Abstract
Recently, suspected ciguatera fish poisoning (CFP) cases caused by the consumption of moray eels, popular seafood for locals and tourists, have been reported in Viet Nam. However, little is known about ciguatoxins (CTXs) in these marine fish. In May 2020, 119 specimens of six moray eel species were collected for CTX detection from Ly Son Island (site 1), Ninh Hai Coast (site 2), Phu Quy Island (site 3), and Spratly Islands (site 4), where suspected CFP from moray eel consumption have occurred. CTX-1B was detected by liquid chromatography–mass spectrometry (LC/MS) analysis in 12 specimens belonging to four Gymnothorax species: (G. fimbriatus, G. flavimarginatus, G. javanicus, and G. undulatus), accounting for about 10% of the total specimens. Remarkably, CTX-1B levels detected in all toxic specimens were beyond the safety threshold of 10 pg/g CTX-1B equivalent. The highest occurrence was observed at site 4 (15.6%) (n = 45), followed by site 1 (10.0%) (n = 40) and site 2 (6.3%) (n = 16); whereas no CTX-1B was detected in any specimens (n = 18) from site 3. These results, for the first time, report the presence of CTX-1B, indicating a CFP risk in Viet Nam from consumption of moray eels.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen G, Steen R, Humann P, DeLoach N (2015) Tropical Pacific Fish Identification, 2nd edn. Star Standard Industries Pte Ltd, Singapore
Allen G, Swainstom R, Ruse J. (1997) Marine Fishes of Tropical Australia and South-East Asia Western Australian Museum, Australia
Bonnet X, Briand MJ, Brischoux F, Letourneur Y, Fauvel T, Bustamante P (2014) Anguilliform fish reveal large scale contamination by mine trace elements in the coral reefs of New Caledonia. Sci Total Environ 470–471:876–882. https://doi.org/10.1016/j.scitotenv.2013.10.027
Briand MJ, Bonnet X, Guillou G, Letourneur Y (2016) Complex food webs in highly diversified coral reefs: Insights from δ13C and δ15N stable isotopes. Food Webs 8:12–22. https://doi.org/10.1016/j.fooweb.2016.07.002
Brischoux F, Bonnet X (2008) Estimating the impact of sea kraits on the anguilliform fish community (congridae, muraenidae, ophichthidae) of New Caledonia. Aquat Living Resour 21:395–399
Bshary R, Hohner A, Ait-el-Djoudi K, Fricke H (2006) Interspecific communicative and coordinated hunting between groupers and Giant moray eels in the Red sea. PLoS Biol 4:e431. https://doi.org/10.1371/journal.pbio.0040431
Burgess WE, Axelrod HR, Hunziker R (2000) Dr. Burgess’s atlas of marine aquarium fishes, 3rd edn. THF Publications, Neptune City, NJ, USA
Caillaud A, De la Iglesia P, Darius HT, Pauillac S, Aligizaki K, Fraga S, Chinain M, Diogène J (2010) Update on methodologies available for ciguatoxin determination: perspectives to confront the onset of ciguatera fish poisoning in Europe. Mar Drugs 8:1838–1907. https://doi.org/10.3390/md8061838
Campora CE, Dierking J, Tamaru CS, Hokama Y, Vincent D (2008) Detection of ciguatoxin in fish tissue using sandwich ELISA and neuroblastoma cell bioassay. J Clin Lab Anal 22:246–253. https://doi.org/10.1002/jcla.20250
Carpenter KE, Niem VH (1999) FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific. Volume 3. Batoid fishes, chimaeras and bony fishes part 1 (Elopidae to Linophrynidae). FAO, Rome
Carpenter KE, Niem VH (2001) FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific. Volume 5. Bony fishes part 3 (Menidae to Pomacentridae). FAO, Rome
Carpenter KE, Niem VH (2002) FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific. Volume 6. Bony fishes part 4 (Labridae to Latimeriidae), estuarine crocodiles, sea turtles, sea snakes and marine mammals. FAO, Rome
Chan WH, Mak YL, Wu JJ, Jin L, Sit WH, Lam JCW, Sadovy de Mitcheson Y, Chan LL, Lam PKS, Murphy MB (2011) Spatial distribution of ciguateric fish in the Republic of Kiribati. Chemosphere 84:117–123. https://doi.org/10.1016/j.chemosphere.2011.02.036
Chinain M, Darius HT, Ung A, Fouc MT, Revel T, Cruchet P, Pauillac S, Laurent D (2010) Ciguatera risk management in French Polynesia: the case study of Raivavae island (Australes Archipelago). Toxicon 56:674–690. https://doi.org/10.1016/j.toxicon.2009.05.032
Dao HV, Pham KX, Hoang BX, Tanioka M, Watanabe R, Suzuki T (2020) Occurrence of tetrodotoxin in three Nassarius gastropod species in Khanh Hoa province Vietnam. Fish Sci 86:181–186. https://doi.org/10.1007/s12562-019-01375-3
Darius HT, Revel T, Cruchet P, Viallon J, GattiSibatHessChinain CMIMPM (2021) Deep-water fish are potential vectors of ciguatera poisoning in the Gambier islands French Polynesia. Marine Drugs 19:644. https://doi.org/10.3390/md19110644
Dickey RW (2008) Ciguatera toxins: chemistry, toxicology, and Detection. In: Botana LM (ed) Seafood and freshwater toxin. CRC Press, pp 477–500
Dolah FMV (2000) Marine algal toxins: origins, health effects, and their increased occurrence. Environ Health Perspect 108:133–141. https://doi.org/10.1289/ehp.00108s1133
EFSA Panel on Contaminants in the Food Chain (2010) Scientific opinion on marine biotoxins in shellfish – emerging toxins: ciguatoxin group. EFSA J 8:1627–1638. https://doi.org/10.2903/j.efsa.2010.1627
Froese R, Pauly D (2021) FishBase. World Wide Web electronic publication.
