Emerging Toxins Accumulation in Shellfish

A special issue of Marine Drugs (ISSN 1660-3397). This special issue belongs to the section "Marine Toxins".

Deadline for manuscript submissions: 31 December 2024 | Viewed by 15623

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CCMAR—Center of Marine Sciences, Campus of Gambelas, University of Algarve, 8005-139 Faro, Portugal
Interests: microalgae; metabolites; biotoxins; chemical-interactions
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Special Issue Information

Dear Colleagues,

While the most common harmful algal bloom (HAB) toxins have been widely reported and explored, a huge range of “emerging toxins” constitute a substantial gap in our understanding. These “emerging toxins” are defined as (i) toxins that appear in waters and seafood where they were previously absent, (ii) non-regulated known toxins, which are considered to be of concern but require additional toxicological evidence before establishing further regulations, and (iii) recently discovered toxins. The lack of occurrence data makes it difficult to fully comprehend the potential impacts of these toxins. Therefore, the purpose of this Special Issue is to encourage the publication of research articles devoted to the detection and quantification of emerging toxins in commercially important shellfish species.

Dr. Sandra Lage
Guest Editor

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Keywords

  • spirolides
  • yessotoxins
  • pectenotoxins
  • palytoxins
  • tetrodotoxins
  • ciguatoxins
  • saxitoxins
  • BMAA
  • occurrence data
  • seafood safety
  • harmful algal blooms

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Published Papers (8 papers)

