The role of toxic planocerid flatworm larvae on tetrodotoxin accumulation in marine bivalves

Okabe, Taiki; Saito, Rion; Yamamoto, Kohei; Watanabe, Riku; Kaneko, Yoshiki; Yanaoka, Mutsumi; Furukoshi, Seika; Yasukawa, Shino; Ito, M.; Oyama, Hikaru; Suo, Rei; Suzuki, Miwa; Takatani, Tomohiro; Arakawa, Osamu; Sugita, Haruo; Itoi, Shiro

doi:10.1016/j.aquatox.2021.105908

Cited by 19 publications

(11 citation statements)

References 36 publications

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“…The hypothesis of an algal source of TTX is also potentially confounded with the increasing knowledge on bacterial components of the phycosphere [54][55][56][57], which may result in microalgal transport of bacterial toxins into bivalves. In addition, as bivalves are not efficient at filtering free-living bacteria directly from seawater as a food source due to their small size [58], it is reasonable to assume that if bacteria are the biological source they may enter the bivalve digestive system as "back-packers", i.e., as part of the phycosphere or from protists [59] or aggregates [60] or via another vector such as toxic flatworm larvae as recently proven by Okabe et al [61].…”

Section: Discussionmentioning

confidence: 99%

Tetrodotoxins in French Bivalve Mollusks—Analytical Methodology, Environmental Dynamics and Screening of Bacterial Strain Collections

Réveillon

Savar

Schaefer

et al. 2021

Toxins

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Tetrodotoxins (TTXs) are potentially lethal paralytic toxins that have been identified in European shellfish over recent years. Risk assessment has suggested comparatively low levels (44 µg TTX-equivalent/kg) but stresses the lack of data on occurrence. Both bacteria and dinoflagellates were suggested as possible biogenic sources, either from an endogenous or exogenous origin. We thus investigated TTXs in (i) 98 shellfish samples and (ii) 122 bacterial strains, isolated from French environments. We optimized a method based on mass spectrometry, using a single extraction step followed by ultrafiltration without Solid Phase Extraction and matrix-matched calibration for both shellfish and bacterial matrix. Limits of detection and quantification were 6.3 and 12.5 µg/kg for shellfish and 5.0 and 10 µg/kg for bacterial matrix, respectively. Even though bacterial matrix resulted in signal enhancement, no TTX analog was detected in any strain. Bivalves (either Crassostrea gigas or Ruditapes philippinarum) were surveyed in six French production areas over 2.5–3 month periods (2018–2019). Concentrations of TTX ranged from ‘not detected’ to a maximum of 32 µg/kg (Bay of Brest, 17 June 2019), with events lasting 2 weeks at maximum. While these results are in line with previous studies, they provide new data of TTX occurrence and confirm that the link between bacteria, bivalves and TTX is complex.

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Section: Discussionmentioning

confidence: 99%

Tetrodotoxins in French Bivalve Mollusks—Analytical Methodology, Environmental Dynamics and Screening of Bacterial Strain Collections

Réveillon

Savar

Schaefer

et al. 2021

Toxins

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“…Interestingly, the larvae of P. multitentaculata and related species were also found to be involved in the toxification of various TTX-bearing fish juveniles, and an edible bivalve, Azumapecten farreri akazara. Flatworm larvae are considered to be important suppliers of the toxin to TTX-bearing organisms [21,22]. Although TTX-bearing flatworms appear to be largely restricted to the genus, Planocera, members of which are widely distributed in the waters around the Japanese archipelago [23][24][25][26][27], and other flatworms such as the cotylean flatworm, Prosthiostomum trilineatum, have also recently been discovered to contain the toxin [28].…”

Section: Introductionmentioning

confidence: 99%

Local Differences in the Toxin Amount and Composition of Tetrodotoxin and Related Compounds in Pufferfish (Chelonodon patoca) and Toxic Goby (Yongeichthys criniger) Juveniles

