Ciguatoxins

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Marine and Freshwater Toxins".

Deadline for manuscript submissions: closed (31 August 2021) | Viewed by 65307

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Hellenic Agricultural Organization—DIMITRA, Veterinary Research Institute of Thessaloniki, Department of Hy-giene and Technology of Food of Animal Origin and Toxicology, 57001 Thermi, Greece
Interests: marine biotoxins; phycotoxins; harmful algal blooms; toxic pufferfish; emerging marine toxins; tetrodotoxins; ciguatoxins; lipophilic toxins; toxic episodes management; phycotoxins regulatory monitoring; marine toxins analysis; mouse bioassay; liquid chromatography mass spectrometry
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Co-Guest Editor
Université Côte d’Azur, CNRS, UMR 7035 ECOSEAS, Nice, France
Interests: food safety; food security; sustainable development; harmful algal blooms; contaminants; risk management; capacity building; marine biotoxins
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Ciguatoxins (CTXs), which are responsible for Ciguatera fish poisoning (CFP), are liposoluble toxins produced by microalgae of the genera Gambierdiscus and Fukuyoa. With an estimated number of 50,000 cases a year worldwide, some fatal, CFP is the most common non-bacterial illness associated with seafood. Until recently, CFP intoxications were considered to be endemic to (sub)tropical regions of the Pacific and Indian Ocean and the Caribbean Sea, but they are nowadays responsible for intoxications in other places around the world. In particular, in Europe, intoxications occur due to both consumption of imported ciguatoxin-contaminated seafood from endemic areas, and consumption of ciguatoxin-contaminated seafood from certain areas of Macaronesia, such as Azores, the Madeira Islands (Portugal), and the Canary Islands (Spain).

The presence of CTXs in fish can be detected via screening methods, such as mouse bioassays, in vitro cell tests, and receptor binding assays, and confirmed using mass-spectrometry-based analyses. However, the lack of commercially available reference materials clearly indicates a challenge for marine toxins research. The increased presence of CTXs, combined with their occurrence in new latitudes and the contribution of climate change, is raising concerns globally. In this context, further investigations regarding CTX presence and origin in aquatic environments, the development of more sophisticated analysis methods, further data on human intoxication incidents, the toxicological potency of CTX analogues, and potential mitigation/regulatory management measures are considered to be extremely important.

This Special Issue aims to focus on new information and scientific evidence mainly with regard to: (i) CTX occurrence in aquatic environments, with an emphasis on edible aquatic organisms; (ii) analysis methods for the determination of CTXs; (iii) advances regarding CTX-producing organisms; (iv) environmental factors involved in the presence of CTXs; and (v) assessment of public health risks related to the presence of CTXs, as well as risk management and mitigation strategies. Studies addressing any other questions of relevance or reviews related to CTXs are also considered to be of interest and welcome for submission.

Dr. Panagiota Katikou
Dr. Marie-Yasmine Dechraoui Bottein
Guest Editors

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Keywords

  • ciguatera fish poisoning (CFP)
  • ciguatoxins
  • climate change
  • Gambierdiscus spp.
  • Fukuyoa spp.
  • analytical methods
  • risk management
  • analogues
  • toxicology
  • occurrence and epidemiology

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Published Papers (18 papers)

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27 pages, 3293 KiB  
Article
Depuration Kinetics and Growth Dilution of Caribbean Ciguatoxin in the Omnivore Lagodon rhomboides: Implications for Trophic Transfer and Ciguatera Risk
by Clayton T. Bennett and Alison Robertson
Toxins 2021, 13(11), 774; https://doi.org/10.3390/toxins13110774 - 01 Nov 2021
Cited by 11 | Viewed by 3318
Abstract
Modeling ciguatoxin (CTX) trophic transfer in marine food webs has significant implications for the management of ciguatera poisoning, a circumtropical disease caused by human consumption of CTX-contaminated seafood. Current models associated with CP risk rely on modeling abundance/presence of CTX-producing epi-benthic dinoflagellates, e.g., [...] Read more.
