Skip to main content
Top
Published in: Virology Journal 1/2023

Open Access 01-12-2023 | Acute Gastroenteritis | Research

Molecular epidemiology analysis of symptomatic and asymptomatic norovirus infections in Chinese infants

Authors: Li-Na Chen, Si-Jie Wang, Song-Mei Wang, Xiao-Li Fu, Wen-Jing Zheng, Zhi-Yong Hao, Hai-Song Zhou, Xin-Jiang Zhang, Yu-Liang Zhao, Chao Qiu, Lorenz von Seidlein, Tian-Yi Qiu, Xuan-Yi Wang

Published in: Virology Journal | Issue 1/2023

Login to get access

Abstract

Background

Norovirus is a leading cause of acute gastroenteritis among children. Previous studies based on symptomatic infections indicated that mutations, rather than recombination drove the evolution of the norovirus ORF2. These characteristics were found in hospital-based symptomatic infections, whereas, asymptomatic infections are frequent and contribute significantly to transmission.

Methods

We conducted the first norovirus molecular epidemiology analysis covering both symptomatic and asymptomatic infections derived from a birth cohort study in the northern China.

Results

During the study, 14 symptomatic and 20 asymptomatic norovirus infections were detected in 32 infants. Out of the 14 strains that caused symptomatic infections, 12 strains were identified as GII.3[P12], and others were GII.4[P31]. Conversely, 17 asymptomatic infections were caused by GII.4[P31], two by GII.2[P16], and one by GII.4[P16]. Regardless of symptomatic and asymptomatic infections, the mutations were detected frequently in the ORF2 region, and almost all recombination were identified in the RdRp-ORF2 region. The majority of the mutations were located around the predefined epitope regions of P2 subdomain indicating a potential for immune evasion.

