渔业科学进展  2023, Vol. 44 Issue (6): 177-189  DOI: 10.19663/j.issn2095-9869.20220519003
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引用本文 

蔡淑珍, 李贻静, 薛亮, 高珺珊, 蔡伟程, 徐明芳, 吴清平, 张菊梅. 我国贝类中人源诺如病毒检出状况的荟萃分析[J]. 渔业科学进展, 2023, 44(6): 177-189. DOI: 10.19663/j.issn2095-9869.20220519003.
CAI Shuzhen, LI Yijing, XUE Liang, GAO Junshan, CAI Weicheng, XU Mingfang, WU Qingping, ZHANG Jumei. Detection of Human Noroviruses in Shellfish in China: A Meta-Analysis[J]. Progress in Fishery Sciences, 2023, 44(6): 177-189. DOI: 10.19663/j.issn2095-9869.20220519003.

基金项目

国家自然科学基金资助项目(31872912); 广东省自然科学基金杰出青年基金项目(2019B151502065); 广东省重点领域研发计划项目(2019B020209001)共同资助

作者简介

蔡淑珍, E-mail: 240793907@qq.com;
李贻静, E-mail: 13707892738@163.com

通讯作者

薛亮, 研究员, E-mail: xueliang@gdim.cn
张菊梅, 研究员, E-mail: zhangjm926@126.com

文章历史

收稿日期:2022-05-19
收修改稿日期:2022-06-06
我国贝类中人源诺如病毒检出状况的荟萃分析
蔡淑珍 1#, 李贻静 1,2#, 薛亮 1, 高珺珊 1, 蔡伟程 1, 徐明芳 2, 吴清平 1, 张菊梅 1     
1. 广东省科学院微生物研究所 华南应用微生物国家重点实验室 广东省微生物安全与健康重点实验室 农业农村部农业微生物组学与精准应用重点实验室 广东 广州 510070;
2. 暨南大学生命科学技术学院 广东 广州 510632
摘要:人源诺如病毒(Human Noroviruses, HuNoVs)是引发食品安全事件的重要病原微生物。贝类为滤食性动物,是HuNoVs污染传播的重要媒介。本研究搜集了我国贝类污染调查的横断面研究文献,综合评价了贝类中HuNoVs的污染现状。通过检索中国知网、维普、万方、中国生物医学文献数据库、PubMed和EMbase数据库,从所获得的600篇关于贝类污染HuNoVs相关文献中筛选纳入37篇。采用Stata 14.0软件进行荟萃分析,结果显示,我国贝类中不同基因型HuNoVs的混合检出率达15% (95% CI: 11%~18%)。亚组分析显示,GⅡ基因群检出率(11%)高于GⅠ基因群(4%);地理位置对贝类中病毒污染水平影响显著(P < 0.01),华南地区、华北地区、华东地区的检出率分别达到19%、17%和11%,而东北和西北地区则分别为4%和9%;此外,季节差异明显,其中,冬季的病毒检出率最高(25%),而夏季仅为10%,春季、秋季则分别为16%和12%;不同品种贝类的病毒污染同样存在差异,其中,牡蛎(Ostreidae) (16%)、贻贝(Mytilus edulis) (10%)和蛤(Mactridae)(9%)中病毒检出率居前三。综上所述,我国贝类中HuNoVs污染较为普遍,地区、季节、贝类品种等因素均对病毒污染存在显著影响。本研究结果有助于综合掌握我国贝类中食源性病毒污染现状,为精准防控食源性HuNoVs传播提供研判依据,促进贝类产业的高质量发展。
关键词中国    贝类    人源诺如病毒    检出率    荟萃分析    横断面研究    
Detection of Human Noroviruses in Shellfish in China: A Meta-Analysis
CAI Shuzhen 1#, LI Yijing 1,2#, XUE Liang 1, GAO Junshan 1, CAI Weicheng 1, XU Mingfang 2, WU Qingping 1, ZHANG Jumei 1     
1. Guangdong Provincial Key Laboratory of Microbial Safety and Health, State Key Laboratory of Applied Microbiology Southern China, Institute of Microbiology, Guangdong Academy of Sciences, Laboratory of Agricultural Microbiomics and Precision Application, Ministry of Agriculture and Rural Affairs, Guangzhou 510070, China;
2. College of Life Science and Technology, Jinan University, Guangzhou 510632, China
Abstract: Human norovirus (HuNoV) is a non-enveloped, single-stranded, positive-stranded RNA virus belonging to the family Caliciviridae. HuNoVs are important pathogenic microorganisms responsible for causing food safety incidents. Numerous species of shellfish are characterized by their abundant nutritional value, excellent healthcare function, and a high economic value. As a filter-feeding animal, shellfish filter the seawater at a rate of 4–20 L per hour and ingest microalgae to meet their physiological needs. Additionally, shellfish are able to continuously accumulate viruses from seawater into their bodies, resulting in a concentration ten or even thousand times higher in their tissues than in the environment. In recent years, more attention has been paid to HuNoV contamination in shellfish in China, and related monitoring studies have been conducted in different areas. However, most of these studies focused on a certain region in a certain period of time, and some species, which are not conducive to a comprehensive understanding of the overall prevalence of HuNoVs in shellfish in China. Meta-analysis refers to the methods which focus on contrasting and combining results from different studies for identifying patterns among the study results or other interesting relationships that may come to light in the context of multiple studies. This study aimed to collect cross-sectional data on the studies conducted on shellfish contamination in China. The search terms used were Norwalk virus, norovirus, shellfish, bivalves, oysters, mussels, clams, cockles, and scallops in all the databases (CNKI, VIP, CBM, WanFang Data, PubMed, Web of Science, Embase, and Cochrane Library). A total of 600 studies on HuNoV contamination of shellfish were initially included in the data. First, 303 duplicate studies were removed, leaving 297 studies remaining. One meta-analysis, 11 reviews, and 16 meeting abstracts were excluded from the first analysis. In the second analysis, abstracts of the remaining 269 studies were read by two independent reviewers, further excluding 221 studies in which experimental designs did not meet the inclusion criteria. After carefully reading the full text of the 48 studies, 11 of them were excluded. Ultimately, 37 studies were included in the final analysis. The total sample size in these 37 studies was 17 162 among which the maximum number of samples in a single study was 2 955, and the minimum was 52, and the total number of HuNoV-contaminated samples was 1 970. The meta-analysis was conducted using Stata 14.0, and the effect size was defined as the prevalence of HuNoVs (percentage). Moreover, the heterogeneity of the studies was examined using Q test (P-value) and I2. The pooled prevalence of HuNoVs in shellfish was found to be 15% with an I2 value of 97.22%, which indicated a strong heterogeneity among the 37 studies. We then grouped them based on genogroups, area, season, and species using a random effect model. As a result, GⅠ and GⅡ were found as the two most prevalent genogroups. As revealed by the results, the prevalence of contamination of GⅠ alone, contamination of GⅡ alone, and the combined contamination of GⅠ and GⅡwas found to be 3%, 10%, and 1%, respectively; both Beijing and Guangdong contributed the most with seven studies, followed by Zhejiang with five studies. In addition, there were four studies conducted each in Jiangsu and Shandong, and Fujian contributed with three studies. Two studies were conducted in Gansu, Guangxi, Hebei, Liaoning, and Shanghai. Only one study has been conducted in Hainan. The geographical location exhibited a significant impact on the prevalence of HuNoVs (P < 0.01), and its prevalence in South China (Guangdong, Guangxi, Hainan), North China (Beijing, Hebei), and East China (Fujian, Jiangsu, Shandong, Shanghai, and Zhejiang) reached 19%, 17%, and 11%, respectively, while those in Northeast China (Liaoning) and Northwest China (Gansu), which were not coastal areas, were 4% and 9%, respectively. HuNoVs contamination in shellfish was found to be significantly correlated with the season. At low temperatures, the virus is more persistent, and shellfish metabolism may be inhibited. Our results showed that the prevalence of HuNoVs was the highest in winter (25%), only 10% in summer, and 16% and 12% in spring and autumn, respectively. HuNoVs may contaminate a wide variety of species during the pre-harvest or post-harvest stages. Oysters, clams, and mussels have been recognized as the most common seafood on the table and therefore these are the most investigated. The results of this meta-analysis revealed that the prevalence of HuNoVs in oysters, mussels, and clams was 16%, 10%, and 9%, respectively. The possible reasons why oysters showed the highest prevalence among all shellfish are as follows. One, the oyster farming area is located in shallow bays, which are easily contaminated by domestic sewage. Second, different oyster tissues contain HuNoV receptors (human histo-blood group antigens (HBGAs)-like carbohydrates) and protein-ligands (oyster heat shock protein 70), which can specifically bind to HuNoVs. In summary, HuNoV contamination in shellfish is common in China, and the region, season, and species exhibit significant effects on the prevalence of HuNoVs. The results of this study are beneficial for gaining insights into the HuNoV contamination in shellfish, demonstrating the importance of continuous HuNoV monitoring. Future studies should establish some effective control measures to ensure the sound growth of the shellfish industry in China.
Key words: China    Shellfish    Human noroviruses    Prevalence    Meta-analysis    Cross-sectional studies    

