Skip to main content
Log in

Comprehensive Study on Enteric Viruses and Indicators in Surface Water in Kyoto, Japan, During 2014–2015 Season

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

Abstract

Certain enteric viruses that are present in the water environment are potential risk factors of waterborne infections. To better understand the impact of viruses in water, both enteric viruses and their potential indicators should be comparatively investigated. In this study, occurrences of GI- and GII-noroviruses (NoVs), sapovirus (SaV), rotavirus (RoV), Aichi virus 1 (AiV-1), enterovirus (EV), and pepper mild mottle virus (PMMoV) were quantitatively determined in surface water samples in Japan. Additionally, the genotype distribution of GI- and GII-NoVs was determined using a next-generation amplicon sequencing. PMMoV was the most abundant virus regardless of season and location, indicating its usefulness as an indicator for the viral contamination of water. Other potential indicators, AiV and EV, were less abundant than GII-NoV. Viruses other than PMMoV showed seasonality, i.e., EV and other viruses (NoVs, SaV, RoV, and AiV-1) became prevalent during summer and winter, respectively. SaV showed a relatively high abundance at a location that was affected by untreated wastewater. Regarding NoV genotypes, GI.1, GI.2, GI.4, GI.5, GI.6, GII.3, GII.4, GII.6, and GII.17 were found from the surface water samples. GII.4 and GII.17 seemed to have contributed to the high abundance of GII-NoV in the samples. Interestingly, GII.17 strains became prevalent in the water samples before becoming prevalent among gastroenteritis patients in Japan. These findings provide further insights into the properties of viruses as contaminants in the water environment.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Asami, T., Katayama, H., Torrey, J. R., Visvanathan, C., & Furumai, H. (2016). Evaluation of virus removal efficiency of coagulation-sedimentation and rapid sand filtration processes in a drinking water treatment plant in Bangkok, Thailand. Water Research, 101, 84–94.

    Article  CAS  Google Scholar 

  • Aw, T. G., Gin, K. Y., Oon, E., Chen, L. L., Woo, E. X., C. H (2009). Prevalence and genotypes of human noroviruses in tropical urban surface waters and clinical samples in Singapore. Applied and Environmental Microbiology, 75(15), 4984–4992.

    Article  CAS  Google Scholar 

  • Aw, T. G., Howe, A., & Rose, J. B. (2014). Metagenomic approaches for direct and cell culture evaluation of the virological quality of wastewater. Journal of Virological Methods, 210, 15–21.

    Article  CAS  Google Scholar 

  • Betancourt, W. Q., Kitajima, M., Wing, A. D., Regnery, J., Drewes, J. E., Pepper, I. L., & Gerba, C. P. (2014). Assessment of virus removal by managed aquifer recharge at three full-scale operations. Journal of Environmental Science and Health. Part A, Toxic/hazardous Substances & Environmental Engineering, 49(14), 1685–1692.

    Article  CAS  Google Scholar 

  • Bibby, K., Viau, E., & Peccia, J. (2011). Viral metagenome analysis to guide human pathogen monitoring in environmental samples. Letters in Applied Microbiology, 52(4), 386–392.

    Article  CAS  Google Scholar 

  • Campos, C. J., & Lees, D. N. (2014). Environmental transmission of human noroviruses in shellfish waters. Applied and Environmental Microbiology, 80(12), 3552–3561.

    Article  Google Scholar 

  • Costán-Longares, A., Mocé-Llivina, L., Avellón, A., Jofre, J., & Lucena, F. (2008). Occurrence and distribution of culturable enteroviruses in wastewater and surface waters of north-eastern Spain. Journal of Applied Microbiology, 105(6), 1945–1955.

    Article  Google Scholar 

  • Cromeans, T., Park, G. W., Costantini, V., Lee, D., Wang, Q., Farkas, T., Lee, A., & Vinjé, J. (2014). Comprehensive comparison of cultivable norovirus surrogates in response to different inactivation and disinfection treatments. Applied and Environmental Microbiology, 80(18), 5743–5751.

    Article  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.

    Article  Google Scholar 

  • de Graaf, M., Villabruna, N., & Koopmans, M. P. (2017). Capturing norovirus transmission. Current Opinion in Virology, 22, 64–70.

    Article  Google Scholar 

  • Dingle, K. E., Lambden, P. R., Caul, E. O., & Clarke, I. N. (1995). Human enteric Caliciviridae: The complete genome sequence and expression of virus-like particles from a genetic group II small round structured virus. Journal of General Virology, 76(9), 2349–2355.

    Article  CAS  Google Scholar 

  • Dinu, S., Nagy, M., Negru, D. G., Popovici, E. D., Zota, L., & Oprișan, G. (2016). Molecular identification of emergent GII.P17-GII.17 norovirus genotype, Romania, 2015. Euro Surveillance, 21(7), 30141.