Ha DV, Uesugi A, Uchida H, Ky PX, Minh DQ, Watanabe R, Matsushima R, Oikawa H, Nagai S, Iwataki M, Fukuyo Y, Suzuki T (2018) Identification of causative ciguatoxins in red snappers Lutjanus bohar implicated in ciguatera fish poisonings in Vietnam. Toxins (basel) 10:420. https://doi.org/10.3390/toxins10100420
Hokama Y, Nishimura K, Takenaka W, Ebesu JS (1998) Simplified solid-phase membrane immunobead assay (MIA) with monoclonal anti-ciguatoxin antibody (MAb-CTX) for detection of ciguatoxin and related polyether toxins. J Nat Toxins 7:1–21
Ikehara T, Kuniyoshi K, Oshiro N, Yasumoto T (2017) Biooxidation of ciguatoxins leads to species-specific toxin profiles. Toxins 9(7):205. https://doi.org/10.3390/toxins9070205
Ineich I, Bonnet X, Brischoux F, Kulbicki M, Séret B, Shine R (2007) Anguilliform fishes and sea kraits: neglected predators in coral-reef ecosystems. Mar Biol 151:793–802. https://doi.org/10.1007/s00227-006-0527-6
Labrousse H, Matile L (1996) Toxicological biotest on diptera larvae to detect ciguatoxins and various other toxic substances. Toxicon 34:881–891. https://doi.org/10.1016/0041-0101(96)00045-1
Legrand AM, Litaudon M, Genthon JN, Bagnis R, Yasumoto T (1989) Isolation and some properties of ciguatoxin. J Appl Phycol 1:183–188. https://doi.org/10.1007/BF00003882
Lehane L (2000) Ciguatera update. Med J Aust 172:176–179. https://doi.org/10.5694/j.1326-5377.2000.tb125546.x
Lehane L, Lewis RJ (2000) Ciguatera: recent advances but the risk remains. Int J Food Microbiol 61:91–125. https://doi.org/10.1016/S0168-1605(00)00382-2
Lewis RJ (1994) Immunological, biochemical and chemical features of ciguatoxins: implications for the detection of ciguateric fish. Mem Qld Mus 34:541–548
Lewis RJ, Jones A (1997) Characterization of ciguatoxins and ciguatoxin congeners present in ciguateric fish by gradient reverse-phase high-performance liquid chromatography/mass spectrometry. Toxicon 35:159–168. https://doi.org/10.1016/S0041-0101(96)00132-8
Lewis RJ, Sellin M (1992) Multiple ciguatoxins in the flesh of fish. Toxicon 30:915–919. https://doi.org/10.1016/0041-0101(92)90390-Q
Lewis RJ, Sellin M (1993) Recovery of ciguatoxin from fish flesh. Toxicon 31:1333–1336. https://doi.org/10.1016/0041-0101(93)90407-A
Lewis RJ, Jones A, Vernoux J-P (1999) HPLC/tandem electrospray mass spectrometry for the determination of sub-ppb levels of Pacific and Caribbean ciguatoxins in crude extracts of fish. Anal Chem 71:247–250. https://doi.org/10.1021/ac980598h
Llewellyn LE (2010) Revisiting the association between sea surface temperature and the epidemiology of fish poisoning in the South Pacific: reassessing the link between ciguatera and climate change. Toxicon 56:691–697. https://doi.org/10.1016/j.toxicon.2009.08.011
Mak YL, Wai T-C, Murphy MB, Chan WH, Wu JJ, Lam JCW, Chan LL, Paul Lam PKS (2013) Pacific ciguatoxins in food web components of coral reef systems in the Republic of Kiribati. Environ Sci Technol 47:14070–14079. https://doi.org/10.1021/es403175d
Murata M, Legrand AM, Ishibashi Y, Fukui M, Yasumoto T (1990) Structures and configurations of ciguatoxin from the moray eel Gymnothorax javanicus and its likely precursor from the dinoflagellate Gambierdiscus toxicus. J Am Chem Soc 112:4380–4386. https://doi.org/10.1021/ja00167a040
Olsen DA, Nellis DW, Wood RS (1984) Ciguatera in the eastern caribbean. Mar Fish Rev 46:13–18