Conclusion

The role of symptomatic as well as asymptomatic infections in the evolution of norovirus needs to be evaluated continuously.
Appendix
Available only for authorised users
Literature
1.
go back to reference Katayama K. Caliciviridae. Nihon Rinsho. 2003;61(Suppl 3):468–74.PubMed Katayama K. Caliciviridae. Nihon Rinsho. 2003;61(Suppl 3):468–74.PubMed
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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
3.
go back to reference Cannon JL, Lopman BA, Payne DC, Vinje J. Birth cohort studies assessing norovirus infection and immunity in young children: a review. Clin Infect Dis. 2019;69:357–65.PubMedPubMedCentralCrossRef Cannon JL, Lopman BA, Payne DC, Vinje J. Birth cohort studies assessing norovirus infection and immunity in young children: a review. Clin Infect Dis. 2019;69:357–65.PubMedPubMedCentralCrossRef
4.
5.
go back to reference Jiang X, Wang M, Wang K, Estes MK. Sequence and genomic organization of Norwalk virus. Virology. 1993;195:51–61.PubMedCrossRef Jiang X, Wang M, Wang K, Estes MK. Sequence and genomic organization of Norwalk virus. Virology. 1993;195:51–61.PubMedCrossRef
6.
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.PubMedCrossRef 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.PubMedCrossRef
7.
go back to reference Tan M, Jiang X. Histo-blood group antigens: a common niche for norovirus and rotavirus. Expert Rev Mol Med. 2014;16: e5.PubMedCrossRef Tan M, Jiang X. Histo-blood group antigens: a common niche for norovirus and rotavirus. Expert Rev Mol Med. 2014;16: e5.PubMedCrossRef
8.
go back to reference Ludwig-Begall LF, Mauroy A, Thiry E. Norovirus recombinants: recurrent in the field, recalcitrant in the lab - a scoping review of recombination and recombinant types of noroviruses. J Gen Virol. 2018;99:970–88.PubMedCrossRef Ludwig-Begall LF, Mauroy A, Thiry E. Norovirus recombinants: recurrent in the field, recalcitrant in the lab - a scoping review of recombination and recombinant types of noroviruses. J Gen Virol. 2018;99:970–88.PubMedCrossRef
9.
go back to reference Huang Z, Yao D, Xiao S, Yang D, Ou X. Full-genome sequences of GII.13[P21] recombinant norovirus strains from an outbreak in Changsha, China. Arch Virol. 2020;165:1647–52.PubMedPubMedCentralCrossRef Huang Z, Yao D, Xiao S, Yang D, Ou X. Full-genome sequences of GII.13[P21] recombinant norovirus strains from an outbreak in Changsha, China. Arch Virol. 2020;165:1647–52.PubMedPubMedCentralCrossRef
10.
go back to reference Wang C, Ao Y, Yu J, Xie X, Deng H, Jin M, Liu L, Duan Z. Complete genome sequence of a novel recombinant GII.P16-GII.1 norovirus associated with a gastroenteritis outbreak in Shandong Province, China, in 2017. Genome Announc. 2018;6:e01483-e1517.PubMedPubMedCentralCrossRef Wang C, Ao Y, Yu J, Xie X, Deng H, Jin M, Liu L, Duan Z. Complete genome sequence of a novel recombinant GII.P16-GII.1 norovirus associated with a gastroenteritis outbreak in Shandong Province, China, in 2017. Genome Announc. 2018;6:e01483-e1517.PubMedPubMedCentralCrossRef
11.
go back to reference Medici MC, Tummolo F, Martella V, Giammanco GM, De Grazia S, Arcangeletti MC, De Conto F, Chezzi C, Calderaro A. Novel recombinant GII.P16_GII.13 and GII.P16_GII.3 norovirus strains in Italy. Virus Res. 2014;188:142–5.PubMedCrossRef Medici MC, Tummolo F, Martella V, Giammanco GM, De Grazia S, Arcangeletti MC, De Conto F, Chezzi C, Calderaro A. Novel recombinant GII.P16_GII.13 and GII.P16_GII.3 norovirus strains in Italy. Virus Res. 2014;188:142–5.PubMedCrossRef
12.
