Skip to main content
Top
Published in: Gut Pathogens 1/2019

Open Access 01-12-2019 | Research

Genotypic prevalence of norovirus GII in gastroenteritis outpatients in Shanghai from 2016 to 2018

Authors: Xiaozhou Kuang, Zheng Teng, Xi Zhang

Published in: Gut Pathogens | Issue 1/2019

Login to get access

Abstract

Background

With the help of an existing citywide comprehensive surveillance on gastroenteritis outpatients, although norovirus genogroup II (NoV GII) was tested routinely, its genotypes were never investigated systematically on a municipal level. This study aimed to understand the prevalence, major genotypes and evolutional trends of NoV GII in Shanghai during the period of 2016–2018, and to provide molecular bases for early warning for any potential NoV outbreaks.

Methods

27 sentinel hospitals from all 16 districts were recruited by stratified probability proportional to size (PPS) method in Shanghai comprehensive diarrhea surveillance programme. Stool samples were collected and screened for NoV GII by real-time reverse transcription polymerase chain reaction (qRT-PCR). For samples that were positive in qRT-PCR, conventional RT-PCR was performed to amplify the ORF1-ORF2 junction of NoV GII gene. Generated sequences were typed by RIVM online genotyping tool, and then strains of interest were analyzed phylogenetically using MEGA 6.0.

Results

A total of 7883 stool samples were collected from diarrhea outpatients, among which 6474 were from adults and 1409 were from children. 13.66% (1077 cases) were screened positive in qRT-PCR for NoV GII, from which 71.96% (775 cases) were sequenced successfully. The top three genotypes were GII.Pe/GII.4 (37%), GII.P17/GII.17 (26%) and GII.P16/GII.2 (17%). While GII.Pe/GII.4 detection rate decreased significantly over the 3 years (from 48.4 to 20.9%); GII.P16/GII.2 appeared for the first time in October 2016 and rose rapidly to 27.0% in 2017, but fell back to 23.4% in 2018. Meanwhile there was a significant increase for both GII.P12/GII.3 and GII.P7/GII.6 recombinant genotypes detected in adult population in 2018. Phylogenic analysis revealed the existence of multiple gene clusters within both of these recombinant genotypes.

