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Genetic Diversity Among Genogroup II Noroviruses and Progressive Emergence of GII.17 in Wastewaters in Italy (2011–2016) Revealed by Next-Generation and Sanger Sequencing

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A Publisher Correction to this article was published on 04 May 2018

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Abstract

Noroviruses (NoV) are a major cause of gastroenteritis worldwide. Recently, a novel variant of NoV GII.17 (GII.P17_GII.17 NoV), termed Kawasaki 2014, has been increasingly reported in NoV outbreaks in Asia, and has also been described in Europe and North America. In this study, sewage samples were investigated to study the occurrence and genetic diversity of NoV genogroup II (GII) along a 6-year period. Moreover, the spread of GII.17 strains (first appearance and occurrence along time) was specifically assessed. A total of 122 sewage samples collected from 2011 to 2016 from four wastewater treatment plants in Rome (Italy) were initially tested using real-time RT-(q)PCR for GII NoV. Positive samples were subsequently subjected to genotypic characterization by RT-nested PCRs using broad-range primes targeting the region C of the capsid gene of GII NoV, and specific primers targeting the same region of GII.17 NoV. In total, eight different genotypes were detected with the broad-range assay: GII.1 (n = 6), GII.2 (n = 8), GII.3 (n = 3), GII.4 (n = 13), GII.6 (n = 3), GII.7 (n = 2), GII.13 (n = 2), and GII.17 (n = 3), with the latter two genotypes detected only in 2016. Specific amplification of GII.17 NoV was successful in 14 out of 110 positive samples, spanned over the years 2013–2016. The amplicons of the broad-range PCR, pooled per year, were further analyzed by next-generation sequencing (NGS) for a deeper analysis of the genotypes circulating in the study period. NGS confirmed the circulation of GII.17 NoV since 2013 and detected, beyond the eight genotypes identified by Sanger sequencing, three additional genotypes regarded as globally uncommon: GII.5, GII.16, and GII.21. This study provides evidence that GII.17 NoV Kawasaki has been circulating in the Italian population before its appearance and identification in clinical cases, and has become a major genotype in 2016. Our results confirm the usefulness of wastewater surveillance coupled with NGS to study the molecular epidemiology of NoV and to monitor the emergence of NoV strains.

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Change history

  • 04 May 2018

    The original version of this article unfortunately contained a mistake. The presentation of Table 1 was incorrect. The corrected table is given below. The original article has been corrected.

References

  • Alam, A., Qureshi, S. A., Vinje, J., & Zaidi, A. (2016). Genetic characterization of norovirus strains in hospitalized children from Pakistan. Journal of Medical Virology, 88, 216–223.

    Article  PubMed  CAS  Google Scholar 

  • Bartnicki, E., Cunha, J. B., Kolawole, A. O., & Wobus, C. E. (2017). Recent advances in understanding noroviruses. F1000Res, 6, 79.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, 98–104.

    Article  PubMed  CAS  Google Scholar 

  • Brown, J. R., Roy, S., Ruis, C., Yara, R. E., Shah, D., Williams, R., et al. (2016). Norovirus whole-genome sequencing by SureSelect target enrichment: A robust and sensitive method. Journal of Clinical Microbiology, 54, 2530–2537.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cannon, J. L., Barclay, L., Collins, N. R., Wikswo, M. E., Castro, C. J., Magaña, L. C., et al. (2017). Genetic and epidemiologic trends of norovirus outbreaks in the United States from 2013 to 2016 demonstrated emergence of novel GII.4 recombinant viruses. Journal of Clinical Microbiology, 55(7), 2208–2221.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chan, M. C. W., Hu, Y., Chen, H., Podkolzin, A. T., Zaytseva, E. V., Komano, J., et al. (2017). Global Spread of Norovirus GII.17 Kawasaki 308, 2014–2016. Emerging Infectious Diseases, 23, 1354–1359.

    Article  Google Scholar 

  • Chan, M. C., Lee, N., Hung, T. N., Kwok, K., Cheung, K., Tin, E. K., et al. (2015). Rapid emergence and predominance of a broadly recognizing and fast-evolving norovirus GII.17 variant in late 2014. Nature Communications, 6, 10061.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen, H., Qian, F., Xu, J., Chan, M., Shen, Z., Zai, S., et al. (2015). A novel norovirus GII.17 lineage contributed to adult gastroenteritis in Shanghai, China, during the winter of 2014-2015. Emerging Microbes & Infections, 4, e67.

