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Published in: BMC Infectious Diseases 1/2018

Open Access 01-12-2018 | Research article

Emergence of norovirus GII.P16-GII.2 strains in patients with acute gastroenteritis in Huzhou, China, 2016–2017

Authors: Jiankang Han, Xiaofang Wu, Liping Chen, Yun Fu, Deshun Xu, Peng Zhang, Lei Ji

Published in: BMC Infectious Diseases | Issue 1/2018

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Abstract

Background

In late 2016, an uncommon recombinant NoV genotype called GII.P16-GII.2 caused a sharp increase in outbreaks of acute gastroenteritis in different countries of Asia and Europe, including China. However, we did not observe a drastic increase in sporadic norovirus cases in the winter of 2016 in Huzhou. Therefore, we investigate the prevalence and genetic diversity of NoVs in the sporadic acute gastroenteritis (AGE) cases from January 2016 to December 2017 in Huzhou City, Zhejiang, China.

Methods

From January 2016 to December 2017, a total of 1001 specimens collected from patients with AGE were screened for NoV by real-time RT-PCR. Partial sequences of the RNA-dependent RNA polymerase (RdRp) and capsid gene of the positive samples were amplified by RT-PCR and sequenced. Genotypes of NoV were confirmed by online NoV typing tool and phylogenetic analysis. Complete VP1 sequences of GII.P16-GII.2 strains detected in this study were further obtained and subjected into sequence analysis.

Results

In total, 204 (20.4%) specimens were identified as NoV-positive. GII genogroup accounted for most of the NoV-infected cases (98.0%, 200/204). NoV infection was found in all age groups tested (< 5, 5–15, 16–20, 21–30, 31–40, 41–50, 51–60, and >60 years), with the 5–15 year age group having the highest detection rate (17/49, 34.7%). Higher activity of NoV infection could be seen in winter-spring season. The predominant NoV genotypes have changed from GII.Pe-GII.4 Sydney2012 and GII.P17-GII.17 in 2016 to GII.P16-GII.2, GII.Pe-GII.4 Sydney2012 and GII.P17-GII.17 in 2017. Phylogenetic analyses revealed that 2016–2017 GII.P16-GII.2 strains were most closely related to Japan 2010–2012 cluster in VP1 region and no common mutations were found in the amino acids of the HBGA-binding sites and the predicted epitopes.

