Toxicological Investigations on the Sea Urchin Tripneustes gratilla (Toxopneustidae, Echinoid) from Anaho Bay (Nuku Hiva, French Polynesia): Evidence for the Presence of Pacific Ciguatoxins

Abstract

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.

Intraspecific Variability in the Toxin Production and Toxin Profiles of In Vitro Cultures of Gambierdiscus polynesiensis (Dinophyceae) from French Polynesia

“…blooms can provide baseline knowledge on the factors likely to influence fish ciguatoxicity in ciguatera-prone areas, and are therefore useful to inform CP risk models. The species G. polynesiensis is regarded as the dominant producer of CTXs in the food webs in French Polynesian lagoons [73]. The aim of the present study was to assess the overall toxin production and to characterize the toxin profiles in four strains of G. polynesiensis from distinct localities in French Polynesia, in relation to their growth stages.…”

Ciguatoxin Occurrence in Food-Web Components of a Cuban Coral Reef Ecosystem: Risk-Assessment Implications

“…g −1 ) than many of the fish species. Ciguatoxin occurrence in invertebrate species has been reported in other studies from the Pacific Islands [39,40], where they have been involved in ciguatera poisoning incidents [41]. However, they have not yet been included on any list of species of concern in the affected countries [42].…”

Tissue Distribution and Elimination of Ciguatoxins in Tridacna maxima (Tridacnidae, Bivalvia) Fed Gambierdiscus polynesiensis

“…Here, LC-MS/MS data indicated that P-CTX3B and P-CTX3C, present in almost similar proportions (assuming the same response factor in LC-MS/MS for P-CTX3B and P-CTX3C), were the only known analogs detected in all tissue samples, even though the potential presence of other CTX congeners at concentrations below the limit of detection of the technique cannot be completely ruled out. Interestingly, P-CTX3B and P-CTX3C were also among the major congeners detected in Tectus niloticus (Gastropod) and Tripneustes gratilla (Echinoid) specimens involved in CFP poisoning events in French Polynesia [ 13 , 14 ], suggesting that both congeners are preferentially bio-accumulated by marine invertebrates.…”

“…These results are consistent with field studies conducted on other marine invertebrates species also involved in CFP poisoning events in French Polynesia, which indicated that Tectus niloticus (Gastropod) and Tripneustes gratilla (Echinoid) have a slow detoxification rate for CTXs. Indeed, based on CBA-N2a results, a 19-fold and 64-fold decrease in the overall ciguatoxicity of Tectus niloticus and Tripneustes gratilla samples, respectively, was observed over a two-year period, but toxin concentrations were still consistently above the safety limit recommended for human consumption [ 13 , 14 ]. Of note, the authors also underlined that these findings may be confounded by the additional accumulation of CTXs over the study period, even in the presence of low cell numbers of Gambierdiscus .…”

“…The clinical manifestations of the disease classically involve gastrointestinal disorders, cold allodynia, itching, paresthesia, asthenia, muscular pain, and dizziness, together with other neurological and cardio-vascular symptoms [ 7 ]. Although coral reef fish are usually regarded as the primary vectors of ciguatera, atypical ciguatera-like poisoning events following the consumption of giant clams ( Tridacna maxima ), marine gastropods ( Tectus niloticus ), and sea urchins ( Tripneustes gratilla ) are also occasionally reported from PICTs, most notably from French Polynesia, New Caledonia, Cook Islands, and the Republic of Vanuatu [ 8 , 9 , 10 , 11 , 12 , 13 , 14 ]. Besides the symptoms typical of CFP, atypical signs were also observed, such as the rapid onset of the disease (occurring within minutes), alteration of taste, burning sensation on the tongue and throat, as well as paralysis.…”