人源诺如病毒(Human Noroviruses, HuNoVs)属于杯状病毒科,是一类无包膜单股正链RNA病毒。根据主衣壳蛋白VP1的多样性,HuNoVs被分为10个基因群(GⅠ-GⅩ),其中,GⅠ、GⅡ、GⅣ、GⅧ和GⅨ可感染人类(Chhabra et al, 2020)。HuNoVs感染剂量低(十几个病毒颗粒就可造成宿主致病)、稳定性高、致病力强,是世界范围内造成人类急性肠胃炎的最常见病原,临床症状包括呕吐(87%)、腹泻(85%)和发热(56%)等,每年造成约42亿美元的直接医疗成本和600亿美元的间接成本损失(Bartsch et al, 2016; Lopman et al, 2016)。

贝类味道鲜美,具有独特的保健功能和药用价值,经济价值大。我国是贝类生产、加工、出口和消费大国。据《2020年中国渔业统计年鉴》数据显示,我国贝类总产量约1458万t,其中,牡蛎(Ostreidae)、贻贝(Mytilus edulis)和蛤蜊(Mactridae)等贝类占70%以上(农业农村部渔业渔政管理局等, 2020)。但食源性病毒污染一直是影响贝类产业健康发展的重要瓶颈问题(Yang et al, 2021; 白昌明等, 2021)。因贝类中检测出HuNoVs而导致产品被召回的事件时有发生,造成了严重的经济损失。贝类属于滤食性动物,通过生物积累过程将养殖水体中的病原微生物吸附至体内(宿志伟等, 2016)。此外,HuNoVs富集于贝类体内后很难通过常规净化手段去除(Battistini et al, 2021; Rupnik et al, 2021)。因此,食用生的或未经过适当煮熟的受污染贝类易导致急性肠胃炎暴发。

