Potential Threats Posed by New or Emerging Marine Biotoxins in UK Waters and Examination of Detection Methodology Used in Their Control: Brevetoxins
Abstract
:1. Introduction
2. Potential Brevetoxin-Producing Phytoplankton Threats for UK Waters
3. Potential New/Emerging Brevetoxin Threats for UK Waters
4. Brevetoxin-Producing Phytoplankton Detection Methods
4.1. Sample Collection
4.2. Sample Enumeration
4.3. Particle Counting Methods
4.4. Molecular Methods
4.5. Indirect Estimates of Phytoplankton Biomass
4.6. Future Monitoring of Karenia
5. Toxin Testing Methods
5.1. Mouse Bioassays
5.2. Chemical Methods
5.2.1. Extraction
5.2.2. Conventional Chromatography Methods
5.2.3. LC–MS Methods
5.3. Biomolecular Methods
5.3.1. Cytotoxicity Assay
5.3.2. Receptor Binding Assays
5.3.3. Immunoassays
5.3.4. Biosensor Methods
6. Suitability of Toxin Testing Methods
6.1. Suitability of Existing and Potential Methods for Brevetoxin Testing
Method | Advantages | Disadvantages |
---|---|---|
Microscopy | Detection of Karenia genus | Detection not species-specific |
Fulfils requirement of legislation | No evidence for shellfish toxicity | |
Particle counting methods | Detection of Karenia genus | Detection may be compromised when analysing dense blooms |
Potentially a more rapid enumeration of cells | Little evidence for suitability for field based monitoring | |
Potential for in-situ analysis | Sample preservation compromises detection | |
Detection not species-specific | ||
Molecular techniques | Enables identification of different Karenia species | Methods still under development, with no reports of application to official testing to date |
Toxic species can be identified for verification purposes | Requires expensive instrumentation and highly trained analysts | |
Mouse bioassay (MBA) | Primary tool for toxicity assessment | Inability to detect all BTXs |
History of use and prevention of sickness | Ethical issues | |
Relatively simple technology | Variable performance | |
Not validated | ||
Cytotoxicity assay | Sensitive functional assay | Matrix effects, high variability |
Use of cultured vs. primary cells | Poor correlation with MBA | |
Used to detect all analogues | Noting limited data on performance characteristics of method | |
Time consuming | ||
Receptor binding assays (RBA) | Simple, sensitive, rapid | Variable affinity for BTX metabolites |
Good performance in collaborative study | Requirement for animal tissues and radiolabel | |
Promising fluorescence-based binding assay | Matrix effects | |
Limited development to date with fluorescence-based binding assay | ||
Immunoassays | Specific for type-B and sensitive | Lower cross reactivity for type-A BTXs |
High throughout, fast turnaround and “in the field” | Screening tool only—no toxicity or profile data provided | |
Low matrix effects | Valuable quantities of toxin required to produce antibodies | |
Good correlation with MBA and LC–MS | Potential issues with commercial kits, with manufacturers changing properties or performance characteristics | |
Good single lab validation and multi-lab study anticipated | ||
Conventional chromatography | Use of MEKC-LIF, LC-UV and LC-FLD reported | Very limited data available for determination of low numbers of toxins |
Some degree of specificity | Lack of standards and equipment | |
Proof of concept required for all appropriate toxins | ||
LC–MS (MS) | Highly specific | Expensive instrumentation |
Sensitive | Lack of all suitable standards | |
Single laboratory validation performed | ||
Biosensor methods | Useful research screening tools | Lack of specificity |
High sensitivity | Expensive instrumentation for biosensors | |
Matrix effects can be diluted |
6.2. Identification of Knowledge Gaps Which Might be Addressed through Further Research or Method Development
- Understanding and identification of additional algal species which produce brevetoxins, in particular those found to grow well in water conditions relevant to the UK at present or in the future;
- Analysis of algal cultures by suitable methods for assessment of presence of BTXs in water samples;
- Identified shellfish species that accumulate BTXs, together with associated accumulation and depuration rates;
- The determination of BTX metabolites by LC-MS profile studies in relevant bivalve species;
- Continued evaluation of MBA-replacement methods, in particular including ELISA and LC–MS/MS;
- Understanding of BTX and BTX metabolites toxicity in relation to human exposure, including long term assessment of intoxicated people to determine potential long term affects.