Oshiro N, Yogi K, Asato S, Sasaki T, Tamanaha K, Hirama M, Yasumoto T, Inafuku Y (2010) Ciguatera incidence and fish toxicity in Okinawa, Japan. Toxicon 56:656–661. https://doi.org/10.1016/j.toxicon.2009.05.036
Phung NH (2001) Fauna of Viet Nam. Publish House of Science and Technology, Ha Noi, Vietnam
Phung NH, Thi NN (1994) List of Vietnamese Marine Fish. Publish House of Science and Technology, Ha Noi, Vietnam
Randall JE, Allen GR, Steene RC (1990) Fishes of the great barrier reef and coral sea. University of Hawaii Press, Honolulu, North America
Roeder K, Erler K, Kibler S, Tester P, Van The H, Nguyen-Ngoc L, Gerdts G, Luckas B (2010) Characteristic profiles of ciguatera toxins in different strains of Gambierdiscus spp. Toxicon 56:731–738. https://doi.org/10.1016/j.toxicon.2009.07.039
Scheuer PJ, Takahashi W, Tsutsumi J, Yoshida T (1967) Ciguatoxin: isolation and chemical nature. Science 155:1267–1268. https://doi.org/10.1126/science.155.3767.1267
Shen SC, Tzeng CS (1993) Fishes of Taiwan. Department of Zoology, National Taiwan University, Taipei, Taiwan
Suzuki T, Ha DV, Uesugi A, Uchida H (2017) Analytical challenges to ciguatoxins. Curr Opin Food Sci 18:37–42. https://doi.org/10.1016/j.cofs.2017.10.004
Wu JJ, Mak YL, Murphy MB, Lam JCW, Chan WH, Wang M, Chan LL, Lam PKS (2011) Validation of an accelerated solvent extraction liquid chromatography–tandem mass spectrometry method for Pacific ciguatoxin-1 in fish flesh and comparison with the mouse neuroblastoma assay. Anal Bioanal Chem 400:3165–3175. https://doi.org/10.1007/s00216-011-4977-4
Wu N, Huan Q, Du K, Hu R, Jiang T-j (2015) Ciguatera toxins in wild coral reef fish along the southern coast of China. Mar Freshw Res 66:1168–1175. https://doi.org/10.1071/MF14215
Yogi K, Oshiro N, Inafuku Y, Hirama M, Yasumoto T (2011) Detailed LC-MS/MS analysis of ciguatoxins revealing distinct regional and species characteristics in fish and causative alga from the Pacific. Anal Chem 83:8886–8891. https://doi.org/10.1021/ac200799j
Zhu J, Lee W-H, Wu J, Zhou S, Yip K-C, Liu X, Kirata T, Chan L-L (2022) The occurrence, distribution, and toxicity of high-risk ciguatera fish species (grouper and snapper) in Kiritimati island and Marakei island of the Republic of Kiribati. Toxins (basel) 14:208. https://doi.org/10.3390/toxins14030208
Acknowledgements
This research was funded by Viet Nam Academy of Science and Technology [project grant number TĐĐTB0.01/21-23]. This paper is a contribution to celebrate the 100th anniversary of the Institute of Oceanography, Viet Nam Academy of Science and Technology. This research collaborated with the General Research Fund of the Hong Kong Research Grants Council, grant number CityU11104821. The authors would deliver thanks to Japan Funds in Trust (JFIT) for supporting the regional collaboration of the IOC/WESTPAC-MTSS (Marine Toxins and Seafood Safety) project.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Appendix A
Rights and permissions
Springer Nature or its licensor 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
Dao, H.V., Le, H.H.K., Le, T.T.T. et al. Ciguatoxin in moray eels raising the risk for seafood safety in Viet Nam. Fish Sci 88, 821–830 (2022). https://doi.org/10.1007/s12562-022-01638-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-022-01638-6