go back to reference Zhou HL, Chen LN, Wang SM, Tan M, Qiu C, Qiu TY, Wang XY. Prevalence and evolution of noroviruses between 1966 and 2019 implications for vaccine design. Pathogens. 2021;10:1012.PubMedPubMedCentralCrossRef Zhou HL, Chen LN, Wang SM, Tan M, Qiu C, Qiu TY, Wang XY. Prevalence and evolution of noroviruses between 1966 and 2019 implications for vaccine design. Pathogens. 2021;10:1012.PubMedPubMedCentralCrossRef
14.
go back to reference Phattanawiboon B, Nonthabenjawan N, Boonyos P, Jetsukontorn C, Towayunanta W, Chuntrakool K, Ngaopravet K, Ruchusatsawat K, Uppapong B, Sangkitporn S, et al. Norovirus transmission mediated by asymptomatic family members in households. PLoS ONE. 2020;15: e0236502.PubMedPubMedCentralCrossRef Phattanawiboon B, Nonthabenjawan N, Boonyos P, Jetsukontorn C, Towayunanta W, Chuntrakool K, Ngaopravet K, Ruchusatsawat K, Uppapong B, Sangkitporn S, et al. Norovirus transmission mediated by asymptomatic family members in households. PLoS ONE. 2020;15: e0236502.PubMedPubMedCentralCrossRef
15.
go back to reference Monica B, Ramani S, Banerjee I, Primrose B, Iturriza-Gomara M, Gallimore CI, Brown DW, Moses PD, Gray JJ, Kang G. Human caliciviruses in symptomatic and asymptomatic infections in children in Vellore, South India. J Med Virol. 2007;79:544–51.PubMedPubMedCentralCrossRef Monica B, Ramani S, Banerjee I, Primrose B, Iturriza-Gomara M, Gallimore CI, Brown DW, Moses PD, Gray JJ, Kang G. Human caliciviruses in symptomatic and asymptomatic infections in children in Vellore, South India. J Med Virol. 2007;79:544–51.PubMedPubMedCentralCrossRef
16.
go back to reference Vielot NA, Brinkman A, DeMaso C, Vilchez S, Lindesmith LC, Bucardo F, Reyes Y, Baric RS, Ryan EP, Braun R, Becker-Dreps S. Breadth and dynamics of human norovirus-specific antibodies in the first year of life. J Pediatric Infect Dis Soc. 2022;11(10):463–6.PubMedPubMedCentralCrossRef Vielot NA, Brinkman A, DeMaso C, Vilchez S, Lindesmith LC, Bucardo F, Reyes Y, Baric RS, Ryan EP, Braun R, Becker-Dreps S. Breadth and dynamics of human norovirus-specific antibodies in the first year of life. J Pediatric Infect Dis Soc. 2022;11(10):463–6.PubMedPubMedCentralCrossRef
18.
go back to reference Huynen P, Mauroy A, Martin C, Savadogo LG, Boreux R, Thiry E, Melin P, De Mol P. Molecular epidemiology of norovirus infections in symptomatic and asymptomatic children from Bobo Dioulasso, Burkina Faso. J Clin Virol. 2013;58:515–21.PubMedCrossRef Huynen P, Mauroy A, Martin C, Savadogo LG, Boreux R, Thiry E, Melin P, De Mol P. Molecular epidemiology of norovirus infections in symptomatic and asymptomatic children from Bobo Dioulasso, Burkina Faso. J Clin Virol. 2013;58:515–21.PubMedCrossRef
20.
go back to reference Qiao N, Wang SM, Wang JX, Kang B, Zhen SS, Zhang XJ, Hao ZY, Ma JC, Qiu C, Zhao YL, et al. Variation analysis of norovirus among children with diarrhea in rural Hebei Province, north of China. Infect Genet Evol. 2017;53:199–205.PubMedCrossRef Qiao N, Wang SM, Wang JX, Kang B, Zhen SS, Zhang XJ, Hao ZY, Ma JC, Qiu C, Zhao YL, et al. Variation analysis of norovirus among children with diarrhea in rural Hebei Province, north of China. Infect Genet Evol. 2017;53:199–205.PubMedCrossRef
21.
go back to reference Chhabra P, Browne H, Huynh T, Diez-Valcarce M, Barclay L, Kosek MN, Ahmed T, Lopez MR, Pan CY, Vinje J. Single-step RT-PCR assay for dual genotyping of GI and GII norovirus strains. J Clin Virol. 2021;134: 104689.PubMedPubMedCentralCrossRef Chhabra P, Browne H, Huynh T, Diez-Valcarce M, Barclay L, Kosek MN, Ahmed T, Lopez MR, Pan CY, Vinje J. Single-step RT-PCR assay for dual genotyping of GI and GII norovirus strains. J Clin Virol. 2021;134: 104689.PubMedPubMedCentralCrossRef
22.
go back to reference Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–25.PubMed Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–25.PubMed
23.
24.
