Abstract
Harmful algal blooms is a widespread problem in aquatic ecosystems, in particular dinoflagellates that produce PSTs which are harmful to animal and human health. To explore the contamination status of PSTs in shellfish in the Southeastern China, a total of 2355 shellfish samples were analyzed by ultra high-performance liquid chromatography–tandem mass spectrometry (UPLC-MS/MS) to study the toxin profiles of the 10 PSTs collected from the southeast coast of China from 2017 to 2021. From 2355 shellfish samples, 257 were detected (10.91%), with the highest value in samples of Perna viridis. Among the six source areas in China, the samples from Fujian recorded the highest detected rate (15.28%). PSTs were found in Fuzhou, Ningde, Quanzhou, Putian, Zhangzhou, and Xiamen, with Quanzhou and Fuzhou having the highest and lowest detection rates of 15.28% and 4.23%, respectively. Saxitoxin (STX), neosaxitoxin (neoSTX), gonyautoxin (GTX1, GTX2, GTX3, GTX4), N-sulfocarbamoyl toxin (GTX5), and decarbamoyl toxin (dcSTX, dcGTX2, dcGTX3) were detected, and GTX5 and dcGTX2 were dominant. In addition, the samples containing PSTs were mostly concentrated in May to August. The study confirms the risks of PSTs to shellfish consumers in the region. It will offer a great foundation for future monitoring of marine toxins and protecting the health of seafood consumers in China. This is the first detailed evaluation of PSTs occurrences and their profiles in shellfish from the Southeastern China over a period of multiple years.
Highlights
2355 mussels from China were analyzed by UPLC-MS/MS for PSTs in 2017–2021.
The predominant PSTs were GTX5, neoSTX and dcGTX2.
Arca granosa and Crassostyea gigas exhibited higher levels than other shellfish.
Shellfish containing PSTs were mostly concentrated in May to August.
Maximum detected level in shellfish was 2137.10 ug STXeq/kg.
Similar content being viewed by others
Data availability
Data supporting the results reported in the article can be found in the figures and tables included in this paper.
References
Andres JK, Yñiguez AT, Maister JM, Turner AD, Olano DEB, Mendoza J, Salvador-Reyes L, Azanza RV (2019) Paralytic shellfish toxin uptake, assimilation, depuration, and transformation in the Southeast Asian green-lipped mussel (Perna viridis). Toxins 11:468–471. https://doi.org/10.3390/toxins11080468
Arjen G, Pol-Hofstad IE, Marnix P, Mulder PPJ, Van DTHJ, Jacob DB( 2010) Marine toxins: chemistry, toxicity, occurrence and detection, with special reference to the Dutch situation. TOXINS 2(4): 878–904. https://doi.org/10.3390/toxins2040878
Botelho MJ, Vale C, Ferreira JG (2019) Seasonal and multi-annual trends of bivalve toxicity by PSTs in Portuguese marine waters. Sci Total Environ 664:1095–1106. https://doi.org/10.1016/j.scitotenv.2019.01.314
Chain E (2009) Scientific Opinion on marine biotoxins in shellfish—Palytoxin group. EFSA J 7:1393. https://doi.org/10.2903/j.efsa.2009.1306
Chen JZ, Hong SP, Cai MR, Chen LI, Zhang, TL (2018) An outbreak of foodborne disease caused by paralytic shellfish toxin. Chinese J Food Hygiene 30: 445–448. https://doi.org/10.13590/j.cjfh.2018.04.022
Chorus I, Welker M (2021) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. CRC Press, Boca Raton (FL), on behalf of the World Health Organization, Geneva, CH. https://doi.org/10.1201/9781003081449
Dean KJ, Hatfield RG, Lee V, Alexander RP, Lewis AM, Maskrey BH, Teixeira Alves M, Hatton B, Coates LN, Capuzzo E (2020) Multiple new paralytic shellfish toxin vectors in offshore North Sea benthos, a deep secret exposed. Mar Drugs 18:400. https://doi.org/10.3390/md18080400
