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Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

CN 11-5983/R

Postal Subscription Code 80-967

2018 Impact Factor: 1.847

Front. Med.    2020, Vol. 14 Issue (1) : 1-7
The epidemiology of norovirus gastroenteritis in China: disease burden and distribution of genotypes
Honglu Zhou1, Songmei Wang2, Lorenz von Seidlein3,4, Xuanyi Wang1,5()
1. Key Laboratory of Medical Molecular Virology of MoE & MoH, and Institutes of Biomedical Sciences, Fudan University, Shanghai 200032, China
2. Laboratory of Molecular Biology, Training Center of Medical Experiments, School of Basic Medical Sciences, Fudan University, Shanghai 200032, China
3. Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand
4. Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford OX1 2JD, UK
5. Children’s Hospital, Fudan University, Shanghai 200032, China
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With the improvements of sanitation and nationwide safe water supply the occurrence of bacterial diarrhea declined remarkably, while viruses became the leading causes of acute gastroenteritis (AGE). Of these viruses, noroviruses (NoVs) are responsible for a considerable burden of gastroenteritis, especially in children<2 years and elderly≥65 years. NoVs circulating in the Chinese population are antigenically highly diverse with the genotype GII.4 being the dominant strain followed by GII.3. Given the widespread contamination in environmental sources, and highly infectious nature of NoVs, vaccination would be the desirable strategy for the control of NoV infections. However, a better understanding of acquired immunity after infection, and a reliable immunological surrogate marker are urgently needed, since two vaccine candidates based on virus-like particles (VLPs) are currently moving into clinical evaluations in China.

Keywords molecular epidemiology      norovirus      disease burden      genotype      China     
Corresponding Author(s): Xuanyi Wang   
Just Accepted Date: 19 November 2019   Online First Date: 11 December 2019    Issue Date: 02 March 2020
 Cite this article:   
Honglu Zhou,Songmei Wang,Lorenz von Seidlein, et al. The epidemiology of norovirus gastroenteritis in China: disease burden and distribution of genotypes[J]. Front. Med., 2020, 14(1): 1-7.
Genotype Sources of data and study design
(hospital-based and outbreaks surveys)
(hospital-based surveys)
(population-based surveillance)
(population-based surveillance)
GI.1 1.6 0.6
GI.2 3.4 2.3
GI.3 2.2 1.7
GI.4 1.4 1.8 0.6
GI.5 2.1 1.4
GI.6 0.7 1.3
GI.7 0.1 1.3
GI.8 0.8 0.8
GI.9 0.2 1.6
GII.1 0.1 2.8
GII.2 0.9 0.8 7.5
GII.3 7.7 9.5 32.5
GII.4 50.1 49.7 30.0 37.7
GII.5 0.1 2.4
GII.6 3.2 1.5 2.5 39.3
GII.7 0.7 0.4 0.6 4.9
GII.8 0.03 0.5
GII.10 0.8
GII.11 1.7
GII.12 3.4 2.4
GII.13 1.2 1.7
GII.14 0.2 0.4
GII.15 0.1 0.6
GII.16 0.1 0.5
GII.17 10.9 8.4 3.3
GII.18 0.6
GII.21 1.2 0.4
GII.22 0.03 0.8
Others 7.46 2.8 26.3 13.1
Tab.1  Genotypes distribution of norovirus by study design in China
Fig.1  The detection rates of norovirus from different sources by seasonality.