    Article  Google Scholar 

  • Gentry, J., Vinjé, J., Guadagnoli, D., & Lipp, E. K. (2009). Norovirus distribution within an estuarine environment. Applied and Environmental Microbiology, 75(17), 5474–5480.

    Article  CAS  Google Scholar 

  • Hamza, I. A., Jurzik, L., Uberla, K., & Wilhelm, M. (2011). Evaluation of pepper mild mottle virus, human picobirnavirus and Torque teno virus as indicators of fecal contamination in river water. Water Research, 45(3), 1358–1368.

    Article  CAS  Google Scholar 

  • Haramoto, E., Kitajima, M., Hata, A., Torrey, J. R., Masago, Y., Sano, D., & Katayama, H. (2018). A review on recent progress in the detection methods and prevalence of human enteric viruses in water. Water Research, 135, 168–186.

    Article  CAS  Google Scholar 

  • Haramoto, E., Kitajima, M., Kishida, N., Konno, Y., Katayama, H., Asami, M., & Akiba, M. (2013). Occurrence of pepper mild mottle virus in drinking water sources in Japan. Applied and Environmental Microbiology, 79(23), 7413–7418.

    Article  CAS  Google Scholar 

  • Hata, A., Hanamoto, S., Shirasaka, Y., Yamashita, N., & Tanaka, H. (2016). Quantitative distribution of infectious F-specific RNA phage genotypes in surface waters. Applied and Environmental Microbiology, 82(14), 4244–4252.

    Article  CAS  Google Scholar 

  • Hata, A., Katayama, H., Kitajima, M., Visvanathan, C., Nol, C., & Furumai, H. (2011). Validation of internal controls for extraction and amplification of nucleic acids from enteric viruses in water samples. Applied and Environmental Microbiology, 77(13), 4336–4343.

    Article  CAS  Google Scholar 

  • Hata, A., Katayama, H., Kojima, K., Sano, S., Kasuga, I., Kitajima, M., & Furumai, H. (2014). Effects of rainfall events on the occurrence and detection efficiency of viruses in river water impacted by combined sewer overflows. Science of the Total Environment, 468–469, 757–763.

    Article  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.

    Article  CAS  Google Scholar 

  • Hot, D., Legeay, O., Jacques, J., Gantzer, C., Caudrelier, Y., Guyard, K., Lange, M., & Andréoletti, L. (2003). Detection of somatic phages, infectious enteroviruses and enterovirus genomes as indicators of human enteric viral pollution in surface water. Water Research, 37(19), 4703–4710.

    Article  CAS  Google Scholar 

  • Jeong, A. Y., Jeong, H. S., Lee, J. S., Park, Y. C., Lee, S. H., Hwang, I. G., Kim, Y. J., Kim, Y. J., Jo, M. Y., Jung, S., Kim, K., & Cheon, D. S. (2013). Occurrence of norovirus infections in asymptomatic food handlers in South Korea. Journal of Clinical Microbiology, 51(2), 598–600.

    Article  Google Scholar 

  • Jiang, S. C., Chu, W., & He, J. W. (2007). Seasonal detection of human viruses and coliphage in Newport Bay, California. Applied and Environmental Microbiology, 73(20), 6468–6474.

    Article  CAS  Google Scholar 

  • Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., Takeda, N., & Katayama, K. (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.

    Article  CAS  Google Scholar 

  • Katayama, H., Haramoto, E., Oguma, K., Yamashita, H., Tajima, A., Nakajima, H., & Ohgaki, S. (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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Kazama, S., Masago, Y., Tohma, K., Souma, N., Imagawa, T., Suzuki, A., Liu, X., Saito, M., Oshitani, H., & Omura, T. (2016). Temporal dynamics of norovirus determined through monitoring of municipal wastewater by pyrosequencing and virological surveillance of gastroenteritis cases. Water Research, 92, 244–253.

    Article  CAS  Google Scholar 

  • Khamrin, P., Kumthip, K., Yodmeeklin, A., Supadej, K., Ukarapol, N., Thongprachum, A., Okitsu, S., Hayakawa, S., Ushijima, H., & Maneekarn, N. (2016). Molecular characterization of norovirus GII.17 detected in healthy adult, intussusception patient, and acute gastroenteritis children in Thailand. Infection, Genetics and Evolution, 44, 330–333.

    Article  CAS  Google Scholar 

  • Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16(2), 111–120.

    Article  CAS  Google Scholar 

  • Kitajima, M., & Gerba, C. P. (2015). Aichi virus 1: Environmental occurrence and behavior. Pathogens, 4(2), 256–268.

