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Genetically distinct genogroup IV norovirus strains identified in wastewater

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We investigated the prevalence and genetic diversity of genogroup IV norovirus (GIV NoV) strains in wastewater in Arizona, United States, over a 13-month period. Among 50 wastewater samples tested, GIV NoVs were identified in 13 (26 %) of the samples. A total of 47 different GIV NoV strains were identified, which were classified into two genetically distinct clusters: the GIV.1 human cluster and a unique genetic cluster closely related to strains previously identified in Japanese wastewater. The results provide additional evidence of the considerable genetic diversity among GIV NoV strains through the analysis of wastewater containing virus strains shed from all populations.

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  1. Green KY (2007) Caliciviridae: the noroviruses. In: Knipe D, Howley P (eds) Fields Virol, 5th edn. Lippincott Williams and Wilkins, Philadelphia, p 949–979

  2. Kroneman A, Vega E, Vennema H et al (2013) Proposal for a unified norovirus nomenclature and genotyping. Arch Virol 158:2059–2068. doi:10.1007/s00705-013-1708-5

    Article  CAS  PubMed  Google Scholar 

  3. Siebenga JJ, Duizer E, Koopmans MPG (2010) Norovirus epidemiology. In: Hansman GS, Jiang X, Green KY (eds) Caliciviruses. Mol Cell Virol. Caister Academic Press, Norfolk, UK, p 1–24

  4. Vinje J, Koopmans MPG (2000) Simultaneous detection and genotyping of “Norwalk-like viruses” by oligonucleotide array in a reverse line blot hybridization format. J Clin Microbiol 38:2595–2601

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Fankhauser RL, Monroe SS, Noel JS et al (2000) Epidemiologic and molecular trends of “Norwalk-like viruses” associated with outbreaks of gastroenteritis in the United States. J Infect Dis 186:1–7

    Article  Google Scholar 

  6. Iritani N, Seto Y, Kubo H et al (2002) Prevalence of “Norwalk-like virus” infections in outbreaks of acute nonbacterial gastroenteritis observed during the 1999-2000 season in Osaka city, Japan. J Med Virol 138:131–138. doi:10.1002/jmv.2121

    Article  Google Scholar 

  7. Lindell AT, Grillner L, Svensson L, Wirgart BZ (2005) Molecular epidemiology of norovirus infections in Stockholm, Sweden, during the years 2000 to 2003: association of the GGIIb genetic cluster with infection in children. J Clin Microbiol 43:1086–1092. doi:10.1128/JCM.43.3.1086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Eden J-S, Lim KL, White PA (2012) Complete genome of the human norovirus GIV.1 strain Lake Macquarie virus. J Virol 86:10251–10252. doi:10.1128/JVI.01604-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ao Y-Y, Yu J-M, Li L-L et al (2014) Detection of human norovirus GIV.1 in China: a case report. J Clin Virol 61:8–11. doi:10.1016/j.jcv.2014.08.002

    Article  Google Scholar 

  10. Muscillo M, Fratini M, Graffeo R et al (2013) GIV noroviruses in wastewaters and in stool specimens from hospitalized patients. Food Environ Virol 5:194–202. doi:10.1007/s12560-013-9121-5

    Article  Google Scholar 

  11. Martella V, Campolo M, Lorusso E et al (2007) Norovirus in captive lion cub (Panthera leo). Emerg Infect Dis 13:1071–1073

    Article  PubMed  PubMed Central  Google Scholar 

  12. Martella V, Lorusso E, Decaro N et al (2008) Detection and molecular characterization of a canine norovirus. Emerg Infect Dis 14:1306–1308. doi:10.3201/eid1408.080062

    Article  PubMed  PubMed Central  Google Scholar 

  13. Ntafis V, Xylouri E, Radogna A et al (2010) Outbreak of canine norovirus infection in young dogs. J Clin Microbiol 48:2605–2608. doi:10.1128/JCM.02528-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Pinto P, Wang Q, Chen N et al (2012) Discovery and genomic characterization of noroviruses from a gastroenteritis outbreak in domestic cats in the US. PLoS One 7:e32739. doi:10.1371/journal.pone.0032739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. van den Berg H, Lodder W, van der Poel W et al (2005) Genetic diversity of noroviruses in raw and treated sewage water. Res Microbiol 156:532–540. doi:10.1016/j.resmic.2005.01.008

