Skip to main content

Advertisement

SpringerLink
Log in

A 1-Year Quantitative Survey of Noro-, Adeno-, Human Boca-, and Hepatitis E Viruses in Raw and Secondarily Treated Sewage from Two Plants in Norway

  • Original Paper
  • Published:
Food and Environmental Virology Aims and scope Submit manuscript

Abstract

A study of enteric viruses in raw and treated sewage from two secondary treatment plants, which received sewage from Oslo city (plant A) and small municipalities in Hedmark county in Norway (plant B), showed high levels of noro-, adeno-, and bocavirus throughout the year. A seasonal variation was observed for adeno- and GII norovirus with higher levels during winter and bocavirus that had more positive samples during winter. The virus concentrations in raw sewage were comparable in the two plants, with medians (log10 genome copies per liter) of 6.1, 6.3, 6.0, and 4.5 for noro GI, noro GII, adeno-, and bocavirus, respectively. The level of hepatitis E virus was not determined as it was below the limit of quantification. The mean log10 virus reduction was 0.55 (plant A) and 1.44 (plant B) with the highest reduction found in the plant with longer hydraulic retention time. The adenoviruses were dominantly serotype 41, while serotype 12 appeared sporadically. Of the 102 raw and treated sewage samples that were tested, eight were positive for hepatitis E virus of which four were from treated sewage. Two of the four obtained gene sequences from hepatitis E virus originated from the rural sewage samples and showed high similarity with a genotype 3 strain of hepatitis E virus detected in local piglets. Two other hepatitis E virus sequences obtained from urban sewage samples showed high similarities with genotype 3 strains isolated from urban sewage in Spain and a human genotype 1 isolate from India. The study gives information on the levels of noroviruses in raw and treated sewage, which is valuable to risk assessment, information indicating that some infections with hepatitis E viruses in Norway have a regional origin and that human bocavirus 2 and 3 are prevalent in the Norwegian population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bellou, M., Kokkinos, P., & Vantarakis, A. (2013). Shellfish-borne viral outbreaks: a systematic review. Food and Environmental Virology, 5(1), 13–23. doi:10.1007/s12560-012-9097-6.

    Article  CAS  PubMed  Google Scholar 

  • Blinkova, O., Rosario, K., Li, L., Kapoor, A., Slikas, B., Bernardin, F., et al. (2009). Frequent detection of highly diverse variants of cardiovirus, cosavirus, bocavirus, and circovirus in sewage samples collected in the United States. Journal of Clinical Microbiology, 47(11), 3507–3513. doi:10.1128/jcm.01062-09.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bosch, A., Guix, S., Sano, D., & Pinto, R. M. (2008). New tools for the study and direct surveillance of viral pathogens in water. Current Opinion in Biotechnology, 19(3), 295–301. doi:10.1016/j.copbio.2008.04.006.

    Article  CAS  PubMed  Google Scholar 

  • Calgua, B., Barardi, C. R., Bofill-Mas, S., Rodriguez-Manzano, J., & Girones, R. (2011). Detection and quantitation of infectious human adenoviruses and JC polyomaviruses in water by immunofluorescence assay. Journal of Virological Methods, 171(1), 1–7. doi:10.1016/j.jviromet.2010.09.013.

    Article  CAS  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 Environment Microbiology, 73(24), 7891–7897. doi:10.1128/aem.01428-07.

    Article  Google Scholar 

  • Erker, J. C., Desai, S. M., & Mushahwar, I. K. (1999). Rapid detection of Hepatitis E virus RNA by reverse transcription-polymerase chain reaction using universal oligonucleotide primers. Journal of Virological Methods, 81(1–2), 109–113.

    Article  CAS  PubMed  Google Scholar 

  • 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. Applied and Environment Microbiology, 78(9), 3400–3406. doi:10.1128/aem.07569-11.

    Article  CAS  Google Scholar 

  • Fong, T. T., Phanikumar, M. S., Xagoraraki, I., & Rose, J. B. (2010). Quantitative detection of human adenoviruses in wastewater and combined sewer overflows influencing a Michigan river. Applied and Environment Microbiology, 76(3), 715–723. doi:10.1128/aem.01316-09.