    Article  Google Scholar 

  • Kitajima, M., Hata, A., Yamashita, T., Haramoto, E., Minagawa, H., & Katayama, H. (2013). Development of a reverse transcription-quantitative PCR system for detection and genotyping of aichi viruses in clinical and environmental samples. Applied and Environmental Microbiology, 79(13), 3952–3958.

    Article  CAS  Google Scholar 

  • Kitajima, M., Iker, B. C., Pepper, I. L., & Gerba, C. P. (2014). Relative abundance and treatment reduction of viruses during wastewater treatment processes—Identification of potential viral indicators. Science of the Total Environment, 488–489, 290–296.

    Article  Google Scholar 

  • Kitajima, M., Oka, T., Haramoto, E., Takeda, N., Katayama, K., & Katayama, H. (2010). Seasonal distribution and genetic diversity of genogroups I, II, and IV noroviruses in the Tamagawa River, Japan. Environmental Science & Technology, 44(18), 7116–7122.

    Article  CAS  Google Scholar 

  • Kitajima, M., Tohya, Y., Matsubara, K., Haramoto, E., Utagawa, E., Katayama, H., & Ohgaki, S. (2008). Use of murine norovirus as a novel surrogate to evaluate resistance of human norovirus to free chlorine disinfection in drinking water supply system. Environmental Engineering Research, 45, 361–370 (in Japanese).

    Google Scholar 

  • Kojima, S., Kageyama, T., Fukushi, S., Hoshino, F. B., Shinohara, M., Uchida, K., Natori, K., Takeda, N., & Katayama, K. (2002). Genogroup-specific PCR primers for detection of Norwalk-like viruses. Journal of Virological Methods, 100(1–2), 107–114.

    Article  CAS  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 Environmental Microbiology, 73(13), 4152–4161.

    Article  Google Scholar 

  • LeBlanc, J. J., Pettipas, J., Gaston, D., Taylor, R., Hatchette, T. F., Booth, T. F., Mandes, R., McDermid, A., & Grudeski, E. (2016). Outbreak of norovirus GII.P17-GII.17 in the Canadian Province of Nova Scotia. Canadian Journal of Infectious Diseases and Medical Microbiology. https://doi.org/10.1155/2016/1280247.

    Article  PubMed  Google Scholar 

  • Lodder, W. J., & de Roda Husman, A. M. (2005). Presence of noroviruses and other enteric viruses in sewage and surface waters in The Netherlands. Applied and Environmental Microbiology, 71(3), 1453–1461.

    Article  CAS  Google Scholar 

  • Lu, J., Sun, L., Fang, L., Yang, F., Mo, Y., Lao, J., Zheng, H., Tan, X., Lin, H., Rutherford, S., Guo, L., Ke, C., & Hui, L. (2015). Gastroenteritis outbreaks caused by norovirus GII.17, Guangdong Province, China, 2014–2015. Emerging Infectious Diseases, 21(7), 1240–1242.

    Article  CAS  Google Scholar 

  • Matsushima, Y., Ishikawa, M., Shimizu, T., Komane, A., Kasuo, S., Shinohara, M., Nagasawa, K., Kimura, H., Ryo, A., Okabe, N., Haga, K., Doan, Y. H., Katayama, K., & Shimizu, H. (2015). Genetic analyses of GII.17 norovirus strains in diarrheal disease outbreaks from December 2014 to March 2015 in Japan reveal a novel polymerase sequence and amino acid substitutions in the capsid region. Euro Surveillance, 20(26), 21173.

    Article  Google Scholar 

  • Nakamura, T., Hamasaki, M., Yoshitomi, H., Ishibashi, T., Yoshiyama, C., Maeda, E., Sera, N., & Yoshida, H. (2015). Environmental surveillance of poliovirus in sewage water around the introduction period for inactivated polio vaccine in Japan. Applied and Environmental Microbiology, 81(5), 1859–1864.

    Article  Google Scholar 

  • Ogorzaly, L., Walczak, C., Galloux, M., Etienne, S., Gassilloud, B., & Cauchie, H. M. (2015). Human Adenovirus diversity in water samples using a next-generation amplicon sequencing approach. Food and Environmental Virology, 7(2), 112–121.

    Article  CAS  Google Scholar 

  • Oka, T., Katayama, K., Hansman, G. S., Kageyama, T., Ogawa, S., Wu, F. T., White, P. A., & Takeda, N. (2006). Detection of human sapovirus by real-time reverse transcription-polymerase chain reaction. Journal of Medical Virology, 78(10), 1347–1353.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Pu, J., Kazama, S., Miura, T., Azraini, N. D., Konta, Y., Ito, H., Ueki, Y., Cahyaningrum, E. E., Omura, T., & Watanabe, T. (2016). Pyrosequencing analysis of norovirus genogroup II distribution in sewage and oysters: First detection of GII.17 Kawasaki 2014 in oysters. Food and Environmental Virology, 8(4), 310–312.

