JIANG Shanshan, ZHANG Chenxiao. Pollution analysis and dietary exposure risk assessment of lipophilic toxins in shellfish from Beibu Gulf seafood market in Guangxi Province[J]. South China Fisheries Science, 2023, 19(4): 158-167. DOI: 10.12131/20230024
Citation: JIANG Shanshan, ZHANG Chenxiao. Pollution analysis and dietary exposure risk assessment of lipophilic toxins in shellfish from Beibu Gulf seafood market in Guangxi Province[J]. South China Fisheries Science, 2023, 19(4): 158-167. DOI: 10.12131/20230024

Pollution analysis and dietary exposure risk assessment of lipophilic toxins in shellfish from Beibu Gulf seafood market in Guangxi Province

More Information
  • Received Date: February 16, 2023
  • Revised Date: February 23, 2023
  • Accepted Date: March 01, 2023
  • Available Online: March 05, 2023
  • Lipophilic shellfish toxins are widely distributed and will be transmitted to consumers through the food chain, posing a great threat to human health. The Beibu Gulf in Guangxi Province is an important mariculture area in China, accounting for more than half of the national output. To estimate the potential dietary exposure risk of coastal residents in that area, and to provide a scientific basis for the establishment of toxin limit standards, we analyzed the contents of lipophilic shellfish toxins by liquid chromatography tandem mass spectrometry. We have used a 24-hour dietary review method to investigate the consumption of marine products by coastal residents for seven consecutive days. Then we calculated the value of estimated daily intake (ESI) of toxins in the diet by using the marine biological toxin point assessment method, and evaluated the edible safety by comparing with the acute reference dose (ARfD) recommended by the European Food Safety Agency. The proportion of samples contaminated with toxins followed a descending order of gyrodimine (GYM) (83.02%), okadaic acid (OA) (51.16%), dinophysis toxin (DTX-2)(40.91%) and homo-yessotoxin (Homo-YTX) (8.6%), with the peak values of 105.4, 31.39, 38.19 and 159.6 µg·kg−1, respectively. The concentrations of toxins varied with different seasons and species. Among the six kinds of shellfish, the highest contents of OA and GYM were found in oyster samples, and the peak values were found in winter and autumn samples, respectively. The contents of DTX-2 in autumn and winter samples were significantly higher than those in spring and summer samples. Homo-YTX was only detected in scallop and mussel samples in summer and autumn. Dietary survey shows that the average daily shellfish consumption of coastal residents in Beibu Gulf was 45 g·d−1. The ESI value in OA toxin was estimated to be 0.26 μg·(kg·d)−1 based on the shellfish consumption and body masses of local residents, less than the ARfD value [0.3 μg·(kg·d)−1] set by the European Union (EU). However, based on the shellfish consumption and body masses of local residents provided by the EU, the ESI value [0.34 μg·(kg·d)−1] was higher than the ARfD value. The results suggest that although the detection rate of lipophilic shellfish toxin in shellfish samples was lower than the safe limit value set by the EU, there is a risk of dietary exposure to OA toxin for the Beibu Gulf residents.
  • [1]
    KONOKI K, ONODA T, WATANBE R, et al. In vitro acylation of okadaic acid in the presence of various bivalves' extracts[J]. Mar Drugs, 2013, 11(2): 300-315.
    [2]
    王亚军, 余新威, 方力, 等. 营养环境对微小亚历山大藻C4生长和产毒的影响[J]. 水产学报, 2017, 41(10): 1588-1598.
    [3]
    VALDIGLESIAS V, PREGO-FARALDO M V, PÁSARO E, et al. Okadaic acid: more than a diarrheic toxin[J]. Mar Drugs, 2013, 11(11): 4328-4349. doi: 10.3390/md11114328
    [4]
    MARTELLI F, CIRLINI M, DELLAFIORA L, et al. Mitigation of marine toxins by interactions with bacteria: the case of okadaic acid and tetrodotoxin[J]. Food Control, 2021(1): 108428.
    [5]
    AUNE T, ESPENES A, AASEN J, et al. Study of possible combined toxic effects of azaspiracid-1 and okadaic acid in mice via the oral route[J]. Toxicon, 2012, 60(5): 895-906. doi: 10.1016/j.toxicon.2012.06.007
    [6]
    EFSA. Scientific Opinion of the Panel on Contaminants in the Food Chain on a request from the European Commission on marine biotoxins in shellfish-pectenotoxin group[J]. EFSA J, 2009, 1109: 1-47.