    Article  Google Scholar 

  • Choi, Y. S., Koo, E. S., Kim, M. S., Choi, J. D., Shin, Y., & Jeong, Y. S. (2017). Re-emergence of a GII.4 norovirus Sydney 2012 variant equipped with GII.P16 RdRp and its predominance over novel variants of GII.17 in South Korea in 2016. Food and Environmental Virology, 9, 168–178.

    Article  PubMed  CAS  Google Scholar 

  • Cowger, T. L., Burns, C. C., Sharif, S., Gary, H. E., Jr., Iber, J., Henderson, E., et al. (2017). The role of supplementary environmental surveillance to complement acute flaccid paralysis surveillance for wild poliovirus in Pakistan: 2011–2013. PLoS ONE, 12, e0180608.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • da Silva, L. D., da Silva, B. R., Junior, E. C., de Lima, I. C., da Penha Junior, E. T., Teixeira, D. M., et al. (2017). Detection and genetic characterization of the emergent GII.17_2014norovirus genotype among children with gastroenteritis from Northern Brazil. Infection, Genetics and Evolution, 48, 1–3.

    Article  PubMed  CAS  Google Scholar 

  • Degiuseppe, J. I., Gomes, K. A., Hadad, M. F., Parra, G. I., & Stupka, J. A. (2016). Detection of novel GII.17 norovirus in Argentina, 2015. Infection, Genetics and Evolution, 47, 121–124.

    Article  PubMed  CAS  Google Scholar 

  • Dinu, S., Nagy, M., Negru, D. G., Popovici, E. D., Zota, L., & Oprisan, G. (2016). Molecular identification of emergent GII.P17-GII.17 norovirus genotype Romania. EuroSurveillance. https://doi.org/10.2807/1560-7917.ES.2016.21.7.30141.

    Article  PubMed  Google Scholar 

  • Eden, J. S., Tanaka, M. M., Boni, M. F., Rawlinson, W. D., & White, P. A. (2013). Recombination within the pandemic norovirus GII.4 lineage. Journal of Virology, 87, 6270–6282.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • El Qazoui, M., Oumzil, H., Baassi, L., El Omari, N., Sadki, K., Amzazi, S., et al. (2014). Rotavirus and norovirus infections among acute gastroenteritis children in Morocco. BMC Infectious Diseases, 3(14), 300.

    Article  Google Scholar 

  • Fukuda, S., Takao, S., Shigemoto, N., Tanizawa, Y., & Seno, M. (2010). Transition of genotypes associated with norovirus gastroenteritis outbreaks in a limited area of Japan, Hiroshima Prefecture, during eight epidemic seasons. Archives of Virology, 155, 111–115.

    Article  PubMed  CAS  Google Scholar 

  • Giammanco, G. M., De Grazia, S., Bonura, F., Cappa, V., Muli, S. L., Pepe, A., et al. (2017). Norovirus GII.17 as major epidemic strain in Italy, winter 2015-16. Emerging Infectious Diseases, 23, 1206–1208.

    Article  PubMed  PubMed Central  Google Scholar 

  • Graaf, M., Vennema, H., Podkolzin, A. T., Hewitt, J., Bucardo, F., Templeton, K., et al. (2015). Emergence of a novel GII.17 norovirus—End of the GII.4 era? EuroSurveillance, 20, 1–8.

    Article  Google Scholar 

  • Green, K. Y. (2013). Caliciviridae: the noroviruses. In Fields Virology (Ed.), Knipe DMHPM (pp. 949–979). Philadelpia: Wolters Kluwer Health/Lippincott Williams and Wilkins.

    Google Scholar 

  • Hellmer, M., Paxeus, N., Magnius, L., Enache, L., Arnholm, B., Johansson, A., et al. (2014). Detection of pathogenic viruses in sewage provided early warnings of hepatitis A virus and norovirus outbreaks. Applied and Environment Microbiology, 80, 6771–6781.