    Article  CAS  Google Scholar 

  • Rosario, K., Nilsson, C., Lim, Y. W., Ruan, Y., & Breitbart, M. (2009). Metagenomic analysis of viruses in reclaimed water. Environmental Microbiology, 11(11), 2806–2820.

    Article  CAS  Google Scholar 

  • Rosario, K., Symonds, E. M., Sinigalliano, C., Stewart, J., & Breitbart, M. (2009). Pepper mild mottle virus as an indicator of fecal pollution. Applied and Environmental Microbiology, 75(22), 7261–7267.

    Article  CAS  Google Scholar 

  • Sano, D., Amarasiri, M., Hata, A., Watanabe, T., & Katayama, H. (2016). Risk management of viral infectious diseases in wastewater reclamation and reuse: Review. Environment International, 91, 220–229.

    Article  CAS  Google Scholar 

  • Schvoerer, E., Ventura, M., Dubos, O., Cazaux, G., Serceau, R., Gournier, N., Dubois, V., Caminade, P., Fleury, H. J., & Lafon, M. E. (2001). Qualitative and quantitative molecular detection of enteroviruses in water from bathing areas and from a sewage treatment plant. Research in Microbiology, 152(2), 179–186.

    Article  CAS  Google Scholar 

  • Sedmak, G., Bina, D., & MacDonald, J. (2003). Assessment of an enterovirus sewage surveillance system by comparison of clinical isolates with sewage isolates from milwaukee, wisconsin, collected august 1994 to december 2002. Applied and Environmental Microbiology, 69(12), 7181–7187.

    Article  CAS  Google Scholar 

  • Sidoti, F., Rittà, M., Costa, C., & Cavallo, R. (2015). Diagnosis of viral gastroenteritis: Limits and potential of currently available procedures. The Journal of Infection in Developing Countries, 9(6), 551–561.

    Article  CAS  Google Scholar 

  • Thongprachum, A., Chan-it, W., Khamrin, P., Saparpakorn, P., Okitsu, S., Takanashi, S., Mizuguchi, M., Hayakawa, S., Maneekarn, N., & Ushijima, H. (2014). Molecular epidemiology of norovirus associated with gastroenteritis and emergence of norovirus GII.4 variant 2012 in Japanese pediatric patients. Infection, Genetics and Evolution, 23, 65–73.

    Article  CAS  Google Scholar 

  • Vainio, K., & Myrmel, M. (2006). Molecular epidemiology of norovirus outbreaks in Norway during 2000 to 2005 and comparison of four norovirus real-time reverse transcriptase PCR assays. Journal of Clinical Microbiology, 44(10), 3695–3702.

    Article  CAS  Google Scholar 

  • Vesikari, T. (2012). Rotavirus vaccination: A concise review. Clinical Microbiology and Infection, 5, 57–63.

    Article  Google Scholar 

  • Vinjé, J. (2015). Advances in laboratory methods for detection and typing of norovirus. Journal of Clinical Microbiology, 53(2), 373–381.

    Article  Google Scholar 

  • Wong, K., Fong, T. T., Bibby, K., & Molina, M. (2012). Application of enteric viruses for fecal pollution source tracking in environmental waters. Environment International, 45, 151–164.

    Article  CAS  Google Scholar 

  • Yamashita, T., Sugiyama, M., Tsuzuki, H., Sakae, K., Suzuki, Y., & Miyazaki, Y. (2000). Application of a reverse transcription-PCR for identification and differentiation of Aichi virus, a new member of the Picornavirus family associated with gastroenteritis in humans. Journal of Clinical Microbiology, 38(8), 2955–2961.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, N., Lin, X., Wang, S., Tao, Z., Xiong, P., Wang, H., Liu, Y., Song, Y., & Xu, A. (2016). Molecular epidemiology of GI and GII noroviruses in sewage: 1-year surveillance in eastern China. Journal of Applied Microbiology, 121(4), 1172–1179.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grant-in-aid for JSPS Fellows (Grant Number: 14J03643) and JSPS KAKENHI (Grant Numbers: JP 26820222 and JP 26289182) from the Japan Society for the Promotion of Science.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akihiko Hata.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hata, A., Hanamoto, S., Ihara, M. et al. Comprehensive Study on Enteric Viruses and Indicators in Surface Water in Kyoto, Japan, During 2014–2015 Season. Food Environ Virol 10, 353–364 (2018). https://doi.org/10.1007/s12560-018-9355-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12560-018-9355-3

Keywords

Navigation