Modeling ciguatoxin (CTX) trophic transfer in marine food webs has significant implications for the management of ciguatera poisoning, a circumtropical disease caused by human consumption of CTX-contaminated seafood. Current models associated with CP risk rely on modeling abundance/presence of CTX-producing epi-benthic dinoflagellates, e.g., Gambierdiscus spp., and are based on studies showing that toxin production is site specific and occurs in pulses driven by environmental factors. However, food web models are not yet developed and require parameterizing the CTX exposure cascade in fish which has been traditionally approached through top-down assessment of CTX loads in wild-caught fish. The primary goal of this study was to provide critical knowledge on the kinetics of C-CTX-1 bioaccumulation and depuration in the marine omnivore Lagodon rhomboides. We performed a two-phase, 17 week CTX feeding trial in L. rhomboides where fish were given either a formulated C-CTX-1 (n = 40) or control feed (n = 37) for 20 days, and then switched to a non-toxic diet for up to 14 weeks. Fish were randomly sampled through time with whole muscle, liver, and other pooled viscera dissected for toxin analysis by a sodium channel-dependent MTT-based mouse neuroblastoma (N2a) assay. The CTX levels measured in all tissues increased with time during the exposure period (days 1 to 20), but a decrease in CTX-specific toxicity with depuration time only occurred in viscera extracts. By the end of the depuration, muscle, liver, and viscera samples had mean toxin concentrations of 189%, 128%, and 42%, respectively, compared to fish sampled at the start of the depuration phase. However, a one-compartment model analysis of combined tissues showed total concentration declined to 56%, resulting in an approximate half-life of 97 d (R2 = 0.43). Further, applying growth dilution correction models to the overall concentration found that growth was a major factor reducing C-CTX concentrations, and that the body burden was largely unchanged, causing pseudo-elimination and a half-life of 143–148 days (R2 = 0.36). These data have important implications for food web CTX models and management of ciguatera poisoning in endemic regions where the frequency of environmental algal toxin pulses may be greater than the growth-corrected half-life of C-CTX in intermediate-trophic-level fish with high site fidelity. Full article
(This article belongs to the Special Issue Ciguatoxins)
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14 pages, 362 KiB  
Article
Screening for Predictors of Chronic Ciguatera Poisoning: An Exploratory Analysis among Hospitalized Cases from French Polynesia
by Clémence Mahana iti Gatti, Kiyojiken Chung, Erwan Oehler, T. J. Pierce, Matthew O. Gribble and Mireille Chinain
Toxins 2021, 13(9), 646; https://doi.org/10.3390/toxins13090646 - 12 Sep 2021
Cited by 7 | Viewed by 2137
Abstract
Ciguatera poisoning is a globally occurring seafood disease caused by the ingestion of marine products contaminated with dinoflagellate produced neurotoxins. Persistent forms of ciguatera, which prove to be highly debilitating, are poorly studied and represent a significant medical issue. The present study aims [...] Read more.
Ciguatera poisoning is a globally occurring seafood disease caused by the ingestion of marine products contaminated with dinoflagellate produced neurotoxins. Persistent forms of ciguatera, which prove to be highly debilitating, are poorly studied and represent a significant medical issue. The present study aims to better understand chronic ciguatera manifestations and identify potential predictive factors for their duration. Medical files of 49 patients were analyzed, and the post-hospitalization evolution of the disease assessed through a follow-up questionnaire. A rigorous logistic lasso regression model was applied to select significant predictors from a list of 37 patient characteristics potentially predictive of having chronic symptoms. Missing data were handled by complete case analysis, and a survival analysis was implemented. All models used standardized variables, and multiple comparisons in the survival analyses were handled by Bonferroni correction. Among all studied variables, five significant predictors of having symptoms lasting ≥3 months were identified: age, tobacco consumption, acute bradycardia, laboratory measures of urea, and neutrophils. This exploratory, hypothesis-generating study contributes to the development of ciguatera epidemiology by narrowing the list from 37 possible predictors to a list of five predictors that seem worth further investigation as candidate risk factors in more targeted studies of ciguatera symptom duration. Full article
(This article belongs to the Special Issue Ciguatoxins)
18 pages, 5872 KiB  
Article
Ciguatoxin-Producing Dinoflagellate Gambierdiscus in the Beibu Gulf: First Report of Toxic Gambierdiscus in Chinese Waters
by Yixiao Xu, Xilin He, Wai Hin Lee, Leo Lai Chan, Douding Lu, Pengbin Wang, Xiaoping Tao, Huiling Li and Kefu Yu
Toxins 2021, 13(9), 643; https://doi.org/10.3390/toxins13090643 - 10 Sep 2021
Cited by 5 | Viewed by 2909
Abstract
Ciguatera poisoning is mainly caused by the consumption of reef fish that have accumulated ciguatoxins (CTXs) produced by the benthic dinoflagellates Gambierdiscus and Fukuyoa. China has a long history of problems with ciguatera, but research on ciguatera causative organisms is very limited, [...] Read more.
Ciguatera poisoning is mainly caused by the consumption of reef fish that have accumulated ciguatoxins (CTXs) produced by the benthic dinoflagellates Gambierdiscus and Fukuyoa. China has a long history of problems with ciguatera, but research on ciguatera causative organisms is very limited, especially in the Beibu Gulf, where coral reefs have been degraded significantly and CTXs in reef fish have exceeded food safety guidelines. Here, five strains of Gambierdiscus spp. were collected from Weizhou Island, a ciguatera hotspot in the Beibu Gulf, and identified by light and scanning electron microscopy and phylogenetic analyses based on large and small subunit rDNA sequences. Strains showed typical morphological characteristics of Gambierdiscus caribaeus, exhibiting a smooth thecal surface, rectangular-shaped 2′, almost symmetric 4″, and a large and broad posterior intercalary plate. They clustered in the phylogenetic tree with G. caribaeus from other locations. Therefore, these five strains belonged to G. caribaeus, a globally distributed Gambierdiscus species. Toxicity was determined through the mouse neuroblastoma assay and ranged from 0 to 5.40 fg CTX3C eq cell−1. The low level of toxicity of G. caribaeus in Weizhou Island, with CTX-contaminated fish above the regulatory level in the previous study, suggests that the long-term presence of low toxicity G. caribaeus might lead to the bioaccumulation of CTXs in fish, which can reach dangerous CTX levels. Alternatively, other highly-toxic, non-sampled strains could be present in these waters. This is the first report on toxic Gambierdiscus from the Beibu Gulf and Chinese waters and will provide a basis for further research determining effective strategies for ciguatera management in the area. Full article
(This article belongs to the Special Issue Ciguatoxins)
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12 pages, 1415 KiB  
Article
An Update on Ciguatoxins and CTX-like Toxicity in Fish from Different Trophic Levels of the Selvagens Islands (NE Atlantic, Madeira, Portugal)
by Pedro Reis Costa, Pablo Estévez, Lucía Soliño, David Castro, Susana Margarida Rodrigues, Viriato Timoteo, José Manuel Leao-Martins, Carolina Santos, Neide Gouveia, Jorge Diogène and Ana Gago-Martínez
Toxins 2021, 13(8), 580; https://doi.org/10.3390/toxins13080580 - 20 Aug 2021
Cited by 24 | Viewed by 3387
Abstract
The Selvagens Islands, which are a marine protected area located at the southernmost point of the Portuguese maritime zone, have been associated with fish harboring ciguatoxins (CTX) and linked to ciguatera fish poisonings. This study reports the results of a field sampling campaign [...] Read more.