go back to reference Yamaoka K, Nakagawa T, Uno T. Application of Akaike’s information criterion (AIC) in the evaluation of linear pharmacokinetic equations. J Pharmacokinet Biopharm. 1978;6:165–75.PubMedCrossRef Yamaoka K, Nakagawa T, Uno T. Application of Akaike’s information criterion (AIC) in the evaluation of linear pharmacokinetic equations. J Pharmacokinet Biopharm. 1978;6:165–75.PubMedCrossRef
25.
go back to reference Hall BG. Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol. 2013;30:1229–35.PubMedCrossRef Hall BG. Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol. 2013;30:1229–35.PubMedCrossRef
26.
go back to reference Nemzer LR. Shannon information entropy in the canonical genetic code. J Theor Biol. 2017;415:158–70.PubMedCrossRef Nemzer LR. Shannon information entropy in the canonical genetic code. J Theor Biol. 2017;415:158–70.PubMedCrossRef
27.
go back to reference Tohma K, Lepore CJ, Martinez M, Degiuseppe JI, Khamrin P, Saito M, Mayta H, Nwaba AUA, Ford-Siltz LA, Green KY, et al. Genome-wide analyses of human noroviruses provide insights on evolutionary dynamics and evidence of coexisting viral populations evolving under recombination constraints. PLoS Pathog. 2021;17: e1009744.PubMedPubMedCentralCrossRef Tohma K, Lepore CJ, Martinez M, Degiuseppe JI, Khamrin P, Saito M, Mayta H, Nwaba AUA, Ford-Siltz LA, Green KY, et al. Genome-wide analyses of human noroviruses provide insights on evolutionary dynamics and evidence of coexisting viral populations evolving under recombination constraints. PLoS Pathog. 2021;17: e1009744.PubMedPubMedCentralCrossRef
29.
go back to reference Fleri W, Paul S, Dhanda SK, Mahajan S, Xu X, Peters B, Sette A. The immune epitope database and analysis resource in epitope discovery and synthetic vaccine design. Front Immunol. 2017;8:278.PubMedPubMedCentralCrossRef Fleri W, Paul S, Dhanda SK, Mahajan S, Xu X, Peters B, Sette A. The immune epitope database and analysis resource in epitope discovery and synthetic vaccine design. Front Immunol. 2017;8:278.PubMedPubMedCentralCrossRef
30.
go back to reference Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. A method and server for predicting damaging missense mutations. Nat Methods. 2010;7:248–9.PubMedPubMedCentralCrossRef Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. A method and server for predicting damaging missense mutations. Nat Methods. 2010;7:248–9.PubMedPubMedCentralCrossRef
31.
go back to reference Adzhubei I, Jordan DM, Sunyaev SR. Predicting functional effect of human missense mutations using PolyPhen-2. Curr Protoc Hum Genet. 2013;Chapter 7:Unit7 20. Adzhubei I, Jordan DM, Sunyaev SR. Predicting functional effect of human missense mutations using PolyPhen-2. Curr Protoc Hum Genet. 2013;Chapter 7:Unit7 20.
32.
go back to reference Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46:W296–303.PubMedPubMedCentralCrossRef Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46:W296–303.PubMedPubMedCentralCrossRef
33.
go back to reference Janson G, Paiardini A. PyMod 3: a complete suite for structural bioinformatics in PyMOL. Bioinformatics. 2021;37:1471–2.PubMedCrossRef Janson G, Paiardini A. PyMod 3: a complete suite for structural bioinformatics in PyMOL. Bioinformatics. 2021;37:1471–2.PubMedCrossRef
34.
go back to reference Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 2015;1:vev003.PubMedPubMedCentralCrossRef Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 2015;1:vev003.PubMedPubMedCentralCrossRef
35.
go back to reference Martin DP, Murrell B, Khoosal A, Muhire B. Detecting and analyzing genetic recombination using RDP4. Methods Mol Biol. 2017;1525:433–60.PubMedCrossRef Martin DP, Murrell B, Khoosal A, Muhire B. Detecting and analyzing genetic recombination using RDP4. Methods Mol Biol. 2017;1525:433–60.PubMedCrossRef
