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Food and Environmental Virology

, Volume 11, Issue 1, pp 9–19 | Cite as

Detection of Norovirus and Rotavirus Present in Suspended and Dissolved Forms in Drinking Water Sources

  • Takayuki MiuraEmail author
  • Arisa Gima
  • Michihiro Akiba
Original Paper
  • 74 Downloads

Abstract

We investigated the present forms of genogroup II norovirus and group A rotavirus in surface water used for drinking water production. River water samples (N = 15) collected at a drinking water treatment plant (DWTP) monthly from June 2017 to August 2018 were fractioned by filtration through 10- and 0.45-μm-pore-size membranes, and viruses present in suspended and dissolved forms were quantitatively detected. Norovirus GII was present in > 10-μm- and 0.45–10-μm-suspended and dissolved forms with detection rates of 33%, 60%, and 87%, respectively. Rotavirus A was detected more frequently than norovirus GII in each form (> 10 μm suspended, 73%; 0.45–10 μm suspended, 93%; dissolved, 100%). We also analyzed surface water samples from 21 DWTPs all over Japan in non-epidemic and epidemic seasons of gastroenteritis. Norovirus GII was detected in 48% and 81% of samples with the concentrations of up to 4.1 and 5.3 log10 copies/L in dissolved form in non-epidemic and epidemic seasons, respectively, and GII.4 Sydney 2012 was predominant genotype followed by GII.2. Rotavirus A was detected in 95% and 86% of samples with the maximum concentrations of 5.5 and 6.3 log10 copies/L in dissolved form in respective seasons. Concentration of norovirus GII was similar in 0.45–10-μm suspended and dissolved forms, while there was a significant difference for rotavirus A (P < 0.01, pared t test), indicating that rotavirus A was less associated with suspended solids in the surface water samples compared to norovirus GII. Our observations provide important implications for understanding of viral behavior in environmental waters.

Keywords

Norovirus Rotavirus Suspended solids Adsorption Surface water Drinking water source 

Notes

Acknowledgements

We are very grateful to people in the 21 waterworks in Japan for their great effort in providing the source water samples. We also thank Nobuko Maeda and Nobuyo Yoshida (National Institute of Public Health), Naoko Arakawa (Kushiro City), Nariko Shinohara (Chiba Prefecture), and Satoshi Matsumura (Suita City) for their technical assistance. This study was supported in part by the Japan Society for the Promotion of Science through KAKENHI (17K14752) and by the Ministry of Health, Labor, and Welfare, Japan through a Health and Labor Sciences Research Grant (H28-Kenki-Ippan-005).

Supplementary material

12560_2018_9361_MOESM1_ESM.docx (352 kb)
Supplementary material 1 (DOCX 352 KB)

