Marine Biotoxins and Seafood Poisoning

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Marine and Freshwater Toxins".

Deadline for manuscript submissions: closed (30 June 2019) | Viewed by 53854

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IRTA Institute of Agrifood Research and Technology, IRTA, Spain

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Portuguese Institute for the Sea and Atmosphere, IPMA, Division of Aquaculture, Bioprospection and Upgrading, Portugal
Interests: climate change and chemical contaminants in seafood; contaminant levels and toxicity of contaminants in seafood; consumer risks and benefits; mitigation strategies to reduce contaminant levels in seafood
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Dear Colleagues,

Worldwide, mollusks and fish may be contaminated by marine toxins (MT) due to the seasonal presence of marine-toxin-producing microalgae. The prevalence of MT has increased globally and the occurrence of MT in temperate regions of tropical areas is nowadays a reality, likely due to climate change. Epidemiological studies are scarce and risk characterization is needed, particularly for emerging toxins. In addition, the economic burden to seafood producers caused by the closure of production areas and insecurity urges the implementation of fast screening tools and the development of predictive modeling tools for stakeholders. Therefore, it is critical to enhance collaborative multi and trans disciplinary actions to introduce innovative strategies to improve shellfish and fish safety and to strengthen industrial competitiveness by developing sensor devices for MT detection and implementing mitigation strategies through processing. Innovative toxicological approaches for seafood safety evaluation are also requested.

Dr. Pedro Reis Costa
Dr. Jorge Diogène
Dr. Antonio Marques
Guest Editors

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Keywords

  • Ciguatoxins
  • Tetrodotoxins
  • PSPs
  • DSPs
  • ASPs
  • fast screening methods
  • climate change
  • epidemiology
  • risk characterization
  • bio-accessibility/cooking

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Published Papers (8 papers)

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Editorial

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2 pages, 205 KiB  
Editorial
Marine Biotoxins and Seafood Poisoning
by Pedro Reis Costa, António Marques and Jorge Diogène
Toxins 2019, 11(10), 558; https://doi.org/10.3390/toxins11100558 - 24 Sep 2019
Cited by 2 | Viewed by 3864
Abstract
Prevalence of marine biotoxins in seafood has been associated with increasing frequency, intensity, and duration of harmful algal blooms, and an increase of the geographical and temporal distribution of harmful algae [...] Full article
(This article belongs to the Special Issue Marine Biotoxins and Seafood Poisoning)

