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Marine Drugs
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Novel Methods for Marine Toxins Detection and Quantification
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Novel Methods for Marine Toxins Detection and Quantification

A special issue of Marine Drugs (ISSN 1660-3397).

Deadline for manuscript submissions: closed (30 November 2021) | Viewed by 24061

Special Issue Editor

Dr. Pedro Reis Costa

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Guest Editor
Laboratório de Fitoplâncton, Departamento do Mar e Recursos Marinhos, Instituto Português do Mar e da Atmosfera, Rua Alfredo Magalhães Ramalho, 6, 1449-006 Lisboa, Portugal
Interests: harmful algal blooms; marine toxins
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Marine biotoxins are secondary metabolites produced by certain microalgae species that accumulate in filter-feeding organisms, such as bivalve molluscs, and pose a threat to whomever consumes them. During the last decade, an important transition occurred in many countries regarding the reference methods used for determination of marine toxins in shellfish. Biological methods based on mouse assays were replaced by chemical methods based on liquid chromatography. This transition raised many urgent needs in terms of knowledge of compounds toxicity, detection of new analogues, strategies for sample cleanup procedures, and matrix effects, among others. At the same time, novel methods for detection of marine toxins are being developed to respond to the need for fast, low cost, in-situ, and real time detection methods. This Special Issue aims to be a forum where researchers devoted to development of novel methods or optimization of critical steps may spread their findings to scientific community, shellfish industry, and environmental agencies.  

Dr. Pedro Reis Costa
Guest Editor

Manuscript Submission Information

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Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2900 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Marine toxins
  • Okadaic Acid
  • Saxitoxins
  • Domoic Acid
  • Emerging Toxins
  • Liquid Chromatography
  • Alternative Methods
  • High-throughput screening
  • In-situ analysis

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Related Special Issue

Published Papers (7 papers)