    [7]
    BLAANCO J, ARÉVALO F, CORREA J, et al. Effect of the industrial steaming on the toxicity, estimated by LC-MS/MS, of mussels exposed for a long time to diarrhetic shellfish poisoning (DSP) toxins[J]. Food Chem, 2015, 177: 240-247. doi: 10.1016/j.foodchem.2015.01.012
    [8]
    OTERO A, CHAPELA M J, ATANASSOVA M, et al. Cyclic imines: chemistry and mechanism of action: a review[J]. Chem Res Toxicol, 2011, 24(11): 1817-1829. doi: 10.1021/tx200182m
    [9]
    EFSA. Opinion of the Scientific Panel on Contaminants in the Food chain on a request from the European Commission on marine biotoxins in shellfish-yessotoxin group[J]. EFSA J, 2008, 907: 1-62.
    [10]
    EFSA panel on contaminants in the food chain (CONTAM). Scientific opinion on marine biotoxins in shellfish-cyclic imines (spirolides, gymnodimines, pinnatoxins and pteriatoxins)[J]. EFSA J, 2010, 8(6): 1628.
    [11]
    徐轶肖, 韦光领, 王玉, 等. 钦州湾海水和香港牡蛎体内脂溶性贝类毒素污染特征[J]. 海洋与湖沼, 2021, 52(1): 144-152. doi: 10.11693/hyhz20200400126
    [12]
    柳阳, 郭伟, 黎全江, 等. 广西北部湾近江牡蛎脂溶性藻毒素污染状况与安全风险评价[J]. 南方水产科学, 2020, 16(4): 108-113. doi: 10.12131/20190212
    [13]
    JI Y, YAN G W, WANG G X, et al. Prevalence and distribution of domoic acid and cyclici mines in bivalve mollusks from Beibu Gulf, China[J]. J Hazard Mater, 2022, 423: 127078. doi: 10.1016/j.jhazmat.2021.127078
    [14]
    WANG Z, DOUCETTE G J. Determination of lipophilic marine biotoxins by liquid chromatography-tandem mass spectrometry in five shellfish species from Washington State, USA[J]. J Chromatogr A, 2021, 1639: 461902. doi: 10.1016/j.chroma.2021.461902
    [15]
    ROURKE W A, JUSTASON A, MARTIN J L, et al. Shellfish toxin uptake and depuration in multiple Atlantic Canadian mollusca species: application to selection of sentinel species in monitoring programs[J]. Toxins, 2021, 13(2): 168. doi: 10.3390/toxins13020168
    [16]
    ZHENG R J, LIN S E, YANG Y, et al. Variability and profiles of lipophilic marine toxins in shellfish from southeastern China in 2017−2020[J]. Toxicon, 2021, 201: 37-45. doi: 10.1016/j.toxicon.2021.08.009
    [17]
    CHEN X, HUANG B Q, ZHAO Q H, et al. Shellfish contamination with lipophilic toxins and dietary exposure assessments from consumption of shellfish products in Shenzhen, China[J]. Ecotoxicol Environ Saf, 2021, 221: 112446. doi: 10.1016/j.ecoenv.2021.112446
    [18]
    海洋讯. 自然资源部发布2021年度《中国海洋灾害公报》[J]. 自然资源通讯, 2022(10): 39-55.
    [19]
    MARTINS J C, DOMÍNGUEZ-PÉREZ D, AZEVEDO C B, et al. Molecular responses of mussel Mytilus galloprovincialis associated to accumulation and depuration of marine biotoxins okadaic acid and dinophysistoxin-1 revealed by shotgun proteomics[J]. Front Mar Sci, 2020, 7: 589822. doi: 10.3389/fmars.2020.589822
    [20]
    刘红河, 秦逍云, 廖仕成, 等. 超高效液相色谱-四极杆串联线性离子阱质谱法测定贝类中的脂溶性贝类毒素[J]. 卫生研究, 2021, 50(6): 967-974.
