Removal properties of human enteric viruses in a pilot-scale membrane bioreactor (MBR) process

Water Research

Volumn 75, Issue , 2015, Pages 282-291

  Miura, Takayuki ^a   Okabe, Satoshi ^a   Nakahara, Yoshihito ^b,c   Sano, Daisuke ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b MITSUBISHI CHEMICAL CORPORATION   (Japan)

^c Wellthy Corporation   (Japan)

Author keywords

Adsorption; Enterovirus; MBR; Mixed liquor suspended solids; Norovirus; Sapovirus

Indexed keywords

ADSORPTION; BIOREACTORS; EFFLUENTS; LIQUIDS; MEMBRANE FOULING; MEMBRANES; MICROFILTRATION; POLYMERASE CHAIN REACTION; VIRUSES;

ENTEROVIRUS; MBR; MIXED LIQUOR SUSPENDED SOLIDS; NOROVIRUS; SAPOVIRUS;

ACTIVATED SLUDGE PROCESS;

POLYVINYLIDENE FLUORIDE; VIRUS RNA; WASTE WATER;

ACTIVATED SLUDGE; ADSORPTION; BIOFOULING; BIOREACTOR; EFFLUENT; MEMBRANE; POLLUTANT REMOVAL; VIRUS; WASTEWATER;

ACTIVATED SLUDGE; ARTICLE; CONTROLLED STUDY; EFFLUENT; ELECTRIC CONDUCTIVITY; ENTERIC VIRUS; ENTEROVIRUS; MEMBRANE REACTOR; MICROFILTRATION; NONHUMAN; NOROVIRUS; PH; PRIORITY JOURNAL; PROCESS CONTROL; REAL TIME POLYMERASE CHAIN REACTION; SAPOVIRUS; SEASONAL VARIATION; SOLID; SUSPENDED PARTICULATE MATTER; VIRUS GENOME; WASTE COMPONENT REMOVAL; WASTE WATER MANAGEMENT; BIOREACTOR; HUMAN; ISOLATION AND PURIFICATION; PILOT STUDY; VIROLOGY; WASTE WATER;

ENTEROVIRUS; MURINE NOROVIRUS; NOROVIRUS; SAPOVIRUS;

BIOREACTORS; ENTEROVIRUS; HUMANS; NOROVIRUS; PILOT PROJECTS; REAL-TIME POLYMERASE CHAIN REACTION; SAPOVIRUS; WASTE WATER;

EID: 84924663417     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2015.02.046     Document Type: Article

References (48)