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Research

12 pages, 7373 KiB  
Article
Quantitation Overcoming Matrix Effects of Lipophilic Toxins in Mytilus galloprovincialis by Liquid Chromatography-Full Scan High Resolution Mass Spectrometry Analysis (LC-HR-MS)
by Camila Q. V. Costa, Inês I. Afonso, Sandra Lage, Pedro Reis Costa, Adelino V. M. Canário and José P. Da Silva
Mar. Drugs 2022, 20(2), 143; https://doi.org/10.3390/md20020143 - 15 Feb 2022
Cited by 9 | Viewed by 3074
Abstract
The analysis of marine lipophilic toxins in shellfish products still represents a challenging task due to the complexity and diversity of the sample matrix. Liquid chromatography coupled with mass spectrometry (LC-MS) is the technique of choice for accurate quantitative measurements in complex samples. [...] Read more.
The analysis of marine lipophilic toxins in shellfish products still represents a challenging task due to the complexity and diversity of the sample matrix. Liquid chromatography coupled with mass spectrometry (LC-MS) is the technique of choice for accurate quantitative measurements in complex samples. By combining unambiguous identification with the high selectivity of tandem MS, it provides the required high sensitivity and specificity. However, LC-MS is prone to matrix effects (ME) that need to be evaluated during the development and validation of methods. Furthermore, the large sample-to-sample variability, even between samples of the same species and geographic origin, needs a procedure to evaluate and control ME continuously. Here, we analyzed the toxins okadaic acid (OA), dinophysistoxins (DTX-1 and DTX-2), pectenotoxin (PTX-2), yessotoxin (YTX) and azaspiracid-1 (AZA-1). Samples were mussels (Mytilus galloprovincialis), both fresh and processed, and a toxin-free mussel reference material. We developed an accurate mass-extracted ion chromatogram (AM-XIC) based quantitation method using an Orbitrap instrument, evaluated the ME for different types and extracts of mussel samples, characterized the main compounds co-eluting with the targeted molecules and quantified toxins in samples by following a standard addition method (SAM). An AM-XIC based quantitation of lipophilic toxins in mussel samples using high resolution and accuracy full scan profiles (LC-HR-MS) is a good alternative to multi reaction monitoring (MRM) for instruments with HR capabilities. ME depend on the starting sample matrix and the sample preparation. ME are particularly strong for OA and related toxins, showing values below 50% for fresh mussel samples. Results for other toxins (AZA-1, YTX and PTX-2) are between 75% and 110%. ME in unknown matrices can be evaluated by comparing their full scan LC-HR-MS profiles with those of known samples with known ME. ME can be corrected by following SAM with AM-XIC quantitation if necessary. Full article
(This article belongs to the Special Issue Novel Methods for Marine Toxins Detection and Quantification)
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13 pages, 890 KiB  
Article
Development of a Fast Liquid Chromatography Coupled to Mass Spectrometry Method (LC-MS/MS) to Determine Fourteen Lipophilic Shellfish Toxins Based on Fused–Core Technology: In-House Validation
by Araceli E. Rossignoli, Carmen Mariño, Helena Martín and Juan Blanco
Mar. Drugs 2021, 19(11), 603; https://doi.org/10.3390/md19110603 - 24 Oct 2021
Cited by 10 | Viewed by 2511
Abstract
Prevalence and incidence of the marine toxins (paralytic, amnesic, and lipophilic toxins) including the so-called emerging toxins (these are, gymnodimines, pinnatoxins, or spirolides among others) have increased in recent years all over the world. Climate change, which is affecting the distribution of their [...] Read more.
Prevalence and incidence of the marine toxins (paralytic, amnesic, and lipophilic toxins) including the so-called emerging toxins (these are, gymnodimines, pinnatoxins, or spirolides among others) have increased in recent years all over the world. Climate change, which is affecting the distribution of their producing phytoplankton species, is probably one of the main causes. Early detection of the toxins present in a particular area, and linking the toxins to their causative phytoplankton species are key tools to minimize the risk they pose for human consumers. The development of both types of studies requires fast and highly sensitive analytical methods. In the present work, we have developed a highly sensitive liquid chromatography-mass spectrometry methodology (LC-MS/MS), using a column with fused-core particle technology, for the determination of fourteen lipophilic toxins in a single run of 3.6 min. The performance of the method was evaluated for specificity, linearity, precision (repeatability and reproducibility) and accuracy by analysing spiked and naturally contaminated samples. The in-house validation was successful, and the limit of detection (LOD) and quantification (LOQ) for all the toxins were far below their regulatory action limits. The method is suitable to be considered in monitoring systems of bivalves for food control. Full article
(This article belongs to the Special Issue Novel Methods for Marine Toxins Detection and Quantification)
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19 pages, 4293 KiB  
Article
Toxicity Screening of a Gambierdiscus australes Strain from the Western Mediterranean Sea and Identification of a Novel Maitotoxin Analogue
by Pablo Estevez, David Castro, José Manuel Leão-Martins, Manoëlla Sibat, Angels Tudó, Robert Dickey, Jorge Diogene, Philipp Hess and Ana Gago-Martinez
Mar. Drugs 2021, 19(8), 460; https://doi.org/10.3390/md19080460 - 15 Aug 2021
Cited by 19 | Viewed by 4125
Abstract
Dinoflagellate species of the genera Gambierdiscus and Fukuyoa are known to produce ciguatera poisoning-associated toxic compounds, such as ciguatoxins, or other toxins, such as maitotoxins. However, many species and strains remain poorly characterized in areas where they were recently identified, such as the [...] Read more.