1 United Nations Inter-agency Group for Child Mortality Estimation (UN IGME). Levels and trends in child mortality: report 2017, Estimates Developed by the UN Inter-agency Group for Child Mortality Estimation. New York: United Nations Children’s Fund, 2017
2 SM Ahmed, AJ Hall, AE Robinson, L Verhoef, P Premkumar, UD Parashar, M Koopmans, BA Lopman. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis 2014; 14(8): 725–730 pmid: 24981041
3 BA Lopman, D Steele, CD Kirkwood, UD Parashar. The vast and varied global burden of norovirus: prospects for prevention and control. PLoS Med 2016; 13(4): e1001999 pmid: 27115709
4 JJ Siebenga, H Vennema, DP Zheng, J Vinjé, BE Lee, XL Pang, EC Ho, W Lim, A Choudekar, S Broor, T Halperin, NB Rasool, J Hewitt, GE Greening, M Jin, ZJ Duan, Y Lucero, M O’Ryan, M Hoehne, E Schreier, RM Ratcliff, PA White, N Iritani, G Reuter, M Koopmans. Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001–2007. J Infect Dis 2009; 200(5): 802–812 pmid: 19627248
5 TN Hoa Tran, E Trainor, T Nakagomi, NA Cunliffe, O Nakagomi. 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(3): 269–277 pmid: 23218993
6 Division of Infectious Disease Chinese Center for Disease Control and Prevention. National Data of Class A, B and C Communicable Diseases in December 2017. Dis Surveill (Ji Bing Jian Ce) 2018; 33(1): 1 (in Chinese)
7 P Zhang, J Zhang. Surveillance on other infectious diarrheal diseases in China from 2014 to 2015. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2017; 38(4): 424–430 (in Chinese)
pmid: 28468056
8 HL Zhou, SS Zhen, JX Wang, CJ Zhang, C Qiu, SM Wang, X Jiang, XY Wang. Burden of acute gastroenteritis caused by norovirus in China: a systematic review. J Infect 2017; 75(3): 216–224 pmid: 28633888
9 RA Bull, PA White. Mechanisms of GII.4 norovirus evolution. Trends Microbiol 2011; 19(5): 233–240 pmid: 21310617
10 MJ Conley, M McElwee, L Azmi, M Gabrielsen, O Byron, IG Goodfellow, D Bhella. Calicivirus VP2 forms a portal-like assembly following receptor engagement. Nature 2019; 565(7739): 377–381 pmid: 30626974
11 J Vinjé. Advances in laboratory methods for detection and typing of norovirus. J Clin Microbiol 2015; 53(2): 373–381 pmid: 24989606
12 R Wyllie, JS Hyams, M Kay. Pediatric Gastrointestinal and Liver Disease (Fourth Edition). Elsevier Saunders,USA. 2011405–408
13 PF Teunis, FH Sukhrie, H Vennema, J Bogerman, MF Beersma, MP Koopmans. Shedding of norovirus in symptomatic and asymptomatic infections. Epidemiol Infect 2015; 143(8): 1710–1717 pmid: 25336060
14 AJ Hall. Noroviruses: the perfect human pathogens? J Infect Dis 2012; 205(11): 1622–1624 pmid: 22573872
15 MM Patel, AJ Hall, J Vinjé, UD Parashar. Noroviruses: a comprehensive review. J Clin Virol 2009; 44(1): 1–8 pmid: 19084472
16 B Imhoff, D Morse, B Shiferaw, M Hawkins, D Vugia, S Lance-Parker, J Hadler, C Medus, M Kennedy, MR Moore, T Van Gilder; Emerging Infections Program FoodNet Working Group. Burden of self-reported acute diarrheal illness in FoodNet surveillance areas, 1998-1999. Clin Infect Dis 2004; 38(Suppl 3): S219–S226 pmid: 15095193
17 J Yu, C Ye, S Lai, W Zhu, Z Zhang, Q Geng, C Xue, W Yang, S Wu, AJ Hall, Q Sun, Z Li. Incidence of norovirus-associated diarrhea, Shanghai, China, 2012–2013. Emerg Infect Dis 2017; 23(2): 312–315 pmid: 28098539
18 JX Wang, HL Zhou, ZJ Mo, SM Wang, ZY Hao, Y Li, SS Zhen, CJ Zhang, XJ Zhang, JC Ma, C Qiu, G Zhao, BM Jiang, X Jiang, RC Li, YL Zhao, XY Wang. Burden of viral gastroenteritis in children living in rural China: population-based surveillance. Int J Infect Dis 2019 October 28. [Epub ahead of print] doi:10.1016/j.ijid.2019.10.029.