The Selvagens Islands, which are a marine protected area located at the southernmost point of the Portuguese maritime zone, have been associated with fish harboring ciguatoxins (CTX) and linked to ciguatera fish poisonings. This study reports the results of a field sampling campaign carried out in September 2018 in these remote and rarely surveyed islands. Fifty-six fish specimens from different trophic levels were caught for CTX-like toxicity determination by cell-based assay (CBA) and toxin content analysis by liquid chromatography with tandem mass spectrometry (LC-MS/MS). Notably, high toxicity levels were found in fish with an intermediate position in the food web, such as zebra seabream (Diplodus cervinus) and barred hogfish (Bodianus scrofa), reaching levels up to 0.75 µg CTX1B equivalent kg−1. The LC-MS/MS analysis confirmed that C-CTX1 was the main toxin, but discrepancies between CBA and LC-MS/MS in D. cervinus and top predator species, such as the yellowmouth barracuda (Sphyraena viridis) and amberjacks (Seriola spp.), suggest the presence of fish metabolic products, which need to be further elucidated. This study confirms that fish from coastal food webs of the Selvagens Islands represent a high risk of ciguatera, raising important issues for fisheries and environmental management of the Selvagens Islands. Full article
(This article belongs to the Special Issue Ciguatoxins)
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19 pages, 1711 KiB  
Article
Experimental Evidence of Ciguatoxin Accumulation and Depuration in Carnivorous Lionfish
by Isabel do Prado Leite, Khalil Sdiri, Angus Taylor, Jérôme Viallon, Hela Ben Gharbia, Luiz Laureno Mafra Júnior, Peter Swarzenski, François Oberhaensli, Hélène Taiana Darius, Mireille Chinain and Marie-Yasmine Dechraoui Bottein
Toxins 2021, 13(8), 564; https://doi.org/10.3390/toxins13080564 - 11 Aug 2021
Cited by 10 | Viewed by 3112
Abstract
Ciguatera poisoning is a food intoxication associated with the consumption of fish or shellfish contaminated, through trophic transfer, with ciguatoxins (CTXs). In this study, we developed an experimental model to assess the trophic transfer of CTXs from herbivorous parrotfish, Chlorurus microrhinos, to [...] Read more.
Ciguatera poisoning is a food intoxication associated with the consumption of fish or shellfish contaminated, through trophic transfer, with ciguatoxins (CTXs). In this study, we developed an experimental model to assess the trophic transfer of CTXs from herbivorous parrotfish, Chlorurus microrhinos, to carnivorous lionfish, Pterois volitans. During a 6-week period, juvenile lionfish were fed naturally contaminated parrotfish fillets at a daily dose of 0.11 or 0.035 ng CTX3C equiv. g−1, as measured by the radioligand-receptor binding assay (r-RBA) or neuroblastoma cell-based assay (CBA-N2a), respectively. During an additional 6-week depuration period, the remaining fish were fed a CTX-free diet. Using r-RBA, no CTXs were detectable in muscular tissues, whereas CTXs were measured in the livers of two out of nine fish sampled during exposure, and in four out of eight fish sampled during depuration. Timepoint pooled liver samples, as analyzed by CBA-N2a, confirmed the accumulation of CTXs in liver tissues, reaching 0.89 ng CTX3C equiv. g−1 after 41 days of exposure, followed by slow toxin elimination, with 0.37 ng CTX3C equiv. g−1 measured after the 6-week depuration. These preliminary results, which need to be pursued in adult lionfish, strengthen our knowledge on CTX transfer and kinetics along the food web. Full article
(This article belongs to the Special Issue Ciguatoxins)
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22 pages, 2119 KiB  
Article
Asynchrony of Gambierdiscus spp. Abundance and Toxicity in the U.S. Virgin Islands: Implications for Monitoring and Management of Ciguatera
by Justin D. Liefer, Mindy L. Richlen, Tyler B. Smith, Jennifer L. DeBose, Yixiao Xu, Donald M. Anderson and Alison Robertson
Toxins 2021, 13(6), 413; https://doi.org/10.3390/toxins13060413 - 10 Jun 2021
Cited by 19 | Viewed by 4232
Abstract
Ciguatera poisoning (CP) poses a significant threat to ecosystem services and fishery resources in coastal communities. The CP-causative ciguatoxins (CTXs) are produced by benthic dinoflagellates including Gambierdiscus and Fukuyoa spp., and enter reef food webs via grazing on macroalgal substrates. In this study, [...] Read more.