    Article  CAS  Google Scholar 

  • Hoa Tran, T. N., Trainor, E., Nakagomi, T., Cunliffe, N. A., & Nakagomi, O. (2013). Molecular epidemiology of noroviruses associated with acute sporadic gastroenteritis in children: Global distribution of genogroups, genotypes and GII.4 variants. Journal of Clinical Virology, 56, 185–193.

    Article  PubMed  CAS  Google Scholar 

  • Hoa-Tran, T. N., Nakagomi, T., Sano, D., Sherchand, J., Pandey, B. D., Cunliffe, N. A., et al. (2015). Molecular epidemiology of noroviruses detected in Nepalese children with acute diarrhea between 2005 and 2011: Increase and predominance of minor genotype GII.13. Infection, Genetics and Evolution, 30, 27–36.

    Article  PubMed  Google Scholar 

  • Iaconelli, M., Divizia, M., Della, Libera S., Di Bonito, P., & La Rosa, G. (2016). Frequent detection and genetic diversity of human bocavirus in urban sewage samples. Food and Environmental Virology, 8, 289–295.

    Article  PubMed  CAS  Google Scholar 

  • Iaconelli, M., Valdazo-Gonzalez, B., Equestre, M., Ciccaglione, A. R., Marcantonio, C., Della, Libera S., et al. (2017). Molecular characterization of human adenoviruses in urban wastewaters using next generation and Sanger sequencing. Water Research, 121, 240–247.

    Article  PubMed  CAS  Google Scholar 

  • Imamura, S., Haruna, M., Goshima, T., Kanezashi, H., Okada, T., & Akimoto, K. (2016). Application of next-generation sequencing to investigation of norovirus diversity in shellfish collected from two coastal sites in Japan from 2013 to 2014. Japanese Journal of Veterinary Research, 64, 113–122.

    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, 1548–1557.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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, 83, e03406-16.

    Article  PubMed  PubMed Central  Google Scholar 

  • Khamrin, P., Kumthip, K., Supadej, K., Thongprachum, A., Okitsu, S., Hayakawa, S., et al. (2017). Noroviruses and sapoviruses associated with acute gastroenteritis in pediatric patients in Thailand: Increased detection of recombinant norovirus GII.P16/GII.13 strains. Archives of Virology, 162(11), 3371–3380.

    Article  PubMed  CAS  Google Scholar 

  • Kim, M. S., Koo, E. S., Choi, Y. S., Kim, J. Y., Yoo, C. H., Yoon, H. J., et al. (2016). Distribution of human norovirus in the coastal waters of South Korea. PLoS ONE, 11, e0163800.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kitajima, M., Iker, B. C., Magill-Collins, A., Gaither, M., Stoehr, J. D., & Gerba, C. P. (2017). Genetic analysis of norovirus strains that caused gastroenteritis outbreaks among river rafters in the Grand Canyon, Arizona. Food and Environmental Virology, 9, 238–240.

    Article  PubMed  Google Scholar 

  • Kiulia, N. M., Mans, J., Mwenda, J. M., & Taylor, M. B. (2014). Norovirus GII.17 predominates in selected surface water sources in Kenya. Food and Environmental Virology, 6(4), 221–231.

    Article  PubMed  CAS  Google Scholar 

  • 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, 107–114.

    Article  PubMed  CAS  Google Scholar 

  • Kokkinos, P. A., Ziros, P. G., Mpalasopoulou, A., Galanis, A., & Vantarakis, A. (2011). Molecular detection of multiple viral targets in untreated urban sewage from Greece. Virol. J., 8(195), 195.

    Article  PubMed  PubMed Central  Google Scholar 

  • Koo, E. S., Kim, M. S., Choi, Y. S., Park, K. S., & Jeong, Y. S. (2017). Occurrence of novel GII.17 and GII.21 norovirus variants in the coastal environment of South Korea in 2015. PLoS One, 12, 237.