References

  1. AFNOR. (2011). U47A Méthodes d’analyse en santé animale. France: Association Française de Normalisation.Google Scholar
  2. Armanious, A., Aeppli, M., Jacak, R., Refardt, D., Sigstam, T., Kohn, T., et al. (2016). Viruses at solid–water interfaces: A systematic assessment of interactions driving adsorption. Environmental Science and Technology, 50(2), 732–743.  https://doi.org/10.1021/acs.est.5b04644.Google Scholar
  3. Bhattarai, R., Davidson, P. C., Kalita, P. K., &Kuhlenschmidt, M. S. (2017). Modeling effect of cover condition and soil type on rotavirus transport in surface flow. Journal of Water Health, 15(4), 545–554.  https://doi.org/10.2166/wh.2017.240.Google Scholar
  4. Boonchan, M., Motomura, K., Inoue, K., Ode, H., Chu, P. Y., Lin, M., et al. (2017). Distribution of norovirus genotypes and subtypes in river water by ultra-deep sequencing-based analysis. Letters in Applied Microbiology, 65(1), 98–104.  https://doi.org/10.1111/lam.12750.Google Scholar
  5. Chaudhry, R. M., Holloway, R. W., Cath, T. Y., &Nelson, K. L. (2015). Impact of virus surface characteristics on removal mechanisms within membrane bioreactors. Water Research, 84,144–152.  https://doi.org/10.1016/j.watres.2015.07.020.Google Scholar
  6. daSilva, A. K., LeGuyader, F.S., LeSaux, J.-C., Pommepuy, M., Montgomery, M. A.&Elimelech, M. (2008). Norovirus removal and particle association in a waste stabilization pond. Environmental Science and Technology, 42(24), 9151–9157.  https://doi.org/10.1021/es802787v.Google Scholar
  7. deGraaf, M., vanBeek, J., &Koopmans, M. P. G. (2016). Human norovirus transmission and evolution in a changing world. Nature Reviews Microbiology, 14(7), 421–433.  https://doi.org/10.1038/nrmicro.2016.48.Google Scholar
  8. Denisova, E., Dowling, W., LaMonica, R., Shaw, R., Scarlata, S., Ruggeri, F., et al. (1999). Rotavirus capsid protein VP5* permeabilizes membranes. Journal of Virology, 73(4), 3147–3153.Google Scholar
  9. Estes, M. K., &Greenberg, H. B. (2013). Rotaviruses. In D. M.Knipe&P. M.Howley (Eds.), Fields virology (Vol. 2, 6th edn., pp. 1347–1401). Philadelphia: Lippincott Williams & Wilkins.Google Scholar
  10. Fauvel, B., Ogorzaly, L., Cauchie, H.-M., &Gantzer, C. (2017). Interactions of infectious F-specific RNA bacteriophages with suspended matter and sediment: Towards an understanding of FRNAPH distribution in a river water system. Science of the Total Environment, 574,960–968.  https://doi.org/10.1016/j.scitotenv.2016.09.115.Google Scholar
  11. Fumian, T. M., Leite, G., Rose, J. P., Prado, T. L., T., &Miagostovich, M. P. (2011). One year environmental surveillance of rotavirus specie A (RVA) genotypes in circulation after the introduction of the Rotarix® vaccine in Rio de Janeiro, Brazil. Water Research, 45(17), 5755–5763.  https://doi.org/10.1016/j.watres.2011.08.039.Google Scholar
  12. Geoghegan, J. L., Senior, A. M., DiGiallonardo, F., &Holmes, E. C. (2016). Virological factors that increase the transmissibility of emerging human viruses. Proceedings of the National Academy of Sciences, 113(15), 4170–4175.  https://doi.org/10.1073/pnas.1521582113.Google Scholar
  13. Hansman, G. S., Biertümpfel, C., Georgiev, I., McLellan, J. S., Chen, L., Zhou, T., et al. (2011). Crystal structures of GII.10 and GII.12 norovirus protruding domains in complex with histo-blood group antigens reveal details for a potential site of vulnerability. Journal of Virology, 85(13), 6687–6701.  https://doi.org/10.1128/jvi.00246-11.Google Scholar
  14. Haramoto, E., Kitajima, M., Hata, A., Torrey, J. R., Masago, Y., Sano, D., et al. (2018). A review on recent progress in the detection methods and prevalence of human enteric viruses in water. Water Research, 135,168–186.  https://doi.org/10.1016/j.watres.2018.02.004.Google Scholar
  15. Haramoto, E., Kitajima, M., Kishida, N., Katayama, H., Asami, M., &Akiba, M. (2012). Occurrence of viruses and protozoa in drinking water sources of Japan and their relationship to indicator microorganisms. Food and Environmental Virology, 4(3), 93–101.  https://doi.org/10.1007/s12560-012-9082-0.Google Scholar