    Article  CAS  Google Scholar 

  • Gibson, K. E. (2014). Viral pathogens in water: occurrence, public health impact, and available control strategies. Current Opinion in Virology, 4, 50–57. doi:10.1016/j.coviro.2013.12.005.

    Article  PubMed  Google Scholar 

  • Grondahl-Rosado, R. C., Yarovitsyna, E., Trettenes, E., Myrmel, M., & Robertson, L. J. (2014). A one year study on the concentrations of norovirus and enteric adenoviruses in wastewater and a surface drinking water source in Norway. Food and Environmental Virology,. doi:10.1007/s12560-014-9161-5.

    PubMed  Google Scholar 

  • Hall, B. G. (2013). Building phylogenetic trees from molecular data with MEGA. Molecular Biology and Evolution, 30(5), 1229–1235. doi:10.1093/molbev/mst012.

    Article  CAS  PubMed  Google Scholar 

  • Hata, A., Kitajima, M., & Katayama, H. (2013). Occurrence and reduction of human viruses, F-specific RNA coliphage genogroups and microbial indicators at a full-scale wastewater treatment plant in Japan. Journal of Applied Microbiology, 114(2), 545–554. doi:10.1111/jam.12051.

    Article  CAS  PubMed  Google Scholar 

  • 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 Environment Microbiology, 71(6), 3131–3136. doi:10.1128/aem.71.6.3131-3136.2005.

    Article  CAS  Google Scholar 

  • Jothikumar, N., Cromeans, T. L., Robertson, B. H., Meng, X. J., & Hill, V. R. (2006). A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. Journal of Virological Methods, 131(1), 65–71. doi:10.1016/j.jviromet.2005.07.004.

    Article  CAS  PubMed  Google Scholar 

  • Kapoor, A., Simmonds, P., Slikas, E., Li, L., Bodhidatta, L., Sethabutr, O., et al. (2010). Human bocaviruses are highly diverse, dispersed, recombination prone, and prevalent in enteric infections. Journal of Infectious Diseases, 201(11), 1633–1643. doi:10.1086/652416.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Katayama, H., Haramoto, E., Oguma, K., Yamashita, H., Tajima, A., Nakajima, H., et al. (2008). One-year monthly quantitative survey of noroviruses, enteroviruses, and adenoviruses in wastewater collected from six plants in Japan. Water Research, 42(6–7), 1441–1448. doi:10.1016/j.watres.2007.10.029.

    Article  CAS  PubMed  Google Scholar 

  • La Rosa, G., Fontana, S., Di Grazia, A., Iaconelli, M., Pourshaban, M., & Muscillo, M. (2007). Molecular identification and genetic analysis of Norovirus genogroups I and II in water environments: comparative analysis of different reverse transcription-PCR assays. Applied and Environment Microbiology, 73(13), 4152–4161. doi:10.1128/aem.00222-07.

    Article  Google Scholar 

  • Logan, C., O’Leary, J. J., & O’Sullivan, N. (2006). Real-time reverse transcription-PCR for detection of rotavirus and adenovirus as causative agents of acute viral gastroenteritis in children. Journal of Clinical Microbiology, 44(9), 3189–3195. doi:10.1128/jcm.00915-06.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Loisy, F., Atmar, R. L., Guillon, P., Le Cann, P., Pommepuy, M., & Le Guyader, F. S. (2005). Real-time RT-PCR for norovirus screening in shellfish. Journal of Virological Methods, 123(1), 1–7. doi:10.1016/j.jviromet.2004.08.023.

    Article  CAS  PubMed  Google Scholar 

  • Lu, X., & Erdman, D. D. (2006). Molecular typing of human adenoviruses by PCR and sequencing of a partial region of the hexon gene. Archives of Virology, 151(8), 1587–1602. doi:10.1007/s00705-005-0722-7.

    Article  CAS  PubMed  Google Scholar 

  • Lysen, M., Thorhagen, M., Brytting, M., Hjertqvist, M., Andersson, Y., & Hedlund, K. O. (2009). Genetic diversity among food-borne and waterborne norovirus strains causing outbreaks in Sweden. Journal of Clinical Microbiology, 47(8), 2411–2418. doi:10.1128/jcm.02168-08.