Dinoflagellate species of the genera Gambierdiscus and Fukuyoa are known to produce ciguatera poisoning-associated toxic compounds, such as ciguatoxins, or other toxins, such as maitotoxins. However, many species and strains remain poorly characterized in areas where they were recently identified, such as the western Mediterranean Sea. In previous studies carried out by our research group, a G. australes strain from the Balearic Islands (Mediterranean Sea) presenting MTX-like activity was characterized by LC-MS/MS and LC-HRMS detecting 44-methyl gambierone and gambieric acids C and D. However, MTX1, which is typically found in some G. australes strains from the Pacific Ocean, was not detected. Therefore, this study focuses on the identification of the compound responsible for the MTX-like toxicity in this strain. The G. australes strain was characterized not only using LC-MS instruments but also N2a-guided HPLC fractionation. Following this approach, several toxic compounds were identified in three fractions by LC-MS/MS and HRMS. A novel MTX analogue, named MTX5, was identified in the most toxic fraction, and 44-methyl gambierone and gambieric acids C and D contributed to the toxicity observed in other fractions of this strain. Thus, G. australes from the Mediterranean Sea produces MTX5 instead of MTX1 in contrast to some strains of the same species from the Pacific Ocean. No CTX precursors were detected, reinforcing the complexity of the identification of CTXs precursors in these regions. Full article
(This article belongs to the Special Issue Novel Methods for Marine Toxins Detection and Quantification)
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10 pages, 1040 KiB  
Article
Stability of Domoic Acid in 50% Methanol Extracts and Raw Fecal Material from Bowhead Whales (Balaena mysticetus)
by Emily K. Bowers, Raphaela Stimmelmayr and Kathi A. Lefebvre
Mar. Drugs 2021, 19(8), 423; https://doi.org/10.3390/md19080423 - 27 Jul 2021
Cited by 1 | Viewed by 2695
Abstract
Domoic acid (DA), the toxin causing amnesic shellfish poisoning (ASP), is produced globally by some diatoms in the genus Pseudo-nitzschia. DA has been detected in several marine mammal species in the Alaskan Arctic, raising health concerns for marine mammals and subsistence communities [...] Read more.
Domoic acid (DA), the toxin causing amnesic shellfish poisoning (ASP), is produced globally by some diatoms in the genus Pseudo-nitzschia. DA has been detected in several marine mammal species in the Alaskan Arctic, raising health concerns for marine mammals and subsistence communities dependent upon them. Gastrointestinal matrices are routinely used to detect Harmful Algal Bloom (HAB) toxin presence in marine mammals, yet DA stability has only been studied extensively in shellfish-related matrices. To address this knowledge gap, we quantified DA in bowhead whale fecal samples at multiple time points for two groups: (1) 50% methanol extracts from feces, and (2) raw feces stored in several conditions. DA concentrations decreased to 70 ± 7.1% of time zero (T0) in the 50% methanol extracts after 2 weeks, but remained steady until the final time point at 5 weeks (66 ± 5.7% T0). In contrast, DA concentrations were stable or increased in raw fecal material after 8 weeks of freezer storage (−20 °C), at room temperature (RT) in the dark, or refrigerated at 1 °C. DA concentrations in raw feces stored in an incubator (37 °C) or at RT in the light decreased to 77 ± 2.8% and 90 ± 15.0% T0 at 8 weeks, respectively. Evaporation during storage of raw fecal material is a likely cause of the increased DA concentrations observed over time with the highest increase to 126 ± 7.6% T0 after 3.2 years of frozen storage. These results provide valuable information for developing appropriate sample storage procedures for marine mammal fecal samples. Full article
(This article belongs to the Special Issue Novel Methods for Marine Toxins Detection and Quantification)
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12 pages, 1968 KiB  
Article
Monitoring the Emergence of Algal Toxins in Shellfish: First Report on Detection of Brevetoxins in French Mediterranean Mussels
by Zouher Amzil, Amélie Derrien, Aouregan Terre Terrillon, Audrey Duval, Coralie Connes, Françoise Marco-Miralles, Elisabeth Nézan and Kenneth Neil Mertens
Mar. Drugs 2021, 19(7), 393; https://doi.org/10.3390/md19070393 - 14 Jul 2021
Cited by 19 | Viewed by 3822
Abstract
In France, four groups of lipophilic toxins are currently regulated: okadaic acid/dinophysistoxins, pectenotoxins, yessotoxins and azaspiracids. However, many other families of toxins exist, which can be emerging toxins. Emerging toxins include both toxins recently detected in a specific area of France but not [...] Read more.
In France, four groups of lipophilic toxins are currently regulated: okadaic acid/dinophysistoxins, pectenotoxins, yessotoxins and azaspiracids. However, many other families of toxins exist, which can be emerging toxins. Emerging toxins include both toxins recently detected in a specific area of France but not regulated yet (e.g., cyclic imines, ovatoxins) or toxins only detected outside of France (e.g., brevetoxins). To anticipate the introduction to France of these emerging toxins, a monitoring program called EMERGTOX was set up along the French coasts in 2018. The single-laboratory validation of this approach was performed according to the NF V03-110 guidelines by building an accuracy profile. Our specific, reliable and sensitive approach allowed us to detect brevetoxins (BTX-2 and/or BTX-3) in addition to the lipophilic toxins already regulated in France. Brevetoxins were detected for the first time in French Mediterranean mussels (Diana Lagoon, Corsica) in autumn 2018, and regularly every year since during the same seasons (autumn, winter). The maximum content found was 345 µg (BTX-2 + BTX-3)/kg in mussel digestive glands in November 2020. None were detected in oysters sampled at the same site. In addition, a retroactive analysis of preserved mussels demonstrated the presence of BTX-3 in mussels from the same site sampled in November 2015. The detection of BTX could be related to the presence in situ at the same period of four Karenia species and two raphidophytes, which all could be potential producers of these toxins. Further investigations are necessary to understand the origin of these toxins. Full article
