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A One Year Study on the Concentrations of Norovirus and Enteric Adenoviruses in Wastewater and A Surface Drinking Water Source in Norway

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Abstract

Enteric viruses transmitted via the faecal-oral route occur in high concentrations in wastewater and may contaminate drinking water sources and cause disease. In order to quantify enteric adenovirus and norovirus genotypes I and II (GI and GII) impacting a drinking source in Norway, samples of surface water (52), wastewater inlet (64) and outlet (59) were collected between January 2011 and April 2012. Samples were concentrated in two steps, using an electropositive disc filter and polyethylene glycol precipitation, followed by nucleic acid extraction and analysis by quantitative polymerase chain reaction. Virus was detected in 47/52 (90.4 %) of surface water, 59/64 (92 %) of wastewater inlet and 55/59 (93 %) of wastewater outlet samples. Norovirus GI occurred in the highest concentrations in surface water (2.51e + 04) and adenovirus in wastewater (2.15e + 07). While adenovirus was the most frequently detected in all matrices, norovirus GI was more frequently detected in surface water and norovirus GII in wastewater. This study is the first in Norway to monitor both sewage and a drinking water source in parallel, and confirms the year-round presence of norovirus and adenovirus in a Norwegian drinking water source.

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References

  • Ahmed, S. M., Lopman, B. A., & Levy, K. (2013). A systematic review and meta-analysis of the global seasonality of norovirus. PLoS ONE, 8(10), e75922. doi:10.1371/journal.pone.0075922.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ayukekbong, J. A., Andersson, M. E., Vansarla, G., Tah, F., Nkuo-Akenji, T., Lindh, M., et al. (2014). Monitoring of seasonality of norovirus and other enteric viruses in Cameroon by real-time PCR: An exploratory study. Epidemiology and Infection, 142(7), 1393–1402.

    Article  CAS  PubMed  Google Scholar 

  • Ballester, N.A, Fontaine, J.H., & Margolin, A.B. (2005). Occurrence and correlations between coliphages and anthropogenic viruses in the Massachusetts Bay using enrichment and ICC-nPCR. Journal of Water and Health, 3(1), 59–68. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/15952453.

  • Bambrick, H., Dear, K., Woodruff, R., Hanigan, I., & McMichael, A. (2008, July 17). Garnaut Climate Change Review: The impacts of climate change on three health outcomes: temperature-related mortality and hospitalisations, salmonellosis and other bacterial gastroenteritis, and population at risk from dengue. Garnaut Review. Retrieved from http://climate.adfi.usq.edu.au/684/.

  • Burns, M., & Valdivia, H. (2007). Modelling the limit of detection in real-time quantitative PCR. European Food Research and Technology, 226(6), 1513–1524. doi:10.1007/s00217-007-0683-z.

    Article  Google Scholar 

  • Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., et al. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry, 55(4), 611–622. doi:10.1373/clinchem.2008.112797.

    Article  CAS  PubMed  Google Scholar 

  • Cashdollar, J. L., Brinkman, N. E., Griffin, S. M., McMinn, B. R., Rhodes, E. R., Varughese, E. A., et al. (2013). Development and evaluation of EPA method 1615 for detection of enterovirus and norovirus in water. Applied and Environmental Microbiology, 79(1), 215–223. doi:10.1128/AEM.02270-12.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Comelli, H. L., Rimstad, E., Larsen, S., & Myrmel, M. (2008). Detection of norovirus genotype I.3b and II.4 in bioaccumulated blue mussels using different virus recovery methods. International Journal of Food Microbiology, 127(1–2), 53–59. doi:10.1016/j.ijfoodmicro.2008.06.003.

    Article  CAS  PubMed  Google Scholar 

  • Costafreda, M. I., Bosch, A., & Pintó, R. M. (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. Applied and Environmental Microbiology, 72(6), 3846–3855. doi:10.1128/AEM.02660-05.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Da Silva, A. K., Kavanagh, O. V., Estes, M. K., & Elimelech, M. (2011). Adsorption and aggregation properties of norovirus GI and GII virus-like particles demonstrate differing responses to solution chemistry. Environmental Science and Technology, 45(2), 520–526. doi:10.1021/es102368d.