Du KM, Lei F, Wu N, Jiang TJ (2013) Paralytic shellfish toxin pollution in the inshore waters of the East China Sea and South China Sea. J Jinan Univ (natural Science and Medicine Edition) 34:343–346
Garcés E, Bravo I, Vila M, Figueroa RI, Masó M, Sampedro N (2004) Relationship between vegetative cells and cyst production during Alexandrium minutum bloom in Arenys de Mar harbour (NW Mediterranean). J Plankton Res 26:637–645. https://doi.org/10.1093/plankt/fbh065
Gerssen A, Pol-Hofstad IE, Poelman M, Mulder PP, Van den Top HJ, De Boer J (2010) Marine toxins: chemistry, toxicity, occurrence and detection, with special reference to the Dutch situation. Toxins 2:878–904. https://doi.org/10.3390/toxins2040878
Giacobbe M, Oliva F, Maimone G (1996) Environmental factors and seasonal occurrence of the dinoflagellate Alexandrium minutum, a PSP potential producer, in a Mediterranean Lagoon. Estuar Coast Shelf Sci 42:539–549. https://doi.org/10.1006/ecss.1996.0035
Griffith AW, Gobler CJ (2020) Harmful algal blooms: a climate change co-stressor in marine and freshwater ecosystems. Harmful Algae 91:101590. https://doi.org/10.1016/j.hal.2019.03.008
Huang HN, Lu JL, Lin SE, Zheng RJ, Lin J (2020) Simultaneous determination of twelve paralytic shellfish poisoning toxins in bivalve molluscs by UPLC-MS/MS and its applications to a food poisoning incident. Toxicon 174:1–7. https://doi.org/10.1016/j.toxicon.2019.11.012
Keyon ASA, Guijt RM, Gaspar A, Kazarian AA, Nesterenko PN, Bolch CJ, Breadmore MC (2014) Capillary electrophoresis for the analysis of paralytic shellfish poisoning toxins in shellfish: comparison of detection methods. Electrophoresis 35:1496–1503. https://doi.org/10.1002/elps.201300353
Leng KM, Wu, N, Du, KM, Deng, GQ, Jiang, TJ (2014) Characteristics of paralytic shellfish toxins in central Guangdong. Marine Environmental Science. Marine Environmental Science 33: 666–671. https://doi.org/10.13634/j.cnki.mes.2014.05.003
Li J, Persson KM (2021) Quick detection method for paralytic shellfish toxins (PSTs) monitoring in freshwater-a review. Chemosphere 265:128591. https://doi.org/10.1016/j.chemosphere.2020.128591
Long M, Krock B, Castrec J, Tillmann U (2021) Unknown extracellular and bioactive metabolites of the genus alexandrium: a review of overlooked toxins. Toxins 13:905. https://doi.org/10.3390/toxins13120905
Moroño A, Arévalo F, Fernández M, Maneiro J, Pazos Y, Salgado C, Blanco J (2003) Accumulation and transformation of DSP toxins in mussels Mytilus galloprovincialis during a toxic episode caused by Dinophysis acuminata. Aquat Toxicol 62:269–280. https://doi.org/10.1016/S0166-445X(02)00105-4
Nielsen LT, Hansen PJ, Krock B, Vismann B (2016) Accumulation, transformation and breakdown of DSP toxins from the toxic dinoflagellate Dinophysis acuta in blue mussels, Mytilus edulis. Toxicon 117:84–93. https://doi.org/10.1016/j.toxicon.2016.03.021
Onofrio MD, Egerton TA, Reece KS, Pease SK, Sanderson MP, Jones W III, Yeargan E, Roach A, DeMent C, Wood A (2021) Spatiotemporal distribution of phycotoxins and their co-occurrence within nearshore waters. Harmful Algae 103:101993. https://doi.org/10.1016/j.hal.2021.101993
Shahmohamadloo RS, Frenken T, Rudman SM, Van West P, Ibelings BW, Trainer VL (2023) Diseases and disorders in fish due to harmful algal blooms. Climate change on diseases and disorders of finfish in cage culture (3rd edition), In Press. CABI, Oxfordshire, UK. https://doi.org/10.1079/9781800621640.0010
Smith ZJ, Martin RM, Wei B, Wilhelm SW, Boyer GL (2019) Spatial and temporal variation in paralytic shellfish toxin production by benthic Microseira (Lyngbya) wollei in a freshwater New York lake. Toxins 11:44–57. https://doi.org/10.3390/toxins11010044