(This article belongs to the Special Issue Novel Methods for Marine Toxins Detection and Quantification)
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14 pages, 1058 KiB  
Article
Improved Isolation Procedures for Okadaic Acid Group Toxins from Shellfish (Mytilus edulis) and Microalgae (Prorocentrum lima)
by Jane Kilcoyne, Stephen Burrell, Cíara Nulty, Rafael Salas, Elliott J. Wright, Isabelle Rajotte and Christopher O. Miles
Mar. Drugs 2020, 18(12), 647; https://doi.org/10.3390/md18120647 - 16 Dec 2020
Cited by 10 | Viewed by 2782
Abstract
Okadaic acid (OA) group toxins may accumulate in shellfish and can result in diarrhetic shellfish poisoning when consumed by humans, and are therefore regulated. Purified toxins are required for the production of certified reference materials used to accurately quantitate toxin levels in shellfish [...] Read more.
Okadaic acid (OA) group toxins may accumulate in shellfish and can result in diarrhetic shellfish poisoning when consumed by humans, and are therefore regulated. Purified toxins are required for the production of certified reference materials used to accurately quantitate toxin levels in shellfish and water samples, and for other research purposes. An improved procedure was developed for the isolation of dinophysistoxin 2 (DTX2) from shellfish (M. edulis), reducing the number of purification steps from eight to five, thereby increasing recoveries to ~68%, compared to ~40% in a previously reported method, and a purity of >95%. Cell densities and toxin production were monitored in cultures of Prorocentrum lima, that produced OA, DTX1, and their esters, over ~1.5 years with maximum cell densities of ~70,000 cells mL−1 observed. Toxin accumulation progressively increased over the study period, to ~0.7 and 2.1 mg L−1 of OA and DTX1 (including their esters), respectively, providing information on appropriate harvesting times. A procedure for the purification of OA and DTX1 from the harvested biomass was developed employing four purification steps, with recoveries of ~76% and purities of >95% being achieved. Purities were confirmed by LC-HRMS, LC-UV, and NMR spectroscopy. Additional stability observations led to a better understanding of the chemistry of these toxins. Full article
(This article belongs to the Special Issue Novel Methods for Marine Toxins Detection and Quantification)
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30 pages, 2591 KiB  
Article
Application of Six Detection Methods for Analysis of Paralytic Shellfish Toxins in Shellfish from Four Regions within Latin America
by Andrew D. Turner, Sophie Tarnovius, Robert G. Hatfield, Mickael Teixeira Alves, Maggie Broadwater, Frances Van Dolah, Ernesto Garcia-Mendoza, Dinorah Medina, Maria Salhi, Alejandra B. Goya, Fernanda Barrera, Daniel Carrasco, Ignacio Rubilar and Benjamin A. Suarez-Isla
Mar. Drugs 2020, 18(12), 616; https://doi.org/10.3390/md18120616 - 3 Dec 2020
Cited by 17 | Viewed by 3563
Abstract
With the move away from use of mouse bioassay (MBA) to test bivalve mollusc shellfish for paralytic shellfish poisoning (PSP) toxins, countries around the world are having to adopt non-animal-based alternatives that fulfil ethical and legal requirements. Various assays have been developed which [...] Read more.
With the move away from use of mouse bioassay (MBA) to test bivalve mollusc shellfish for paralytic shellfish poisoning (PSP) toxins, countries around the world are having to adopt non-animal-based alternatives that fulfil ethical and legal requirements. Various assays have been developed which have been subjected to single-laboratory and multi-laboratory validation studies, gaining acceptance as official methods of analysis and approval for use in some countries as official control testing methods. The majority of validation studies conducted to date do not, however, incorporate shellfish species sourced from Latin America. Consequently, this study sought to investigate the performance of five alternative PSP testing methods together with the MBA, comparing the PSP toxin data generated both qualitatively and quantitatively. The methods included a receptor binding assay (RBA), two liquid chromatography with fluorescence detection (LC-FLD) methods including both pre-column and post-column oxidation, liquid chromatography with tandem mass spectrometry (LC-MS/MS) and a commercial lateral flow assay (LFA) from Scotia. A total of three hundred and forty-nine shellfish samples from Argentina, Mexico, Chile and Uruguay were assessed. For the majority of samples, qualitative results compared well between methods. Good statistical correlations were demonstrated between the majority of quantitative results, with a notably excellent correlation between the current EU reference method using pre-column oxidation LC-FLD and LC-MS/MS. The LFA showed great potential for qualitative determination of PSP toxins, although the findings of high numbers of false-positive results and two false negatives highlighted that some caution is still needed when interpreting results. This study demonstrated that effective replacement methods are available for countries that no longer wish to use the MBA, but highlighted the importance of comparing toxin data from the replacement method using local shellfish species of concern before implementing new methods in official control testing programs. Full article
(This article belongs to the Special Issue Novel Methods for Marine Toxins Detection and Quantification)
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