我国近年来对贝类中HuNoVs污染的重视程度不断提高,多个省份均陆续开展了相关风险监测,但上述研究多集中在某一区域、部分季节、部分品种,研究结果分散,不利于全面掌握我国贝类HuNoVs污染现状。荟萃分析是将多个目的相同的研究结果进行合并分析的统计学方法。因此,本研究搜集有关中国贝类污染调查的横断面研究,用荟萃分析系统归纳我国近年来贝类中检出HuNoVs的现状,针对贝类采样的地区、季节以及种类等差异进行系统分析。本研究结果有助于在大空间范围、大时间跨度的视角下了解我国贝类中HuNoVs污染风险现状,从而为我国经济贝类中食源性病毒的精准防控提供数据支撑。

1 资料与方法 1.1 纳入与排除标准 1.1.1 研究类型

横断面研究。

1.1.2 研究对象

中国地区受HuNoVs污染的贝类。

1.1.3 效应量(effect size)

检出率。

1.1.4 排除标准

重复发表的文献;研究设计不符合纳入标准;数据不全且无法获得;被多篇文章重复发表的同一批数据等。

1.2 文献检索策略

计算机检索中国知网、维普、万方、中国生物医学文献数据库、PubMed、Web of Science、Embase和Cochrane Library数据库,搜集关于我国贝类中HuNoVs污染情况的横断面研究,检索时限均为建库至2021年12月31日。检索采取主题词和自由词相结合的方式,检索策略根据不同数据库进行调整。中文检索词包括诺如病毒、诺瓦克病毒、海产品、贝类、双壳贝类、牡蛎、生蚝、贻贝、青口(Perna viridis)、蛤、扇贝和蚶。英文检索词包括norovirus、norwalk virus、seafood、shellfish、bivalves、oyster、mussel、cockle、scallop、clam和China。以PubMed为例,具体检索策略见图 1,文献筛选流程及结果见图 2

图 1 PubMed检索策略 Fig.1 Retrieval strategy in PubMed
图 2 文献筛选流程 Fig.2 Flow chart of the search strategy and selection of studies
1.3 资料提取

对拟纳入的文献进行详细阅读,资料提取内容主要包括:①纳入研究的基本信息,包括文献题目、第一作者、发表时间等;②研究对象的基本特征,包括各文献的研究省份、贝类种类、调查样本数、检测方法、HuNoVs基因群、季度分布等关键信息。

1.4 统计分析

采用Stata 14.0软件进行荟萃分析。采用Q检验(P值)和I2分析研究的异质性,若P > 0.10且I2≤50%,则采用固定效应模型;若P < 0.10且I2 > 50%,则采用随机效应模型。效应量为HuNoVs的检出率,并提供其95%置信区间(confidence interval, CI)。按照HuNoVs基因群、地区分布、季节分布和贝类种类进行亚组分析。最后,采用Begg's检验对文献发表偏倚进行评估。

2 结果 2.1 纳入文献基本情况

本次分析纳入的37篇文献中,均为横断面研究。单项研究中最大的样本数量为2 955份,最小为52份。表 1记录了各个地区纳入的文献数量,表 2总结了纳入文献的具体信息。

表 1 我国不同地区纳入的文献数量 Tab.1 The number of included articles in different regions of China
表 2 贝类中人源诺如病毒检出率的荟萃分析中纳入研究的详细信息 Tab.2 Detailed information of the studies included in meta-analysis of the human noroviruses detected in shellfish
2.2 荟萃分析结果

共纳入37篇文献,总样本量17 162份,HuNoVs污染的贝类有1 970份。基于随机效应进行荟萃分析,得出37个研究汇总的效应量0.15,95%置信区间为0.11~0.18,异质性检验P < 0.01,I2=97.22%,具有统计学意义。具体情况见以下森林图(图 3)。

图 3 贝类中人源诺如病毒检出率的荟萃分析的森林图 Fig.3 Forest map of the meta-analysis of human noroviruses detected in shellfish
2.3 亚组分析结果

以基因群、地区、季度和贝类种类作为分组因素进行亚组分析,结果如表 3所示,各个亚组内和亚组间的检出率差异均有统计学意义(P < 0.01),但同时各亚组均存在较高的异质性(I2 > 50%),故均采用随机效应模型合并效应量。在贝类中,单一GⅠ基因群污染、单一GⅡ基因群污染以及GⅠ和GⅡ基因群混合污染的检出率分别为3%、10%和1%;不同地区的病毒污染水平差异显著,其中,华南地区(广东省、广西壮族自治区、海南省)检出率高达19%,华北(北京市、河北省)和华东地区(福建省、江苏省、山东省、上海市、浙江省)的检出率次之,分别为17%和11%,西北(甘肃省)和东北(辽宁省)地区的检出率最低,分别为9%和4%;病毒污染水平有明显的季节性差异,春季、夏季、秋季和冬季的检出率分别是16%、10%、12%和25%;不同贝类种类的病毒污染水平存在明显差异,牡蛎、贻贝和蛤的检出率相对较高,分别是16%、10%和9%,而蚶和蛏的检出率均为5%,扇贝的检出率仅为4%。

表 3 贝类中人源诺如病毒检出率的亚组荟萃分析结果汇总 Tab.3 Summary of subgroup meta-analysis of human noroviruss detected in shellfish
3 讨论

HuNoVs是引发全球食品安全事件的重要病原,其中,受污染的贝类是其重要媒介之一。我国作为贝类生产消费大国,有必要定期对贝类进行病毒监测,了解中国不同地区、不同季节、不同贝类的HuNoVs污染差异。本研究严格按照文献的纳入和排除标准进行文献的筛选,纳入文献的研究样本达17 162份,涉及多个省份和地区,相对于单个的横断面调查,更具有代表性。国家标准GB 4789.42-2016规定了食品中HuNoVs的检测方法是实时荧光定量PCR (Real-time quantitative PCR,RT-qPCR)。在37项纳入研究中,大部分研究(32项)采用了RT-qPCR方法对贝类中HuNoVs进行定量检测。另外,有5项研究仅通过逆转录(巢式)PCR法结合凝胶电泳的方法判断贝类的核酸样本是否扩增出目的条带或测序分型,也被纳入了本次荟萃分析。

