitoring of norovirus in a sewage treatment plant in Rio de Janeiro, Brazil. J Water Health 8:158-165. http://dx.doi.org/10.2166/wh.2009.012.
56. Rajko-Nenow P, Waters A, Keaveney S, Flannery J, Tuite G, Coughlan S, O'Flaherty V, Dore W. 2013. Norovirus genotypes present in oysters and in effluent from a wastewater treatment plant during the seasonal peak of infections in Ireland in 2010. Appl Environ Microbiol 79:2578-2587. http://dx.doi.org/10.1128/AEM.03557-12.
57. Kitajima M, Haramoto E, Phanuwan C, Katayama H, Ohgaki S. 2009. Detection of genogroup IV norovirus in wastewater and river water in Japan. Lett Appl Microbiol 49:655-658. http://dx.doi.org/10.1111/j.1472-765X.2009.02718.x.
58. van den Berg H, Lodder W, van der Poel W, Vennema H, de Roda Husman AM. 2005. Genetic diversity of noroviruses in raw and treated sewage water. Res Microbiol 156:532-540. http://dx.doi.org/10.1016/j.resmic.2005.01.008.
59. La Rosa G, Iaconelli M, Pourshaban M, Muscillo M. 2010. Detection and molecular characterization of noroviruses from five sewage treatment plants in central Italy. Water Res 44:1777-1784. http://dx.doi.org/10.1016/j.watres.2009.11.055.
60. Pusch D, Oh DY, Wolf S, Dumke R, Schroter-Bobsin U, Hohne M, Roske I, Schreier E. 2005. Detection of enteric viruses and bacterial indicators in German environmental waters. Arch Virol 150:929-947. http://dx.doi.org/10.1007/s00705-004-0467-8.
61. Simmons FJ, Xagoraraki I. 2011. Release of infectious human enteric viruses by full-scale wastewater utilities. Water Res 45:3590-3598. http://dx.doi.org/10.1016/j.watres.2011.04.001.
62. Helsel DR. 2006. Fabricating data: how substituting values for nondetects can ruin results, and what can be done about it. Chemosphere 65:2434-2439. http://dx.doi.org/10.1016/j.chemosphere.2006.04.051.
63. Nauta MJ. 2010. "Campylobacter transfer from naturally contaminated chicken thighs to cutting boards is inversely related to initial load," a comment on: J Food Prot 72:1836-1840 (2009). J Food Prot 73:6-7. (Author reply, 73:7-8.).
64. Iwai M, Hasegawa S, Obara M, Nakamura K, Horimoto E, Takizawa T, Kurata T, Sogen S, Shiraki K. 2009. Continuous presence of noroviruses and sapoviruses in raw sewage reflects infections among inhabitants of Toyama, Japan (2006 to 2008). Appl Environ Microbiol 75:1264-1270. http://dx.doi.org/10.1128/AEM.01166-08.
65. Lodder WJ, de Roda Husman AM. 2005. Presence of noroviruses and other enteric viruses in sewage and surface waters in The Netherlands. Appl Environ Microbiol 71:1453-1461. http://dx.doi.org/10.1128/AEM.71.3.1453-1461.2005.
66. Prado T, Silva DM, Guilayn WC, Rose TL, Gaspar AM, Miagostovich MP. 2011. Quantification and molecular characterization of enteric viruses detected in effluents from two hospital wastewater treatment plants. Water Res 45:1287-1297. http://dx.doi.org/10.1016/j.watres.2010.10.012.
67. Mounts AW, Ando T, Koopmans M, Bresee JS, Noel J, Glass RI. 2000. Cold weather seasonality of gastroenteritis associated with Norwalk-like viruses. J Infect Dis 181(Suppl 2):S284-S287. http://dx.doi.org/10.1086/315586.
68. Laverick MA, Wyn-Jones AP, Carter MJ. 2004. Quantitative RT-PCR for the enumeration of noroviruses (Norwalk-like viruses) in water and sewage. Lett Appl Microbiol 39:127-136. http://dx.doi.org/10.1111/j.1472-765X.2004.01534.x.
69. Dancho BA, Chen H, Kingsley DH. 2012. Discrimination between infectious and non-infectious human norovirus using porcine gastric mucin. Int J Food Microbiol 155:222-226. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.02.010.