Research

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13 pages, 2488 KiB  
Article
Paralytic Shellfish Toxin Uptake, Assimilation, Depuration, and Transformation in the Southeast Asian Green-Lipped Mussel (Perna viridis)
by John Kristoffer Andres, Aletta T. Yñiguez, Jennifer Mary Maister, Andrew D. Turner, Dave Eldon B. Olano, Jenelyn Mendoza, Lilibeth Salvador-Reyes and Rhodora V. Azanza
Toxins 2019, 11(8), 468; https://doi.org/10.3390/toxins11080468 - 9 Aug 2019
Cited by 23 | Viewed by 7133
Abstract
Bivalve molluscs represent an important food source within the Philippines, but the health of seafood consumers is compromised through the accumulation of harmful algal toxins in edible shellfish tissues. In order to assess the dynamics of toxin risk in shellfish, this study investigated [...] Read more.
Bivalve molluscs represent an important food source within the Philippines, but the health of seafood consumers is compromised through the accumulation of harmful algal toxins in edible shellfish tissues. In order to assess the dynamics of toxin risk in shellfish, this study investigated the uptake, depuration, assimilation, and analogue changes of paralytic shellfish toxins in Perna viridis. Tank experiments were conducted where mussels were fed with the toxic dinoflagellate Alexandrium minutum. Water and shellfish were sampled over a six day period to determine toxin concentrations in the shellfish meat and water, as well as algal cell densities. The maximum summed toxin concentration determined was 367 µg STX eq./100 g shellfish tissue, more than six times higher than the regulatory action limit in the Philippines. Several uptake and depuration cycles were observed during the study, with the first observed within the first 24 h coinciding with high algal cell densities. Toxin burdens were assessed within different parts of the shellfish tissue, with the highest levels quantified in the mantle during the first 18 h period but shifting towards the gut thereafter. A comparison of toxin profile data evidenced the conversion of GTX1,4 in the source algae to the less potent GTX2,3 in the shellfish tissue. Overall, the study illustrated the temporal variability in Perna viridis toxin concentrations during a modelled algal bloom event, and the accumulation of toxin from the water even after toxic algae were removed. Full article
(This article belongs to the Special Issue Marine Biotoxins and Seafood Poisoning)
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16 pages, 2706 KiB  
Article
Paralytic Shellfish Toxins and Ocean Warming: Bioaccumulation and Ecotoxicological Responses in Juvenile Gilthead Seabream (Sparus aurata)
by Vera Barbosa, Marta Santos, Patrícia Anacleto, Ana Luísa Maulvault, Pedro Pousão-Ferreira, Pedro Reis Costa and António Marques
Toxins 2019, 11(7), 408; https://doi.org/10.3390/toxins11070408 - 13 Jul 2019
Cited by 10 | Viewed by 5258
Abstract
Warmer seawater temperatures are expected to increase harmful algal blooms (HABs) occurrence, intensity, and distribution. Yet, the potential interactions between abiotic stressors and HABs are still poorly understood from ecological and seafood safety perspectives. The present study aimed to investigate, for the first [...] Read more.
Warmer seawater temperatures are expected to increase harmful algal blooms (HABs) occurrence, intensity, and distribution. Yet, the potential interactions between abiotic stressors and HABs are still poorly understood from ecological and seafood safety perspectives. The present study aimed to investigate, for the first time, the bioaccumulation/depuration mechanisms and ecotoxicological responses of juvenile gilthead seabream (Sparus aurata) exposed to paralytic shellfish toxins (PST) under different temperatures (18, 21, 24 °C). PST were detected in fish at the peak of the exposure period (day five, 0.22 µg g−1 N-sulfocarbamoylGonyautoxin-1-2 (C1 and C2), 0.08 µg g−1 Decarbamoylsaxitoxin (dcSTX) and 0.18 µg g−1 Gonyautoxin-5 (B1)), being rapidly eliminated (within the first 24 h of depuration), regardless of exposure temperature. Increased temperatures led to significantly higher PST contamination (275 µg STX eq. kg−1). During the trial, fish antioxidant enzyme activities (superoxide dismutase, SOD; catalase, CAT; glutathione S-transferase, GST) in both muscle and viscera were affected by temperature, whereas a significant induction of heat shock proteins (HSP70), Ubiquitin (Ub) activity (viscera), and lipid peroxidation (LPO; muscle) was observed under the combination of warming and PST exposure. The differential bioaccumulation and biomarker responses observed highlight the need to further understand the interactive effects between PST and abiotic stressors, to better estimate climate change impacts on HABs events, and to develop mitigation strategies to overcome the potential risks associated with seafood consumption. Full article