经荟萃分析发现,我国贝类中食源性HuNoVs的检出率达15%。接着,从贝类采样的地区、季节以及种类等分别进行亚组分析。需要说明的是,部分研究由于没有区分具体的HuNoVs基因群、采样地区不局限于中国地理大区、季节数据无法提取等,未纳入相应的亚组。HuNoVs具有多样性,亚组分析结果显示,单一GⅠ或GⅡ基因群的检出率分别为3%和10%,GⅠ和GⅡ基因群的混合检出率为1%。就优势基因群而言,贝类与水环境和临床监测的结果一致。关于全球范围内水源中的HuNoVs污染的荟萃分析结果显示,GⅠ基因群、GⅡ基因群及GⅠ和GⅡ基因群混合污染的检出率分别为16%、20.6%和12.8% (Ekundayo et al, 2021)。此外,有研究评估了发展中国家急性胃肠炎的患病率,显示HuNoVs的总患病率为17%,其中,GⅡ基因群的患病率(15%)高于GⅠ基因群(1%)(Nguyen et al, 2017)。综合以上分析,HuNoVs在人群、环境和食品中很可能存在循环传播路径。

表 2详细记录了各项研究中贝类样本的来源,其中有35项研究集中在某一省份,有2项研究多于一个省份(Tao et al, 2018; Ma et al, 2013)。将各项研究的样本来源按我国的地理大区进行归纳,显示主要集中在华南和华东地区(表 1)。本研究结果显示,不同地区贝类中HuNoVs的污染水平存在差异。具体来说,华南(广东省、广西壮族自治区、海南省)和华北地区,(北京市、河北省)的检出率分别为19%和17%;华东(福建省、江苏省、山东省、上海市、浙江省)、西北(甘肃省)和东北(辽宁省)地区的检出率较低,分别为11%、9%和4%。可能的原因如下:华南(10项)、华北(9项)和华东(18项)地区对贝类进行了更多的HuNoVs检测,因此,报告的检出率更高。而东北和西北地区仅各有2项研究,因此,监测的贝类样本数量有限。虽然贝类主要养殖于沿海地区,但其销售范围遍布全国各地。这一现象说明目前关于我国非沿海地区的市售贝类中病毒监测的数据较少,容易使消费者低估或忽视当地贝类中病毒污染的食用风险。实际上,贝类的生产条件在不同地区之间可能存在很大差异,农业投入和技术、HuNoVs的流行病学特点、养殖用水质量、运输渠道及加工方式等情况均可能会影响贝类中病毒污染的发生和水平。

不同季节的贝类的HuNoVs污染水平存在较大差异。冬季(25%)和春季(16%)的检出率高于夏季(10%)和秋季(12%)。水温低于5 ℃和较大的污水排放量已被证实是贝类HuNoVs污染的主要风险因素(Campos et al, 2017)。冬季缺乏紫外线、环境温度低,给HuNoVs的存活提供了良好的条件。同时,该季节是贝类的收获季节,消费量激增。在广东省进行的一项研究探讨了季节对HuNoVs检出率的影响。冬季和春季期间在养殖水体(20.0%)、牡蛎(50.0%)和肠胃炎病例(20.7%)中检测到更多HuNoVs,而夏季和秋季的检出率分别为6.2%、10.9%和17.6% (王安娜等, 2016)。另外,系统发育分析显示出相同基因型HuNoVs在养殖水体、海产品和人群之间的循环,证实了水源、食品和人群之间存在密切的相关性(王安娜等, 2016)。我国HuNoVs感染导致的疫情暴发具有明显的季节性,多以春季和秋冬季为高发。大多数疫情发生在较冷的季节。2013—2014年广西壮族自治区暴发疫情主要集中在3月、10月和11月(王晶等, 2016),广东省则主要发生在冬季和春季(杨芬等, 2017);2016年北京市疫情集中在春季和冬季(蔡伟等, 2018);2015—2016年河北省疫情主要发生在4—6月和12月(刘莹莹等, 2017);2018—2019年福建省漳州市暴发疫情的季节高峰主要在2—3月和9—12月(郭丽清等, 2020)。位于中国西南部的青藏高原HuNoVs感染率非常低(余建兴等, 2015),可能与该地区不常食用贝类的饮食习惯有一定联系。

我国不同贝类中HuNoVs污染水平存在差异。在所有的贝类中,牡蛎是被研究最多的品种,同时也是HuNoVs检出率最高的(16%)。究其原因,牡蛎产量高,是占目前生食比例较大的品种,并且近年来有逐渐增多的趋势。另外,牡蛎的养殖场所位于浅海湾,容易受生活污水的污染。此外,牡蛎的不同组织中均含有HuNoVs的受体(类组织血型抗原)(Tian et al, 2008)和病毒吸附介质(热休克蛋白70)(Zhang et al, 2021b),可特异性结合HuNoVs (Wang et al, 2008a; Wang et al, 2008b),导致牡蛎污染病毒含量可达到周围养殖水体的几十倍到上千倍(Yang et al, 2021)。因此,食用加工不当的牡蛎可能更容易引发食品安全事件。2014年上海美食节引发了一起食品安全事件,83%的病例与牡蛎消费有关,其中GⅡ.4 Sydney_2012、GⅡ.13、GⅠ.2、GⅠ.5为主要基因型(Wang et al, 2015)。牡蛎养殖区人群长期生活在高风险环境中,且伴有高危饮食习惯,HuNoVs GⅡ.17血清抗体总阳性率高达88.2% (172/195)(覃霖, 2017)。