  16. Ishii, S., Kitamura, G., Segawa, T., Kobayashi, A., Miura, T., Sano, D., et al. (2014). Microfluidic quantitative PCR for simultaneous quantification of multiple viruses in environmental water samples. Applied and Environmental Microbiology, 80(24), 7505–7511.  https://doi.org/10.1128/aem.02578-14.Google Scholar
  17. 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.  https://doi.org/10.1128/jcm.41.4.1548-1557.2003.Google Scholar
  18. Katayama, H., Shimasaki, A., &Ohgaki, S. (2002). Development of a virus concentration method and its application to detection of enterovirus and Norwalk virus from coastal seawater. Applied and Environmental Microbiology, 68(3), 1033–1039.  https://doi.org/10.1128/aem.68.3.1033-1039.2002.Google Scholar
  19. Kazama, S., Masago, Y., Tohma, K., Souma, N., Imagawa, T., Suzuki, A., et al. (2016). Temporal dynamics of norovirus determined through monitoring of municipal wastewater by pyrosequencing and virological surveillance of gastroenteritis cases. Water Research, 92,244–253.  https://doi.org/10.1016/j.watres.2015.10.024.Google Scholar
  20. Kazama, S., Miura, T., Masago, Y., Konta, Y., Tohma, K., Manaka, T., et al. (2017). Environmental surveillance of norovirus genogroups I and II for sensitive detection of epidemic variants. Applied and Environmental Microbiology.  https://doi.org/10.1128/aem.03406-16.Google Scholar
  21. Kim, I. S., Trask, S. D., Babyonyshev, M., Dormitzer, P. R., &Harrison, S. C. (2010). Effect of mutations in VP5* hydrophobic loops on rotavirus cell entry. Journal of Virology, 84(12), 6200–6207.  https://doi.org/10.1128/jvi.02461-09.Google Scholar
  22. Kishida, N., Morita, H., Haramoto, E., Asami, M., &Akiba, M. (2012). One-year weekly survey of noroviruses and enteric adenoviruses in the Tone River water in Tokyo metropolitan area, Japan. Water Research, 46(9), 2905–2910.  https://doi.org/10.1016/j.watres.2012.03.010.Google Scholar
  23. Kitajima, M., Haramoto, E., Phanuwan, C., Katayama, H., &Ohgaki, S. (2009). Detection of genogroup IV norovirus in wastewater and river water in Japan. Letters in Applied Microbiology, 49(5), 655–658.  https://doi.org/10.1111/j.1472-765X.2009.02718.x.Google Scholar
  24. Kitajima, M., Oka, T., Haramoto, E., Takeda, N., Katayama, K., &Katayama, H. (2010a). Seasonal distribution and genetic diversity of genogroups I, II, and IV noroviruses in the Tamagawa River, Japan. Environmental Science and Technology, 44(18), 7116–7122.  https://doi.org/10.1021/es100346a.Google Scholar
  25. Kitajima, M., Oka, T., Takagi, H., Tohya, Y., Katayama, H., Takeda, N., et al. (2010b). Development and application of a broadly reactive real-time reverse transcription-PCR assay for detection of murine noroviruses. Journal of Virological Methods, 169(2), 269–273.  https://doi.org/10.1016/j.jviromet.2010.07.018.Google Scholar
  26. Kojima, S., Kageyama, T., Fukushi, S., Hoshino, F. B., Shinohara, M., Uchida, K., et al. (2002). Genogroup-specific PCR primers for detection of Norwalk-like viruses. Journal of Virological Methods, 100(1–2), 107–114.  https://doi.org/10.1016/s0166-0934(01)00404-9.Google Scholar
  27. Kroneman, A., Vennema, H., Deforche, K., Avoort, H. v. d, Peñaranda, S., Oberste, M. S., et al. (2011). An automated genotyping tool for enteroviruses and noroviruses. Journal of Clinical Virology, 51(2), 121–125.  https://doi.org/10.1016/j.jcv.2011.03.006.Google Scholar
  28. Kumar, S., Stecher, G., &Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870–1874.  https://doi.org/10.1093/molbev/msw054.Google Scholar
  29. LaRosa, G., Sanseverino, I., Della Libera, S., Iaconelli, M., Ferrero, V. E. V., Caracciolo, B., A., et al (2017). The impact of anthropogenic pressure on the virological quality of water from the Tiber River, Italy. Letters in Applied Microbiology, 65(4), 298–305.  https://doi.org/10.1111/lam.12774.Google Scholar