19 J Yu, S Lai, X Wang, Q Liao, L Feng, L Ran, W Xu, Y Qiu, Z Zhang, M Li, J Wu, W Liu, Z Yuan, Y Chen, S Zhao, X Wang, Z Zhao, H Yu, H Jing, Z Li, W Yang. Analysis of epidemiology characteristics of norovirus among diarrheal outpatients in 27 provinces in China, 2009−2013. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2015; 36(3): 199–204 (in Chinese)
pmid: 25975393
20 Y Lian, S Wu, L Luo, B Lv, Q Liao, Z Li, JJ Rainey, AJ Hall, L Ran. Epidemiology of norovirus outbreaks reported to the Public Health Emergency Event Surveillance System, China, 2014–2017. Viruses 2019; 11(4): E342 pmid: 30979014
21 K Simmons, M Gambhir, J Leon, B Lopman. Duration of immunity to norovirus gastroenteritis. Emerg Infect Dis 2013; 19(8): 1260–1267 pmid: 23876612
22 XJ Song, J Zhang, GQ Shi. Epidemiological characteristics of acute gastroenteritis outbreaks caused by norovirus in China, 2000–2013. Dis Surveill (Ji Bing Jian Ce) 2017; 32(2): 127–131 (in Chinese)
23 AP Fan, AH Zhang, J Lie. Systematic evaluation of literatures on epidemiological characteristics of viral diarrhea outbreaks in China. Mod Prev Med (Xian Dai Yu Fang Yi Xue) 2016; 43(6): 965–978 (in Chinese)
24 JS Li, AP Deng, YL Mo, H Li, LM Sun. A Norovirus caused gastroenteritis outbreak in a nursing home in Guangdong. Dis Surveill (Ji Bing Jian Ce) 2015; 30(3): 242–244 (in Chinese)
25 J Yi, K Wahl, BK Sederdahl, RR Jerris, CS Kraft, C McCracken, S Gillespie, EJ Anderson, AE Kirby, AL Shane, CL Moe. Molecular epidemiology of norovirus in children and the elderly in Atlanta, Georgia, United States. J Med Virol 2016; 88(6): 961–970 pmid: 26600094
26 AJ Hall, BA Lopman, DC Payne, MM Patel, PA Gastañaduy, J Vinjé, UD Parashar. Norovirus disease in the United States. Emerg Infect Dis 2013; 19(8): 1198–1205 pmid: 23876403
27 Shanghai Municipal Statistics Bureau, Survey Office of the National Bureau of Statistics in Shanghai. 2018 Shanghai Statistical Yearbook. Beijing: China Statistics Press, 2018
28 AL Corwin, R Soderquist, M Edwards, A White, J Beecham, P Mills, RP Larasati, D Subekti, T Ansari, J Burans, B Oyofo. Shipboard impact of a probable Norwalk virus outbreak from coastal Japan. Am J Trop Med Hyg 1999; 61(6): 898–903 pmid: 10674667
29 MS Bailey, CI Gallimore, LD Lines, AD Green, BA Lopman, JJ Gray, DW Brown. Viral gastroenteritis outbreaks in deployed British troops during 2002-7. J R Army Med Corps 2008; 154(3): 156–159 pmid: 19202819
30 A Mayet, V Andreo, G Bedubourg, S Victorion, J Plantec, B Soullie, J Meynard, J Dedieu, P Polveche, R Migliani. Food-borne outbreak of norovirus infection in a French military parachuting unit, April 2011. Euro Surveill 2011; 16(30): pii.19930
31 FJX Neo, JJP Loh, P Ting, WX Yeo, CQH Gao, VJM Lee, BH Tan, CG Ng. Outbreak of caliciviruses in the Singapore military, 2015. BMC Infect Dis 2017; 17(1): 719 pmid: 29137606
32 WX Yang, HD Shi, L Yao, XL Wang, H Shen, QJ Shen, LL Song, XB He. Prevention and treatment of an norovirus outbreak in a military base. Mil Med J Southeast Chin (Dong Nan Guo Fang Yi Yao) 2019; 21(1): 87–88 (in Chinese)
33 P Wang, WB Goggins, EYY Chan. 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: 414–422 pmid: 29940452
34 E Robilotti, S Deresinski, BA Pinsky. Norovirus. Clin Microbiol Rev 2015; 28(1): 134–164 pmid: 25567225