Ciguatera poisoning (CP) poses a significant threat to ecosystem services and fishery resources in coastal communities. The CP-causative ciguatoxins (CTXs) are produced by benthic dinoflagellates including Gambierdiscus and Fukuyoa spp., and enter reef food webs via grazing on macroalgal substrates. In this study, we report on a 3-year monthly time series in St. Thomas, US Virgin Islands where Gambierdiscus spp. abundance and Caribbean-CTX toxicity in benthic samples were compared to key environmental factors, including temperature, salinity, nutrients, benthic cover, and physical data. We found that peak Gambierdiscus abundance occurred in summer while CTX-specific toxicity peaked in cooler months (February–May) when the mean water temperatures were approximately 26–28 °C. These trends were most evident at deeper offshore sites where macroalgal cover was highest year-round. Other environmental parameters were not correlated with the CTX variability observed over time. The asynchrony between Gambierdiscus spp. abundance and toxicity reflects potential differences in toxin cell quotas among Gambierdiscus species with concomitant variability in their abundances throughout the year. These results have significant implications for monitoring and management of benthic harmful algal blooms and highlights potential seasonal and highly-localized pulses in reef toxin loads that may be transferred to higher trophic levels. Full article
(This article belongs to the Special Issue Ciguatoxins)
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12 pages, 3444 KiB  
Article
Characteristic Distribution of Ciguatoxins in the Edible Parts of a Grouper, Variola louti
by Naomasa Oshiro, Hiroya Nagasawa, Kyoko Kuniyoshi, Naoki Kobayashi, Yoshiko Sugita-Konishi, Hiroshi Asakura and Takeshi Yasumoto
Toxins 2021, 13(3), 218; https://doi.org/10.3390/toxins13030218 - 17 Mar 2021
Cited by 19 | Viewed by 2666
Abstract
Ciguatera fish poisoning (CFP) is one of the most frequently encountered seafood poisoning syndromes; it is caused by the consumption of marine finfish contaminated with ciguatoxins (CTXs). The majority of CFP cases result from eating fish flesh, but a traditional belief exists among [...] Read more.
Ciguatera fish poisoning (CFP) is one of the most frequently encountered seafood poisoning syndromes; it is caused by the consumption of marine finfish contaminated with ciguatoxins (CTXs). The majority of CFP cases result from eating fish flesh, but a traditional belief exists among people that the head and viscera are more toxic and should be avoided. Unlike the viscera, scientific data to support the legendary high toxicity of the head is scarce. We prepared tissue samples from the fillet, head, and eyes taken from five yellow-edged lyretail (Variola louti) individuals sourced from Okinawa, Japan, and analyzed the CTXs by LC-MS/MS. Three CTXs, namely, CTX1B, 52-epi-54-deoxyCTX1B, and 54-deoxyCTX1B, were confirmed in similar proportions. The toxins were distributed nearly evenly in the flesh, prepared separately from the fillet and head. Within the same individual specimen, the flesh in the fillet and the flesh from the head, tested separately, had the same level and composition of toxins. We, therefore, conclude that flesh samples for LC-MS/MS analysis can be taken from any part of the body. However, the tissue surrounding the eyeball displayed CTX levels two to four times higher than those of the flesh. The present study is the first to provide scientific data demonstrating the high toxicity of the eyes. Full article
(This article belongs to the Special Issue Ciguatoxins)
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22 pages, 4719 KiB  
Article
Effects of pH and Nutrients (Nitrogen) on Growth and Toxin Profile of the Ciguatera-Causing Dinoflagellate Gambierdiscus polynesiensis (Dinophyceae)
by Sébastien Longo, Manoëlla Sibat, Hélène Taiana Darius, Philipp Hess and Mireille Chinain
Toxins 2020, 12(12), 767; https://doi.org/10.3390/toxins12120767 - 04 Dec 2020
Cited by 15 | Viewed by 2700
Abstract
Ciguatera poisoning is a foodborne disease caused by the consumption of seafood contaminated with ciguatoxins (CTXs) produced by dinoflagellates in the genera Gambierdiscus and Fukuyoa. Ciguatera outbreaks are expected to increase worldwide with global change, in particular as a function of its [...] Read more.