Turner AD, McNabb PS, Harwood DT, Selwood AI, Boundy MJ (2015) Single-laboratory validation of a multitoxin ultra-performance LC-Hydrophilic interaction LC-MS/MS method for quantitation of paralytic shellfish toxins in bivalve shellfish. J AOAC INTERNATIONAL 98:609–621. https://doi.org/10.5740/jaoacint.14-275
Vale P (2020) Shellfish contamination with marine biotoxins in Portugal and spring tides: a dangerous health coincidence. Environ Sci Pollut Res 27:41143–41156. https://doi.org/10.1007/s11356-020-10389-9
Walker JR, Merit JE, Thomas-Tran R, Tang DT, Du Bois J (2019) Divergent synthesis of natural derivatives of (+)-saxitoxin including 11-saxitoxinethanoic acid. Angew Chem 131:1703–1707. https://doi.org/10.1002/anie.201811717
Wang Z, Xiao SY, Huang W, Pan LB, Wan Y, Guo QF, Li SG, Luo XR (2017) Spatio-temporal analysis of paralytic shellfish toxins in Shenzhen sea area. Chinese J Food Hygiene 29: 89–92. https://doi.org/10.13590/j.cjfh.2017.01.020
Woo CK, Bahna SL (2011) Not all shellfish “allergy” is allergy! Clin Transl Allergy 1:1–7. https://doi.org/10.1186/2045-7022-1-3
World Health Organization (2020) Cyanobacterial toxins: microcystins. background document for development of WHO guidelines for drinking-water quality and guidelines for safe recreational water environments. World Health Organization: Geneva, Switzerland
Wu SW, Zeng M, Lu DP, Luo YD (2008) Analysis of paralytic shellfish toxins in Guangdong coastal waters in the sping of 2005. Oceanogr Res 26:49–54. https://doi.org/10.3969/j.issn.1001-909X.2008.04.007
Yao J, Jin W, Li D, Xu D, Wen S, Liu R, Liang Y, Lu S (2019) Geographical distribution and seasonal variation in paralytic shellfish toxins in the coastal water of the South China Sea. Toxicon 168:67–75. https://doi.org/10.1016/j.toxicon.2019.06.221
Wang ZH, Zhao JG, Zhang Y, Cao Y (2009) Phytoplankton community structure and environmental parameters in aquaculture areas of Daya Bay, South China Sea. J Environ Sci 21:1268–1275. https://doi.org/10.1016/S1001-0742(08)62414-6
Zhou M, Li J, Luckas B, Yu R, Yan T, Hummert C, Kastrup S (1999) A recent shellfish toxin investigation in China. Mar Pollut Bull 39:331–334. https://doi.org/10.1016/S0025-326X(99)00026-0
Zhou Y, Li S, Zhang J, Zhang J, Wang Z, Pan L, Huang B, Huang K, Chen X, Zhao Q (2022) Dietary exposure assessment of paralytic shellfish toxins through shellfish consumption in Shenzhen population, China. Environ Sci Pollut Res 29:10222–10234. https://doi.org/10.1007/s11356-021-16249-4
Funding
This work was financially supported by the Construction of Fujian Provincial Scientific and Technological Innovation Platform, China (Grant No. 2019Y2001), Health Science and Technology Program of Fujian Province, China (Grant No. 2020GGA022), and Basic Scientific Research Project of Fujian Public Welfare Scientific Research Institute, China (Grant No. 2022R1006005).
Author information
Authors and Affiliations
Contributions
Renjin Zheng: investigation, data curation; Yafang Yang: investigation, writing—original draft preparation; Wenting Zhang: formal analysis, methodology; Yongyou Hua: supervision, writing—reviewing and editing.
Corresponding author
Ethics declarations
Conflict of interests
The authors declare no competing interests.
Additional information
Responsible Editor: Lotfi Aleya
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zheng, R., Yang, Y., Zhang, W. et al. Contamination status of paralytic shellfish toxins in shellfish from Southeastern China in 2017–2021. Environ Sci Pollut Res 30, 34728–34740 (2023). https://doi.org/10.1007/s11356-022-24732-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-24732-9