Conclusions

We report the emergence of GII.P16-GII.2 strains and characterize the molecular epidemiological patterns NoV infection between January 2016 and December 2017 in Huzhou. The predominant genotypes of NoV during our study period are diverse. VP1 amino acid sequences of 2016–2017 GII.P16-GII.2 strains remain static after one year of circulation.
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Literature
1.
go back to reference Patel MM, Hall AJ, Vinje J, Parashar UD. Noroviruses: a comprehensive review. J Clin Virol. 2009;44:1–8.CrossRefPubMed Patel MM, Hall AJ, Vinje J, Parashar UD. Noroviruses: a comprehensive review. J Clin Virol. 2009;44:1–8.CrossRefPubMed
2.
go back to reference Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD, Koopmans M, Lopman BA. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14:725–30.CrossRefPubMed Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD, Koopmans M, Lopman BA. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14:725–30.CrossRefPubMed
3.
go back to reference Green KY, Ando T, Balayan MS, Berke T, Clarke IN, Estes MK, Matson DO, Nakata S, Neill JD, Studdert MJ, et al. Taxonomy of the caliciviruses. J Infect Dis. 2000;181(Suppl 2):S322–30.CrossRefPubMed Green KY, Ando T, Balayan MS, Berke T, Clarke IN, Estes MK, Matson DO, Nakata S, Neill JD, Studdert MJ, et al. Taxonomy of the caliciviruses. J Infect Dis. 2000;181(Suppl 2):S322–30.CrossRefPubMed
4.
go back to reference Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK. X-ray crystallographic structure of the Norwalk virus capsid. Science. 1999;286:287–90.CrossRefPubMed Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK. X-ray crystallographic structure of the Norwalk virus capsid. Science. 1999;286:287–90.CrossRefPubMed
5.
go back to reference Vongpunsawad S, Venkataram Prasad BV, Estes MK. Norwalk virus minor capsid protein VP2 associates within the VP1 Shell domain. J Virol. 2013;87:4818–25.CrossRefPubMedPubMedCentral Vongpunsawad S, Venkataram Prasad BV, Estes MK. Norwalk virus minor capsid protein VP2 associates within the VP1 Shell domain. J Virol. 2013;87:4818–25.CrossRefPubMedPubMedCentral
6.
go back to reference Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS. Norovirus classification and proposed strain nomenclature. Virology. 2006;346:312–23.CrossRefPubMed Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS. Norovirus classification and proposed strain nomenclature. Virology. 2006;346:312–23.CrossRefPubMed
8.
go back to reference Bok K, Abente EJ, Realpe-Quintero M, Mitra T, Sosnovtsev SV, Kapikian AZ, Green KY. Evolutionary dynamics of GII.4 noroviruses over a 34-year period. J Virol. 2009;83:11890–901.CrossRefPubMedPubMedCentral Bok K, Abente EJ, Realpe-Quintero M, Mitra T, Sosnovtsev SV, Kapikian AZ, Green KY. Evolutionary dynamics of GII.4 noroviruses over a 34-year period. J Virol. 2009;83:11890–901.CrossRefPubMedPubMedCentral
9.
go back to reference Hoa Tran TN, Trainor E, Nakagomi T, Cunliffe NA, Nakagomi O. Molecular epidemiology of noroviruses associated with acute sporadic gastroenteritis in children: global distribution of genogroups, genotypes and GII.4 variants. J Clin Virol. 2013;56:185–93.CrossRefPubMed Hoa Tran TN, Trainor E, Nakagomi T, Cunliffe NA, Nakagomi O. Molecular epidemiology of noroviruses associated with acute sporadic gastroenteritis in children: global distribution of genogroups, genotypes and GII.4 variants. J Clin Virol. 2013;56:185–93.CrossRefPubMed
10.