    Google Scholar 

  • Kroneman, A., Vega, E., Vennema, H., Vinje, J., White, P. A., Hansman, G., et al. (2013). Proposal for a unified norovirus nomenclature and genotyping. Archives of Virology, 158, 2059–2068.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kroneman, A., Vennema, H., Deforche, K., Avoort, H., Penaranda, S., Oberste, M. S., et al. (2011). An automated genotyping tool for enteroviruses and noroviruses. Journal of Clinical Virology, 51, 121–125.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, S., Nei, M., Dudley, J., & Tamura, K. (2008). MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics, 9, 299–306.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumthip, K., Khamrin, P., Saikruang, W., Supadej, K., Ushijima, H., & Maneekarn, N. (2017). Comparative evaluation of norovirus infection in children with acute gastroenteritis by rapid immunochromatographic test, RT-PCR and real-time RT-PCR. Journal of Tropical Pediatrics. https://doi.org/10.1093/tropej/fmx014.

    Article  PubMed  Google Scholar 

  • La Bella, G., Martella, V., Basanisi, M. G., Nobili, G., Terio, V., & La Salandra, G. (2017). Food-borne viruses in shellfish: Investigation on Norovirus and HAV presence in Apulia (SE Italy). Food and Environmental Virology, 9, 179–186.

    Article  PubMed  CAS  Google Scholar 

  • La Rosa, G., Della Libera, S., Iaconelli, M., Proroga, Y. T., De, M. D., Martella, V., et al. (2017). Detection of Norovirus GII.17 Kawasaki 2014 in shellfish, marine water and underwater sewage discharges in Italy. Food and Environmental Virology. https://doi.org/10.1007/s12560-017-9290-8.

    Article  PubMed  Google Scholar 

  • La Rosa, G., Libera, S. D., Iaconelli, M., Ciccaglione, A. R., Bruni, R., Taffon, S., et al. (2014). Surveillance of hepatitis A virus in urban sewages and comparison with cases notified in the course of an outbreak, Italy 2013. BMC Infectious Diseases, 14, 419.

    Article  PubMed  PubMed Central  Google Scholar 

  • LeBlanc, J. J., Pettipas, J., Gaston, D., Taylor, R., Hatchette, T. F., Booth, T. F., et al. (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  PubMed Central  Google Scholar 

  • Lee, C. C., Feng, Y., Chen, S. Y., Tsai, C. N., Lai, M. W., & Chiu, C. H. (2015). Emerging norovirus GII.17 in Taiwan. Clinical Infectious Diseases, 61, 1762–1764.

    PubMed  Google Scholar 

  • Lu, J., Sun, L., Fang, L., Yang, F., Mo, Y., Lao, J., et al. (2015). Gastroenteritis outbreaks caused by norovirus GII.17, Guangdong Province, China, 2014–2015. Emerging Infectious Diseases, 21, 1240–1242.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mabasa, V. V., Meno, K. D., Taylor, M. B., & Mans, J. (2017). Environmental surveillance for noroviruses in selected South African wastewaters 2015–2016: Emergence of the novel GII.17. Food and Environmental Virology. https://doi.org/10.1007/s12560-017-9316-2.

    Article  PubMed  Google Scholar 

  • Maletskaya, O. V., Tibilov, A. G., Prislegina, D. A., Gazieva, G. K., Otaraeva, N. I., Volynkina, A. S., et al. (2016). Epidemiologic features ofnorovirus infection outbreak in the Republic of North Ossetia-Alania. Zhurnal Mikrobiologii, Epidemiologii, I Immunobiologii, 2, 69–74.

    Google Scholar 

  • Mans, J., Murray, T. Y., Nadan, S., Netshikweta, R., Page, N. A., & Taylor, M. B. (2016). Norovirus diversity in children with gastroenteritis in South Africa from 2009 to 2013: GII.4 variants and recombinant strains predominate. Epidemiology and Infection, 144, 907–916.

    Article  PubMed  CAS  Google Scholar 

  • Matsushima, Y., Ishikawa, M., Shimizu, T., Komane, A., Kasuo, S., Shinohara, M., et al. (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. EuroSurveillance, 20(26), 21173.

    Article  PubMed  Google Scholar 

  • Medici, M. C., Tummolo, F., Calderaro, A., Chironna, M., Giammanco, G. M., De Grazia, S., et al. (2015). Identification of the novel Kawasaki 2014 GII.17 human norovirus strain in Italy, 2015. EuroSurveillance, 20, 30010.

    Article  PubMed  Google Scholar 

  • Medici, M. C., Tummolo, F., Martella, V., Chezzi, C., Arcangeletti, M. C., De Conto, F., et al. (2014a). Epidemiological and molecular features of norovirus infections in Italian children affected with acute gastroenteritis. Epidemiology and Infection, 142, 2326–2335.