Conclusion

Unlike the alternating circulation of GII.4 and non-GII.4 NoV observed in 2016 or 2017, the genotype profile of NoV GII in 2018 was characterized by the co-prevalence of multiple recombinant genotypes. A recent increase in detection rate in less reported recombinant genotypes such as GII.P12/GII.3 and GII.P7/GII.6 among adult population calls for a continuing close monitoring on NoV GII genotypes in case of potential local outbreaks.
Appendix
Available only for authorised users
Literature
1.
go back to reference Ahmed SM, Hall AJ, Robinson AE, et al. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14(8):725–30.CrossRef Ahmed SM, Hall AJ, Robinson AE, et al. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14(8):725–30.CrossRef
2.
go back to reference Centers for Disease Control and Prevention. Emergence of new norovirus strain GII.4 Sydney—United States, 2012. MMWR Morb Mortal Wkly Rep. 2013;62(3):55. Centers for Disease Control and Prevention. Emergence of new norovirus strain GII.4 Sydney—United States, 2012. MMWR Morb Mortal Wkly Rep. 2013;62(3):55.
3.
go back to reference Van Beek J, Ambert-Balay K, Botteldoorn N, et al. Indications for worldwide increased norovirus activity associated with emergence of a new variant of genotype II.4, late 2012. Eurosurveillance. 2013;18(1):8–9.PubMed Van Beek J, Ambert-Balay K, Botteldoorn N, et al. Indications for worldwide increased norovirus activity associated with emergence of a new variant of genotype II.4, late 2012. Eurosurveillance. 2013;18(1):8–9.PubMed
4.
go back to reference Bartsch SM, Lopman BA, Ozawa S, et al. Global economic burden of norovirus gastroenteritis. PLoS ONE. 2016;11(4):e0151219.CrossRef Bartsch SM, Lopman BA, Ozawa S, et al. Global economic burden of norovirus gastroenteritis. PLoS ONE. 2016;11(4):e0151219.CrossRef
5.
go back to reference Li J, Pan H, Xiao WJ, et al. Epidemiological and etiological surveillance study of infectious diarrhea in Shanghai in 2013–2015. Zhonghua Yu Fang Yi Xue Za Zhi. 2017;51(12):1113–7.PubMed Li J, Pan H, Xiao WJ, et al. Epidemiological and etiological surveillance study of infectious diarrhea in Shanghai in 2013–2015. Zhonghua Yu Fang Yi Xue Za Zhi. 2017;51(12):1113–7.PubMed
6.
go back to reference Xue Y, Pan H, Hu J, et al. Epidemiology of norovirus infections among diarrhea outpatients in a diarrhea surveillance system in Shanghai, China: a cross-sectional study. BMC Infect Dis. 2015;15:183.CrossRef Xue Y, Pan H, Hu J, et al. Epidemiology of norovirus infections among diarrhea outpatients in a diarrhea surveillance system in Shanghai, China: a cross-sectional study. BMC Infect Dis. 2015;15:183.CrossRef
7.
go back to reference De Graaf M, Van Beek J, Koopmans MPG. Human norovirus transmission and evolution in a changing world. Nat Rev Microbiol. 2016;14:421.CrossRef De Graaf M, Van Beek J, Koopmans MPG. Human norovirus transmission and evolution in a changing world. Nat Rev Microbiol. 2016;14:421.CrossRef
8.
go back to reference He Y, Jin M, Chen K, et al. Gastroenteritis outbreaks associated with the emergence of the new GII.4 Sydney norovirus variant during the epidemic of 2012/13 in Shenzhen City, China. PLoS ONE. 2016;11(11):e0165880.CrossRef He Y, Jin M, Chen K, et al. Gastroenteritis outbreaks associated with the emergence of the new GII.4 Sydney norovirus variant during the epidemic of 2012/13 in Shenzhen City, China. PLoS ONE. 2016;11(11):e0165880.CrossRef
10.
go back to reference Ao Y, Cong X, Jin M, et al. Genetic analysis of reemerging GII.P16-GII.2 noroviruses in 2016–2017 in China. J Infect Dis. 2018;218(1):133–43.CrossRef Ao Y, Cong X, Jin M, et al. Genetic analysis of reemerging GII.P16-GII.2 noroviruses in 2016–2017 in China. J Infect Dis. 2018;218(1):133–43.CrossRef
11.
go back to reference Shen Z, Wang G, Zai SB, et al. The detection of novel norovirus Sydney strain GII.4 in Shanghai. Chin J Virol. 2013;6:608–14. Shen Z, Wang G, Zai SB, et al. The detection of novel norovirus Sydney strain GII.4 in Shanghai. Chin J Virol. 2013;6:608–14.
12.
go back to reference Pan LF, et al. The novel norovirus genotype GII.17 is the predominant strain in diarrheal patients in Shanghai, China. Gut Pathog. 2016;8(1):49.CrossRef Pan LF, et al. The novel norovirus genotype GII.17 is the predominant strain in diarrheal patients in Shanghai, China. Gut Pathog. 2016;8(1):49.CrossRef
13.