    Article  PubMed  Google Scholar 

  • Da Silva, A. K., Le Saux, J.-C., Parnaudeau, S., Pommepuy, M., Elimelech, M., & Le Guyader, F. S. (2007). 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, 73(24), 7891–7897. doi:10.1128/AEM.01428-07.

    Article  PubMed Central  PubMed  Google Scholar 

  • Espinosa, A. C., Arias, C. F., Sánchez-Colón, S., & Mazari-Hiriart, M. (2009). Comparative study of enteric viruses, coliphages and indicator bacteria for evaluating water quality in a tropical high-altitude system. Environmental Health, 8(1), 49. doi:10.1186/1476-069X-8-49.

    Article  PubMed Central  PubMed  Google Scholar 

  • Fout, G. S., Dahling, D. R., & Safferman, R. S. (1996). ICR Microbial Laboratory Manual. Washington, DC: U.S. Environmental Protection Agency.

  • Gibbons, C. D., Rodríguez, R. A., Tallon, L., & Sobsey, M. D. (2010). Evaluation of positively charged alumina nanofibre cartridge filters for the primary concentration of noroviruses, adenoviruses and male-specific coliphages from seawater. Journal of Applied Microbiology, 109(2), 635–641. doi:10.1111/j.1365-2672.2010.04691.x.

    CAS  PubMed  Google Scholar 

  • Hamza, I. A., Jurzik, L., Stang, A., Sure, K., Uberla, K., & Wilhelm, M. (2009). Detection of human viruses in rivers of a densly-populated area in Germany using a virus adsorption elution method optimized for PCR analyses. Water Research, 43(10), 2657–2668. doi:10.1016/j.watres.2009.03.020.

    Article  CAS  PubMed  Google Scholar 

  • Hurst, C.J., Dahling, D.R., Safferman, R.S., & Goyke, T. (1984). Comparison of commercial beef extracts and similar materials for recovering viruses from environmental samples. Canadian Journal of Microbiology, 30(10), 1253–1263. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/6095985.

  • Ikner, L. A., Gerba, C. P., & Bright, K. R. (2012). Concentration and recovery of viruses from water: a comprehensive review. Food and Environmental Virology, 4(2), 41–67. doi:10.1007/s12560-012-9080-2.

    Article  PubMed  Google Scholar 

  • Ikner, L. A., Soto-Beltran, M., & Bright, K. R. (2011). New method using a positively charged microporous filter and ultrafiltration for concentration of viruses from tap water. Applied and Environmental Microbiology, 77(10), 3500–3506. doi:10.1128/AEM.02705-10.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • ILSI. (1996). Risk Science Institute Pathogen Risk Assessment Working Group. A conceptual framework to assess the risks of human disease following exposure to pathogens. Risk Analysis, 16(6), 841–848. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/8972112.

  • Johansen, S.S. (2005). Bivariate frequency analysis of flood characteristics at Glomma and Gudbrandsdalslågen. University of Oslo. Retrieved from https://www.duo.uio.no//handle/10852/12354.

  • Jothikumar, N., Cromeans, T. L., Hill, V. R., Lu, X., Sobsey, M. D., & Erdman, D. D. (2005). Quantitative real-time PCR assays for detection of human adenoviruses and identification of serotypes 40 and 41. Applied and Environmental Microbiology, 71(6), 3131–3136. doi:10.1128/AEM.71.6.3131-3136.2005.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., et al. (2003). Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of Clinical Microbiology, 41(4), 1548–1557. doi:10.1128/JCM.41.4.1548-1557.2003.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Karim, M. R., Rhodes, E. R., Brinkman, N., Wymer, L., & Fout, G. S. (2009). New electropositive filter for concentrating enteroviruses and noroviruses from large volumes of water. Applied and Environmental Microbiology, 75(8), 2393–2399. doi:10.1128/AEM.00922-08.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kvitsand, H. M. L., & Fiksdal, L. (2010). Waterborne disease in Norway: emphasizing outbreaks in groundwater systems. Water Science and Technology, 61(3), 563–571. doi:10.2166/wst.2010.863.

    Article  PubMed  Google Scholar 

  • Laine, J., Huovinen, E., Virtanen, M. J., Snellman, M., Lumio, J., Ruutu, P., et al. (2010). An extensive gastroenteritis outbreak after drinking-water contamination by sewage effluent, Finland. Epidemiology and Infection, 139(7), 1105–1113. doi:10.1017/S0950268810002141.