    Article  PubMed Central  PubMed  Google Scholar 

  • Maunula, L., Kaupke, A., Vasickova, P., Soderberg, K., Kozyra, I., Lazic, S., et al. (2013). Tracing enteric viruses in the European berry fruit supply chain. International Journal of Food Microbiology, 167(2), 177–185. doi:10.1016/j.ijfoodmicro.2013.09.003.

    Article  PubMed  Google Scholar 

  • Mena, K. D., & Gerba, C. P. (2009). Waterborne adenovirus. Reviews of Environmental Contamination and Toxicology, 198, 133–167. doi:10.1007/978-0-387-09647-6_4.

    CAS  PubMed  Google Scholar 

  • Myrmel, M., Berg, E. 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.

    CAS  PubMed  Google Scholar 

  • Neske, F., Blessing, K., Tollmann, F., Schubert, J., Rethwilm, A., Kreth, H. W., et al. (2007). Real-time PCR for diagnosis of human bocavirus infections and phylogenetic analysis. Journal of Clinical Microbiology, 45(7), 2116–2122. doi:10.1128/jcm.00027-07.

    Article  CAS  PubMed Central  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, 43(4), 1117–1125. doi:10.1016/j.watres.2008.11.053.

    Article  CAS  PubMed  Google Scholar 

  • Phillips, G., Tam, C. C., Rodrigues, L. C., & Lopman, B. (2010). Prevalence and characteristics of asymptomatic norovirus infection in the community in England. Epidemiology and Infection, 138(10), 1454–1458. doi:10.1017/s0950268810000439.

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Manzano, J., Alonso, J. L., Ferrus, M. A., Moreno, Y., Amoros, I., Calgua, B., et al. (2012). Standard and new faecal indicators and pathogens in sewage treatment plants, microbiological parameters for improving the control of reclaimed water. Water Science and Technology, 66(12), 2517–2523. doi:10.2166/wst.2012.233.

    Article  CAS  PubMed  Google Scholar 

  • Rohayem, J. (2009). Norovirus seasonality and the potential impact of climate change. Clinical Microbiology & Infection, 15(6), 524–527. doi:10.1111/j.1469-0691.2009.02846.x.

    Article  CAS  Google Scholar 

  • Schildgen, O. (2013). Human bocavirus: lessons learned to date. Pathogens, 2(1), 1–12. doi:10.3390/pathogens2010001.

    Article  PubMed Central  PubMed  Google Scholar 

  • Svraka, S., Duizer, E., Vennema, H., de Bruin, E., van der Veer, B., Dorresteijn, B., et al. (2007). Etiological role of viruses in outbreaks of acute gastroenteritis in The Netherlands from 1994 through 2005. Journal of Clinical Microbiology, 45(5), 1389–1394. doi:10.1128/jcm.02305-06.

    Article  PubMed Central  PubMed  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30(12), 2725–2729. doi:10.1093/molbev/mst197.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • WHO. (2011). Guidelines for drinking water quality (Vol. 4). Geneva: World Health Organization.

    Google Scholar 

  • Widen, F., Sundqvist, L., Matyi-Toth, A., Metreveli, G., Belak, S., Hallgren, G., et al. (2011). Molecular epidemiology of hepatitis E virus in humans, pigs and wild boars in Sweden. Epidemiology and Infection, 139(3), 361–371. doi:10.1017/s0950268810001342.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The study was funded by the Norwegian Research Council, Grant number 173021/I10.

Author information

Author notes

  1. H. Lange

    Present address: Norwegian Institute of Public Health, Oslo, Norway

Authors and Affiliations

  1. Department of Food Safety and Infection Biology, Faculty of Veterinary Medicine and Biosciences, Norwegian University of Life Sciences, Oslo, Norway

    M. Myrmel, H. Lange & E. Rimstad

Authors
  1. M. Myrmel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. Lange
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Rimstad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Myrmel.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Myrmel, M., Lange, H. & Rimstad, E. A 1-Year Quantitative Survey of Noro-, Adeno-, Human Boca-, and Hepatitis E Viruses in Raw and Secondarily Treated Sewage from Two Plants in Norway. Food Environ Virol 7, 213–223 (2015). https://doi.org/10.1007/s12560-015-9200-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12560-015-9200-x

Keywords

Search

Navigation