    [21]
    QIU J B, CHEN H D, JI Y, et al. Evaluation of different strategies to minimize thematrix effects on LC-MS/MS analysis of multiple lipophilic shellfish toxins in both acidic and alkaline chromatographic conditions[J]. Toxicon, 2020, 188: 16-26. doi: 10.1016/j.toxicon.2020.10.002
    [22]
    赵丽云, 马冠生, 朴建华, 等. 2010-2012中国居民营养与健康状况监测总体方案[J]. 中华预防医学杂志, 2016, 50(3): 204-207.
    [23]
    TWINER M J, El-ADKI R, KILCOYNE J, et al. Comparative effects of the marine algal toxins azaspiracid-1, -2, and -3 on Jurkat T lymphocyte cells[J]. Chem Res Toxicol, 2012, 25(3): 747-754. doi: 10.1021/tx200553p
    [24]
    ALVES R N, RAMBLA-ALEGRE M, BRAGA A C, et al. Bioaccessibility of lipophilic and hydrophilic marine biotoxins in seafood: an in vitro digestion approach[J]. Food Chem Toxicol, 2019, 129: 153-161. doi: 10.1016/j.fct.2019.04.041
    [25]
    EFSA. Scientific opinion of the panel on contaminants in the food chain on a request from the European commission on marine biotoxins in shellfish-summary on regulated marine biotoxins[J]. EFSA J, 2009, 1306: 1-23.
    [26]
    白志毅, 温鹏超, 袁立, 等. 我国淡水贝类种质资源现状与保护利用[J]. 水产学报, 2022, 46(1): 149-157.
    [27]
    丁剑楠, 张闪闪, 武旭跃, 等. 太湖贡湖湾水体中微囊藻毒素的时空分布及健康风险评估[J]. 生态环境学报, 2018, 27(11): 2095-2101.
    [28]
    CHEN J H, HAN T Z, LI X T, et al. Occurrence and distribution of marine natural organic pollutants: lipophilic marine algal toxins in the Yellow Sea and the Bohai Sea, China[J]. Sci Total Environ, 2018, 612: 931-939. doi: 10.1016/j.scitotenv.2017.08.304
    [29]
    查道军, 李嫒芳, 丁任业, 等. 大亚湾大鹏澳海域贝类和浮游植物中脂溶性毒素及软骨藻酸研究[J]. 海洋环境科学, 2022, 41(5): 753-760. doi: 10.13634/j.cnki.mes.2022.05.016
    [30]
    WU H Y, YAO J H, GUO M M, et al. Distribution of marine lipophilic toxins in shellfish products collected from the Chinese market[J]. Mar Drugs, 2015, 13(7): 4281-4295. doi: 10.3390/md13074281
    [31]
    韩蕾, 赵芮, 刘昭, 等. 大田软海绵酸和鳍藻毒素时间分辨荧光免疫层析试纸条的研制与应用[J]. 海洋环境科学, 2022, 41(5): 783-790.
    [32]
    郑旭颖, 李兆新, 孙晓杰, 等. 渤海海域唐山贝类养殖区腹泻性和麻痹性贝类毒素的监测与风险评估[J]. 渔业科学进展, 2022, 43: 1-12.
    [33]
    BLANCO J, ARÉVALO F, CORREA J, et al. Lipophilic toxins in Galicia (NW Spain) between 2014 and 2017: incidence on the main molluscan species and analysis of the monitoring efficiency[J]. Toxins, 2019, 11(10): 612. doi: 10.3390/toxins11100612
    [34]
    LEITE I do P, SANDRINI-NETO L, SQUELLA F L, et al. Toxin accumulation, detoxification and oxidative stress in bivalve (Anomalocardia flexuosa) exposed to the dinoflagellate Prorocentrumlima[J]. Aquat Toxicol, 2021, 232: 105738.
    [35]
    LEI L, NING W C, YG C, et al. Seasonal variability of Protoceratium reticulatum and yessotoxins in Japanese scallop Patinopecten yessoensis in northern Yellow Sea of China[J]. Toxicon, 2017, 139: 31-34.