Ciguatera poisoning is a foodborne disease caused by the consumption of seafood contaminated with ciguatoxins (CTXs) produced by dinoflagellates in the genera Gambierdiscus and Fukuyoa. Ciguatera outbreaks are expected to increase worldwide with global change, in particular as a function of its main drivers, including changes in sea surface temperature, acidification, and coastal eutrophication. In French Polynesia, G. polynesiensis is regarded as the dominant source of CTXs entering the food web. The effects of pH (8.4, 8.2, and 7.9), Nitrogen:Phosphorus ratios (24N:1P vs. 48N:1P), and nitrogen source (nitrates vs. urea) on growth rate, biomass, CTX levels, and profiles were examined in four clones of G. polynesiensis at different culture age (D10, D21, and D30). Results highlight a decrease in growth rate and cellular biomass at low pH when urea is used as a N source. No significant effect of pH, N:P ratio, and N source on the overall CTX content was observed. Up to ten distinct analogs of Pacific ciguatoxins (P-CTXs) could be detected by liquid chromatography-tandem mass spectrometry (LC-MS/MS) in clone NHA4 grown in urea, at D21. Amounts of more oxidized P-CTX analogs also increased under the lowest pH condition. These data provide interesting leads for the custom production of CTX standards. Full article
(This article belongs to the Special Issue Ciguatoxins)
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28 pages, 4841 KiB  
Article
Evidence for the Range Expansion of Ciguatera in French Polynesia: A Revisit of the 2009 Mass-Poisoning Outbreak in Rapa Island (Australes Archipelago)
by Mireille Chinain, Clémence Mahana iti Gatti, André Ung, Philippe Cruchet, Taina Revel, Jérôme Viallon, Manoëlla Sibat, Patrick Varney, Victoire Laurent, Philipp Hess and Hélène Taiana Darius
Toxins 2020, 12(12), 759; https://doi.org/10.3390/toxins12120759 - 01 Dec 2020
Cited by 24 | Viewed by 3158
Abstract
Ciguatera poisoning (CP) results from the consumption of seafood contaminated with ciguatoxins (CTXs). This disease is highly prevalent in French Polynesia with several well-identified hotspots. Rapa Island, the southernmost inhabited island in the country, was reportedly free of CP until 2007. This study [...] Read more.
Ciguatera poisoning (CP) results from the consumption of seafood contaminated with ciguatoxins (CTXs). This disease is highly prevalent in French Polynesia with several well-identified hotspots. Rapa Island, the southernmost inhabited island in the country, was reportedly free of CP until 2007. This study describes the integrated approach used to investigate the etiology of a fatal mass-poisoning outbreak that occurred in Rapa in 2009. Symptoms reported in patients were evocative of ciguatera. Several Gambierdiscus field samples collected from benthic assemblages tested positive by the receptor binding assay (RBA). Additionally, the toxicity screening of ≈250 fish by RBA indicated ≈78% of fish could contain CTXs. The presence of CTXs in fish was confirmed by liquid chromatography tandem mass spectrometry (LC-MS/MS). The potential link between climate change and this range expansion of ciguatera to a subtropical locale of French Polynesia was also examined based on the analysis of temperature time-series data. Results are indicative of a global warming trend in Rapa area. A five-fold reduction in incidence rates was observed between 2009 and 2012, which was due in part to self-regulating behavior among individuals (avoidance of particular fish species and areas). Such observations underscore the prominent role played by community outreach in ciguatera risk management. Full article
(This article belongs to the Special Issue Ciguatoxins)
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17 pages, 2912 KiB  
Article
Stereoselective Synthesis of the I–L Fragment of the Pacific Ciguatoxins
by J. Stephen Clark and Michael Popadynec
Toxins 2020, 12(12), 740; https://doi.org/10.3390/toxins12120740 - 24 Nov 2020
Cited by 3 | Viewed by 2574
Abstract
The I–L ring system found in all the Pacific ciguatoxins has been prepared from a tricyclic precursor in a highly stereoselective manner. Subtle differences in the reactivity of the enones present in the seven- and eight-membered rings of the tricyclic ether starting material [...] Read more.
The I–L ring system found in all the Pacific ciguatoxins has been prepared from a tricyclic precursor in a highly stereoselective manner. Subtle differences in the reactivity of the enones present in the seven- and eight-membered rings of the tricyclic ether starting material have been exploited to allow selective protection of the enone in the eight-membered ring. Subsequent distereoselective allylation of the seven-membered ring has been accomplished by a palladium-mediated Tsuji-Trost reaction. The K-ring methyl and hydroxyl groups have been installed in a highly stereoselective manner by sequential conjugate reduction and enolate oxidation reactions. Ring L has been constructed by a use of a novel relay ring-closing metathesis reaction to complete the tetracyclic framework, which possesses the functionality necessary for elaboration of rings I and L and the introduction of ring M. Full article
(This article belongs to the Special Issue Ciguatoxins)
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23 pages, 2764 KiB  
Article
Further Advance of Gambierdiscus Species in the Canary Islands, with the First Report of Gambierdiscus belizeanus
by Àngels Tudó, Greta Gaiani, Maria Rey Varela, Takeshi Tsumuraya, Karl B. Andree, Margarita Fernández-Tejedor, Mònica Campàs and Jorge Diogène
Toxins 2020, 12(11), 692; https://doi.org/10.3390/toxins12110692 - 31 Oct 2020
Cited by 27 | Viewed by 2861
Abstract
Ciguatera Poisoning (CP) is a human food-borne poisoning that has been known since ancient times to be found mainly in tropical and subtropical areas, which occurs when fish or very rarely invertebrates contaminated with ciguatoxins (CTXs) are consumed. The genus of marine benthic [...] Read more.