35 SW Sang, ZT Zhao, JJ Suo, YB Xing, N Jia, Y Gao, MM Du, LJ Xie, CY Deng, SW Ren, YX Liu. Characteristics of outbreak and epidmeiology of norovirus gastroenteritis in China. Chin J Nosocomiology (Zhong Hua Yi Yuan Gan Ran Xue Za Zhi) 2011; 21(20): 4245–4247 (in Chinese)
36 N Qiao, H Ren, L Liu. Genomic diversity and phylogeography of norovirus in China. BMC Med Genomics 2017; 10(Suppl 3): 51 pmid: 28984198
37 N Qiao, XY Wang, L Liu. Temporal evolutionary dynamics of norovirus GII.4 variants in China between 2004 and 2015. PLoS One 2016; 11(9): e0163166 pmid: 27649572
38 Y Ao, J Wang, H Ling, Y He, X Dong, X Wang, J Peng, H Zhang, M Jin, Z Duan. Norovirus GII.P16/GII.2-associated gastroenteritis, China, 2016. Emerg Infect Dis 2017; 23(7): 1172–1175 pmid: 28430563
39 K Kwok, S Niendorf, N Lee, TN Hung, LY Chan, S Jacobsen, EAS Nelson, TF Leung, RWM Lai, PKS Chan, MCW Chan. 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): 1852–1855 pmid: 29048294
40 YY Ao, X Cong, M Jin, XM Sun, JJ Wang, Q Zhang, J Song, JM Yu, J Cui, JX Qi, M Tian, ZJ Duan. Genetic analysis of reemerging GII.P16-GII.2 noroviruses in 2016–2017 in China. J Infect Dis 2018; 218(1): 133–143 pmid: 28585917
41 J Lu, L Fang, L Sun, H Zeng, Y Li, H Zheng, S Wu, F Yang, T Song, J Lin, C Ke, Y Zhang, J Vinjé, H Li. Association of GII.P16-GII.2 recombinant norovirus strain with increased norovirus outbreaks, Guangdong, China, 2016. Emerg Infect Dis 2017; 23(7): 1188– 1190 pmid: 28430561
42 H Liang, Q Jiang, GW Dai, YL Mo, L Fang, H Li, J Wen, XQ Lin, ZK Hu, XL Deng, Q Huang, YH Zhang. Survey on norovirus contamination in commercial oysters in Guangdong Province from 2011 to 2012. Chin J Food Hygi (Zhong Guo Shi Pin Wei Sheng Za Zhi) 2013; 25(4): 359–362 (in Chinese)
43 H Ming, J Fan, L Wu, L Yue, X Gao, Y Liang. Contamination of typical human enteric viruses in economic shellfish along the Chinese coast. Acta Microbiologica Sinica (Wei Sheng Wu Xue Bao) 2014; 54(1): 69–79 (in Chinese)
pmid: 24783856
44 Y Wang, X Yan, C Shi, J Zhang. Monitoring and analysis of Norovirus in lettuce and strawberry from markets in Qinhuangdao. Food Safe Qual Detec Technol (Shi Pin An Quan Zhi Liang Jian Ce Xue Bao) 2018; 9(22): 6059–6063 (in Chinese)
45 L Luo, XW Wu, YF Liu, QY Li, HP Xie, YJ Wu, L Li, LY Jiang, X Yang. The molecular epidemiology characteristics of norovirus in environment and clinical samples in Guangzhou from 2009 to 2011. Chin J Prev Med (Zhonghua Yu Fang Yi Xue Za Zhi) 2013; 47(1): 40–43 (in Chinese)
pmid: 23601521
46 SS Liu, ZX Tao, ST Wang, N Zhou, XJ Lin, YY Song, AQ Xu. Norovirus molecular epidmeiology based on environmental sewage surveillance. Chin J Virol (Bing Du Xue Bao) 2018; 34(3): 342–348 (in Chinese)
47 TL Chen, XQ Deng. Investigation of environmental sample virus contamination in the norovirus epidemic. Chin J Child Heal Care (Zhongguo Er Tong Bao Jian Za Zhi) 2018; 26(8): 921–923 (in Chinese)
48 AN Wang, XW Zhong, L Qin, Z Wang, RF Chen, H Lin, Q Huang, YH Zhang. Circulation routes of norovirus among population and environment in coastal area. S China J Prev Med 2016; 42(2): 101–107
49 L Bonifait, R Charlebois, A Vimont, N Turgeon, M Veillette, Y Longtin, J Jean, C Duchaine. Detection and quantification of airborne norovirus during outbreaks in healthcare facilities. Clin Infect Dis 2015; 61(3): 299–304 pmid: 25900175
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