    Article  PubMed  CAS  Google Scholar 

  • Medici, M. C., Tummolo, F., Martella, V., Giammanco, G. M., De Grazia, S., Arcangeletti, M. C., et al. (2014b). Novel recombinant GII.P16_GII.13 and GII.P16_GII.3 norovirus strains in Italy. Virus Research, 188, 142–145.

    Article  PubMed  CAS  Google Scholar 

  • Myrmel, M., Lange, H., & Rimstad, E. (2015). 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 and Environmental Virology, 7(3), 213–223.

    Article  PubMed  CAS  Google Scholar 

  • Nakjarung, K., Bodhidatta, L., Neesanant, P., Lertsethtakarn, P., Sethabutr, O., Vansith, K., et al. (2016). Molecular epidemiology and genetic diversity of norovirus in young children in Phnom Penh, Cambodia. Journal of Tropical Medicine, 2016, 2707121.

    Article  PubMed  PubMed Central  Google Scholar 

  • Parra, G. I., & Green, K. Y. (2015). Genome of emerging norovirus GII.17, United States, 2014. Emerging Infectious Diseases, 21, 1477–1479.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Patel, M. M., Widdowson, M. A., Glass, R. I., Akazawa, K., Vinje, J., & Parashar, U. D. (2008). Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerging Infectious Diseases, 14, 1224–1231.

    Article  PubMed  PubMed Central  Google Scholar 

  • Portal, T. M., Siqueira, J. A., Costa, L. C., Lima, I. C., Lucena, M. S., Bandeira Rda, S., et al. (2016). Caliciviruses in hospitalized children, São Luís, Maranhão, 1997–1999: Detection of norovirus GII.12. Braz. Journal of Microbiolgy, 47(3), 724–730.

    Google Scholar 

  • Prevost, B., Lucas, F. S., Ambert-Balay, K., Pothier, P., Moulin, L., & Wurtzer, S. (2015). Deciphering the diversities of astroviruses and noroviruses in wastewater treatment plant effluents by a high-throughput sequencing method. Applied and Environment Microbiology, 81, 7215–7222.

    Article  CAS  Google Scholar 

  • Pringle, K., Lopman, B., Vega, E., Vinje, J., Parashar, U. D., & Hall, A. J. (2015). Noroviruses: Epidemiology, immunity and prospects for prevention. Future Microbiology, 10, 53–67.

    Article  PubMed  CAS  Google Scholar 

  • Pu, J., Kazama, S., Miura, T., Azraini, N. D., Konta, Y., Ito, H., et al. (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  PubMed  CAS  Google Scholar 

  • Qin, M., Dong, X. G., Jing, Y. Y., Wei, X. X., Wang, Z. E., Feng, H. R., et al. (2016). A waterborne gastroenteritis outbreak caused by norovirus GII.17 in a hotel, Hebei, China. Food and Environmental Virology, 8(3), 180–186.

    Article  PubMed  Google Scholar 

  • Rackoff, L. A., Bok, K., Green, K. Y., & Kapikian, A. Z. (2013). Epidemiology and evolution of rotaviruses and noroviruses from an archival WHO Global Study in Children (1976–1979) with implications for vaccine design. PLoS ONE, 8, e59394.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rahman, M., Rahman, R., Nahar, S., Hossain, S., Ahmed, S., Golam Faruque, A. S., et al. (2016). Norovirus diarrhea in Bangladesh, 2010–2014: Prevalence, clinical features, and genotypes. Journal of Medical Virology, 88, 1742–1750.

    Article  PubMed  CAS  Google Scholar 

  • Rajko-Nenow, P., Waters, A., Keaveney, S., Flannery, J., Tuite, G., Coughlan, S., et al. (2013). Norovirus genotypes present in oysters and in effluent from a wastewater treatment plant during the seasonal peak of infections in Ireland in 2010. Applied and Environment Microbiology, 79, 2578–2587.

    Article  CAS  Google Scholar 

  • Rupprom, K., Chavalitshewinkoon-Petmitr, P., Diraphat, P., & Kittigul, L. (2017). Evaluation of real-time RT-PCR assays for detection and quantification of norovirus genogroups I and II. Virologica Sinica, 32, 139–146.