Ciguatera Poisoning (CP) is a human food-borne poisoning that has been known since ancient times to be found mainly in tropical and subtropical areas, which occurs when fish or very rarely invertebrates contaminated with ciguatoxins (CTXs) are consumed. The genus of marine benthic dinoflagellates Gambierdiscus produces CTX precursors. The presence of Gambierdiscus species in a region is one indicator of CP risk. The Canary Islands (North Eastern Atlantic Ocean) is an area where CP cases have been reported since 2004. In the present study, samplings for Gambierdiscus cells were conducted in this area during 2016 and 2017. Gambierdiscus cells were isolated and identified as G. australes, G. excentricus, G. caribaeus, and G. belizeanus by molecular analysis. In this study, G. belizeanus is reported for the first time in the Canary Islands. Gambierdiscus isolates were cultured, and the CTX-like toxicity of forty-one strains was evaluated with the neuroblastoma cell-based assay (neuro-2a CBA). G. excentricus exhibited the highest CTX-like toxicity (9.5–2566.7 fg CTX1B equiv. cell−1) followed by G. australes (1.7–452.6.2 fg CTX1B equiv. cell−1). By contrast, the toxicity of G. belizeanus was low (5.6 fg CTX1B equiv. cell−1), and G. caribaeus did not exhibit CTX-like toxicity. In addition, for the G. belizeanus strain, the production of CTXs was evaluated with a colorimetric immunoassay and an electrochemical immunosensor resulting in G. belizeanus producing two types of CTX congeners (CTX1B and CTX3C series congeners) and can contribute to CP in the Canary Islands. Full article
(This article belongs to the Special Issue Ciguatoxins)
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18 pages, 2190 KiB  
Article
Assessment of Ciguatera and Other Phycotoxin-Related Risks in Anaho Bay (Nuku Hiva Island, French Polynesia): Molecular, Toxicological, and Chemical Analyses of Passive Samplers
by Mélanie Roué, Kirsty F. Smith, Manoella Sibat, Jérôme Viallon, Kévin Henry, André Ung, Laura Biessy, Philipp Hess, Hélène Taiana Darius and Mireille Chinain
Toxins 2020, 12(5), 321; https://doi.org/10.3390/toxins12050321 - 13 May 2020
Cited by 14 | Viewed by 3395
Abstract
Ciguatera poisoning is a foodborne illness caused by the consumption of seafood contaminated with ciguatoxins (CTXs) produced by dinoflagellates from the genera Gambierdiscus and Fukuyoa. The suitability of Solid Phase Adsorption Toxin Tracking (SPATT) technology for the monitoring of dissolved CTXs in [...] Read more.
Ciguatera poisoning is a foodborne illness caused by the consumption of seafood contaminated with ciguatoxins (CTXs) produced by dinoflagellates from the genera Gambierdiscus and Fukuyoa. The suitability of Solid Phase Adsorption Toxin Tracking (SPATT) technology for the monitoring of dissolved CTXs in the marine environment has recently been demonstrated. To refine the use of this passive monitoring tool in ciguateric areas, the effects of deployment time and sampler format on the adsorption of CTXs by HP20 resin were assessed in Anaho Bay (Nuku Hiva Island, French Polynesia), a well-known ciguatera hotspot. Toxicity data assessed by means of the mouse neuroblastoma cell-based assay (CBA-N2a) showed that a 24 h deployment of 2.5 g of resin allowed concentrating quantifiable amounts of CTXs on SPATT samplers. The CTX levels varied with increasing deployment time, resin load, and surface area. In addition to CTXs, okadaic acid (OA) and dinophysistoxin-1 (DTX1) were also detected in SPATT extracts using liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS), consistent with the presence of Gambierdiscus and Prorocentrum species in the environment, as assessed by quantitative polymerase chain reaction (qPCR) and high-throughput sequencing (HTS) metabarcoding analyses conducted on passive window screen (WS) artificial substrate samples. Although these preliminary findings await further confirmation in follow-up studies, they highlight the usefulness of SPATT samplers in the routine surveillance of CP risk on a temporal scale, and the monitoring of other phycotoxin-related risks in ciguatera-prone areas. Full article
(This article belongs to the Special Issue Ciguatoxins)
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14 pages, 1664 KiB  
Article
Evaluation of Matrix Issues in the Applicability of the Neuro-2a Cell Based Assay on the Detection of CTX in Fish Samples
by David Castro, Ronald Manger, Oscar Vilariño and Ana Gago-Martínez
Toxins 2020, 12(5), 308; https://doi.org/10.3390/toxins12050308 - 09 May 2020
Cited by 16 | Viewed by 2755
Abstract
Ciguatoxins (CTXs) are a group of neurotoxins responsible for the syndrome ciguatera fish poisoning (CFP) as a result of the consumption of contaminated fish. The presence of these toxins has been detected around the Pacific, Caribbean and Indian coasts. Recent reports indicate the [...] Read more.
Ciguatoxins (CTXs) are a group of neurotoxins responsible for the syndrome ciguatera fish poisoning (CFP) as a result of the consumption of contaminated fish. The presence of these toxins has been detected around the Pacific, Caribbean and Indian coasts. Recent reports indicate the emergence of CFP in other geographic areas, in particular in European coasts, of the Canary Islands (Spain) and Madeira (Portugal). A neuroblastoma cell line of murine origin (N2a) has been applied to assay different groups of neurotoxins, acting on voltage-gated sodium channel (VGSC) of excitable cells, N2a-MTT. The great potential of N2a-MTT as a sensitive tool for the CTXs screening is clearly recognized, notably because it allows the detection of these toxins at levels below recommended as security levels. However, the complexity of the matrix is a critical point on the application of N2a-MTT, which needs to be evaluated. The aim of this work is to provide recommendations for an implemented N2a-MTT method for CTXs determination in fish that avoids matrix effects, particularly those related to high lipid content. Full article
(This article belongs to the Special Issue Ciguatoxins)
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20 pages, 5835 KiB  
Article
Use of Mass Spectrometry to Determine the Diversity of Toxins Produced by Gambierdiscus and Fukuyoa Species from Balearic Islands and Crete (Mediterranean Sea) and the Canary Islands (Northeast Atlantic)
by Pablo Estevez, Manoëlla Sibat, José Manuel Leão-Martins, Angels Tudó, Maria Rambla-Alegre, Katerina Aligizaki, Jorge Diogène, Ana Gago-Martinez and Philipp Hess
Toxins 2020, 12(5), 305; https://doi.org/10.3390/toxins12050305 - 07 May 2020
Cited by 27 | Viewed by 3878
Abstract
Over the last decade, knowledge has significantly increased on the taxonomic identity and distribution of dinoflagellates of the genera Gambierdiscus and Fukuyoa. Additionally, a number of hitherto unknown bioactive metabolites have been described, while the role of these compounds in ciguatera poisoning [...] Read more.
