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Mar Drugs
2018 Apr 06;164:. doi: 10.3390/md16040122.
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Toxicological Investigations on the Sea Urchin Tripneustes gratilla (Toxopneustidae, Echinoid) from Anaho Bay (Nuku Hiva, French Polynesia): Evidence for the Presence of Pacific Ciguatoxins.
Darius HT
,
Roué M
,
Sibat M
,
Viallon J
,
Gatti CMII
,
Vandersea MW
,
Tester PA
,
Litaker RW
,
Amzil Z
,
Hess P
,
Chinain M
.
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The sea urchin Tripneustes gratilla (Toxopneustidae, Echinoids) is a source of protein for many islanders in the Indo-West Pacific. It was previously reported to occasionally cause ciguatera-like poisoning; however, the exact nature of the causative agent was not confirmed. In April and July 2015, ciguatera poisonings were reported following the consumption of T.gratilla in Anaho Bay (Nuku Hiva Island, Marquesas archipelago, French Polynesia). Patient symptomatology was recorded and sea urchin samples were collected from Anaho Bay in July 2015 and November 2016. Toxicity analysis using the neuroblastoma cell-based assay (CBA-N2a) detected the presence of ciguatoxins (CTXs) in T.gratilla samples. Gambierdiscus species were predominant in the benthic assemblages of Anaho Bay, and G.polynesiensis was highly prevalent in in vitro cultures according to qPCR results. Liquid chromatography-tandem mass spectrometry (LC-MS/MS) analyses revealed that P-CTX-3B was the major ciguatoxin congener in toxic sea urchin samples, followed by 51-OH-P-CTX-3C, P-CTX-3C, P-CTX-4A, and P-CTX-4B. Between July 2015 and November 2016, the toxin content in T.gratilla decreased, but was consistently above the safety limit allowed for human consumption. This study provides evidence of CTX bioaccumulation in T.gratilla as a cause of ciguatera-like poisoning associated with a documented symptomatology.
Figure 2. Maps of (A) French Polynesia and (B) Moorea Island (Society archipelago), Rurutu Island (Australes archipelago), and Nuku Hiva Island (Marquesas archipelago).
Figure 3. Dose-response curves of neuro-2a cells not treated with ouabain and veratridine (OV−; open symbols) and treated with ouabain and veratridine (OV+; solid symbols), when exposed to increasing concentrations of liposoluble fractions of Gambierdiscus strains isolated from Anaho Bay. Liposoluble fractions from NHA1 (○/●), NHA4 (◇/◆), NHA9 (□/■), NHA14 (△/▲), NHA22 (▽/▼), NHA24 (○/●). Data represent the mean ± SD of three independent experiments (each concentration run in triplicate). The dotted vertical line corresponds to the maximum concentration of dry extract (MCE = 10,000 pg/µL) for matrix interference.
Figure 4. Dose-response curves of neuro-2a cells in OV− (open symbols) and OV+ (solid symbols) conditions, when exposed to increasing concentrations of Tripneustes gratilla fractions (Anaho Bay, July 2015). (a) Liposoluble fractions LF70/30 (○/●), LF90/10 (△/▲) and LF100 (□/■); (b) hydrosoluble fractions HF50/50 (▽/▼), HF70/30 (◇/◆), HF90/10 (○/●), and HF100 (/). Data represent the mean ± SD of two independent experiments (each concentration run in triplicate). The dotted vertical line corresponds to the maximum concentration of dry extract (MCE = 10,000 pg/µL) for matrix interferences.
Figure 5. Dose-response curves of neuro-2a cells in OV− (open symbols) and OV+ (solid symbols) conditions, when exposed to increasing concentrations of Tripneustes gratilla fractions (Anaho Bay, November 2016). Liposoluble fractions LF70/30 (○/●), LF90/10 (△/▲), and LF100 (□/■). Data represent the mean ± SD of two independent experiments (each concentration run in triplicate). The two last points of LF90/10 in OV− and OV+ conditions were not included in the curve, as they increased and were above the MCE. The dotted vertical line corresponds to the maximum concentration of dry extract (MCE = 10,000 pg/µL) for matrix interferences.
Figure 6. LC-MS/MS chromatograms obtained for (A) a mix of P-CTX standards (provided by Institut Louis Malardé) and solid phase extraction–purified extracts of Tripneustes gratilla collected from Anaho Bay in (B) July 2015 and (C) November 2016. Chromatograms were acquired following the procedure described in Section 4.5, in positive multireaction monitoring mode.
Figure 7. Maps of (A,B) French Polynesia, (C) Marquesas archipelago, and (D) study site of Anaho Bay on Nuku Hiva Island.
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