由于单个率荟萃分析的特点,本研究所纳入研究存在较高的异质性(I2>50%);纳入研究均为横断面研究,受纳入研究的研究设计所限,如样本数量、贝类前处理方法和检测方法存在差异,多种偏倚无法避免。此外,大多数纳入研究没有报告定量限的信息,这使得不同实验室数据的比较变得困难。

食源性病毒污染已成为影响我国贝类产业健康发展的重要因素之一。目前,基于污水和贝类的净化处理工艺仅对大多数细菌污染物有效,而对病毒的净化效率较低,因此,与病毒相关的胃肠炎和肝炎暴发持续存在(Marsh et al, 2018)。考虑到贝类消费的健康益处、全球人口增加以及粮食需求增加,保障贝类产品安全至关重要。“从海洋到餐桌”、“从码头到菜品”,受食源性病毒污染贝类的危害性需得到更广泛的认识。

本研究是首次对我国贝类HuNoVs污染水平的系统性回顾。研究表明,可以通过监测贝类的HuNoVs污染情况来揭示当地流行病学的可行性和重要性。未来,需要完善“人–环–食”链条中食源性病毒污染监测网络,建立精准的防控技术体系,从而保障我国贝类产业良性发展以及消费者健康。

参考文献
BAI C M, XIN L S, WANG C M. Malacoherpesviruses and their associated damages to mollusk aquaculture industry. Progress in Fishery Sciences, 2021, 42(1): 214-226 [白昌明, 辛鲁生, 王崇明. 软体动物疱疹病毒及其对贝类养殖产业的危害. 渔业科学进展, 2021, 42(1): 214-226]
BAI J, LI X J, WANG Z, et al. Establishment and application of RT-PCR in the detection of norovirus in shellfish. Chinese Journal of Health Laboratory Technology, 2016, 26(16): 2285-2287 [白颉, 李孝军, 王泽, 等. 贝类中诺如病毒实时荧光定量PCR检测方法的建立及应用. 中国卫生检验杂志, 2016, 26(16): 2285-2287]
BAI X, ZHANG S H, SHI C, et al. Investigation on norovirus contamination of shellfish in Hebei Province in 2015-2016. Journal of Food Safety and Quality, 2018, 9(15): 4152-4157 [白雪, 张淑红, 时晨, 等. 2015-2016年河北省贝类水产品中诺如病毒污染状况研究. 食品安全质量检测学报, 2018, 9(15): 4152-4157]
BARTSCH S M, LOPMAN B A, OZAWA S, et al. Global economic burden of norovirus gastroenteritis. PLoS OneⅡ, 2016, e0151219
BATTISTINI R, MASOTTI C, LISTORTI V, et al. Norovirus persistence in oysters to prolonged commercial purification. Pathogens, 2021, 10(8): 944 DOI:10.3390/pathogens10080944
Bureau of Fishery and Fishery Administration, Ministry of Agriculture and Rural Areas, National Aquatic Technology Promotion Station, China Fisheries Society. 2020 China fisheries statistics yearbook. Beijing: China Agriculture Press, 2020 [农业农村部渔业渔政管理局, 全国水产技术推广总站, 中国水产学会. 2020年中国渔业统计年鉴. 北京: 中国农业出版社, 2020]
CAI W, LIU L X, MA N, et al. Epidemiological investigation and analysis of the norovirus infection outbreaks in Beijing in 2016. Chinese Journal of Viral Diseases, 2018, 8(4): 288-292 [蔡伟, 刘丽霞, 马宁, 等. 2016年北京市诺如病毒感染暴发疫情流行病学调查分析. 中国病毒病杂志, 2018, 8(4): 288-292]
CAMPOS C J A, KERSHAW S, MORGAN O C, et al. Risk factors for norovirus contamination of shellfish water catchments in England and Wales. International Journal of Food Microbiology, 2017, 241: 318-324 DOI:10.1016/j.ijfoodmicro.2016.10.028
CHHABRA P, GRAAF M, PARRA G I, et al. Corrigendum: Updated classification of norovirus genogroups and genotypes. The Journal of General Virology, 2020, 100(10): 1393-1406
EKUNDAYO T C, IGERE B E, OLUWAFEMI Y D, et al. Human norovirus contamination in water sources: A systematic review and meta-analysis. Environmental Pollution, 2021, 291: 118164 DOI:10.1016/j.envpol.2021.118164
GAO J, GONG L M, CHEN Y, et al. Investigation on norovirus contamination in shellfish. Preventive Medicine, 2013, 25(9): 59-61 [高见, 龚黎明, 陈寅, 等. 贝类中诺如病毒污染状况调查. 浙江预防医学, 2013, 25(9): 59-61 DOI:10.3969/j.issn.1007-0931.2013.09.021]
GUO L Q, XU M Y, LIN S Y, et al. Molecular epidemiological characteristics of norovirus outbreaks in Zhangzhou City from 2018 to 2019. International Journal of Virology, 2020, 27(5): 394-397 [郭丽清, 许美燕, 林淑银, 等. 2018-2019年漳州市诺如病毒暴发疫情的分子流行病学特征. 国际病毒学杂志, 2020, 27(5): 394-397]
JIA T H, WANG Y J, YANG M S, et al. Contamination, genotype and epidemiological trends of norovirus in oysters collected from the market in Shanghai. Journal of Biology, 2021, 38(4): 38-42 [贾添慧, 王永杰, 杨明树, 等. 上海市售牡蛎中诺如病毒的污染及基因型和流行趋势分析. 生物学杂志, 2021, 38(4): 38-42]
JIANG T, HAN C H, ZHANG H Y, et al. The detection of noroviruses in oysters sold in Beijing by using Taqman-based one-step reverse transcription-polymerase chain reaction assays and quantitative analysis. Chinese Journal of Food Hygiene, 2017, 29(2): 126-130 [江涛, 韩春卉, 张宏元, 等. 北京市市售牡蛎中诺如病毒核酸检测及定量分析. 中国食品卫生杂志, 2017, 29(2): 126-130]