go back to reference Niendorf S, Jacobsen S, Faber M, et al. Steep rise in norovirus cases and emergence of a new recombinant strain GII.P16-GII.2, Germany, winter 2016. Eurosurveillance. 2017;22(4):30447.CrossRef Niendorf S, Jacobsen S, Faber M, et al. Steep rise in norovirus cases and emergence of a new recombinant strain GII.P16-GII.2, Germany, winter 2016. Eurosurveillance. 2017;22(4):30447.CrossRef
14.
go back to reference Bidalot M, Théry L, Kaplon J, et al. Emergence of new recombinant noroviruses GII.p16-GII.4 and GII.p16-GII.2, France, winter 2016 to 2017. Eurosurveillance. 2017;22(15):30508.CrossRef Bidalot M, Théry L, Kaplon J, et al. Emergence of new recombinant noroviruses GII.p16-GII.4 and GII.p16-GII.2, France, winter 2016 to 2017. Eurosurveillance. 2017;22(15):30508.CrossRef
15.
go back to reference Kwok K, Niendorf S, Lee N, 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(11):1852–5.CrossRef Kwok K, Niendorf S, Lee N, 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(11):1852–5.CrossRef
16.
go back to reference Liu J, Li S, Wang C, et al. Genomic characterization of GII.3 noroviruses isolated from children in Zhengzhou city, China, 2015/16. Arch Virol. 2018;163(10):2737–42.CrossRef Liu J, Li S, Wang C, et al. Genomic characterization of GII.3 noroviruses isolated from children in Zhengzhou city, China, 2015/16. Arch Virol. 2018;163(10):2737–42.CrossRef
17.
go back to reference Dabilla N, Almeida TNV, Franco FC, et al. Recombinant noroviruses detected in Mid-West region of Brazil in two different periods 2009–2011 and 2014–2015: atypical breakpoints of recombination and detection of distinct GII.P7-GII.6 lineages. Infect Genet Evol. 2019;68:47–53.CrossRef Dabilla N, Almeida TNV, Franco FC, et al. Recombinant noroviruses detected in Mid-West region of Brazil in two different periods 2009–2011 and 2014–2015: atypical breakpoints of recombination and detection of distinct GII.P7-GII.6 lineages. Infect Genet Evol. 2019;68:47–53.CrossRef
18.
go back to reference Dong X, Qin M, Wang Z, et al. Should we pay attention to recombinant norovirus strain GII.P7/GII.6? J Infect Public Health. 2019;12:403–9.CrossRef Dong X, Qin M, Wang Z, et al. Should we pay attention to recombinant norovirus strain GII.P7/GII.6? J Infect Public Health. 2019;12:403–9.CrossRef
20.
go back to reference Cannon JL, Barclay L, Collins NR, et al. Genetic and epidemiologic trends of norovirus outbreaks in the United States from 2013 to 2016 demonstrated emergence of novel GII.4 recombinant viruses. J Clin Microbiol. 2017;55(7):2208–21.CrossRef Cannon JL, Barclay L, Collins NR, et al. Genetic and epidemiologic trends of norovirus outbreaks in the United States from 2013 to 2016 demonstrated emergence of novel GII.4 recombinant viruses. J Clin Microbiol. 2017;55(7):2208–21.CrossRef
22.
go back to reference Tamura K, Peterson D, Peterson N, et al. MEGA5: molecular evolutionary genetic analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–9.CrossRef Tamura K, Peterson D, Peterson N, et al. MEGA5: molecular evolutionary genetic analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–9.CrossRef
23.
go back to reference Yu J, Lai S, Wang X, et al. Analysis of epidemiology characteristics of norovirus among diarrheal outpatients in 27 provinces in China, 2009–2013. Zhonghua Liu Xing Bing Xue Za Zhi. 2015;36(3):199–204.PubMed Yu J, Lai S, Wang X, et al. Analysis of epidemiology characteristics of norovirus among diarrheal outpatients in 27 provinces in China, 2009–2013. Zhonghua Liu Xing Bing Xue Za Zhi. 2015;36(3):199–204.PubMed
24.
go back to reference Zhang SX, Li L, Yin JW, et al. Emergence of human caliciviruses among diarrhea cases in southwest China. BMC Infect Dis. 2016;16(1):511.CrossRef Zhang SX, Li L, Yin JW, et al. Emergence of human caliciviruses among diarrhea cases in southwest China. BMC Infect Dis. 2016;16(1):511.CrossRef
25.
go back to reference Jiang CL, Xu Y, Liu Y, et al. Analysis of rotavirus and norovirus infections among infants with diarrhea in an outpatient in Nanjing. Int J Virol. 2018;25(6):392–6. Jiang CL, Xu Y, Liu Y, et al. Analysis of rotavirus and norovirus infections among infants with diarrhea in an outpatient in Nanjing. Int J Virol. 2018;25(6):392–6.
26.
go back to reference Wang P, Goggins W, Chan E. A time-series study of the association of rainfall, relative humidity and ambient temperature with hospitalizations for rotavirus and norovirus infection among children in Hong Kong. Sci Total Environ. 2018;643:414–22.CrossRef Wang P, Goggins W, Chan E. A time-series study of the association of rainfall, relative humidity and ambient temperature with hospitalizations for rotavirus and norovirus infection among children in Hong Kong. Sci Total Environ. 2018;643:414–22.CrossRef