    Article  PubMed  CAS  Google Scholar 

  • Supadej, K., Khamrin, P., Kumthip, K., Kochjan, P., Yodmeeklin, A., Ushijima, H., et al. (2017). Wide variety of recombinant strains of norovirus GII in pediatric patients hospitalized with acute gastroenteritis in Thailand during 2005 to 2015. Infection, Genetics and Evolution, 52, 44–51.

    Article  PubMed  Google Scholar 

  • Timurkan, M. O., Aydin, H., & Aktas, O. (2017). Frequency and molecular characterization of human norovirus in Erzurum, Turkey. Turkish Journal of Medical Scinces, 47, 960–966.

    Article  Google Scholar 

  • Valentini, D., Ianiro, G., Di Bartolo, I., Di Camillo, C., Boccuzzi, E., Vittucci, A. C., et al. (2017). Hospital-acquired rotavirus and norovirus acute gastroenteritis in a pediatric unit, in 2014–2015. Journal of Medical Virology, 89(10), 1768–1774.

    Article  PubMed  CAS  Google Scholar 

  • Vega, E., Barclay, L., Gregoricus, N., Shirley, S. H., Lee, D., & Vinje, J. (2014). Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013. Journal of Clinical Microbiology, 52, 147–155.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Victoria, M., Tort, L. F., Lizasoain, A., Garcia, M., Castells, M., Berois, M., et al. (2016). Norovirus molecular detection in Uruguayan sewage samples reveals a high genetic diversity and GII.4 variant replacement along time. Journal of Applied Microbiology, 120, 1427–1435.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Woods, J. W., Calci, K. R., Marchant-Tambone, J. G., & Burkhardt, W., III. (2016). Detection and molecular characterization of norovirus from oysters implicated in outbreaks in the US. Food Microbiology, 59, 76–84.

    Article  PubMed  Google Scholar 

  • Yoon, J. S., Lee, S. G., Hong, S. K., Lee, S. A., Jheong, W. H., Oh, S. S., et al. (2008). Molecular epidemiology of norovirus infections in children with acute gastroenteritis in South Korea in November 2005 through November 2006. Journal of Clinical Microbiology, 46, 1474–1477.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhirakovskaia, E. V., Tikunov, A. Y., Bodnev, S. A., Klemesheva, V. V., Netesov, S. V., & Tikunova, N. V. (2015). Molecular epidemiology of noroviruses associated with sporadic gastroenteritis in children in Novosibirsk, Russia, 2003–2012. Journal of Medical Virology, 87(5), 740–753.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, N., Lin, X., Wang, S., Tao, Z., Xiong, P., Wang, H., et al. (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  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Professor Herbert W. Virgin, Washington University (St. Louis, Missouri, United States), for providing the murine NoV strain used as sample process control.

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Authors and Affiliations

  1. Department of Food Safety, Nutrition and Veterinary Public Health, Istituto Superiore di Sanità, Rome, Italy

    E. Suffredini

  2. Department of Environment and Health, Istituto Superiore di Sanità, Rome, Italy

    M. Iaconelli, S. Della Libera, F. Bignami & G. La Rosa

  3. Department of Cell Biology and Neurosciences, Istituto Superiore di Sanità, Rome, Italy

    M. Equestre

  4. The National Institute for Biological Standards and Control, The Medicines and Healthcare Products Regulatory Agency, Blanche Lane, South Mimms, Potters Bar, Herts, EN6 3QG, UK

    B. Valdazo-González

  5. Department of Infectious Diseases, Istituto Superiore di Sanità, Rome, Italy

    A. R. Ciccaglione & C. Marcantonio

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  1. E. Suffredini
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Correspondence to G. La Rosa.

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The original version of this article was revised: The original version of this article unfortunately contained a mistake. The presentation of Table 1 was incorrect. The corrected table is given below.

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Suffredini, E., Iaconelli, M., Equestre, M. et al. Genetic Diversity Among Genogroup II Noroviruses and Progressive Emergence of GII.17 in Wastewaters in Italy (2011–2016) Revealed by Next-Generation and Sanger Sequencing. Food Environ Virol 10, 141–150 (2018). https://doi.org/10.1007/s12560-017-9328-y

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