1. Arvelo W., Sosa S.M., Juliao P., López M.R., Estevéz A., López B., Morales-Betoulle M.E., González M., Gregoricus N.A., Hall A.J., Vinje J., Parashar U., Lindblade K.A. Norovirus outbreak of probable waterborne transmission with high attack rate in a Guatemalan resort. J. Clin. Virol. 2012, 55(1):8-11.
2. Bae J., Schwab K.J. 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. 2008, 74(2):477-484.
3. Charles K.J., Shore J., Sellwood J., Laverick M., Hart A., Pedley S. Assessment of the stability of human viruses and coliphage in groundwater by PCR and infectivity methods. J. Appl. Microbiol. 2009, 106(6):1827-1837.
4. Chen C.H., Hsu B.M., Wan M.T. Molecular detection and prevalence of enterovirus within environmental water in Taiwan. J. Appl. Microbiol. 2008, 104(3):817-823.
5. da Silva A.K., Kavanagh O.V., Estes M.K., Elimelech M. Adsorption and aggregation properties of norovirus GI and GII virus-like particles demonstrate differing responses to solution chemistry. Environ. Sci. Technol. 2011, 45(2):520-526.
6. da Silva A.K., Le Guyader F.S., Le Saux J.C., Pommepuy M., Montgomery M.A., Elimelech M. Norovirus removal and particle association in a waste stabilization pond. Environ. Sci. Technol. 2008, 42(24):9151-9157.
7. 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(24):7891-7897.
8. Gao D.-W., Wen Z.-D., Li B., Liang H. Membrane fouling related to microbial community and extracellular polymeric substances at different temperatures. Bioresour. Technol. 2013, 143(0):172-177.
9. Gerba C.P. Adv. Appl. Microbiol 1984, 133-168. Academic Press. I.L. Allen (Ed.).
10. Gerba C.P., Goyal S.M., Hurst C.J., Labelle R.L. Type and strain dependence of enterovirus adsorption to activated sludge, soils and estuarine sediments. Water Res. 1980, 14(9):1197-1198.
11. Giammanco G.M., Di Bartolo I., Purpari G., Costantino C., Rotolo V., Spoto V., Geraci G., Bosco G., Petralia A., Guercio A., Macaluso G., Calamusa G., De Grazia S., Ruggeri F.M., Vitale F., Maida C.M., Mammina C. Investigation and control of a norovirus outbreak of probable waterborne transmission through a municipal groundwater system. J. Water Health 2014, 12(3):452-464.
12. Green K.Y. Fields Virology 2007, 949-979. Lippincott Williams & Wilkins, Philadelphia. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, S.E. Straus (Eds.).
13. Hata A., Kitajima M., Katayama H. Occurrence and reduction of human viruses, F-specific RNA coliphage genogroups and microbial indicators at a full-scale wastewater treatment plant in Japan. J. Appl. Microbiol. 2013, 114(2):545-554.
14. Hirani Z.M., DeCarolis J.F., Adham S.S., Jacangelo J.G. Peak flux performance and microbial removal by selected membrane bioreactor systems. Water Res. 2010, 44(8):2431-2440.
15. Iwai M., Yoshida H., Matsuura K., Fujimoto T., Shimizu H., Takizawa T., Nagai Y. Molecular epidemiology of echoviruses 11 and 13, based on an environmental surveillance conducted in Toyama prefecture, 2002-2003. Appl. Environ. Microbiol. 2006, 72(9):6381-6387.
16. Japan Sewage Works Association Standard Methods for the Examination of Wastewater 1997, Japan Sewage Works Association.
17. Ji Z., Wang X., Zhang C., Miura T., Sano D., Funamizu N., Okabe S. Occurrence of hand-foot-and-mouth disease pathogens in domestic sewage and secondary effluent in Xi'an, China. Microbes Environ. 2012, 27(3):288-292.
18. Kageyama T., Kojima S., Shinohara M., Uchida K., Fukushi S., Hoshino F.B., Takeda N., Katayama K. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J. Clin. Microbiol. 2003, 41(4):1548-1557.
19. Kato T., Miura T., Okabe S., Sano D. Bayesian modeling of enteric virus density in wastewater using left-censored data. Food Environ. Virol. 2013, 1-9.
20. Kitajima M., Oka T., Takagi H., Tohya Y., Katayama H., Takeda N., Katayama K. Development and application of a broadly reactive real-time reverse transcription-PCR assay for detection of murine noroviruses. J. Virol. Methods 2010, 169(2):269-273.
21. Kuo D.H.W., Simmons F.J., Blair S., Hart E., Rose J.B., Xagoraraki I. Assessment of human adenovirus removal in a full-scale membrane bioreactor treating municipal wastewater. Water Res. 2010, 44(5):1520-1530.
22. Lewis G.D., Metcalf T.G. Polyethylene glycol precipitation for recovery of pathogenic viruses, including hepatitis A virus and human rotavirus, from oyster, water, and sediment samples. Appl. Environ. Microbiol. 1988, 54(8):1983-1988.
23. Lodder W.J., de Roda Husman A.M. Presence of noroviruses and other enteric viruses in sewage and surface waters in the Netherlands. Appl. Environ. Microbiol. 2005, 71(3):1453-1461.
24. 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):1-7.