  30. Larsson, C., Andersson, Y., Allestam, G., Lindqvist, A., Nenonen, N., &Bergstedt, O. (2014). Epidemiology and estimated costs of a large waterborne outbreak of norovirus infection in Sweden. Epidemiology and Infection, 142(3), 592–600.  https://doi.org/10.1017/S0950268813001209.Google Scholar
  31. LeMennec, C., Parnaudeau, S., Rumebe, M., LeSaux, J.-C., Piquet, J.-C., &LeGuyader, S. F. (2017). Follow-up of norovirus contamination in an oyster production area linked to repeated outbreaks. Food and Environmental Virology, 9(1), 54–61.  https://doi.org/10.1007/s12560-016-9260-6.Google Scholar
  32. Li, D., Breiman, A., LePendu, J., &Uyttendaele, M. (2015). Binding to histo-blood group antigen-expressing bacteria protects human norovirus from acute heat stress. Frontiers in Microbiology.  https://doi.org/10.3389/fmicb.2015.00659.Google Scholar
  33. Liu, P., Chien, Y.-W., Papafragkou, E., Hsiao, H.-M., Jaykus, L.-A., &Moe, C. (2009). Persistence of human noroviruses on food preparation surfaces and human hands. Food and Environmental Virology, 1(3–4), 141–147.  https://doi.org/10.1007/s12560-009-9019-4.Google Scholar
  34. Loisy, F., Atmar, R. L., Guillon, P., LeCann, P., Pommepuy, M., &LeGuyader, F. S. (2005). Real-time RT-PCR for norovirus screening in shellfish. Journal of Virological Methods, 123(1), 1–7.Google Scholar
  35. Mackowiak, M., Leifels, M., Hamza, I. A., Jurzik, L., &Wingender, J. (2018). Distribution of Escherichia coli, coliphages and enteric viruses in water, epilithic biofilms and sediments of an urban river in Germany. Science of the Total Environment, 626,650–659.  https://doi.org/10.1016/j.scitotenv.2018.01.114.Google Scholar
  36. Masachessi, G., Pisano, M. B., Prez, V. E., Martínez, L. C., Michelena, J. F., Martínez-Wassaf, M., et al. (2018). Enteric viruses in surface waters from Argentina: Molecular and viable-virus detection. Applied and Environmental Microbiology.  https://doi.org/10.1128/aem.02327-17.Google Scholar
  37. Mathijs, E., Stals, A., Baert, L., Botteldoorn, N., Denayer, S., Mauroy, A., et al. (2012). A review of known and hypothetical transmission routes for noroviruses. Food and Environmental Virology, 4(4), 131–152.  https://doi.org/10.1007/s12560-012-9091-z.Google Scholar
  38. Michen, B., &Graule, T. (2010). Isoelectric points of viruses. Journal of Applied Microbiology, 109(2), 388–397.  https://doi.org/10.1111/j.1365-2672.2010.04663.x.Google Scholar
  39. Miura, T., Okabe, S., Nakahara, Y., &Sano, D. (2015). Removal properties of human enteric viruses in a pilot-scale membrane bioreactor (MBR) process. Water Research, 75,282–291.  https://doi.org/10.1016/j.watres.2015.02.046.Google Scholar
  40. Miura, T., Sano, D., Suenaga, A., Yoshimura, T., Fuzawa, M., Nakagomi, T., et al. (2013). Histo-blood group antigen-like substances of human enteric bacteria as specific adsorbents for human noroviruses. Journal of Virology, 87(17), 9441–9451.  https://doi.org/10.1128/jvi.01060-13.Google Scholar
  41. Miura, T., Schaeffer, J., LeSaux, J.-C., LeMehaute, P., &LeGuyader, F. S. (2018). Virus type-specific removal in a full-scale membrane bioreactor treatment process. Food and Environmental Virology, 10(2), 176–186.  https://doi.org/10.1007/s12560-017-9330-4.Google Scholar
  42. Moreira, N. A., &Bondelind, M. (2017). Safe drinking water and waterborne outbreaks. Journal of Water Health, 15(1), 83–96.  https://doi.org/10.2166/wh.2016.103.Google Scholar
  43. Moresco, V., Damazo, N. A., &Barardi, C. R. M. (2016). Rotavirus vaccine stability in the aquatic environment. Journal of Applied Microbiology, 120(2), 321–328.  https://doi.org/10.1111/jam.13021.Google Scholar
  44. Morioka, I., Kamiyoshi, N., Nishiyama, M., Yamamura, T., Minamikawa, S., Iwatani, S., et al. (2017). Changes in the numbers of patients with acute gastroenteritis after voluntary introduction of the rotavirus vaccine in a Japanese children’s primary emergency medical center. Environmental Health and Preventive Medicine, 22(1), 15.  https://doi.org/10.1186/s12199-017-0638-3.Google Scholar