36.
go back to reference Martin D, Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics. 2000;16:562–3.PubMedCrossRef Martin D, Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics. 2000;16:562–3.PubMedCrossRef
37.
go back to reference Wang LP, Zhou SX, Wang X, Lu QB, Shi LS, Ren X, Zhang HY, Wang YF, Lin SH, Zhang CH, et al. Etiological, epidemiological, and clinical features of acute diarrhea in China. Nat Commun. 2021;12:2464.PubMedPubMedCentralCrossRef Wang LP, Zhou SX, Wang X, Lu QB, Shi LS, Ren X, Zhang HY, Wang YF, Lin SH, Zhang CH, et al. Etiological, epidemiological, and clinical features of acute diarrhea in China. Nat Commun. 2021;12:2464.PubMedPubMedCentralCrossRef
38.
go back to reference Zhou HL, Zhen SS, Wang JX, Zhang CJ, Qiu C, Wang SM, Jiang X, Wang XY. Burden of acute gastroenteritis caused by norovirus in China: a systematic review. J Infect. 2017;75:216–24.PubMedCrossRef Zhou HL, Zhen SS, Wang JX, Zhang CJ, Qiu C, Wang SM, Jiang X, Wang XY. Burden of acute gastroenteritis caused by norovirus in China: a systematic review. J Infect. 2017;75:216–24.PubMedCrossRef
39.
go back to reference Utsumi T, Lusida MI, Dinana Z, Wahyuni RM, Yamani LN, Juniastuti, Soetjipto, Matsui C, Deng L, Abe T, et al. Occurrence of norovirus infection in an asymptomatic population in Indonesia. Infect Genet Evol. 2017;55:1–7. Utsumi T, Lusida MI, Dinana Z, Wahyuni RM, Yamani LN, Juniastuti, Soetjipto, Matsui C, Deng L, Abe T, et al. Occurrence of norovirus infection in an asymptomatic population in Indonesia. Infect Genet Evol. 2017;55:1–7.
41.
go back to reference Parker SP, Cubitt WD, Jiang X. Enzyme immunoassay using baculovirus-expressed human calicivirus (Mexico) for the measurement of IgG responses and determining its seroprevalence in London, UK. J Med Virol. 1995;46:194–200.PubMedCrossRef Parker SP, Cubitt WD, Jiang X. Enzyme immunoassay using baculovirus-expressed human calicivirus (Mexico) for the measurement of IgG responses and determining its seroprevalence in London, UK. J Med Virol. 1995;46:194–200.PubMedCrossRef
42.
go back to reference Parker SP, Cubitt WD, Jiang XJ, Estes MK. Seroprevalence studies using a recombinant Norwalk virus protein enzyme immunoassay. J Med Virol. 1994;42:146–50.PubMedCrossRef Parker SP, Cubitt WD, Jiang XJ, Estes MK. Seroprevalence studies using a recombinant Norwalk virus protein enzyme immunoassay. J Med Virol. 1994;42:146–50.PubMedCrossRef
43.
go back to reference Vielot NA, Brinkman A, DeMaso C, Vilchez S, Lindesmith LC, Bucardo F, Reyes Y, Baric RS, Ryan EP, Braun R, Becker-Dreps S. Breadth and dynamics of human norovirus-specific antibodies in the first year of life. J Pediatric Infect Dis Soc. 2022;11:463–6.PubMedPubMedCentralCrossRef Vielot NA, Brinkman A, DeMaso C, Vilchez S, Lindesmith LC, Bucardo F, Reyes Y, Baric RS, Ryan EP, Braun R, Becker-Dreps S. Breadth and dynamics of human norovirus-specific antibodies in the first year of life. J Pediatric Infect Dis Soc. 2022;11:463–6.PubMedPubMedCentralCrossRef
44.
go back to reference Jing Y, Qian Y, Huo Y, Wang LP, Jiang X. Seroprevalence against Norwalk-like human caliciviruses in Beijing, China. J Med Virol. 2000;60:97–101.PubMedCrossRef Jing Y, Qian Y, Huo Y, Wang LP, Jiang X. Seroprevalence against Norwalk-like human caliciviruses in Beijing, China. J Med Virol. 2000;60:97–101.PubMedCrossRef
45.
go back to reference Zhang S, Chen TH, Wang J, Dong C, Pan J, Moe C, Chen W, Yang L, Wang X, Tang H, et al. Symptomatic and asymptomatic infections of rotavirus, norovirus, and adenovirus among hospitalized children in Xi’an, China. J Med Virol. 2011;83:1476–84.PubMedCrossRef Zhang S, Chen TH, Wang J, Dong C, Pan J, Moe C, Chen W, Yang L, Wang X, Tang H, et al. Symptomatic and asymptomatic infections of rotavirus, norovirus, and adenovirus among hospitalized children in Xi’an, China. J Med Virol. 2011;83:1476–84.PubMedCrossRef