(This article belongs to the Special Issue Marine Biotoxins and Seafood Poisoning)
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15 pages, 3048 KiB  
Article
Discovery of a Potential Human Serum Biomarker for Chronic Seafood Toxin Exposure Using an SPR Biosensor
by Kathi A. Lefebvre, Betsy Jean Yakes, Elizabeth Frame, Preston Kendrick, Sara Shum, Nina Isoherranen, Bridget E. Ferriss, Alison Robertson, Alicia Hendrix, David J. Marcinek and Lynn Grattan
Toxins 2019, 11(5), 293; https://doi.org/10.3390/toxins11050293 - 23 May 2019
Cited by 11 | Viewed by 4857
Abstract
Domoic acid (DA)-producing harmful algal blooms (HABs) have been present at unprecedented geographic extent and duration in recent years causing an increase in contamination of seafood by this common environmental neurotoxin. The toxin is responsible for the neurotoxic illness, amnesic shellfish poisoning (ASP), [...] Read more.
Domoic acid (DA)-producing harmful algal blooms (HABs) have been present at unprecedented geographic extent and duration in recent years causing an increase in contamination of seafood by this common environmental neurotoxin. The toxin is responsible for the neurotoxic illness, amnesic shellfish poisoning (ASP), that is characterized by gastro-intestinal distress, seizures, memory loss, and death. Established seafood safety regulatory limits of 20 μg DA/g shellfish have been relatively successful at protecting human seafood consumers from short-term high-level exposures and episodes of acute ASP. Significant concerns, however, remain regarding the potential impact of repetitive low-level or chronic DA exposure for which there are no protections. Here, we report the novel discovery of a DA-specific antibody in the serum of chronically-exposed tribal shellfish harvesters from a region where DA is commonly detected at low levels in razor clams year-round. The toxin was also detected in tribal shellfish consumers’ urine samples confirming systemic DA exposure via consumption of legally-harvested razor clams. The presence of a DA-specific antibody in the serum of human shellfish consumers confirms long-term chronic DA exposure and may be useful as a diagnostic biomarker in a clinical setting. Adverse effects of chronic low-level DA exposure have been previously documented in laboratory animal studies and tribal razor clam consumers, underscoring the potential clinical impact of such a diagnostic biomarker for protecting human health. The discovery of this type of antibody response to chronic DA exposure has broader implications for other environmental neurotoxins of concern. Full article
(This article belongs to the Special Issue Marine Biotoxins and Seafood Poisoning)
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9 pages, 6987 KiB  
Article
Toxicity and Toxin Composition of the Greater Blue-Ringed Octopus Hapalochlaena lunulata from Ishigaki Island, Okinawa Prefecture, Japan
by Manabu Asakawa, Takuya Matsumoto, Kohei Umezaki, Kyoichiro Kaneko, Ximiao Yu, Gloria Gomez-Delan, Satoshi Tomano, Tamao Noguchi and Susumu Ohtsuka
Toxins 2019, 11(5), 245; https://doi.org/10.3390/toxins11050245 - 29 Apr 2019
Cited by 24 | Viewed by 12652
Abstract
The toxicity of the greater blue-ringed octopus Hapalochlaena lunulata, whose bite is fatal to humans, was examined to better understand and prevent deaths from accidental bites. Living specimens were collected from tide pools on Ishigaki Island, Okinawa Prefecture, Japan, in November and [...] Read more.
The toxicity of the greater blue-ringed octopus Hapalochlaena lunulata, whose bite is fatal to humans, was examined to better understand and prevent deaths from accidental bites. Living specimens were collected from tide pools on Ishigaki Island, Okinawa Prefecture, Japan, in November and December of 2015, 2016, and 2017. The specimens were examined for the anatomical distribution of the toxicity, which was expressed in terms of mouse units (MU), by the standard bioassay method for tetrodotoxin (TTX) in Japan. Paralytic toxicity to mice was detected in all of the soft parts. The posterior salivary glands exhibited the highest toxicity score with a maximum level of 9276 MU/g, which was