KE D F, ZHANG Y H. Survey on norovirus contamination of oysters cultured in Guangdong Province. Chinese Journal of Disease Control and Prevention, 2012, 16(10): 881-884 [柯丹枫, 张永慧. 广东养殖牡蛎的诺如病毒污染状况调查. 中华疾病控制杂志, 2012, 16(10): 881-884]
KE M Y, WANG K M, CHEN J L, et al. Investigation and analysis of norovirus contamination in market sale oyster in Xiamen in 2014. Chinese Journal of Health Laboratory Technology, 2015, 25(10): 1634-1637 [柯明月, 王坤明, 陈佳璐, 等. 2014年厦门地区市售牡蛎诺如病毒污染状况调查分析. 中国卫生检验杂志, 2015, 25(10): 1634-1637]
KOU X X, WU A W, FAN H Y. Survey on norovirus contamination in commercial oysters in Guangdong Province. Modern Preventive Medicine, 2018, 45(24): 4439-4442 [寇晓霞, 吴爱武, 范宏英. 广东省市售牡蛎中诺如病毒污染调查. 现代预防医学, 2018, 45(24): 4439-4442]
LI H B, SHAO Y P, ZHANG H P, et al. Survey of norovirus in shellfish in Nantong City. Chinese Journal of Health Laboratory Technology, 2011, 21(9): 2310-2311 [李海波, 邵亚萍, 张宏萍, 等. 南通地区沿海贝类诺瓦克病毒携带情况调查. 中国卫生检验杂志, 2011, 21(9): 2310-2311]
LI P, HUANG H, YU Q, et al. Molecular detection of norovirus in commercially available oysters in the city of Haikou. Journal of Pathogen Biology, 2017, 12(5): 447-449, 455 [李平, 黄涵, 余倩, 等. 海口市市售牡蛎中诺如病毒的分子检测. 中国病原生物学杂志, 2017, 12(5): 447-449, 455]
LI Y F, ZHANG D R, LIU Y, et al. Detection and result analysis of norovirus contamination in shellfish, vegetable and fruit in Lanzhou area of Gansu Province. Food and Nutrition in China, 2018, 24(7): 34-37 [李羽翡, 张德荣, 刘煜, 等. 甘肃省兰州地区贝类海鲜、蔬菜水果中诺如病毒污染监测分析. 中国食物与营养, 2018, 24(7): 34-37 DOI:10.3969/j.issn.1006-9577.2018.07.008]
LI Z. Research on pollution status and risk assessment of Norwalk-like viruses in shellfish in Qingdao. Master's Thesis of Ocean University of China, 2007, 1-76 [李振. 青岛地区贝类中诺瓦克样病毒污染状况调查与风险评估初探. 中国海洋大学硕士研究生学位论文, 2007, 1-76]
LIANG H, JIANG Q, DAI G W, et al. Survey on norovirus contamination in commercial oysters in Guangdong Province from 2011 to 2012. Chinese Journal of Food Hygiene, 2013, 25(4): 359-362 [梁辉, 蒋琦, 戴光伟, 等. 2011-2012年广东省市售牡蛎中诺如病毒污染调查分析. 中国食品卫生杂志, 2013, 25(4): 359-362]
LIU X J, FU Y X, YE L Q, et al. The norovirus contamination status in oysters and mussels in Fujian Province from 2015to 2016. Jiangsu Journal of Preventive Medicine, 2019, 30(4): 386-388 [刘雪杰, 傅祎欣, 叶玲清, 等. 2015-2016年福建省市售牡蛎贻贝中诺如病毒污染情况. 江苏预防医学, 2019, 30(4): 386-388]
LIU X J, LI M Z, YE L Q, et al. Survey of norovirus in oysters collected from commercial harvesting farm in Fujian Province. Chinese Journal of Food Hygiene, 2021, 30(1): 53-57 [刘雪杰, 李闽真, 叶玲清, 等. 福建省养殖环节牡蛎中诺如病毒污染状况分析. 中国食品卫生杂志, 2021, 30(1): 53-57]
LIU Y H. Investigation on main biological and heavy metal pollution of bivalve and evaluation on ecological risk in Liaodong Bay. Doctoral Dissertation of Northeast Agricultural University, 2020, 1-133 [刘永华. 辽东湾近海双壳贝类主要生物和重金属污染现状调查及生态风险评价. 东北农业大学博士研究生学位论文, 2020, 1-133]
LIU Y Y, YU Q L, SU T, et al. Analysis of molecular characteristics of aggregation epidemic induced by norovirus infection in Hebei Province, 2015-2016. Chinese Journal of Experimental and Clinical Virology, 2017, 31(5): 434-437 [刘莹莹, 于秋丽, 苏通, 等. 河北省2015-2016年诺如病毒感染性腹泻疫情的病原分子特征分析. 中华实验和临床病毒学杂志, 2017, 31(5): 434-437]
LIU Z T, ZHOU S J, WANG J, et al. Analysis of norovirus contamination in oysters in Guangdong Province from 2011to 2017. South China Journal of Preventive Medicine, 2019, 45(2): 194-197 [刘志婷, 周少君, 王建, 等. 2011-2017年广东省牡蛎中诺如病毒污染状况分析. 华南预防医学, 2019, 45(2): 194-197]
LOPMAN B A, STEELE D, KIRKWOOD C D, et al. The vast and varied global burden of norovirus: Prospects for prevention and control. PLoS Medicine, 2016, 13(4): e1001999
LÜS L, TAN D M, ZENG X Y, et al. Prevalence of norovirus contamination in oysters in Guangxi, 2014. Practical Preventive Medicine, 2017, 24(3): 284-286 [吕素玲, 谭冬梅, 曾献莹, 等. 2014年广西牡蛎诺如病毒污染状况调查. 实用预防医学, 2017, 24(3): 284-286]