Over the last decade, knowledge has significantly increased on the taxonomic identity and distribution of dinoflagellates of the genera Gambierdiscus and Fukuyoa. Additionally, a number of hitherto unknown bioactive metabolites have been described, while the role of these compounds in ciguatera poisoning (CP) remains to be clarified. Ciguatoxins and maitotoxins are very toxic compounds produced by these dinoflagellates and have been described since the 1980s. Ciguatoxins are generally described as the main contributors to this food intoxication. Recent reports of CP in temperate waters of the Canary Islands (Spain) and the Madeira archipelago (Portugal) triggered the need for isolation and cultivation of dinoflagellates from these areas, and their taxonomic and toxicological characterization. Maitotoxins, and specifically maitotoxin-4, has been described as one of the most toxic compounds produced by these dinoflagellates (e.g., G. excentricus) in the Canary Islands. Thus, characterization of toxin profiles of Gambierdiscus species from adjacent regions appears critical. The combination of liquid chromatography coupled to either low- or high-resolution mass spectrometry allowed for characterization of several strains of Gambierdiscus and Fukuyoa from the Mediterranean Sea and the Canary Islands. Maitotoxin-3, two analogues tentatively identified as gambieric acid C and D, a putative gambierone analogue and a putative gambieroxide were detected in all G. australes strains from Menorca and Mallorca (Balearic Islands, Spain) while only maitotoxin-3 was present in an F. paulensis strain of the same region. An unidentified Gambierdiscus species (Gambierdiscus sp.2) from Crete (Greece) showed a different toxin profile, detecting both maitotoxin-3 and gambierone, while the availability of a G. excentricus strain from the Canary Islands (Spain) confirmed the presence of maitotoxin-4 in this species. Overall, this study shows that toxin profiles not only appear to be species-specific but probably also specific to larger geographic regions. Full article
(This article belongs to the Special Issue Ciguatoxins)
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7 pages, 1871 KiB  
Communication
Liquid Chromatography Coupled to High-Resolution Mass Spectrometry for the Confirmation of Caribbean Ciguatoxin-1 as the Main Toxin Responsible for Ciguatera Poisoning Caused by Fish from European Atlantic Coasts
by Pablo Estevez, Manoella Sibat, José Manuel Leão-Martins, Pedro Reis Costa, Ana Gago-Martínez and Philipp Hess
Toxins 2020, 12(4), 267; https://doi.org/10.3390/toxins12040267 - 21 Apr 2020
Cited by 27 | Viewed by 3819
Abstract
Ciguatera poisoning (CP) is a common seafood intoxication mainly caused by the consumption of fish contaminated by ciguatoxins. Recent studies showed that Caribbean ciguatoxin-1 (C-CTX1) is the main toxin causing CP through fish caught in the Northeast Atlantic, e.g., Canary Islands (Spain) and [...] Read more.
Ciguatera poisoning (CP) is a common seafood intoxication mainly caused by the consumption of fish contaminated by ciguatoxins. Recent studies showed that Caribbean ciguatoxin-1 (C-CTX1) is the main toxin causing CP through fish caught in the Northeast Atlantic, e.g., Canary Islands (Spain) and Madeira (Portugal). The use of liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS) combined with neuroblastoma cell assay (N2a) allowed the initial confirmation of the presence of C-CTX1 in contaminated fish samples from the abovementioned areas, nevertheless the lack of commercially available reference materials for these particular ciguatoxin (CTX) analogues has been a major limitation to progress research. The EuroCigua project allowed the preparation of C-CTX1 laboratory reference material (LRM) from fish species (Seriola fasciata) from the Madeira archipelago (Portugal). This reference material was used to implement a liquid chromatography coupled to high-resolution mass spectrometry (LC-HRMS) for the detection of C-CTX1, acquisition of full-scan as well as collision-induced mass spectra of this particular analogue. Fragmentation pathways were proposed based on fragments obtained. The optimized LC-HRMS method was then applied to confirm C-CTX1 in fish (Bodianus scrofa) caught in the Selvagens Islands (Portugal). Full article
(This article belongs to the Special Issue Ciguatoxins)
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Review

Jump to: Research

21 pages, 3447 KiB  
Review
Digital Technologies and Open Data Sources in Marine Biotoxins’ Risk Analysis: The Case of Ciguatera Fish Poisoning
by Panagiota Katikou
Toxins 2021, 13(10), 692; https://doi.org/10.3390/toxins13100692 - 30 Sep 2021
Cited by 5 | Viewed by 2703
Abstract
Currently, digital technologies influence information dissemination in all business sectors, with great emphasis put on exploitation strategies. Public administrations often use information systems and establish open data repositories, primarily supporting their operation but also serving as data providers, facilitating decision-making. As such, risk [...] Read more.