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Research

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24 pages, 3380 KiB  
Article
Investigating Non-Native Ribbon Worm Cephalothrix simula as a Potential Source of Tetrodotoxin in British Bivalve Shellfish
by Monika Dhanji-Rapkova, Robert G. Hatfield, David I. Walker, Chantelle Hooper, Sarah Alewijnse, Craig Baker-Austin, Andrew D. Turner and Jennifer M. Ritchie
Mar. Drugs 2024, 22(10), 458; https://doi.org/10.3390/md22100458 - 5 Oct 2024
Viewed by 934
Abstract
Tetrodotoxin (TTX) is a potent marine neurotoxin found in several phylogenetically diverse organisms, some of which are sought as seafood. Since 2015, TTX has been reported in bivalve shellfish from several estuarine locations along the Mediterranean and European Atlantic coasts, posing an emerging [...] Read more.
Tetrodotoxin (TTX) is a potent marine neurotoxin found in several phylogenetically diverse organisms, some of which are sought as seafood. Since 2015, TTX has been reported in bivalve shellfish from several estuarine locations along the Mediterranean and European Atlantic coasts, posing an emerging food safety concern. Although reports on spatial and temporal distribution have increased in recent years, processes leading to TTX accumulation in European bivalves are yet to be described. Here, we explored the hypothesis that the ribbon worm species Cephalothrix simula, known to contain high levels of TTX, could play a role in the trophic transfer of the toxin into shellfish. During a field study at a single location in southern England, we confirmed C. simula DNA in seawater adjacent to trestle-farmed Pacific oysters Magallana gigas (formerly Crassostrea gigas) with a history of TTX occurrence. C. simula DNA in seawater was significantly higher in June and July during the active phase of toxin accumulation compared to periods of either no or continually decreasing TTX concentrations in M. gigas. In addition, C. simula DNA was detected in oyster digestive glands collected on 15 June 2021, the day with the highest recorded C. simula DNA abundance in seawater. These findings show evidence of a relationship between C. simula and TTX occurrence, providing support for the hypothesis that bivalves may acquire TTX through filter-feeding on microscopic life forms of C. simula present in the water column at particular periods each year. Although further evidence is needed to confirm such feeding activity, this study significantly contributes to discussions about the biological source of TTX in European bivalve shellfish. Full article
(This article belongs to the Special Issue Emerging Toxins Accumulation in Shellfish)
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12 pages, 2244 KiB  
Article
Cyanotoxins in Epipelic and Epiphytic Cyanobacteria from a Hypersaline Coastal Lagoon, an Environmental Hazard in Climate Warming Times and a Potential Source of New Compounds
by Yerai Gómez-Leyva, Alejandro Torrecillas and Marina Aboal
Mar. Drugs 2024, 22(8), 334; https://doi.org/10.3390/md22080334 - 24 Jul 2024
Viewed by 1017
Abstract
Cyanobacterial biodiversity and potential toxicity in coastal lagoons have barely been studied despite these transitional water systems being very important in conservation and for the preservation of economic resources. Most of these transitional systems have been affected by eutrophication, and climate change will [...] Read more.
Cyanobacterial biodiversity and potential toxicity in coastal lagoons have barely been studied despite these transitional water systems being very important in conservation and for the preservation of economic resources. Most of these transitional systems have been affected by eutrophication, and climate change will severely affect them by promoting cyanobacteria growth, especially in Mediterranean areas. This study aims to characterize the diversity of epipelic and epiphytic cyanobacteria species in a Mediterranean coastal lagoon and their potential for toxins production (microcystins and saxitoxins). Strains were isolated and genetically identified. Toxins were extracted and quantified by LC/MS-MS. All the taxa belong to the former Oscillatoriales. The presence of Nodosilinea and Toxifilum is reported for the first time for Spanish waters, but Pseudanabaena, Phormidium, Geitlerinema and Synechococcus also formed part of benthic mats. All the strains contained Microcystin-YR (MC-YR), but saxitoxin (STX) was present only in the extracts of Nodosilinea and Pseudanabena. MC-LY, MC-LW and [D-Asp3] MC-LR were detected in the extracts of Synechococcus and MC-LF in Toxifilum, but at concentrations that did not permit quantification. Toxins production by epipelic and epiphytic strains in coastal lagoons may represent a hazard, but also an opportunity to obtain potentially interesting compounds that should be further studied. Full article
(This article belongs to the Special Issue Emerging Toxins Accumulation in Shellfish)
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16 pages, 728 KiB  
Article
Occurrence and Exposure Assessment of Lipophilic Shellfish Toxins in the Zhejiang Province, China
by Qin Weng, Ronghua Zhang, Pinggu Wu, Jiang Chen, Xiaodong Pan, Chenyang Zheng, Dong Zhao, Jikai Wang, Hexiang Zhang, Xiaojuan Qi, Junde Han, Zijie Lu and Biao Zhou
Mar. Drugs 2024, 22(6), 239; https://doi.org/10.3390/md22060239 - 24 May 2024
Cited by 1 | Viewed by 1057
Abstract
Although lipophilic shellfish toxins (LSTs) pose a significant threat to the health of seafood consumers, their systematic investigation and risk assessment remain scarce. The goals of this study were as follows: (1) analyze LST levels in commercially available shellfish in Zhejiang province, China, [...] Read more.
Although lipophilic shellfish toxins (LSTs) pose a significant threat to the health of seafood consumers, their systematic investigation and risk assessment remain scarce. The goals of this study were as follows: (1) analyze LST levels in commercially available shellfish in Zhejiang province, China, and determine factors influencing LST distribution; (2) assess the acute dietary risk of exposure to LSTs for local consumers during the red tide period; (3) explore potential health risks of LSTs in humans; and (4) study the acute risks of simultaneous dietary exposure to LSTs and paralytic shellfish toxins (PSTs). A total of 546 shellfish samples were collected. LSTs were detected in 89 samples (16.3%) at concentrations below the regulatory limits. Mussels were the main shellfish species contaminated with LSTs. Spatial variations were observed in the yessotoxin group. Acute exposure to LSTs based on multiple scenarios was low. The minimum tolerable exposure durations for LSTs calculated using the mean and the 95th percentile of consumption data were 19.7 and 4.9 years, respectively. Our findings showed that Zhejiang province residents are at a low risk of combined exposure to LSTs and PSTs; however, the risk may be higher for children under 6 years of age in the extreme scenario. Full article
(This article belongs to the Special Issue Emerging Toxins Accumulation in Shellfish)
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11 pages, 5294 KiB  
Communication
First Report of Pinnatoxin-G (PnTX-G) in a Marine–Coastal Area of the Adriatic Sea Associated with the Presence of the Dinoflagellate Vulcanodinium rugosum
by Monica Cangini, Sonia Dall’Ara, Silva Rubini, Barbara Bertasi, Paolo Rizzi, Giovanni Dell’Orfano, Stefania Milandri, Stefano Manfredini, Erika Baldini and Silvia Vertuani
Mar. Drugs 2024, 22(3), 122; https://doi.org/10.3390/md22030122 - 5 Mar 2024
Viewed by 1698
Abstract
This study reports the first detection of the marine neurotoxin pinnatoxin-G (PnTX-G) in clams collected in the northwestern Adriatic Sea (Italy). It also represents the first report of the potential toxin-producing dinoflagellate, Vulcanodinium rugosum, in Italian seas. This result, from the coasts [...] Read more.