go back to reference Ji L, Wu X, Yao W, Chen L, Xu D, Shen Y, Shen J, Han J. Rapid emergence of novel GII.4 sub-lineages noroviruses associated with outbreaks in Huzhou, China, 2008–2012. PLoS One. 2013;8:e82627.CrossRefPubMedPubMedCentral Ji L, Wu X, Yao W, Chen L, Xu D, Shen Y, Shen J, Han J. Rapid emergence of novel GII.4 sub-lineages noroviruses associated with outbreaks in Huzhou, China, 2008–2012. PLoS One. 2013;8:e82627.CrossRefPubMedPubMedCentral
11.
go back to reference Wu X, Han J, Chen L, Xu D, Shen Y, Zha Y, Zhu X, Ji L. Prevalence and genetic diversity of noroviruses in adults with acute gastroenteritis in Huzhou, China, 2013-2014. Arch Virol. 2015;160:1705–13.CrossRefPubMedPubMedCentral Wu X, Han J, Chen L, Xu D, Shen Y, Zha Y, Zhu X, Ji L. Prevalence and genetic diversity of noroviruses in adults with acute gastroenteritis in Huzhou, China, 2013-2014. Arch Virol. 2015;160:1705–13.CrossRefPubMedPubMedCentral
12.
go back to reference de Graaf M, van Beek J, Vennema H, Podkolzin AT, Hewitt J, Bucardo F, Templeton K, Mans J, Nordgren J, Reuter G, et al. Emergence of a novel GII.17 norovirus - end of the GII.4 era? Euro Surveill. 2015;20:21178.CrossRefPubMedPubMedCentral de Graaf M, van Beek J, Vennema H, Podkolzin AT, Hewitt J, Bucardo F, Templeton K, Mans J, Nordgren J, Reuter G, et al. Emergence of a novel GII.17 norovirus - end of the GII.4 era? Euro Surveill. 2015;20:21178.CrossRefPubMedPubMedCentral
13.
go back to reference Zhang P, Chen L, Fu Y, Ji L, Wu X, Xu D, Han J. Clinical and molecular analyses of norovirus-associated sporadic acute gastroenteritis: the emergence of GII.17 over GII.4, Huzhou, China, 2015. BMC Infect Dis. 2016;16:717.CrossRefPubMedPubMedCentral Zhang P, Chen L, Fu Y, Ji L, Wu X, Xu D, Han J. Clinical and molecular analyses of norovirus-associated sporadic acute gastroenteritis: the emergence of GII.17 over GII.4, Huzhou, China, 2015. BMC Infect Dis. 2016;16:717.CrossRefPubMedPubMedCentral
14.
go back to reference Ao Y, Wang J, Ling H, He Y, Dong X, Wang X, Peng J, Zhang H, Jin M, Duan Z. Norovirus GII.P16/GII.2-associated gastroenteritis, China, 2016. Emerg Infect Dis. 2017;23:1172–5.CrossRefPubMedPubMedCentral Ao Y, Wang J, Ling H, He Y, Dong X, Wang X, Peng J, Zhang H, Jin M, Duan Z. Norovirus GII.P16/GII.2-associated gastroenteritis, China, 2016. Emerg Infect Dis. 2017;23:1172–5.CrossRefPubMedPubMedCentral
15.
go back to reference Thongprachum A, Okitsu S, Khamrin P, Maneekarn N, Hayakawa S, Ushijima H. Emergence of norovirus GII.2 and its novel recombination during the gastroenteritis outbreak in Japanese children in mid-2016. Infect Genet Evol. 2017;51:86–8.CrossRefPubMed Thongprachum A, Okitsu S, Khamrin P, Maneekarn N, Hayakawa S, Ushijima H. Emergence of norovirus GII.2 and its novel recombination during the gastroenteritis outbreak in Japanese children in mid-2016. Infect Genet Evol. 2017;51:86–8.CrossRefPubMed
16.
go back to reference Niendorf S, Jacobsen S, Faber M, Eis-Hubinger AM, Hofmann J, Zimmermann O, Hohne M, Bock CT. Steep rise in norovirus cases and emergence of a new recombinant strain GII.P16-GII.2, Germany, winter 2016. Euro Surveill. 2017;22:30447.CrossRefPubMedPubMedCentral Niendorf S, Jacobsen S, Faber M, Eis-Hubinger AM, Hofmann J, Zimmermann O, Hohne M, Bock CT. Steep rise in norovirus cases and emergence of a new recombinant strain GII.P16-GII.2, Germany, winter 2016. Euro Surveill. 2017;22:30447.CrossRefPubMedPubMedCentral
17.
go back to reference Bidalot M, Thery L, Kaplon J, De Rougemont A, Ambert-Balay K. Emergence of new recombinant noroviruses GII.p16-GII.4 and GII.p16-GII.2, France, winter 2016 to 2017. Euro Surveill. 2017;22:30508.CrossRefPubMedPubMedCentral Bidalot M, Thery L, Kaplon J, De Rougemont A, Ambert-Balay K. Emergence of new recombinant noroviruses GII.p16-GII.4 and GII.p16-GII.2, France, winter 2016 to 2017. Euro Surveill. 2017;22:30508.CrossRefPubMedPubMedCentral