classified as “strongly toxic” (more than 1000 MU/g tissue) according to the classification of toxicity established by the Ministry of Health, Labor and Welfare of Japan, followed by the hepatopancreas (21.1 to 734.3 MU/g), gonads (not detectable to 167.6 MU/g), arms (5.3 to 130.2 MU/g), and other body areas (17.3 to 107.4 MU/g). Next, the toxin from the salivary glands was partially purified by a Sep-Pak C18 cartridge and an Amicon Ultra Centrifugal Filter with a 3000-Da cut-off, and analyzed by liquid chromatography-mass spectrometry (LC-MS) equipped with a φ2.0 × 150-mm (5 μm) TSKgel Amide-80 column (Tosoh, Tokyo, Japan) with a mixture of 16 mM ammonium formate buffer (pH 5.5) and acetonitrile (ratio 3:7, v/v) as a mobile phase. This study aimed to clarify the toxicity and the composition of TTX and its derivatives in this toxic octopus. The main toxin in this toxic octopus was identified as TTX, along with 4-epi TTX, 4, 9-anhydroTTX and 6-epi TTX. Further, the toxicity of this species is also significant from a food hygiene point of view. Full article
(This article belongs to the Special Issue Marine Biotoxins and Seafood Poisoning)
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18 pages, 4746 KiB  
Article
Paralytic Shellfish Toxins in Surf Clams Mesodesma donacium during a Large Bloom of Alexandrium catenella Dinoflagellates Associated to an Intense Shellfish Mass Mortality
by Gonzalo Álvarez, Patricio A. Díaz, Marcos Godoy, Michael Araya, Iranzu Ganuza, Roberto Pino, Francisco Álvarez, José Rengel, Cristina Hernández, Eduardo Uribe and Juan Blanco
Toxins 2019, 11(4), 188; https://doi.org/10.3390/toxins11040188 - 29 Mar 2019
Cited by 53 | Viewed by 7836
Abstract
In late February 2016, a harmful algal bloom (HAB) of Alexandrium catenella was detected in southern Chiloé, leading to the banning of shellfish harvesting in an extended geographical area (~500 km). On April 24, 2016, this bloom produced a massive beaching (an accumulation [...] Read more.
In late February 2016, a harmful algal bloom (HAB) of Alexandrium catenella was detected in southern Chiloé, leading to the banning of shellfish harvesting in an extended geographical area (~500 km). On April 24, 2016, this bloom produced a massive beaching (an accumulation on the beach surface of dead or impaired organisms which were drifted ashore) of surf clams Mesodesma donacium in Cucao Bay, Chiloé. To determine the effect of paralytic shellfish poisoning (PSP) toxins in M. donacium, samples were taken from Cucao during the third massive beaching detected on May 3, 2016. Whole tissue toxicity evidence a high interindividual variability with values which ranged from 1008 to 8763 μg STX eq 100 g−1 and with a toxin profile dominated by GTX3, GTX1, GTX2, GTX4, and neoSTX. Individuals were dissected into digestive gland (DG), foot (FT), adductor muscle (MU), and other body fractions (OBF), and histopathological and toxin analyses were carried out on the obtained fractions. Some pathological conditions were observed in gill and digestive gland of 40–50% of the individuals that correspond to hemocyte aggregation and haemocytic infiltration, respectively. The most toxic tissue was DG (2221 μg STX eq 100 g−1), followed by OBF (710 μg STX eq 100 g−1), FT (297 μg STX eq 100 g−1), and MU (314 μg STX eq 100 g−1). The observed surf clam mortality seems to have been mainly due to the desiccation caused by the incapability of the clams to burrow. Considering the available information of the monitoring program and taking into account that this episode was the first detected along the open coast of the Pacific Ocean in southern Chiloé, it is very likely that the M. donacium population from Cucao Bay has not had a recurrent exposition to A. catenella and, consequently, that it has not been subjected to high selective pressure for PSP resistance. However, more research is needed to determine the effects of PSP toxins on behavioral and physiological responses, nerve sensitivity, and genetic/molecular basis for the resistance or sensitivity of M. donacium. Full article
(This article belongs to the Special Issue Marine Biotoxins and Seafood Poisoning)
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16 pages, 1245 KiB  
Article
Development and Application of Immunoaffinity Column Purification and Ultrahigh Performance Liquid Chromatography-Tandem Mass Spectrometry for Determination of Domoic Acid in Shellfish
by Si Chen, Xiaojun Zhang, Zhongyong Yan, Yangyang Hu and Yibo Lu
Toxins 2019, 11(2), 83; https://doi.org/10.3390/toxins11020083 - 1 Feb 2019