  45. Pang, X., Cao, M., Zhang, M., &Lee, B. (2011). Increased sensitivity for various rotavirus genotypes in stool specimens by amending three mismatched nucleotides in the forward primer of a real-time RT-PCR assay. Journal of Virological Methods, 172(1–2), 85–87.  https://doi.org/10.1016/j.jviromet.2010.12.013.Google Scholar
  46. Pang, X. L., Lee, B., Boroumand, N., Leblanc, B., Preiksaitis, J. K., &Yu Ip, C. C. (2004). Increased detection of rotavirus using a real time reverse transcription-polymerase chain reaction (RT-PCR) assay in stool specimens from children with diarrhea. Journal of Medical Virology, 72(3), 496–501.  https://doi.org/10.1002/jmv.20009.Google Scholar
  47. Pérez-Sautu, U., Sano, D., Guix, S., Kasimir, G., Pintó, R. M., &Bosch, A. (2012). Human norovirus occurrence and diversity in the Llobregat river catchment, Spain. Environmental Microbiology, 14(2), 494–502.  https://doi.org/10.1111/j.1462-2920.2011.02642.x.Google Scholar
  48. Polo, D., Garcia-Fernandez, I., Fernandez-Ibanez, P., &Romalde, J. L. (2015). Solar water disinfection (SODIS): Impact on hepatitis A virus and on a human Norovirus surrogate under natural solar conditions. International Microbiology, 18(1), 41–49.  https://doi.org/10.2436/20.1501.01.233.Google Scholar
  49. Prevost, B., Lucas, F. S., Goncalves, A., Richard, F., Moulin, L., &Wurtzer, S. (2015). Large scale survey of enteric viruses in river and waste water underlines the health status of the local population. Environment International, 79,42–50.  https://doi.org/10.1016/j.envint.2015.03.004.Google Scholar
  50. Prez, V. E., Martínez, L. C., Victoria, M., Giordano, M. O., Masachessi, G., Ré, V. E., et al. (2018). Tracking enteric viruses in green vegetables from central Argentina: Potential association with viral contamination of irrigation waters. Science of the Total Environment, 637–638,665–671.  https://doi.org/10.1016/j.scitotenv.2018.05.044.Google Scholar
  51. Samandoulgou, I., Fliss, I., &Jean, J. (2015). Zeta potential and aggregation of virus-like particle of human norovirus and feline calicivirus under different physicochemical conditions. Food and Environmental Virology, 7(3), 249–260.  https://doi.org/10.1007/s12560-015-9198-0.Google Scholar
  52. Sano, D., Ueki, Y., Watanabe, T., &Omura, T. (2006). Membrane separation of indigenous noroviruses from sewage sludge and treated wastewater. Water Science and Technology, 54(3), 77.  https://doi.org/10.2166/wst.2006.451.Google Scholar
  53. Seitz, S. R., Leon, J. S., Schwab, K. J., Lyon, G. M., Dowd, M., McDaniels, M., et al. (2011). Norovirus infectivity in humans and persistence in water. Applied and Environmental Microbiology, 77(19), 6884–6888.  https://doi.org/10.1128/aem.05806-11.Google Scholar
  54. Sokolova, E., Petterson, S. R., Dienus, O., Nyström, F., Lindgren, P.-E., &Pettersson, T. J. R. (2015). Microbial risk assessment of drinking water based on hydrodynamic modelling of pathogen concentrations in source water. Science of the Total Environment, 526,177–186.  https://doi.org/10.1016/j.scitotenv.2015.04.040.Google Scholar
  55. Tort, L. F. L., Victoria, M., Lizasoain, A., García, M., Berois, M., Cristina, J., et al. (2015). Detection of common, emerging and uncommon VP4, and VP7 human group A rotavirus genotypes from urban sewage samples in Uruguay. Food and Environmental Virology, 7(4), 342–353.  https://doi.org/10.1007/s12560-015-9213-5.Google Scholar
  56. Waldman, P., Meseguer, A., Lucas, F., Moulin, L., &Wurtzer, S. (2017). Interaction of human enteric viruses with microbial compounds: Implication for virus persistence and disinfection treatments. Environmental Science and Technology, 51(23), 13633–13640.  https://doi.org/10.1021/acs.est.7b03875.Google Scholar

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Authors and Affiliations

  1. 1.Department of Environmental HealthNational Institute of Public HealthWakoJapan
  2. 2.National Institute of Public HealthWakoJapan

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