    Article  PubMed  Google Scholar 

  16. La Rosa G, Pourshaban M, Iaconelli M, Muscillo M (2008) Detection of genogroup IV noroviruses in environmental and clinical samples and partial sequencing through rapid amplification of cDNA ends. Arch Virol 153:2077–2083. doi:10.1007/s00705-008-0241-4

    Article  PubMed  Google Scholar 

  17. Kitajima M, Haramoto E, Phanuwan C et al (2009) Detection of genogroup IV norovirus in wastewater and river water in Japan. Lett Appl Microbiol 49:655–658. doi:10.1111/j.1472-765X.2009.02718.x

    Article  CAS  PubMed  Google Scholar 

  18. La Rosa G, Iaconelli M, Pourshaban M et al (2010) Molecular detection and genetic diversity of norovirus genogroup IV: a yearlong monitoring of sewage throughout Italy. Arch Virol 155:589–593. doi:10.1007/s00705-010-0619-y

    Article  CAS  PubMed  Google Scholar 

  19. Kitajima M, Oka T, Haramoto E et al (2010) Seasonal distribution and genetic diversity of genogroups I, II, and IV noroviruses in the Tamagawa River, Japan. Environ Sci Technol 44:7116–7122. doi:10.1021/es100346a

    Article  CAS  PubMed  Google Scholar 

  20. Kitajima M, Oka T, Haramoto E et al (2011) Genetic diversity of genogroup IV noroviruses in wastewater in Japan. Lett Appl Microbiol 52:181–184. doi:10.1111/j.1472-765X.2010.02980.x

    Article  CAS  PubMed  Google Scholar 

  21. Han T-H, Kim S-C, Kim S-T et al (2014) Detection of norovirus genogroup IV, klassevirus, and pepper mild mottle virus in sewage samples in South Korea. Arch Virol 159:457–463. doi:10.1007/s00705-013-1848-7

    Article  CAS  PubMed  Google Scholar 

  22. Teixeira DM, Hernandez JM, Silva LD et al (2015) Occurrence of norovirus GIV in environmental water samples from Belém city, Amazon Region, Brazil. Food Environ Virol. doi:10.1007/s12560-015-9220-6

    PubMed  Google Scholar 

  23. Kitajima M, Iker BC, Pepper IL, Gerba CP (2014) Relative abundance and treatment reduction of viruses during wastewater treatment processes—identification of potential viral indicators. Sci Total Environ 488–489:290–296. doi:10.1016/j.scitotenv.2014.04.087

    Article  PubMed  Google Scholar 

  24. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  25. Kitajima M, Oka T, Takagi H et al (2010) Development and application of a broadly reactive real-time reverse transcription-PCR assay for detection of murine noroviruses. J Virol Methods 169:269–273. doi:10.1016/j.jviromet.2010.07.018

    Article  CAS  PubMed  Google Scholar 

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The authors would like to thank Kelly Reynolds at the University of Arizona Mel and Enid Zuckerman College of Public Health for her laboratory contributions, and two anonymous wastewater treatment plants in southern Arizona for providing wastewater samples. This study was partly supported by National Science Foundation (NSF) Water and Environmental Technology (WET) Center and Water Resources Research Center (WRRC), the University of Arizona. We also wish to acknowledge the support of the Japan Society for the Promotion of Science (JSPS) to Masaaki Kitajima, under JSPS Postdoctoral Fellowships for Research Abroad. Andri T. Rachmadi was a recipient of a 2012 Fulbright Master of Science and Technology Scholarship.

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Correspondence to Masaaki Kitajima.

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Kitajima, M., Rachmadi, A.T., Iker, B.C. et al. Genetically distinct genogroup IV norovirus strains identified in wastewater. Arch Virol 161, 3521–3525 (2016).

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