LUO H P, GAO F, YU H Y, et al. Survey on the contamination of norovirus in shellfish, vegetable, fruit and ready-to-eat seafood from markets in Beijing. Chinese Journal of Food Hygiene, 2017, 29(2): 218-222 [骆海朋, 高飞, 于海瑶, 等. 北京市市售贝类、蔬菜、浆果、即食海产品中诺如病毒污染状况检测及检测方法探析. 中国食品卫生杂志, 2017, 29(2): 218-222]
MA L P, ZHAO F, YAO L, et al. The presence of genogroupⅡnorovirus in retail shellfish from seven coastal cities in China. Food and Environmental Virology, 2013, 5(2): 81-86
MARSH Z, SHAH M, WIKSWO M E, et al. Epidemiology of foodborne norovirus outbreaks-United States, 2009-2015. Food Safety, 2018, 6(2): 58-66
NGUYEN G T, PHAN K, TENG I, et al. A systematic review and meta-analysis of the prevalence of norovirus in cases of gastroenteritis in developing countries. Medicine, 2017, 96(40)
NI Y L, ZHENG D Y, JIANG T, et al. Norovirus prevalence survey in bivalves mollusks in Jiangsu Province from 2015to 2016. Jiangsu Journal of Preventive Medicine, 2017, 28(4): 395-397, 402 [倪云龙, 郑东宇, 江涛, 等. 2015-2016年江苏地区双壳贝类海产品中诺如病毒携带状况. 江苏预防医学, 2017, 28(4): 395-397, 402]
QIN L. Relationship between GⅡ. 4 norovirus infection and block HBGA receptor of population in oyster culture area. Master's Thesis of Southern Medical University, 2017, 1-66 [覃霖. 牡蛎养殖区人群GⅡ. 4诺如病毒感染与HBGA受体阻断的关系研究. 南方医科大学硕士研究生学位论文, 2017, 1-66]
RUPNIK A, DORÉ W, DEVILLY L, et al. Evaluation of norovirus reduction in environmentally contaminated Pacific oysters during laboratory controlled and commercial depuration. Food and Environmental Virology, 2021, 13(2): 229-240
SHI S S, JIA T H, YANG M S, et al. Investigation and analysis of norovirus pollution in mussel cultured in Gouqi Island. Journal of Microbiology, 2020, 40(5): 73-81 [时沙沙, 贾添慧, 杨明树, 等. 枸杞岛养殖贻贝中诺如病毒污染情况调查与分析. 微生物学杂志, 2020, 40(5): 73-81]
SU Z W, ZHAO F, LIU Y P, et al. Monitoring of diarhettic shellfish poisons in aquatic environment by solid phase adsorbent toxin tracking technology. Progress in Fishery Sciences, 2016, 37(6): 144-150 [宿志伟, 赵峰, 刘远平, 等. 固相吸附毒素跟踪技术监测牡蛎养殖区中腹泻性贝毒. 渔业科学进展, 2016, 37(6): 144-150]
TAN D M, LYU S L, LIU W, et al. Utility of droplet digital PCRassay for quantitative detection of norovirus in shellfish, from production to consumption in Guangxi, China. Biomedical and Environmental Sciences, 2018, 31(10): 713-720
TAO J, CHUNHUI H, FANNING S, et al. Norovirus contamination in retail oysters from Beijing and Qingdao, China. Food Control, 2018, 86: 415-419
TIAN P, ENGELBREKTSON A L, MANDRELL R E. Seasonal tracking of histo-blood group antigen expression and norovirus binding in oyster gastrointestinal cells. Journal of Food Protection, 2008, 71(8): 1696-1700
WANG A N, ZHONG X W, QIN L, et al. Circulation routes of norovirus among population and environment in coastal area. South China Journal of Preventive Medicine, 2016, 42(2): 101-107 [王安娜, 钟贤武, 覃霖, 等. 诺如病毒在沿海地区人群和环境中的循环传播路径研究. 华南预防医学, 2016, 42(2): 101-107]
WANG D P, WU Q P, KOU X X, et al. Distribution of norovirus in oyster tissues. Journal of Applied Microbiology, 2008a, 105(6): 1966-1972
WANG D P, WU Q P, YAO L, et al. New target tissue for food-borne virus detection in oysters. Letters in Applied Microbiology, 2008b, 47(5): 405-409
WANG H L, ZHANG H, WU B, et al. Monitoring analysis of diarrhea virus from marine seashells and foodborne diarrhea cases in Zhoushan City. Chinese Journal of Food Hygiene, 2018, 30(4): 415-420 [王虹玲, 张辉, 吴昺. 舟山市海产贝类和食源性腹泻病例中肠道腹泻病毒监测. 中国食品卫生杂志, 2018, 30(4): 415-420]
WANG J H, ZOU W W, LI N, et al. The detection of norovirus in mussels sold in Beijing by using TaqMan-based one-step quantitative RT-PCR assays. Chinese Journal of Food Hygiene, 2017, 29(5): 592-595 [王佳慧, 邹文玮, 李楠, 等. 贻贝中诺如病毒荧光定量反转录PCR检测及北京市污染情况调查. 中国食品卫生杂志, 2017, 29(5): 592-595]
