Calicivirus Removal in a Membrane Bioreactor Wastewater Treatment Plant

ABSTRACT To evaluate membrane bioreactor wastewater treatment virus removal, a study was conducted in southwest France. Samples collected from plant influent, an aeration basin, membrane effluent, solid sludge, and effluent biweekly from October 2009 to June 2010 were analyzed for calicivirus (norovirus and sapovirus) by real-time reverse transcription-PCR (RT-PCR) using extraction controls to perform quantification. Adenovirus and Escherichia coli also were analyzed to compare removal efficiencies. In the influent, sapovirus was always present, while the norovirus concentration varied temporally, with the highest concentration being detected from February to May. All three human norovirus genogroups (GI, GII, and GIV) were detected in effluent, but GIV was never detected in effluent; GI and GII were detected in 50% of the samples but at low concentrations. In the effluent, sapovirus was identified only once. An adenovirus titer showing temporal variation in influent samples was identified only twice in effluent. E. coli was always below the limit of detection in the effluent. Overall, the removal of calicivirus varied from 3.3 to greater than 6.8 log units, with no difference between the two main genogroups. Our results also demonstrated that the viruses are blocked by the membrane in the treatment plant and are removed from the plant as solid sludge.

[1]  I. Xagoraraki,et al.  Removal of human enteric viruses by a full-scale membrane bioreactor during municipal wastewater processing. , 2011, Water research.

[2]  T. Oka,et al.  Genetic diversity of genogroup IV noroviruses in wastewater in Japan , 2011, Letters in applied microbiology.

[3]  R. Tauxe,et al.  Foodborne Illness Acquired in the United States—Unspecified Agents , 2011, Emerging infectious diseases.

[4]  L. Rodrigues,et al.  Risk factors for symptomatic and asymptomatic norovirus infection in the community , 2010, Epidemiology and Infection.

[5]  D. Sano,et al.  Quantification and Genotyping of Human Sapoviruses in the Llobregat River Catchment, Spain , 2010, Applied and Environmental Microbiology.

[6]  R. Atmar Noroviruses: State of the Art , 2010, Food and Environmental Virology.

[7]  M. Pommepuy,et al.  Environmental Conditions Leading to Shellfish Contamination and Related Outbreaks , 2010, Food and Environmental Virology.

[8]  J. Roberts,et al.  Effects of Source Water Quality on Chlorine Inactivation of Adenovirus, Coxsackievirus, Echovirus, and Murine Norovirus , 2010, Applied and Environmental Microbiology.

[9]  M. Verani,et al.  Evaluation of Adenovirus and E. coli as indicators for human enteric viruses presence in mussels produced in La Spezia Gulf (Italy) , 2010, Letters in applied microbiology.

[10]  K. Hedlund,et al.  Epidemiology and Genotype Analysis of Emerging Sapovirus-Associated Infections across Europe , 2010, Journal of Clinical Microbiology.

[11]  M. Iaconelli,et al.  Molecular detection and genetic diversity of norovirus genogroup IV: a yearlong monitoring of sewage throughout Italy , 2010, Archives of Virology.

[12]  J. Rose,et al.  Assessment of human adenovirus removal in a full-scale membrane bioreactor treating municipal wastewater. , 2010, Water research.

[13]  D. Mara,et al.  Estimation of norovirus infection risks to consumers of wastewater-irrigated food crops eaten raw. , 2010, Journal of water and health.

[14]  C. Johnsen,et al.  Genetic diversity of sapovirus infections in Danish children 2005-2007. , 2009, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[15]  A. Bosch,et al.  Risk Assessment in Shellfish-Borne Outbreaks of Hepatitis A , 2009, Applied and Environmental Microbiology.

[16]  K. Hedlund,et al.  Genetic Diversity among Food-Borne and Waterborne Norovirus Strains Causing Outbreaks in Sweden , 2009, Journal of Clinical Microbiology.

[17]  Andreas Matussek,et al.  Prevalence of norovirus and factors influencing virus concentrations during one year in a full-scale wastewater treatment plant. , 2009, Water research.

[18]  Kazuya Nakamura,et al.  Continuous Presence of Noroviruses and Sapoviruses in Raw Sewage Reflects Infections among Inhabitants of Toyama, Japan (2006 to 2008) , 2009, Applied and Environmental Microbiology.

[19]  M. Elimelech,et al.  Norovirus removal and particle association in a waste stabilization pond. , 2008, Environmental science & technology.

[20]  A. Bosch,et al.  Detection and Quantification of Noroviruses in Shellfish , 2008, Applied and Environmental Microbiology.

[21]  B. Lesjean,et al.  Survey of the European MBR market: trends and perspectives , 2008 .

[22]  D. Graham,et al.  Norwalk Virus Shedding after Experimental Human Infection , 2008, Emerging infectious diseases.