This study reports the first detection of the marine neurotoxin pinnatoxin-G (PnTX-G) in clams collected in the northwestern Adriatic Sea (Italy). It also represents the first report of the potential toxin-producing dinoflagellate, Vulcanodinium rugosum, in Italian seas. This result, from the coasts of the Emilia-Romagna Region, indicates a successful colonization process, reflecting conditions in France where V. rugosum was initially documented. In this case, the concentration of PnTXs was very low, making further sampling necessary to fully understand the extent of the phenomenon. Discussions on the need to obtain more data to support a proper risk assessment and the need to implement a monitoring program that includes emerging marine biotoxins are also included. Full article
(This article belongs to the Special Issue Emerging Toxins Accumulation in Shellfish)
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19 pages, 2499 KiB  
Article
Acute Effects of Brevetoxin-3 Administered via Oral Gavage to Mice
by Peggy Barbe, Jordi Molgó, Robert Thai, Apolline Urman, Denis Servent, Nathalie Arnich and Mathilde Keck
Mar. Drugs 2023, 21(12), 644; https://doi.org/10.3390/md21120644 - 16 Dec 2023
Viewed by 2101
Abstract
Brevetoxins (BTXs) constitute a family of lipid-soluble toxic cyclic polyethers mainly produced by Karenia brevis, which is the main vector for a foodborne syndrome known as neurotoxic shellfish poisoning (NSP) in humans. To prevent health risks associated with the consumption of contaminated shellfish [...] Read more.
Brevetoxins (BTXs) constitute a family of lipid-soluble toxic cyclic polyethers mainly produced by Karenia brevis, which is the main vector for a foodborne syndrome known as neurotoxic shellfish poisoning (NSP) in humans. To prevent health risks associated with the consumption of contaminated shellfish in France, the French Agency for Food, Environmental and Occupational Health & Safety (ANSES) recommended assessing the effects of BTXs via an acute oral toxicity study in rodents. Here, we investigated the effect of a single oral administration in both male and female mice with several doses of BTX-3 (100 to 1,500 µg kg−1 bw) during a 48 h observation period in order to provide toxicity data to be used as a starting point for establishing an acute oral reference dose (ARfD). We monitored biological parameters and observed symptomatology, revealing different effects of this toxin depending on the sex. Females were more sensitive than males to the impact of BTX-3 at the lowest doses on weight loss. For both males and females, BTX-3 induced a rapid, transient and dose-dependent decrease in body temperature, and a transient dose-dependent reduced muscle activity. Males were more sensitive to BTX-3 than females with more frequent observations of failures in the grip test, convulsive jaw movements, and tremors. BTX-3’s impacts on symptomatology were rapid, appearing during the 2 h after administration, and were transient, disappearing 24 h after administration. The highest dose of BTX-3 administered in this study, 1,500 µg kg−1 bw, was more toxic to males, leading to the euthanasia of three out of five males only 4 h after administration. BTX-3 had no effect on water intake, and affected neither the plasma chemistry parameters nor the organs’ weight. We identified potential points of departure that could be used to establish an ARfD (decrease in body weight, body temperature, and muscle activity). Full article
(This article belongs to the Special Issue Emerging Toxins Accumulation in Shellfish)
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23 pages, 3670 KiB  
Article
Five Years Monitoring the Emergence of Unregulated Toxins in Shellfish in France (EMERGTOX 2018–2022)
by Zouher Amzil, Amélie Derrien, Aouregan Terre Terrillon, Véronique Savar, Thomas Bertin, Marion Peyrat, Audrey Duval, Korian Lhaute, Nathalie Arnich, Vincent Hort and Marina Nicolas
Mar. Drugs 2023, 21(8), 435; https://doi.org/10.3390/md21080435 - 31 Jul 2023
Cited by 11 | Viewed by 2428
Abstract
Shellfish accumulate microalgal toxins, which can make them unsafe for human consumption. In France, in accordance with EU regulations, three groups of marine toxins are currently under official monitoring: lipophilic toxins, saxitoxins, and domoic acid. Other unregulated toxin groups are also present in [...] Read more.
Shellfish accumulate microalgal toxins, which can make them unsafe for human consumption. In France, in accordance with EU regulations, three groups of marine toxins are currently under official monitoring: lipophilic toxins, saxitoxins, and domoic acid. Other unregulated toxin groups are also present in European shellfish, including emerging lipophilic and hydrophilic marine toxins (e.g., pinnatoxins, brevetoxins) and the neurotoxin β-N-methylamino-L-alanine (BMAA). To acquire data on emerging toxins in France, the monitoring program EMERGTOX was set up along the French coasts in 2018. Three new broad-spectrum LC-MS/MS methods were developed to quantify regulated and unregulated lipophilic and hydrophilic toxins and the BMAA group in shellfish (bivalve mollusks and gastropods). A single-laboratory validation of each of these methods was performed. Additionally, these specific, reliable, and sensitive operating procedures allowed the detection of groups of EU unregulated toxins in shellfish samples from French coasts: spirolides (SPX-13-DesMeC, SPX-DesMeD), pinnatoxins (PnTX-G, PnTX-A), gymnodimines (GYM-A), brevetoxins (BTX-2, BTX-3), microcystins (dmMC-RR, MC-RR), anatoxin, cylindrospermopsin and BMAA/DAB. Here, we present essentially the results of the unregulated toxins obtained from the French EMERGTOX monitoring plan during the past five years (2018–2022). Based on our findings, we outline future needs for monitoring to protect consumers from emerging unregulated toxins. Full article
(This article belongs to the Special Issue Emerging Toxins Accumulation in Shellfish)
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20 pages, 2551 KiB  
Article
Exploration of Vulcanodinium rugosum Toxins and their Metabolism Products in Mussels from the Ingril Lagoon Hotspot in France
by Vincent Hort, Isabel Bastardo-Fernández and Marina Nicolas
Mar. Drugs 2023, 21(8), 429; https://doi.org/10.3390/md21080429 - 29 Jul 2023
Cited by 2 | Viewed by 3215
Abstract
Over the year 2018, we assessed toxin contamination of shellfish collected on a monthly basis in Ingril Lagoon, France, a site known as a hotspot for Vulcanodinium rugosum growth. This short time-series study gave an overview of the presence and seasonal variability of [...] Read more.
Over the year 2018, we assessed toxin contamination of shellfish collected on a monthly basis in Ingril Lagoon, France, a site known as a hotspot for Vulcanodinium rugosum growth. This short time-series study gave an overview of the presence and seasonal variability of pinnatoxins, pteriatoxins, portimines and kabirimine, all associated with V. rugosum, in shellfish. Suspect screening and targeted analysis approaches were implemented by means of liquid chromatography coupled to both low- and high-resolution mass spectrometry. We detected pinnatoxin-A and pinnatoxin-G throughout the year, with maximum levels for each one observed in June (6.7 µg/kg for pinnatoxin-A; 467.5 µg/kg for pinnatoxin-G), whereas portimine-A was detected between May and September (maximum level = 75.6 µg/kg). One of the main findings was the identification of a series of fatty acid esters of pinnatoxin-G (n = 13) although the levels detected were low. The profile was dominated by the palmitic acid conjugation of pinnatoxin-G. The other 12 fatty acid esters had not been reported in European shellfish to date. In addition, after thorough investigations, two compounds were detected, with one being probably identified as portimine-B, and the other one putatively attributed to pteriatoxins. If available, reference materials would have ensured full identification. Monitoring of these V. rugosum emerging toxins and their biotransformation products will contribute towards filling the data gaps pointed out in risk assessments and in particular the need for more contamination data for shellfish. Full article
(This article belongs to the Special Issue Emerging Toxins Accumulation in Shellfish)
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Review