Ito

Furukawa

Yasukawa

et al. 2022

Toxins

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Tetrodotoxin (TTX)-bearing fish ingest TTX from their preys through the food chain and accumulate TTX in their bodies. Although a wide variety of TTX-bearing organisms have been reported, the missing link in the TTX supply chain has not been elucidated completely. Here, we investigated the composition of TTX and 5,6,11-trideoxyTTX in juveniles of the pufferfish, Chelonodon patoca, and toxic goby, Yongeichthys criniger, using LC–MS/MS, to resolve the missing link in the TTX supply chain. The TTX concentration varied among samples from different localities, sampling periods and fish species. In the samples from the same locality, the TTX concentration was significantly higher in the toxic goby juveniles than in the pufferfish juveniles. The concentration of TTX in all the pufferfish juveniles was significantly higher than that of 5,6,11-trideoxyTTX, whereas the compositional ratio of TTX and 5,6,11-trideoxyTTX in the goby was different among sampling localities. However, the TTX/5,6,11-trideoxyTTX ratio in the goby was not different among samples collected from the same locality at different periods. Based on a species-specific PCR, the detection rate of the toxic flatworm (Planocera multitentaculata)-specific sequence (cytochrome c oxidase subunit I) also varied between the intestinal contents of the pufferfish and toxic goby collected at different localities and periods. These results suggest that although the larvae of the toxic flatworm are likely to be responsible for the toxification of the pufferfish and toxic goby juveniles by TTX, these fish juveniles are also likely to feed on other TTX-bearing organisms depending on their habitat, and they also possess different accumulation mechanisms of TTX and 5,6,11-trideoxyTTX.

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“…These levels were comparable to those found in naturally contaminated bivalves, and the method could be a feasible solution to investigate TTX uptake in different bivalve species in a controlled environment. On the other hand, Okabe et al (2021) fed M. galloprovincialis with the larvae of the toxic marine flatworm Planocera multitentaculata; while monitoring the toxin concentration, they found a steady decrease from week 1 to week 4. A similar trend was found by Bordin et al (2019) while monitoring TTX presence in bivalves from the Marano Lagoon (Northern Adriatic Basin, Italy) across a yearly period (during 2019).…”

Section: Ttx Presence In Live Bivalve Mollusks and Causative Factors ...mentioning

confidence: 99%

“…On the other hand, Okabe et al. (2021) fed M. galloprovincialis with the larvae of the toxic marine flatworm Planocera multitentaculata ; while monitoring the toxin concentration, they found a steady decrease from week 1 to week 4. A similar trend was found by Bordin et al.…”

Section: Ttx Presence In Live Bivalve Mollusks and Causative Factors ...mentioning

confidence: 99%

Tetrodotoxin in live bivalve mollusks from Europe: Is it to be considered an emerging concern for food safety?

Antonelli

Salerno

Bordin

et al. 2021

Comp Rev Food Sci Food Safe

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Tetrodotoxins (TTXs) are a group of potent neurotoxins named after the Tetraodontidae fish family (pufferfish). TTXs have been reported in several animal taxa, both terrestrial and marine. The ingestion of TTX‐contaminated flesh can cause serious neurotoxic symptomatology and can eventually lead to death. Traditionally, TTXs have been associated with Asian countries, in particular with pufferfish consumption. However, they have also been reported in bivalve mollusks farmed in the Pacific area and, recently, in European seas. In Europe, different countries have reported TTXs, especially those bordering the Mediterranean Sea. As a consequence, in 2017 the European Food Safety Authority (EFSA) released an opinion with reference to TTX present in marine gastropods and bivalves, proposing a safety limit of 44 µg/kg TTXs in shellfish meat, below which no adverse effects should be observed in humans. Nevertheless, this limit has been exceeded on many occasions in European shellfish and, while for bivalves there have been no registered human intoxications, that is not the case for marine gastropods. However, TTXs have not yet been included in the list of marine biotoxins officially monitored in live bivalve mollusks within the European Union (EU). Thus, the aims of this manuscript are to discuss the increasing occurrence of TTXs in live bivalve mollusks from European sea waters, to acknowledge the still ongoing knowledge gaps that should be covered and to stimulate constructive debate on the eventuality of adopting a shared regulatory context, at least in the EU, for monitoring and managing this potential threat to food safety.

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The role of toxic planocerid flatworm larvae on tetrodotoxin accumulation in marine bivalves

Cited by 19 publications

References 36 publications

Tetrodotoxins in French Bivalve Mollusks—Analytical Methodology, Environmental Dynamics and Screening of Bacterial Strain Collections

Tetrodotoxins in French Bivalve Mollusks—Analytical Methodology, Environmental Dynamics and Screening of Bacterial Strain Collections

Local Differences in the Toxin Amount and Composition of Tetrodotoxin and Related Compounds in Pufferfish (Chelonodon patoca) and Toxic Goby (Yongeichthys criniger) Juveniles

Tetrodotoxin in live bivalve mollusks from Europe: Is it to be considered an emerging concern for food safety?

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