    [36]
    VILARIÑO N, LOUZAO M, ABAL P, et al. Human poisoning from marine toxins: unknowns for optimal consumer protection[J]. Toxins, 2018, 10(8): 324. doi: 10.3390/toxins10080324
    [37]
    EFSA Panel on Contaminants in the Food Chain (CONTAM). Statement on further elaboration of the consumption figure of 400 g shellfish meat on the basis of new consumption data[J]. EFSA J, 2010, 8(8): 1706. doi: 10.2903/j.efsa.2010.1706
    [38]
    MCCARRON P, KILCOYNE J, HESS P. Effects of cooking and heat treatment on concentration and tissue distribution of okadaic acid and dinophysistoxin-2 in mussels (Mytilus edulis)[J]. Toxicon, 2008, 51(6): 1081-1089. doi: 10.1016/j.toxicon.2008.01.009
    [39]
    DÍEZ-QUIJADA JIMÉNEZ L, GUZMÁNGUILLÉN R, CASCAJOSA LIRA A, et al. In vitro assessment of cyanotoxins bioaccessibility in raw and cooked mussels[J]. Food Chem Toxicol, 2020, 140: 111391. doi: 10.1016/j.fct.2020.111391
  • Related Articles

    [1]WANG Yongjin, ZHANG Xun, ZHANG Yu, ZHOU Aizhong, LI Ziniu, WANG Shuaijie, LIU Longteng, WANG Lumin. Influence of main structural parameters on performance of bottom trawl with large-size mesh[J]. South China Fisheries Science, 2021, 17(4): 66-73. DOI: 10.12131/20210026
    [2]YANG Bingzhong, YANG Lin, TAN Yongguang, YAN Lei, ZHANG Peng, LI Jie. Size selectivity of combined square mesh and diamond mesh codends of shrimp beam trawl in South China Sea[J]. South China Fisheries Science, 2018, 14(1): 105-113. DOI: 10.3969/j.issn.2095-0780.2018.01.014
    [3]YAN Lei, LI Yanan, TAN Yongguang, YANG Lin, YANG Bingzhong, ZHANG Peng, CHEN Sen, LI Jie. Mesh size selectivity of Harpodon nehereus gillnet in northern South China Sea[J]. South China Fisheries Science, 2016, 12(2): 75-80. DOI: 10.3969/j.issn.2095-0780.2016.02.011
    [4]YANG Bingzhong, YANG Lin, TAN Yongguang, ZHANG Peng, YAN Lei, CHEN Sen. Preliminary analysis of relationship between mesh size of gillnet and body characteristics of target species in the South China Sea[J]. South China Fisheries Science, 2015, 11(6): 94-99. DOI: 10.3969/j.issn.2095-0780.2015.06.013
    [5]NIU Zhikai, LIU Baosuo, ZHANG Dongling, TAN Caigang, ZHANG Bo, CHEN Mingqiang, FAN Sigang, JIANG Song, HUANG Guiju, LI Youning, YU Dahui. Comparative analysis of growth traits and shell-closing strength among hybrid populations from three geographical groups of pearl oyster (Pinctada fucata)[J]. South China Fisheries Science, 2015, 11(1): 26-32. DOI: 10.3969/j.issn.2095-0780.2015.01.004
    [6]YANG Bingzhong, YANG Lin, TAN Yongguang, ZHANG Peng, YAN Lei. Relationship between body characteristic of Scomberomorus and the mesh size[J]. South China Fisheries Science, 2013, 9(5): 120-125. DOI: 10.3969/j.issn.2095-0780.2013.05.018
    [7]ZHANG Xu-feng, ZHANG Peng, TAN Yong-guang, YANG Lin. Analysis on catch selectivity of 30.3 mm square mesh codend oftrawl in Northern South China Sea[J]. South China Fisheries Science, 2006, 2(2): 51-55.
    [8]GE Zhangzi, LIANG Zhenlin, TOKAI Tadashi. Mesh size selectivity of white spotted ell pot in coast of Japan[J]. South China Fisheries Science, 2006, 2(1): 58-61.
    [9]GE Chang-zi. The review on the analysis of mesh size selectivity of trawl cod-end[J]. South China Fisheries Science, 2005, 1(4): 30-35.
    [10]ZHANG Peng, YANG Lin, ZHANG Xu-feng, TANG Yong-guang. Study on selectivity of different mesh size gillnet for Nemipterus virgatus in South China Sea[J]. South China Fisheries Science, 2005, 1(2): 61-66.
  • Cited by

    Periodical cited type(10)

    1. 米锐,周遵春,孟楠. 海参内脏酶解物和体壁溶出物的护肤功效评价. 现代食品科技. 2023(01): 222-229 .