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18 pages, 535 KiB  
Review
A Review of Cyclic Imines in Shellfish: Worldwide Occurrence, Toxicity and Assessment of the Risk to Consumers
by Sarah C. Finch, D. Tim Harwood, Michael J. Boundy and Andrew I. Selwood
Mar. Drugs 2024, 22(3), 129; https://doi.org/10.3390/md22030129 - 11 Mar 2024
Cited by 1 | Viewed by 2130
Abstract
Cyclic imines are a class of lipophilic shellfish toxins comprising gymnodimines, spirolides, pinnatoxins, portimines, pteriatoxins, prorocentrolides, spiro-prorocentrimine, symbiomines and kabirimine. They are structurally diverse, but all share an imine moiety as part of a bicyclic ring system. These compounds are produced by marine [...] Read more.
Cyclic imines are a class of lipophilic shellfish toxins comprising gymnodimines, spirolides, pinnatoxins, portimines, pteriatoxins, prorocentrolides, spiro-prorocentrimine, symbiomines and kabirimine. They are structurally diverse, but all share an imine moiety as part of a bicyclic ring system. These compounds are produced by marine microalgal species and are characterized by the rapid death that they induce when injected into mice. Cyclic imines have been detected in a range of shellfish species collected from all over the world, which raises the question as to whether they present a food safety risk. The European Food Safety Authority (EFSA) considers them to be an emerging food safety issue, and in this review, the risk posed by these toxins to shellfish consumers is assessed by collating all available occurrence and toxicity data. Except for pinnatoxins, the risk posed to human health by the cyclic imines appears low, although this is based on only a limited dataset. For pinnatoxins, two different health-based guidance values have been proposed at which the concentration should not be exceeded in shellfish (268 and 23 µg PnTX/kg shellfish flesh), with the discrepancy caused by the application of different uncertainty factors. Pinnatoxins have been recorded globally in multiple shellfish species at concentrations of up to 54 times higher than the lower guidance figure. Despite this observation, pinnatoxins have not been associated with recorded human illness, so it appears that the lower guidance value may be conservative. However, there is insufficient data to generate a more robust guidance value, so additional occurrence data and toxicity information are needed. Full article
(This article belongs to the Special Issue Emerging Toxins Accumulation in Shellfish)
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