46.
go back to reference Zweigart MR, Becker-Dreps S, Bucardo F, Gonzalez F, Baric RS, Lindesmith LC. Serological humoral immunity following natural infection of children with high burden gastrointestinal viruses. Viruses. 2021;13:2023.CrossRef Zweigart MR, Becker-Dreps S, Bucardo F, Gonzalez F, Baric RS, Lindesmith LC. Serological humoral immunity following natural infection of children with high burden gastrointestinal viruses. Viruses. 2021;13:2023.CrossRef
47.
go back to reference Labayo HKM, Pajuelo MJ, Tohma K, Ford-Siltz LA, Gilman RH, Cabrera L, Mayta H, Sanchez GJ, Cornejo AT, Bern C, et al. Norovirus-specific immunoglobulin A in breast milk for protection against norovirus-associated diarrhea among infants. EClinicalMedicine. 2020;27: 100561.PubMedPubMedCentralCrossRef Labayo HKM, Pajuelo MJ, Tohma K, Ford-Siltz LA, Gilman RH, Cabrera L, Mayta H, Sanchez GJ, Cornejo AT, Bern C, et al. Norovirus-specific immunoglobulin A in breast milk for protection against norovirus-associated diarrhea among infants. EClinicalMedicine. 2020;27: 100561.PubMedPubMedCentralCrossRef
48.
go back to reference Newman KL, Moe CL, Kirby AE, Flanders WD, Parkos CA, Leon JS. Norovirus in symptomatic and asymptomatic individuals: cytokines and viral shedding. Clin Exp Immunol. 2016;184:347–57.PubMedPubMedCentralCrossRef Newman KL, Moe CL, Kirby AE, Flanders WD, Parkos CA, Leon JS. Norovirus in symptomatic and asymptomatic individuals: cytokines and viral shedding. Clin Exp Immunol. 2016;184:347–57.PubMedPubMedCentralCrossRef
49.
go back to reference Teunis PF, Sukhrie FH, Vennema H, Bogerman J, Beersma MF, Koopmans MP. Shedding of norovirus in symptomatic and asymptomatic infections. Epidemiol Infect. 2015;143:1710–7.PubMedCrossRef Teunis PF, Sukhrie FH, Vennema H, Bogerman J, Beersma MF, Koopmans MP. Shedding of norovirus in symptomatic and asymptomatic infections. Epidemiol Infect. 2015;143:1710–7.PubMedCrossRef
50.
go back to reference Jeong MH, Song YH, Ju SY, Kim SH, Kwak HS, An ES. Surveillance to prevent the spread of norovirus outbreak from asymptomatic food handlers during the PyeongChang 2018 Olympics. J Food Prot. 2021;84:1819–23.PubMedCrossRef Jeong MH, Song YH, Ju SY, Kim SH, Kwak HS, An ES. Surveillance to prevent the spread of norovirus outbreak from asymptomatic food handlers during the PyeongChang 2018 Olympics. J Food Prot. 2021;84:1819–23.PubMedCrossRef
51.
go back to reference Wu QS, Xuan ZL, Liu JY, Zhao XT, Chen YF, Wang CX, Shen XT, Wang YX, Wang L, Hu Y. Norovirus shedding among symptomatic and asymptomatic employees in outbreak settings in Shanghai, China. BMC Infect Dis. 2019;19:592.PubMedPubMedCentralCrossRef Wu QS, Xuan ZL, Liu JY, Zhao XT, Chen YF, Wang CX, Shen XT, Wang YX, Wang L, Hu Y. Norovirus shedding among symptomatic and asymptomatic employees in outbreak settings in Shanghai, China. BMC Infect Dis. 2019;19:592.PubMedPubMedCentralCrossRef
52.
go back to reference Ozawa K, Oka T, Takeda N, Hansman GS. Norovirus infections in symptomatic and asymptomatic food handlers in Japan. J Clin Microbiol. 2007;45:3996–4005.PubMedPubMedCentralCrossRef Ozawa K, Oka T, Takeda N, Hansman GS. Norovirus infections in symptomatic and asymptomatic food handlers in Japan. J Clin Microbiol. 2007;45:3996–4005.PubMedPubMedCentralCrossRef
53.
go back to reference Allen DJ, Adams NL, Aladin F, Harris JP, Brown DW. Emergence of the GII-4 norovirus Sydney 2012 strain in England, winter 2012–2013. PLoS ONE. 2014;9: e88978.PubMedPubMedCentralCrossRef Allen DJ, Adams NL, Aladin F, Harris JP, Brown DW. Emergence of the GII-4 norovirus Sydney 2012 strain in England, winter 2012–2013. PLoS ONE. 2014;9: e88978.PubMedPubMedCentralCrossRef