[23]  S. Ohgaki,et al.  Quantitative detection of sapoviruses in wastewater and river water in Japan , 2008, Letters in applied microbiology.

[24]  K. Oguma,et al.  One-year monthly quantitative survey of noroviruses, enteroviruses, and adenoviruses in wastewater collected from six plants in Japan. , 2008, Water research.

[25]  S. Judd The status of membrane bioreactor technology. , 2008, Trends in biotechnology.

[26]  M. Elimelech,et al.  Evaluation of Removal of Noroviruses during Wastewater Treatment, Using Real-Time Reverse Transcription-PCR: Different Behaviors of Genogroups I and II , 2007, Applied and Environmental Microbiology.

[27]  M. Iturriza-Gómara,et al.  Detection by PCR of eight groups of enteric pathogens in 4,627 faecal samples: re-examination of the English case-control Infectious Intestinal Disease Study (1993–1996) , 2007, European Journal of Clinical Microbiology & Infectious Diseases.

[28]  Kevin Purcell,et al.  Lack of Usefulness of an Abnormal White Blood Cell Count for Predicting a Concurrent Serious Bacterial Infection in Infants and Young Children Hospitalized With Respiratory Syncytial Virus Lower Respiratory Tract Infection , 2007, The Pediatric infectious disease journal.

[29]  Liu Jun-xin,et al.  Virus rejection with two model human enteric viruses in membrane bioreactor system , 2007 .

[30]  T. Oka,et al.  Human sapoviruses: genetic diversity, recombination, and classification , 2007, Reviews in medical virology.

[31]  D. Sano,et al.  Sapovirus in Water, Japan , 2007, Emerging infectious diseases.

[32]  K. Oguma,et al.  Seasonal profiles of human noroviruses and indicator bacteria in a wastewater treatment plant in Tokyo, Japan. , 2006, Water science and technology : a journal of the International Association on Water Pollution Research.

[33]  T. Oka,et al.  Detection of human sapovirus by real‐time reverse transcription‐polymerase chain reaction , 2006, Journal of medical virology.

[34]  M. C. Tomei,et al.  Effect of feed/inoculum ratio on anaerobic digestion of sonicated sludge. , 2006, Water science and technology : a journal of the International Association on Water Pollution Research.

[35]  D. Sano,et al.  Membrane separation of indigenous noroviruses from sewage sludge and treated wastewater. , 2006, Water science and technology : a journal of the International Association on Water Pollution Research.

[36]  R. Litaker,et al.  Rapid One-Step Quantitative Reverse Transcriptase PCR Assay with Competitive Internal Positive Control for Detection of Enteroviruses in Environmental Samples , 2006, Applied and Environmental Microbiology.

[37]  M. Myrmel,et al.  Enteric viruses in inlet and outlet samples from sewage treatment plants. , 2006, Journal of water and health.

[38]  B Björlenius,et al.  Removal of viruses, parasitic protozoa and microbial indicators in conventional and membrane processes in a wastewater pilot plant. , 2006, Water research.

[39]  Roger I. Glass,et al.  Use of TaqMan Real-Time Reverse Transcription-PCR for Rapid Detection, Quantification, and Typing of Norovirus , 2006, Journal of Clinical Microbiology.

[40]  D. Sano,et al.  Norovirus pathway in water environment estimated by genetic analysis of strains from patients of gastroenteritis, sewage, treated wastewater, river water and oysters. , 2005, Water research.

[41]  Chii Shang,et al.  Bacteriophage MS-2 removal by submerged membrane bioreactor. , 2005, Water research.

[42]  Harry Vennema,et al.  Genetic diversity of noroviruses in raw and treated sewage water. , 2005, Research in microbiology.

[43]  A. M. de Roda Husman,et al.  Presence of Noroviruses and Other Enteric Viruses in Sewage and Surface Waters in The Netherlands , 2005, Applied and Environmental Microbiology.

[44]  Marion Koopmans,et al.  Foodborne viruses: an emerging problem , 2003, International Journal of Food Microbiology.

[45]  L. Schwartzbrod,et al.  Best Viral Elution Method Available for Quantification of Enteroviruses in Sludge by Both Cell Culture and Reverse Transcription-PCR , 2001, Applied and Environmental Microbiology.

[46]  K. Kawamura,et al.  Coliphage rejection under ultramembrane filtration , 1996 .

[47]  B. Lesjean,et al.  Ten persistent myths and the realities of membrane bioreactor technology for municipal applications. , 2011, Water science and technology : a journal of the International Association on Water Pollution Research.

[48]  Xi Jiang,et al.  Caliciviruses : molecular and cellular virology , 2010 .

[49]  D. Chandler,et al.  Advances towards integrated biodetection systems for environmental molecular microbiology. , 2002, Current issues in molecular biology.