    Article  PubMed  Google Scholar 

  • Larsson, C., Andersson, Y., Allestam, G., Lindqvist, A., Nenonen, N., & Bergstedt, O. (2013). Epidemiology and estimated costs of a large waterborne outbreak of norovirus infection in Sweden. Epidemiology and Infection, 142(3), 592–600. doi:10.1017/S0950268813001209.

    Article  PubMed  Google Scholar 

  • Lees, D. (2010). International standardisation of a method for detection of human pathogenic viruses in molluscan shellfish. Food and Environmental Virology, 2(3), 146–155. doi:10.1007/s12560-010-9042-5.

    Article  Google Scholar 

  • Maunula, L., Miettinen, I.T., & von Bonsdorff, C.-H. (2005). Norovirus outbreaks from drinking water. Emerging Infectious Diseases, 11(11), 1716–1721. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/21251349.

  • Maunula, L., Söderberg, K., Vahtera, H., Vuorilehto, V.-P., Von Bonsdorff, C.-H., Valtari, M., et al. (2012). Presence of human noro- and adenoviruses in river and treated wastewater, a longitudinal study and method comparison. Journal of Water and Health, 10(1), 87–99. doi:10.2166/wh.2011.095.

    Article  PubMed  Google Scholar 

  • Myrmel, M., Berg, E.M.M., Grinde, B., & Rimstad, E. (2006). Enteric viruses in inlet and outlet samples from sewage treatment plants. Journal of Water and Health, 4(2), 197–209. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/16813012.

  • Myrmel, M., & Rimstad, E. (2000). Antigenic diversity of Norwalk-like viruses: expression of the capsid protein of a genogroup I virus, distantly related to Norwalk virus. Archives of Virology, 145(4), 711–723. doi:10.1007/s007050050665.

    Article  CAS  PubMed  Google Scholar 

  • 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 Research. Retrieved from http://liu.diva-portal.org/smash/record.jsf?pid=diva2:210971.

  • Nygård, K., Gondrosen, B., & Lund, V. (2003). Sykdomsutbrudd forårsaket av drikkevann i Norge. Tidsskrift For Den Norske Lægeforening, (23), 3410–3413. Retrieved from http://tidsskriftet.no/article/933966.

  • Ottoson, J., Hansen, A., Björlenius, B., Norder, H., & Stenström, T. A. A. (2006). Removal of viruses, parasitic protozoa and microbial indicators in conventional and membrane processes in a wastewater pilot plant. Water Research, 40(7), 1449–1457. doi:10.1016/j.watres.2006.01.039.

    Article  CAS  PubMed  Google Scholar 

  • Patel, M. M., Hall, A. J., Vinjé, J., & Parashar, U. D. (2009). Noroviruses: a comprehensive review. Journal of Clinical Virology, 44(1), 1–8. doi:10.1016/j.jcv.2008.10.009.

    Article  CAS  PubMed  Google Scholar 

  • Patel, M. M., Widdowson, M.-A., Glass, R. I., Akazawa, K., Vinjé, J., & Parashar, U. D. (2008). Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerging Infectious Diseases, 14(8), 1224–1231. doi:10.3201/eid1408.071114.

    Article  PubMed Central  PubMed  Google Scholar 

  • Pintó, R. M., Costafreda, M. I., & Bosch, A. (2009). Risk assessment in shellfish-borne outbreaks of hepatitis A. Applied and Environmental Microbiology, 75(23), 7350–7355. doi:10.1128/AEM.01177-09.

    Article  PubMed Central  PubMed  Google Scholar 

  • Rodríguez-Lázaro, D., Cook, N., Ruggeri, F. M., Sellwood, J., Nasser, A., Nascimento, M. S. J., et al. (2012). Virus hazards from food, water and other contaminated environments. FEMS Microbiology Reviews, 36(4), 786–814. doi:10.1111/j.1574-6976.2011.00306.x.

    Article  PubMed  Google Scholar 

  • Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M.-A., Roy, S. L., et al. (2011). Foodborne illness acquired in the United States—major pathogens. Emerging Infectious Diseases, 17(1), 7–15. doi:10.3201/eid1701.P11101.

