Progress in Fishery Sciences (Dec 2023)
Detection of Human Noroviruses in Shellfish in China: A Meta-Analysis
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.
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