Cited by 12 | Viewed by 4971
Abstract
Domoic acid (DA) is a neurotoxin associated with amnesic shellfish poisoning (ASP). Though LC coupled to tandem mass spectrometry (LC-MS/MS) has become the preferred method for DA determination, traditional sample pretreatment is still labor-intensive. In this study, a simple, efficient and selective method [...] Read more.
Domoic acid (DA) is a neurotoxin associated with amnesic shellfish poisoning (ASP). Though LC coupled to tandem mass spectrometry (LC-MS/MS) has become the preferred method for DA determination, traditional sample pretreatment is still labor-intensive. In this study, a simple, efficient and selective method for LC-MS/MS analysis of DA in shellfish was established by optimizing clean-up procedures on a self-assembly immunoaffinity column (IAC). Shellfish was extracted with 75% methanol twice and diluted with phosphate buffered saline (PBS, 1:2). The mixture was purified on IAC as follows: preconditioned with PBS, loaded with sample, washed by 50% MeOH, and eluted with MeOH containing 2% ammonium hydroxide. Concentrated analyte was monitored by multiple reaction monitoring (MRM) using electrospray (ESI) positive ion mode throughout the LC gradient elution. Based on the post-extraction addition method, matrix effects for various shellfish matrices were found to be less than 8%. The developed method was fully validated by choosing mussel as the representative matrix. The method had a limit of detection (LOD) of 0.02 µg·g−1, showed excellent linear correlation in the range of 0.05–40 µg·g−1, and obtained ideal recoveries (91–94%), intra-day RSDs (6–8%) and inter-day RSDs (3–6%). The method was successfully applied to DA determination in 59 shellfish samples, with a detection rate of 10% and contaminated content of 0.1–14.9 µg·g−1. Full article
(This article belongs to the Special Issue Marine Biotoxins and Seafood Poisoning)
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14 pages, 1522 KiB  
Article
Combined Cytotoxicity of the Phycotoxin Okadaic Acid and Mycotoxins on Intestinal and Neuroblastoma Human Cell Models
by Aiko Hayashi, Juan José Dorantes-Aranda, John P. Bowman and Gustaaf Hallegraeff
Toxins 2018, 10(12), 526; https://doi.org/10.3390/toxins10120526 - 8 Dec 2018
Cited by 18 | Viewed by 5708
Abstract
Mycotoxins are emerging toxins in the marine environment, which can co-occur with algal toxins to exert synergistic or antagonistic effects for human seafood consumption. The current study assesses the cytotoxicity of the algal toxin okadaic acid, shellfish, and dust storm-associated mycotoxins alone or [...] Read more.
Mycotoxins are emerging toxins in the marine environment, which can co-occur with algal toxins to exert synergistic or antagonistic effects for human seafood consumption. The current study assesses the cytotoxicity of the algal toxin okadaic acid, shellfish, and dust storm-associated mycotoxins alone or in combination on human intestinal (HT-29) and neuroblastoma (SH-SY5Y) cell lines. Based on calculated IC50 (inhibitory concentration 50%) values, mycotoxins and the algal toxin on their own exhibited increased cytotoxicity in the order of sydowinin A < sydowinin B << patulin < alamethicin < sydowinol << gliotoxin ≈ okadaic acid against the HT-29 cell line, and sydowinin B < sydowinin A << alamethicin ≈ sydowinol < patulin, << gliotoxin < okadaic acid against the SH-SY5Y cell line. Combinations of okadaic acid–sydowinin A, –alamethicin, –patulin, and –gliotoxin exhibited antagonistic effects at low-moderate cytotoxicity, but became synergistic at high cytotoxicity, while okadaic acid–sydowinol displayed an antagonistic relationship against HT-29 cells. Furthermore, only okadaic acid–sydowinin A showed synergism, while okadaic acid–sydowinol, –alamethicin, –patulin, and –gliotoxin combinations demonstrated antagonism against SH-SY5Y. While diarrhetic shellfish poisoning (DSP) from okadaic acid and analogues in many parts of the world is considered to be a comparatively minor seafood toxin syndrome, our human cell model studies suggest that synergisms with certain mycotoxins may aggravate human health impacts, depending on the concentrations. These findings highlight the issues of the shortcomings of current regulatory approaches, which do not regulate for mycotoxins in shellfish and treat seafood toxins as if they occur as single toxins. Full article
(This article belongs to the Special Issue Marine Biotoxins and Seafood Poisoning)
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