Identification of ciguatoxins in a shark involved in a fatal food poisoning in the Indian Ocean
Résumé
Severe food poisoning events after the consumption of sharks have been reported since the 1940s; however, there has been no clear understanding of their cause. Herein, we report for the first time the presence of ciguatoxins (CTXs) in sharks. The identification by mass spectrometry of CTXs, including two new analogues, in a bull shark (Carcharhinus leucas) that was consumed by humans, causing the poisoning and death of 11 people in Madagascar in 2013 is described. Typical neurotoxic ciguatera symptoms were recorded in patients, and toxicological assays on extracts of the shark demonstrated CTX-like activity. These results confirm this episode as a ciguatera poisoning event and expand the range of pelagic fish species that are involved in ciguatera in the Indian Ocean. Additionally, gambieric acid D, a molecule originally described in CTX-producing microalgae, was identified for the first time in fish. This finding can contribute to a better understanding of trophic relations within food webs. The present work confirms that consumption of sharks from the Indian Ocean should be considered a ciguatera risk, and actions should be taken to evaluate its magnitude and risk in order to manage shark fisheries. Ciguatera is a well-known food poisoning that occurs when fish containing ciguatoxins (CTXs) are consumed. These potent neurotoxins are produced by microalgae of the genus Gambierdiscus 1-3 and Fukuyoa 4, 5. Ciguatoxins produced by these microalgae may be transferred along the food web, eventually reaching carnivorous fish like barracuda or amberjack. Ciguatera is the main cause of seafood poisoning due to the consumption of fish, and estimations point out around 50,000-500,000 people are affected by ciguatera each year 6 , although these should be re-evaluated for a better assessment of the present impact of ciguatera. Numerous incidences of human poisoning after the consumption of several species of shark have been reported since the 1940s. These cases have been proposed to be ciguatera events according to the toxicity in animal assays or due to the symptoms in patients 7. However, the presence of CTXs has never been confirmed in sharks. In Madagascar, a first possible event of ciguatera was described in 1993, after the consumption of shark in Manakara (south-east coast) and was noted for its unprecedented severity. Several hundred people (between 200 and 500 depending on the different authors) were poisoned due to the consumption of a shark, either a bull shark (Carcharhinus leucas) or a pigeye shark (C. amboinensis), two species that are difficult to distinguish. This event resulted in the death of between 60 and 98 people, depending on the different authors, a fatality rate of 20 to 30% 8, 9. In this particular event, patients presented almost exclusively neurological symptoms. Boisier et al. identified two toxic extracts from the liver of the shark, which were proposed to be the causative agent of the poisoning, and tentatively named the new toxins as carchatoxin-A and carchatoxin-B 9. However, the toxicity levels of the shark flesh did not match that of the liver extracts, and thus, toxicity remained unexplained. No further information 1 Marine Environmental Monitoring, IRTA, Ctra. Poble Nou, km 5.5, 43540, Sant Carles de la,
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