54.
go back to reference Fu J, Ai J, Bao C, Zhang J, Wu Q, Zhu L, Hu J, Xing Z. Evolution of the GII.3[P12] norovirus from 2010 to 2019 in Jiangsu, China. Gut Pathog. 2021;13:34.PubMedPubMedCentralCrossRef Fu J, Ai J, Bao C, Zhang J, Wu Q, Zhu L, Hu J, Xing Z. Evolution of the GII.3[P12] norovirus from 2010 to 2019 in Jiangsu, China. Gut Pathog. 2021;13:34.PubMedPubMedCentralCrossRef
55.
go back to reference Zhu X, He Y, Wei X, Kong X, Zhang Q, Li J, Jin M, Duan Z. Molecular epidemiological characteristics of gastroenteritis outbreaks caused by norovirus GII4 Sydney [P31] strains - China, October 2016–December 2020. China CDC Wkly. 2021;3:1127–32.PubMedPubMedCentralCrossRef Zhu X, He Y, Wei X, Kong X, Zhang Q, Li J, Jin M, Duan Z. Molecular epidemiological characteristics of gastroenteritis outbreaks caused by norovirus GII4 Sydney [P31] strains - China, October 2016–December 2020. China CDC Wkly. 2021;3:1127–32.PubMedPubMedCentralCrossRef
56.
go back to reference Lun JH, Hewitt J, Yan GJH, Enosi Tuipulotu D, Rawlinson WD, White PA. Recombinant GII.P16/GII.4 Sydney 2012 was the dominant norovirus identified in Australia and New Zealand in 2017. Viruses. 2018;10:548.PubMedPubMedCentralCrossRef Lun JH, Hewitt J, Yan GJH, Enosi Tuipulotu D, Rawlinson WD, White PA. Recombinant GII.P16/GII.4 Sydney 2012 was the dominant norovirus identified in Australia and New Zealand in 2017. Viruses. 2018;10:548.PubMedPubMedCentralCrossRef
58.
go back to reference Lindesmith LC, Costantini V, Swanstrom J, Debbink K, Donaldson EF, Vinje J, Baric RS. Emergence of a norovirus GII.4 strain correlates with changes in evolving blockade epitopes. J Virol. 2013;87:2803–13.PubMedPubMedCentralCrossRef Lindesmith LC, Costantini V, Swanstrom J, Debbink K, Donaldson EF, Vinje J, Baric RS. Emergence of a norovirus GII.4 strain correlates with changes in evolving blockade epitopes. J Virol. 2013;87:2803–13.PubMedPubMedCentralCrossRef
59.
go back to reference Donaldson EF, Lindesmith LC, Lobue AD, Baric RS. Viral shape-shifting: norovirus evasion of the human immune system. Nat Rev Microbiol. 2010;8:231–41.PubMedPubMedCentralCrossRef Donaldson EF, Lindesmith LC, Lobue AD, Baric RS. Viral shape-shifting: norovirus evasion of the human immune system. Nat Rev Microbiol. 2010;8:231–41.PubMedPubMedCentralCrossRef
60.
61.
go back to reference Deval J, Jin Z, Chuang YC, Kao CC. Structure(s), function(s), and inhibition of the RNA-dependent RNA polymerase of noroviruses. Virus Res. 2017;234:21–33.PubMedCrossRef Deval J, Jin Z, Chuang YC, Kao CC. Structure(s), function(s), and inhibition of the RNA-dependent RNA polymerase of noroviruses. Virus Res. 2017;234:21–33.PubMedCrossRef
63.
64.
go back to reference Smertina E, Urakova N, Strive T, Frese M. Calicivirus RNA-dependent RNA polymerases: evolution, structure, protein dynamics, and function. Front Microbiol. 2019;10:1280.PubMedPubMedCentralCrossRef Smertina E, Urakova N, Strive T, Frese M. Calicivirus RNA-dependent RNA polymerases: evolution, structure, protein dynamics, and function. Front Microbiol. 2019;10:1280.PubMedPubMedCentralCrossRef
65.
Metadata
Title
Molecular epidemiology analysis of symptomatic and asymptomatic norovirus infections in Chinese infants
Authors
Li-Na Chen
Si-Jie Wang
Song-Mei Wang
Xiao-Li Fu
Wen-Jing Zheng
Zhi-Yong Hao
Hai-Song Zhou
Xin-Jiang Zhang
Yu-Liang Zhao
Chao Qiu
Lorenz von Seidlein
Tian-Yi Qiu
Xuan-Yi Wang
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2023
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-023-02024-z

Other articles of this Issue 1/2023

Virology Journal 1/2023 Go to the issue