    2. 刘文亮,周永波,曾荣急,单勇军,黄世英,李健. 海参内脏精深加工难点与对策. 食品工业科技. 2023(20): 458-466 .
    3. 颜琳,姜双双,闫欣,姚艳艳,常丽荣,李长青. 皱纹盘鲍腹足抗氧化肽的制备及其工艺优化. 食品与发酵工业. 2019(17): 123-128 .
    4. 张金杨,胡晓,李来好,杨贤庆,吴燕燕,林婉玲,邓建朝,荣辉,黄卉. 罗非鱼酶解物矿物离子结合能力及其结合物抗氧化活性. 食品与发酵工业. 2018(05): 76-81 .
    5. 姜卉,金文刚,许景光,吴海涛,王笑涵,商文慧,韩佳润,唐越. 热变性对海参肠酶解物活性的影响. 食品工业科技. 2018(14): 29-33 .
    6. 何传波,邵杰,魏好程,熊何健,吴国宏,马英,吴建勇. 鲍内脏蛋白肽抗氧化和免疫调节活性. 食品科学. 2018(05): 206-212 .
    7. 吴燕燕,张婉,李来好,王锦旭,胡晓,杨少玲. 海萝藻中类菌胞素氨基酸的种类分析及抗氧化性能. 中国食品学报. 2018(05): 264-272 .
    8. 潘南,吴靖娜,苏永昌,陈贝,苏捷,郑昇阳,刘智禹. 福建养殖仿刺参抗氧化多肽的酶解工艺优化及其对过氧化氢诱导的血管内皮细胞EA.hy926损伤的保护作用. 食品工业科技. 2018(24): 183-191 .
    9. 杨伊然,胡晓,杨贤庆,李来好,陈胜军,吴燕燕,林婉玲,黄卉,马海霞. 蓝圆鲹蛋白酶解物的螯合矿物离子活性研究. 食品科学. 2017(03): 88-93 .
    10. 陶海英,闫鸣艳,尹利端. 刺参内脏蛋白酶解液抗氧化活性研究. 食品研究与开发. 2015(11): 58-61 .

    Other cited types(12)

Catalog

    Recommendations
    Establishment and application of qpcr and raa-lfd based onrecagene for detection ofpseudomonas anguilliseptica
    WANG Yilin et al., SOUTH CHINA FISHERIES SCIENCE, 2025
    Effect of blanching treatment on oyster meat quality during refrigeration and frozen storage
    CUI Junwei et al., SOUTH CHINA FISHERIES SCIENCE, 2025
    Hctlr1 involved in antimicrobial immune response by myd88-nf-κb signaling pathway inhyriopsis cumingii
    LU Junyi et al., SOUTH CHINA FISHERIES SCIENCE, 2024
    Research on fish feeding intensity classification model based on axial feature calibration and temporal segment network
    XU Bo et al., SOUTH CHINA FISHERIES SCIENCE, 2024
    The effects of forced aeration and initial moisture level on red pigment and biomass production by monascus ruber in packed bed solid state fermentation.
    F. M. Said et al., INTERNATIONAL JOURNAL OF ENVIRONMENTAL SCIENCE AND DEVELOPMENT, 2010
    Optimization and characterization of free and cross-linked enzymes aggregate from solid-state fermented materials
    CHEMICAL AND NATURAL RESOURCES ENGINEERING JOURNAL (FORMALLY KNOWN AS BIOLOGICAL AND NATURAL RESOURCES ENGINEERING JOURNAL), 2023
    Novel nacl reduction technologies for dry-cured meat products and their mechanisms: a comprehensive review
    Jia, Shiliang et al., FOOD CHEMISTRY, 2024
    Effects of different thermal processing methods on bioactive components, phenolic compounds, and antioxidant activities of qingke (highland hull-less barley)
    Hong, Qingyue et al., FOOD SCIENCE AND HUMAN WELLNESS, 2023
    Heat transfer augmentation, endothermic pyrolysis and surface coking of hydrocarbon fuel in manifold microchannels at a supercritical pressure
    INTERNATIONAL COMMUNICATIONS IN HEAT AND MASS TRANSFER, 2025
    Large-scale manufacturing of human gallbladder epithelial cell products and derived hepatocytes via a chemically defined approach
    TRENDS IN BIOTECHNOLOGY
    Powered by
    Article views PDF downloads Cited by(22)
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return