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


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.


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


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


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


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。


1 资料与方法 1.1 纳入与排除标准 1.1.1 研究类型


1.1.2 研究对象


1.1.3 效应量(effect size)


1.1.4 排除标准


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


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)。


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。


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