Prevalence and Etiological Characteristics of Norovirus Infection in China: A Systematic Review and Meta-Analysis

Abstract

Norovirus is a common cause of sporadic cases and outbreaks of gastroenteritis worldwide, although its prevalence and the dominant genotypes responsible for gastroenteritis outbreaks remain obscure. A systematic review was conducted on norovirus infection in China between January 2009 and March 2021. A meta-analysis and beta-binomial regression model were used to explore the epidemiological and clinical characteristics of norovirus infection and the potential factors contributing to the attack rate of the norovirus outbreaks, respectively. A total of 1132 articles with 155,865 confirmed cases were included, with a pooled positive test rate of 11.54% among 991,786 patients with acute diarrhea and a pooled attack rate of 6.73% in 500 norovirus outbreaks. GII.4 was the predominant genotype in both the etiological surveillance and outbreaks, followed by GII.3 in the etiological surveillance, and GII.17 in the outbreaks, with the proportion of recombinant genotypes increasing in recent years. A higher attack rate in the norovirus outbreaks was associated with age group (older adults), settings (nurseries, primary schools, etc.) and region (North China). The nation-wide pooled positive rate in the etiological surveillance of norovirus is lower than elsewhere in the global population, while the dominant genotypes are similar in both the etiological surveillance and the outbreak investigations. This study contributes to the understanding of norovirus infection with different genotypes in China. The prevention and control of norovirus outbreaks during the cold season should be intensified, with special attention paid to and enhanced surveillance performed in nurseries, schools and nursing homes from November to March.

Keywords: China; etiological characteristics; meta-analysis; norovirus.

Figure 1

Flow diagram of the literature review. CNKI: China National Knowledge Infrastructure; Wanfang: Wanfang Database; CQVIP: Chongqing VIP Chinese Science and Technology Journal Database.

Figure 2

Temporal distribution of reported norovirus infections and genotypes in China. (A) number of articles, outbreaks and reported cases infected with norovirus over the publication year. (B) genotype of norovirus reported from studies on etiological surveillance and outbreak investigation over the publication year. Numbers in parentheses indicate the number of outbreaks. * Includes GI.2, GI.3, GI.4, GI.5, GI.7, GI.8, GI.9, and GI.Pd. # Includes GII.1, GII.P1, GII.P2, GII.P3, GII.P4, GII.5, GII.P5, GII.6, GII.P6, GII.7, GII.P7, GII.8, GII.P8, GII.10, GII.11, GII.P12, GII.13, GII.P13, GII.14, GII.15, GII.16, GII.P16, GII.P17, GII.21, GII.P21, GII.22, GII.P22, GII.P31, GII.b, GII.e, GII.g and GII.Pg.

Figure 3

Characteristics of the distribution of norovirus outbreaks in China by region, age and setting. Number of outbreaks and attack rate estimated using meta-analysis based on outbreak investigations between North and South China by year (A), month (B), monthly number of outbreaks and attack rate estimated using meta-analysis based on outbreak investigations by age (C) and setting (D). N (n) indicates the number of articles (outbreaks) included in this analysis. For the attack rate, the mean and a 95% CI are presented. * Indicates either a quite high mean attack rate or a wide 95% CI, which was presented in North China in 2012 (3.79% [95% CI: 0.42, 26.85]), in 2019 (17.39% [95% CI: 14.46, 20.76]), in February (17.68% [95% CI: 9.34, 30.93]), in older adults in February (27.85% [95% CI: 17.96, 37.73]), in children in May (17.70% [95% CI: 9.44, 30.73]), at restaurants in February (12.58% [95% CI: 2.86, 41.30]) and March (12.90% [95% CI: 0.70, 75.79]), at a community in May (40.54%), at workplaces in February (79.41%) and April (20.01% [95% CI: 8.36, 40.71]). ^§ Indicates households, transportations, welfares, military settings, prisons, multiple setting types and multiple school types on panel D.

Figure 4

Genotype characteristics of norovirus outbreaks in China by region, age and setting. The monthly number of outbreaks and the attack rate were estimated using a meta-analysis based on the outbreak investigation by virus genotypes (A), and the numbers of outbreaks and reported cases for different norovirus genotypes norovirus by region (B), by age (C), and setting (D). N (n) indicates the number of articles (outbreaks) included in this analysis. For the attack rate, the mean and a 95% CI are presented. * Indicates either a quite high mean attack rate or a wide 95% CI, which was presented for GII.2 in North China (15.94% [95% CI: 4.37, 44.04]), for GII.12 in North China (43.52%). ^# Indicates GI.2, GI.3, GI.5, GII.6, GII.7, GII.8, GII.14, and GII.21 on panel A, panel B, and panel D and GI.3, GI.5, GII.6, GII.7, GII.8, GII.14, and GII.21 on panel C. ^§ Indicates households, transportations, welfares, military settings, prisons, multiple setting types and multiple school types on panel D.