27.
go back to reference Kauppinen A, Miettinen IT. Persistence of norovirus GII genome in drinking water and wastewater at different temperatures. Pathogens. 2017;6(4):1.CrossRef Kauppinen A, Miettinen IT. Persistence of norovirus GII genome in drinking water and wastewater at different temperatures. Pathogens. 2017;6(4):1.CrossRef
28.
go back to reference Bozkurt H, D’souza DH, Davidson PM. Thermal inactivation of foodborne enteric viruses and their viral surrogates in foods. J Food Prot. 2015;78(8):1597–617.CrossRef Bozkurt H, D’souza DH, Davidson PM. Thermal inactivation of foodborne enteric viruses and their viral surrogates in foods. J Food Prot. 2015;78(8):1597–617.CrossRef
29.
go back to reference Tan DM, Lyu SL, Liu W, et al. Utility of droplet digital pcr assay for quantitative detection of norovirus in shellfish, from production to consumption in Guangxi, China. Biomed Environ Sci. 2018;31(10):713–20.PubMed Tan DM, Lyu SL, Liu W, et al. Utility of droplet digital pcr assay for quantitative detection of norovirus in shellfish, from production to consumption in Guangxi, China. Biomed Environ Sci. 2018;31(10):713–20.PubMed
30.
go back to reference Huo Y, Cai A, Yang H, et al. Complete nucleotide sequence of a norovirus GII.4 genotype: evidence for the spread of the newly emerged pandemic Sydney 2012 strain to China. Virus Genes. 2014;48(2):356–60.CrossRef Huo Y, Cai A, Yang H, et al. Complete nucleotide sequence of a norovirus GII.4 genotype: evidence for the spread of the newly emerged pandemic Sydney 2012 strain to China. Virus Genes. 2014;48(2):356–60.CrossRef
31.
go back to reference Wu F, Chen H, Yen C, et al. Epidemiology and molecular characteristics of norovirus GII.4 Sydney outbreaks in Taiwan, January 2012–December 2013. J Med Virol. 2015;87(9):1462–70.CrossRef Wu F, Chen H, Yen C, et al. Epidemiology and molecular characteristics of norovirus GII.4 Sydney outbreaks in Taiwan, January 2012–December 2013. J Med Virol. 2015;87(9):1462–70.CrossRef
32.
go back to reference Lu J, Sun L, Fang L, et al. Gastroenteritis outbreaks caused by norovirus GII.17, Guangdong Province, China, 2014–2015. Emerg Infect Dis. 2015;21(7):1240–2.CrossRef Lu J, Sun L, Fang L, et al. Gastroenteritis outbreaks caused by norovirus GII.17, Guangdong Province, China, 2014–2015. Emerg Infect Dis. 2015;21(7):1240–2.CrossRef
33.
go back to reference Matsushima Y, Ishikawa M, Shimizu T, et al. 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. 2015;20(26):21173.CrossRef Matsushima Y, Ishikawa M, Shimizu T, et al. 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. 2015;20(26):21173.CrossRef
34.
go back to reference Parra GI, Green KY. Genome of emerging norovirus GII.17, United States, 2014. Emerg Infect Dis. 2015;21(8):1477–9.CrossRef Parra GI, Green KY. Genome of emerging norovirus GII.17, United States, 2014. Emerg Infect Dis. 2015;21(8):1477–9.CrossRef
35.
go back to reference Chan MC, Kwok K, Zhang L, et al. Bimodal seasonality and alternating predominance of norovirus GII.4 and non-GII.4, Hong Kong, China, 2014–2017(1). Emerg Infect Dis. 2018;24(4):767–9.CrossRef Chan MC, Kwok K, Zhang L, et al. Bimodal seasonality and alternating predominance of norovirus GII.4 and non-GII.4, Hong Kong, China, 2014–2017(1). Emerg Infect Dis. 2018;24(4):767–9.CrossRef
36.
go back to reference Langat P, Raghwani J, Dudas G, et al. Genome-wide evolutionary dynamics of influenza B viruses on a global scale. PLoS Pathog. 2017;13(12):e1006749.CrossRef Langat P, Raghwani J, Dudas G, et al. Genome-wide evolutionary dynamics of influenza B viruses on a global scale. PLoS Pathog. 2017;13(12):e1006749.CrossRef
38.
go back to reference Boon D, Mahar JE, Abente EJ, et al. Comparative evolution of GII.3 and GII.4 norovirus over a 31-year period. J Virol. 2011;85(17):8656–66.CrossRef Boon D, Mahar JE, Abente EJ, et al. Comparative evolution of GII.3 and GII.4 norovirus over a 31-year period. J Virol. 2011;85(17):8656–66.CrossRef
Metadata
Title
Genotypic prevalence of norovirus GII in gastroenteritis outpatients in Shanghai from 2016 to 2018
Authors
Xiaozhou Kuang
Zheng Teng
Xi Zhang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2019
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-019-0321-x

Other articles of this Issue 1/2019

Gut Pathogens 1/2019 Go to the issue