18.
go back to reference Jothikumar N, Lowther JA, Henshilwood K, Lees DN, Hill VR, Vinje J. Rapid and sensitive detection of noroviruses by using TaqMan-based one-step reverse transcription-PCR assays and application to naturally contaminated shellfish samples. Appl Environ Microbiol. 2005;71:1870–5.CrossRefPubMedPubMedCentral Jothikumar N, Lowther JA, Henshilwood K, Lees DN, Hill VR, Vinje J. Rapid and sensitive detection of noroviruses by using TaqMan-based one-step reverse transcription-PCR assays and application to naturally contaminated shellfish samples. Appl Environ Microbiol. 2005;71:1870–5.CrossRefPubMedPubMedCentral
19.
go back to reference Vennema H, de Bruin E, Koopmans M. Rational optimization of generic primers used for Norwalk-like virus detection by reverse transcriptase polymerase chain reaction. J Clin Virol. 2002;25:233–5.CrossRefPubMed Vennema H, de Bruin E, Koopmans M. Rational optimization of generic primers used for Norwalk-like virus detection by reverse transcriptase polymerase chain reaction. J Clin Virol. 2002;25:233–5.CrossRefPubMed
20.
go back to reference Kojima S, Kageyama T, Fukushi S, Hoshino FB, Shinohara M, Uchida K, Natori K, Takeda N, Katayama K. Genogroup-specific PCR primers for detection of Norwalk-like viruses. J Virol Methods. 2002;100:107–14.CrossRefPubMed Kojima S, Kageyama T, Fukushi S, Hoshino FB, Shinohara M, Uchida K, Natori K, Takeda N, Katayama K. Genogroup-specific PCR primers for detection of Norwalk-like viruses. J Virol Methods. 2002;100:107–14.CrossRefPubMed
21.
23.
go back to reference Kobayashi M, Matsushima Y, Motoya T, Sakon N, Shigemoto N, Okamoto-Nakagawa R, Nishimura K, Yamashita Y, Kuroda M, Saruki N, et al. Molecular evolution of the capsid gene in human norovirus genogroup II. Sci Rep. 2016;6:29400.CrossRefPubMedPubMedCentral Kobayashi M, Matsushima Y, Motoya T, Sakon N, Shigemoto N, Okamoto-Nakagawa R, Nishimura K, Yamashita Y, Kuroda M, Saruki N, et al. Molecular evolution of the capsid gene in human norovirus genogroup II. Sci Rep. 2016;6:29400.CrossRefPubMedPubMedCentral
24.
go back to reference Lu J, Fang L, Sun L, Zeng H, Li Y, Zheng H, Wu S, Yang F, Song T, Lin J, et al. Association of GII.P16-GII.2 recombinant Norovirus strain with increased Norovirus outbreaks, Guangdong, China, 2016. Emerg Infect Dis. 2017;23:1188–90.CrossRefPubMedPubMedCentral Lu J, Fang L, Sun L, Zeng H, Li Y, Zheng H, Wu S, Yang F, Song T, Lin J, et al. Association of GII.P16-GII.2 recombinant Norovirus strain with increased Norovirus outbreaks, Guangdong, China, 2016. Emerg Infect Dis. 2017;23:1188–90.CrossRefPubMedPubMedCentral
25.
go back to reference Kwok K, Niendorf S, Lee N, Hung TN, Chan LY, Jacobsen S, Nelson EAS, Leung TF, Lai RWM, Chan PKS, et al. Increased detection of emergent recombinant Norovirus GII.P16-GII.2 strains in young adults, Hong Kong, China, 2016-2017. Emerg Infect Dis. 2017;23:1852–5.CrossRefPubMedPubMedCentral Kwok K, Niendorf S, Lee N, Hung TN, Chan LY, Jacobsen S, Nelson EAS, Leung TF, Lai RWM, Chan PKS, et al. Increased detection of emergent recombinant Norovirus GII.P16-GII.2 strains in young adults, Hong Kong, China, 2016-2017. Emerg Infect Dis. 2017;23:1852–5.CrossRefPubMedPubMedCentral
26.
go back to reference Fu JG, Shi C, Xu C, Lin Q, Zhang J, Yi QH, Bao CJ, Huo X, Zhu YF, Ai J, et al. Outbreaks of acute gastroenteritis associated with a re-emerging GII.P16-GII.2 norovirus in the spring of 2017 in Jiangsu, China. PLoS One. 2017;12:e0186090.CrossRefPubMedPubMedCentral Fu JG, Shi C, Xu C, Lin Q, Zhang J, Yi QH, Bao CJ, Huo X, Zhu YF, Ai J, et al. Outbreaks of acute gastroenteritis associated with a re-emerging GII.P16-GII.2 norovirus in the spring of 2017 in Jiangsu, China. PLoS One. 2017;12:e0186090.CrossRefPubMedPubMedCentral