25. Lu R., Mosiman D., Nguyen T.H. Mechanisms of MS2 bacteriophage removal by fouled ultrafiltration membrane subjected to different cleaning methods. Environ. Sci. Technol. 2013, 47(23):13422-13429.
26. Ma Z., Wen X., Zhao F., Xia Y., Huang X., Waite D., Guan J. Effect of temperature variation on membrane fouling and microbial community structure in membrane bioreactor. Bioresour. Technol. 2013, 133(0):462-468.
27. Marti E., Monclús H., Jofre J., Rodriguez-Roda I., Comas J., Balcázar J.L. Removal of microbial indicators from municipal wastewater by a membrane bioreactor (MBR). Bioresour. Technol. 2011, 102(8):5004-5009.
28. Michen B., Graule T. Isoelectric points of viruses. J. Appl. Microbiol. 2010, 109(2):388-397.
29. Miura T., Masago Y., Sano D., Omura T. Development of an effective method for recovery of viral genomic RNA from environmental silty sediments for quantitative molecular detection. Appl. Environ. Microbiol. 2011, 77(12):3975-3981.
30. Miura T., Sano D., Suenaga A., Yoshimura T., Fuzawa M., Nakagomi T., Nakagomi O., Okabe S. Histo-blood group antigen-like substances of human enteric bacteria as specific adsorbents for human noroviruses. J. Virol. 2013, 87(17):9441-9451.
31. Miyoshi T., Tsuyuhara T., Ogyu R., Kimura K., Watanabe Y. Seasonal variation in membrane fouling in membrane bioreactors (MBRs) treating municipal wastewater. Water Res. 2009, 43(20):5109-5118.
32. Monpoeho S., Dehée A., Mignotte B., Schwartzbrod L., Marechal V., Nicolas J.C., Billaudel S., Férré V. Quantification of enterovirus RNA in sludge samples using single tube real-time RT-PCR. Biotechniques 2000, 29(1):88-93.
33. Nordgren J., Matussek A., Mattsson A., Svensson L., Lindgren P.E. Prevalence of norovirus and factors influencing virus concentrations during one year in a full-scale wastewater treatment plant. Water Res. 2009, 43(4):1117-1125.
34. Oka T., Katayama K., Hansman G.S., Kageyama T., Ogawa S., Wu F.-T., White P.A., Takeda N. Detection of human sapovirus by real-time reverse transcription-polymerase chain reaction. J. Med. Virol. 2006, 78(10):1347-1353.
35. Ottoson J., Hansen A., Björlenius B., Norder H., Stenström T.A. Removal of viruses, parasitic protozoa and microbialindicators in conventional and membrane processes in a wastewater pilot plant. Water Res. 2006, 40(7):1449-1457.
36. Racaniello V.R. Fields Virology 2007, 795-838. Lippincott Williams & Wilkins, Philadelphia. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, S.E. Straus (Eds.).
37. Shanker S., Choi J.-M., Sankaran B., Atmar R.L., Estes M.K., Prasad B.V.V. Structural analysis of histo-blood group antigen binding specificity in a norovirus GII.4 epidemic variant: implications for epochal evolution. J. Virol. 2011, 85(17):8635-8645.
38. Shimizu H., Nakashima K. Surveillance of hand, foot, andmouth disease for a vaccine. Lancet Infect. Dis. 2014, 14(4):262-263.
39. Shirato H., Ogawa S., Ito H., Sato T., Kameyama A., Narimatsu H., Xiaofan Z., Miyamura T., Wakita T., Ishii K., Takeda N. Noroviruses distinguish between type 1 and type 2 histo-blood group antigens for binding. J. Virol. 2008, 82(21):10756-10767.
40. Shirato-Horikoshi H., Ogawa S., Wakita T., Takeda N., Hansman G.S. Binding activity of norovirus and sapovirus to histo-blood group antigens. Arch. Virol. 2007, 152(3):457-461.
41. Sima L.C., Schaeffer J., Le Saux J.C., Parnaudeau S., Elimelech M., Le Guyader F.S. Calicivirus removal in a membrane bioreactor wastewater treatment plant. Appl. Environ. Microbiol. 2011, 77(15):5170-5177.
42. Simmons F.J., Kuo D.H.W., Xagoraraki I. Removal of human enteric viruses by a full-scale membrane bioreactor during municipal wastewater processing. Water Res. 2011, 45(9):2739-2750.
43. Soga-Momoki T. Surveillance of enterovirus infections in Yokohama City from 2004 to 2008. Jpn. J. Infect. Dis. 2009, 62(6):471-473.
44. U.S. EPA Environmental Regulations and Technology, Control of Pathogens and Vector Attraction in Sewage Sludge 2003, EPA/625/R-92/013, U.S. Environmental Protection Agency, Cincinnati.
45. 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(18):4271-4280.
46. Wang Q., Zhang Z., Saif L.J. Stability of and attachment to lettuce by a culturable porcine sapovirus surrogate for human caliciviruses. Appl. Environ. Microbiol. 2012, 78(11):3932-3940.
47. Wu J., Li H., Huang X. Indigenous somatic coliphage removal from a real municipal wastewater by a submerged membrane bioreactor. Water Res. 2010, 44(6):1853-1862.
48. Zheng H., Lu J., Zhang Y., Yoshida H., Guo X., Liu L., Li H., Zeng H., Fang L., Mo Y., Yi L., Chosa T., Xu W., Ke C. Prevalence of nonpolio enteroviruses in the sewage of Guangzhou City, China, from 2009 to 2012. Appl. Environ. Microbiol. 2013, 79(24):7679-7683.