WANG J, JU Y, ZHOU K J, et al. Epidemiological characteristics of norovirus diarrhea outbreak in Guangxi, 2013-2014. Modern Preventive Medicine, 2016, 43(14): 2639-2642 [王晶, 居昱, 周开姣, 等. 2013-2014年广西诺如病毒腹泻暴发疫情特征分析. 现代预防医学, 2016, 43(14): 2639-2642]
WANG Y Q, JIN B, CUI H Y, et al. Detection of norovirus and rotavirus and analysis of the genetic characteristics on clams sold in Beijing. Capital Journal of Public Health, 2021, 15(1): 18-22 [王永全, 靳博, 崔海洋, 等. 北京市市售花蛤诺如病毒和轮状病毒检出情况及基因特征分析. 首都公共卫生, 2021, 15(1): 18-22]
WANG Y, ZHANG J, SHEN Z, et al. The impact of calicivirus mixed infection in an oyster-associated outbreak during a food festival. Journal of Clinical Virology, 2015, 73: 55-63
WU L M, TENG Z, CUI X Q, et al. Norovirus contamination and genotypes in shellfish in Shanghai. Journal of Environmental and Occupational Medicine, 2021, 38(8): 888-893 [吴立梦, 滕峥, 崔晓青, 等. 上海市贝类水产品诺如病毒污染状况及基因分型. 环境与职业医学, 2021, 38(8): 888-893]
XU F F, JIN X X, QIU L X, et al. Study on noroviruses in marine & aquatic products in market of Jiangbei District, Ningbo. Chinese Journal of Health Laboratory Technology, 2013, 23(11): 2506-2507, 2509 [徐奋奋, 金晓霞, 裘立晓, 等. 宁波市江北区市售海水产品中检出诺如病毒. 中国卫生检验杂志, 2013, 23(11): 2506-2507, 2509]
YAN H Q, GAO Z Y, LIU B W, et al. Investigation of norovirus contamination in commercial oysters in Beijing. International Journal of Virology, 2018, 25(6): 386-388 [严寒秋, 高志勇, 刘白薇, 等. 北京市市售牡蛎诺如病毒污染状况调查. 国际病毒学杂志, 2018, 25(6): 386-388]
YAN H Q, WANG Y Q, TIAN Y, et al. Surveillance of norovirus contamination on scallops sold in Beijing. Chinese Journal of Food Hygiene, 2020, 32(4): 427-431 [严寒秋, 王永全, 田祎, 等. 北京市市售扇贝中诺如病毒监测分析. 中国食品卫生杂志, 2020, 32(4): 427-431]
YAN X, YANG K. Monitoring and analysis of norovirus in shellfish in Qinhuangdao seafood. Chinese Journal of Health Laboratory Technology, 2017, 27(1): 115-116, 119 [闫鑫, 杨坤. 秦皇岛市海产品贝类中诺如病毒监测分析. 中国卫生检验杂志, 2017, 27(1): 115-116, 119]
YANG F, SUN L M, LI H, et al. Analysis on risk factors for norovirus outbreaks in Guangdong Province, 2008-2015. Chinese Journal of Epidemiology, 2017, 37(8): 906-910 [杨芬, 孙立梅, 李晖, 等. 广东省2008-2015年诺如病毒感染暴发的危险因素分析. 中华流行病学杂志, 2017, 37(8): 906-910]
YANG J L, XUE L, CAI W C, et al. Survey of norovirus genogroupⅡcontamination in commercial oysters in Guangzhou from 2020 to 2021. Science and Technology of Food Industry, 2022, 43(10): 271-278 [杨家乐, 薛亮, 蔡伟程, 等. 2020-2021年广州市售牡蛎中GⅡ型诺如病毒污染情况调查. 食品工业科技, 2022, 43(10): 271-278]
YANG M, ZHAO F, TONG L, et al. Contamination, bioaccumulation mechanism, detection, and control of human norovirus in bivalve shellfish: A review. Critical Reviews in Food Science and Nutrition, 2021, 1-14
YU J X, WANG X, LIAO Q H, et al. Analysis of epidemiology characteristics of norovirus among diarrheal outpatients in27 provinces in China, 2009-2013. Chinese Journal of Epidemiology, 2015, 36(3): 199-204 [余建兴, 王鑫, 廖巧红, 等. 中国27省(市、自治区) 2009-2013年门诊腹泻病例诺如病毒流行特征分析. 中华流行病学杂志, 2015, 36(3): 199-204]
ZHANG H N, LIU D L, ZHANG Z L, et al. Surveillance of human norovirus in oysters collected from production area in Shandong Province, China during 2017-2018. Food Control, 2021a, 121: 107649
ZHANG L. Establishment and application of pretreatment methods for efficient detection of norovirus in oysters. Master's Thesis of Guangdong University of Technology, 2020, 1-84 [张乐. 牡蛎中诺如病毒高效检测的前处理方法建立及应用. 广东工业大学硕士研究生学位论文, 2020, 1-84]
ZHANG Z L, LIU D L, WU Q P, et al. Oyster heat shock protein70 plays a role in binding of human noroviruses. Applied and Environmental Microbiology, 2021b, 87(18): e0079021
ZHU X L, LIU Y K, ZHU H R, et al. Survey of norovirus contamination of bivalves mollusks in farmer's market in Lianyungang City in 2019. Journal of Food Safety and Quality, 2021, 12(4): 1632-1635 [朱晓露, 刘彦凯, 朱鸿儒, 等. 2019年连云港市农贸市场双壳贝类中诺如病毒污染状况调查. 食品安全质量检测学报, 2021, 12(4): 1632-1635]