Public Health Risks Associated with Tetrodotoxin and Its Analogues in European Waters: Recent Advances after The EFSA Scientific Opinion

Abstract

Tetrodotoxin (TTX) and its analogues are naturally occurring toxins responsible worldwide for human intoxication cases and fatalities, mainly associated with pufferfish consumption. In the last decade, TTXs were detected in marine bivalves and gastropods from European waters. As TTXs are not regulated or monitored at EU level, their unexpected occurrence in shellfish raised concerns as a food safety hazard and revealed the necessity of a thorough assessment on the public health risks associated with their presence. For this reason, the European Food Safety Authority (EFSA) was requested by the European Commission to provide a scientific opinion, finally adopted in March 2017, according to which a provisional concentration below 44 μg TTX equivalents/kg shellfish meat, based on a large portion size of 400 g, was considered not to result in adverse effects in humans. The EFSA expert panel, however, recognized a number of shortcomings and uncertainties related to the unavailability of sufficient scientific data and provided relevant recommendations for future research to overcome these data gaps identified in order to further refine the risk assessment on TTXs. The present review aims to summarize the knowledge obtained towards addressing these recommendations in the two years following publication of the EFSA opinion, at the same time highlighting the points requiring further investigation.

First Detection of Tetrodotoxin in Bivalves and Gastropods from the French Mainland Coasts

“…This range is in agreement with the salinity observed in other locations where TTX-positive samples were collected. In the Marano Lagoon in Italy, the measured salinity was 33 g/L, whereas, in the Galician "rías" in Spain, salinity was 35 g/L [13,31].…”

“…Furthermore, 2017 was the year with the lowest number of samples exceeding the European health hazard threshold in this country (n = 1). Italy is an exception: in 2017 and 2018, concentrations of 541 and 216 µg TTX/kg were respectively observed in two mussel samples (Mytilus galloprovincialis) from the same sampling site "Ficariol San Piero" located in the Marano Lagoon [31].…”

Seasonal and Spatial Variations in Bacterial Communities From Tetrodotoxin-Bearing and Non-tetrodotoxin-Bearing Clams

“…Many bacterial genera have been reported as potential producers of TTX, the most common being Bacillus , Pseudomonas , Aeromonas , Vibrio , Actinomyces , and Shewanella ( Pratheepa and Vasconcelos, 2013 ), and over 150 TTX-producing strains are described in the literature ( Magarlamov et al, 2017 ; Katikou, 2019 ). With less than 1% of bacteria being culturable there are challenges with isolating, culturing and thus characterizing TTX producers and it is likely that many other strains may be TTX producers ( Chau et al, 2011 ).…”

“…Exogenous or symbiotic bacteria are commonly touted as the most likely TTX-producers, with a wide diversity of species and strains implicated. There are reports in the literature of at least 150 TTX-producing bacterial strains, with Vibrio species comprising more than 30% of records, followed by Bacillus, Pseudomonas, Actinomyces, and Micrococcus (Turner et al, 2018;Katikou, 2019). However, it is estimated that less than 1% of all bacteria are culturable, making isolation, culturing and confirmation of toxin production in bacteria a significant challenge (Chau et al, 2011).…”

Occurrence of Tetrodotoxin in Bivalves and Gastropods from Harvesting Areas and Other Natural Spaces in Spain

“…The results obtained in previous research on different bivalve molluscs from the Galician Rias on the west coast of Spain, where mussels in particular represent a very important resource, revealed low levels of TTX in only two samples out of 286 samples from infaunal areas, and at very low concentrations—2.3 μg/kg in cockles and below 0.9 μg/kg in oysters [7]. Further work developed in the same project did not find positive samples in 72 analyzed samples (cited in [22]). This study, together with a study on different intertidal molluscs and echinoderms from Portugal in which no bivalves positive for TTX were found (seven analyzed samples) [23], are the only studies regarding TTX in molluscs along the Iberian Peninsula.…”