    Article  PubMed Central  PubMed  Google Scholar 

  • Sherwood, V., Burgert, H.-G., Chen, Y.-H., Sanghera, S., Katafigiotis, S., Randall, R. E., et al. (2007). Improved growth of enteric adenovirus type 40 in a modified cell line that can no longer respond to interferon stimulation. The Journal of General Virology, 88(Pt 1), 71–76. doi:10.1099/vir.0.82445-0.

    Article  CAS  PubMed  Google Scholar 

  • Simmons, F. J., & Xagoraraki, I. (2011). Release of infectious human enteric viruses by full-scale wastewater utilities. Water Research, 45(12), 3590–3598. doi:10.1016/j.watres.2011.04.001.

    Article  CAS  PubMed  Google Scholar 

  • Sterk, A., Schijven, J., de Nijs, T., & de Roda Husman, A. M. (2013). Direct and indirect effects of climate change on the risk of infection by water-transmitted pathogens. Environmental Science and Technology,. doi:10.1021/es403549s.

    PubMed  Google Scholar 

  • Stetler, R.E., Morris, M.E., & Safferman, R.S. (1992). Processing procedures for recovering enteric viruses from wastewater sludges. Journal of Virological Methods, 40(1), 67–75. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1331161.

  • Tirado, M. C., Clarke, R., Jaykus, L. A., McQuatters-Gollop, A., & Frank, J. M. (2010). Climate change and food safety: a review. Food Research International, 43(7), 1745–1765. doi:10.1016/j.foodres.2010.07.0.

    Article  Google Scholar 

  • Vega, E., Barclay, L., Gregoricus, N., Shirley, S. H., Lee, D., & Vinjé, J. (2014). Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009–2013. Journal of Clinical Microbiology, 52(1), 147–155. doi:10.1128/JCM.02680-13.

  • White, P. A. (2014). Evolution of norovirus. Clinical Microbiology and Infection. doi:10.1111/1469-0691.12746.

    PubMed  Google Scholar 

  • WHO. (2011). WHO guidelines for drinking-water quality. In: (World Health Organisation, Ed.) (4th edition, Vol. 38, p. 541). Geneva, Switzerland: World Health Organisation. Retrieved from http://www.who.int/water_sanitation_health/publications/2011/dwq_guidelines/en/index.html.

  • Wilhelmi, I., Roman, E., & Sánchez-Fauquier, A. (2003). Viruses causing gastroenteritis. Clinical Microbiology and Infection, 9(4), 247–262. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/19100169.

  • Wilson, I.G. (1997). Inhibition and facilitation of nucleic acid amplification. Applied and Environmental Microbiology, 63(10), 3741–3751. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=168683&tool=pmcentrez&rendertype=abstract.

  • World Health Organisation. (2005). The World Health Report 2004: Changing History. Geneva, Switzerland. Retrieved from http://www.who.int/whr/2004/en/index.html.

  • World Health Organisation. (2013). The World Health Report 2013: Research for Universal Health Coverage. Geneva, Switzerland. Retrieved from http://www.who.int/whr/2013/report/en/index.html.

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Acknowledgments

This work has been developed within the VISK project, from the Interreg IV A programme, financed by the European Union Regional Development Fund. Lena Solli Sal was the main contact at the DWTP and provided the data on water parameters. We would also like to thank Tor Håkonsen (VA-support AS, Kløfta, Norway) and Arve Heistad, Razak Seidu and Vegard Nilsen (Norwegian University of Life Sciences, Ås, Norway) for their useful discussions around the data collection and analysis.

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  1. Department of Food Safety and Infection Biology, Microbiology, Immunology and Parasitology, Faculty of Veterinary Science and Biomedicine, Norwegian University of Life Sciences, Postbox 8146 Dep., 0033, Oslo, Norway

    Ricardo C. Grøndahl-Rosado, Ekaterina Yarovitsyna, Mette Myrmel & Lucy J. Robertson

  2. Virology Section, National Veterinary Institute, Oslo, Norway

    Elin Trettenes

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  1. Ricardo C. Grøndahl-Rosado
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  2. Ekaterina Yarovitsyna
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Correspondence to Lucy J. Robertson.

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Grøndahl-Rosado, R.C., Yarovitsyna, E., Trettenes, E. et al. A One Year Study on the Concentrations of Norovirus and Enteric Adenoviruses in Wastewater and A Surface Drinking Water Source in Norway. Food Environ Virol 6, 232–245 (2014). https://doi.org/10.1007/s12560-014-9161-5

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