28.
go back to reference Parra GI, Squires RB, Karangwa CK, Johnson JA, Lepore CJ, Sosnovtsev SV, Green KY. Static and evolving Norovirus genotypes: implications for epidemiology and immunity. PLoS Pathog. 2017;13:e1006136.CrossRefPubMedPubMedCentral Parra GI, Squires RB, Karangwa CK, Johnson JA, Lepore CJ, Sosnovtsev SV, Green KY. Static and evolving Norovirus genotypes: implications for epidemiology and immunity. PLoS Pathog. 2017;13:e1006136.CrossRefPubMedPubMedCentral
29.
go back to reference Iritani N, Kaida A, Abe N, Sekiguchi J, Kubo H, Takakura K, Goto K, Ogura H, Seto Y. Increase of GII.2 norovirus infections during the 2009-2010 season in Osaka City, Japan. J Med Virol. 2012;84:517–25.CrossRefPubMed Iritani N, Kaida A, Abe N, Sekiguchi J, Kubo H, Takakura K, Goto K, Ogura H, Seto Y. Increase of GII.2 norovirus infections during the 2009-2010 season in Osaka City, Japan. J Med Virol. 2012;84:517–25.CrossRefPubMed
30.
go back to reference Motomura K, Boonchan M, Noda M, Tanaka T, Takeda N. Norovirus epidemics caused by new GII.2 chimera viruses in 2012-2014 in Japan. Infect Genet Evol. 2016;42:49–52.CrossRefPubMed Motomura K, Boonchan M, Noda M, Tanaka T, Takeda N. Norovirus epidemics caused by new GII.2 chimera viruses in 2012-2014 in Japan. Infect Genet Evol. 2016;42:49–52.CrossRefPubMed
31.
go back to reference Mizukoshi F, Nagasawa K, Doan YH, Haga K, Yoshizumi S, Ueki Y, Shinohara M, Ishikawa M, Sakon N, Shigemoto N, et al. Molecular Evolution of the RNA-Dependent RNA Polymerase and Capsid Genes of Human Norovirus Genotype GII.2 in Japan during 2004–2015. Front Microbiol. 2017;8:705.CrossRefPubMedPubMedCentral Mizukoshi F, Nagasawa K, Doan YH, Haga K, Yoshizumi S, Ueki Y, Shinohara M, Ishikawa M, Sakon N, Shigemoto N, et al. Molecular Evolution of the RNA-Dependent RNA Polymerase and Capsid Genes of Human Norovirus Genotype GII.2 in Japan during 2004–2015. Front Microbiol. 2017;8:705.CrossRefPubMedPubMedCentral
32.
go back to reference Nagasawa K, Matsushima Y, Motoya T, Mizukoshi F, Ueki Y, Sakon N, Murakami K, Shimizu T, Okabe N, Nagata N, et al. Phylogeny and Immunoreactivity of Norovirus GII.P16-GII.2, Japan, winter 2016-17. Emerg Infect Dis. 2018;24:144–8.CrossRefPubMedPubMedCentral Nagasawa K, Matsushima Y, Motoya T, Mizukoshi F, Ueki Y, Sakon N, Murakami K, Shimizu T, Okabe N, Nagata N, et al. Phylogeny and Immunoreactivity of Norovirus GII.P16-GII.2, Japan, winter 2016-17. Emerg Infect Dis. 2018;24:144–8.CrossRefPubMedPubMedCentral
33.
go back to reference Tohma K, Lepore CJ, Ford-Siltz LA, Parra GI. Phylogenetic Analyses Suggest that Factors Other Than the Capsid Protein Play a Role in the Epidemic Potential of GII.2 Norovirus. mSphere. 2017;2:e00187–17.CrossRefPubMedPubMedCentral Tohma K, Lepore CJ, Ford-Siltz LA, Parra GI. Phylogenetic Analyses Suggest that Factors Other Than the Capsid Protein Play a Role in the Epidemic Potential of GII.2 Norovirus. mSphere. 2017;2:e00187–17.CrossRefPubMedPubMedCentral
Metadata
Title
Emergence of norovirus GII.P16-GII.2 strains in patients with acute gastroenteritis in Huzhou, China, 2016–2017
Authors
Jiankang Han
Xiaofang Wu
Liping Chen
Yun Fu
Deshun Xu
Peng Zhang
Lei Ji
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2018
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-018-3259-6

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