Currently, digital technologies influence information dissemination in all business sectors, with great emphasis put on exploitation strategies. Public administrations often use information systems and establish open data repositories, primarily supporting their operation but also serving as data providers, facilitating decision-making. As such, risk analysis in the public health sector, including food safety authorities, often relies on digital technologies and open data sources. Global food safety challenges include marine biotoxins (MBs), being contaminants whose mitigation largely depends on risk analysis. Ciguatera Fish Poisoning (CFP), in particular, is a MB-related seafood intoxication attributed to the consumption of fish species that are prone to accumulate ciguatoxins. Historically, CFP occurred endemically in tropical/subtropical areas, but has gradually emerged in temperate regions, including European waters, necessitating official policy adoption to manage the potential risks. Researchers and policy-makers highlight scientific data inadequacy, under-reporting of outbreaks and information source fragmentation as major obstacles in developing CFP mitigation strategies. Although digital technologies and open data sources provide exploitable scientific information for MB risk analysis, their utilization in counteracting CFP-related hazards has not been addressed to date. This work thus attempts to answer the question, “What is the current extent of digital technologies’ and open data sources’ utilization within risk analysis tasks in the MBs field, particularly on CFP?”, by conducting a systematic literature review of the available scientific and grey literature. Results indicate that the use of digital technologies and open data sources in CFP is not negligible. However, certain gaps are identified regarding discrepancies in terminology, source fragmentation and a redundancy and downplay of social media utilization, in turn constituting a future research agenda for this under-researched topic. Full article
(This article belongs to the Special Issue Ciguatoxins)
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22 pages, 6514 KiB  
Review
Ciguatera in the Indian Ocean with Special Insights on the Arabian Sea and Adjacent Gulf and Seas: A Review
by Nazima Habibi, Saif Uddin, Marie-Yasmine Dechraoui Bottein and Mohd Faizuddin
Toxins 2021, 13(8), 525; https://doi.org/10.3390/toxins13080525 - 27 Jul 2021
Cited by 15 | Viewed by 4695
Abstract
The dinoflagellates of the genus Gambierdiscus are found in almost all oceans and seas between the coordinates 35° N and 35° S. Gambierdiscus and Fukuyoa are producers of ciguatoxins (CTXs), which are known to cause foodborne disease associated with contaminated seafood. The occurrence [...] Read more.
The dinoflagellates of the genus Gambierdiscus are found in almost all oceans and seas between the coordinates 35° N and 35° S. Gambierdiscus and Fukuyoa are producers of ciguatoxins (CTXs), which are known to cause foodborne disease associated with contaminated seafood. The occurrence and effects of CTXs are well described in the Pacific and the Caribbean. However, historically, their properties and presence have been poorly documented in the Indian Ocean (including the Bay of Bengal, Andaman Sea, and the Gulf). A higher occurrence of these microorganisms will proportionately increase the likelihood of CTXs entering the food chain, posing a severe threat to human seafood consumers. Therefore, comprehensive research strategies are critically important for developing effective monitoring and risk assessments of this emerging threat in the Indian Ocean. This review presents the available literature on ciguatera occurrence in the region and its adjacent marginal waters: aiming to identify the data gaps and vectors. Full article
(This article belongs to the Special Issue Ciguatoxins)
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27 pages, 2702 KiB  
Review
Advances in Detecting Ciguatoxins in Fish
by Tibor Pasinszki, Jimaima Lako and Todd E. Dennis
Toxins 2020, 12(8), 494; https://doi.org/10.3390/toxins12080494 - 31 Jul 2020
Cited by 28 | Viewed by 8229
Abstract
Ciguatera fish poisoning (CFP) is currently the most common marine biotoxin food poisoning worldwide, associated with human consumption of circumtropical fish and marine invertebrates that are contaminated with ciguatoxins. Ciguatoxins are very potent sodium-channel activator neurotoxins, that pose risks to human health at [...] Read more.
Ciguatera fish poisoning (CFP) is currently the most common marine biotoxin food poisoning worldwide, associated with human consumption of circumtropical fish and marine invertebrates that are contaminated with ciguatoxins. Ciguatoxins are very potent sodium-channel activator neurotoxins, that pose risks to human health at very low concentrations (>0.01 ng per g of fish flesh in the case of the most potent Pacific ciguatoxin). Symptoms of CFP are nonspecific and intoxication in humans is often misdiagnosed. Presently, there is no medically approved treatment of ciguatera. Therefore, to mitigate the risks of CFP, reliable detection of ciguatoxins prior to consumption of fish tissue is acutely needed, which requires application of highly sensitive and quantitative analytical tests. During the last century a number of methods have been developed to identify and quantify the concentration of ciguatoxins, including in vivo animal assays, cell-based assays, receptor binding assays, antibody-based immunoassays, electrochemical methods, and analytical techniques based on coupling of liquid chromatography with mass spectrometry. Development of these methods, their various advantages and limitations, as well as future challenges are discussed in this review. Full article
(This article belongs to the Special Issue Ciguatoxins)
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