6.3. Global Regimes
7. Conclusions: Proposed Options for Routine Monitoring of Phytoplankton and Toxins to Meet Legal Requirements
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Abraham, A.; Wang, Y.; El Said, K.R.; Plakas, S.M. Characterisation of brevetoxin metabolisms in Karenia. brevis bloom-exposed clams (Mercenaria sp.) by LC-MS/MS. Toxicon 2012, 60, 1030–1040. [Google Scholar]
- Wang, W. Development of Novel Liquid Chromatography-Electrospray Tandem Mass Spectrometry Approaches for the Structural Characterisation of Brevetoxins Including in vitro Metabolites. Ph.D. Theses, University of New Orleans, New Orleans, LA, USA, 2007; p. 600. [Google Scholar]
- Tubaro, A.; Sosa, S.; Hungerford, J. Toxicology and diversity of marine toxins. In Veterinary Toxicology: Basic and Clinical Principles; Gupta, R.C., Ed.; Elsevier: New York, NY, USA, 2012; pp. 896–936. [Google Scholar]
- Plakas, S.M.; Dickey, R.W. Advances in monitoring and toxicity assessment of brevetoxins in molluscan shellfish. Toxicon 2010, 56, 137–149. [Google Scholar] [CrossRef] [PubMed]
- Watkins, S.M.; Reich, A.; Fleming, L.E.; Hammond, R. Neurotoxic shellfish poisoning. Mar. Drugs 2008, 6, 431–455. [Google Scholar] [CrossRef] [PubMed]
- FAO (Food and Agriculture Organisation of the United Nations). Marine Biotoxins; FAO Food and Nutrition Paper 80; FAO: Rome, Italy, 2004; pp. 1–287. [Google Scholar]
- Baden, D.G.; Mende, T.J. Toxicity of two toxins from the Florida red tide marine dinoflagellate, Ptychodiscus brevis. Toxicon 1982, 20, 457–461. [Google Scholar] [CrossRef] [PubMed]
- Leighfield, T.A.; Muha, N.; Ramsdell, J.S. Tissue distribution of amino acid- and lipid-brevetoxins after intravenous administration to C57BL/6 Mice. Chem. Res. Toxicol. 2014, 27, 1166–1175. [Google Scholar] [CrossRef] [PubMed]
- Sayer, A.N.; Hu, Q.; Bourdelais, A.J.; Baden, D.G.; Gibson, J.E. The inhibition of CHO-K1-BH4 cell proliferation and induction of chromosomal aberrations by brevetoxins in vitro. Food Chem. Toxicol. 2006, 44, 1082–1091. [Google Scholar] [CrossRef] [PubMed]
- Murell, R.N.; Gibson, J.E. Brevetoxins 2, 3, 6,and 9 show variability in potency and cause significant induction of DNA damage and apoptosis in Jurkat E6-1 cells. Arch. Toxicol. 2009, 83, 1009–1019. [Google Scholar] [CrossRef] [PubMed]
- EFSA (2010). EFSA Panel on Contaminants in the Food Chain (CONTAM): Scientific Opinion on marine biotoxins in shellfish—Emerging toxins: Brevetoxin group. EFSA J. 2010, 8, 1677. [Google Scholar]
- Bourdelais, A.J.; Jacobs, H.M.; Wright, J.L.C.; Bigwarfe, P.M.; Baden, D.G. A new polyether ladder compound produced by the dinoflagellate, Karenia brevis. J. Nat. Prod. 2005, 28, 2–6. [Google Scholar] [CrossRef]
- Pierce, R.H.; Henry, M.S. Harmful algal toxins of the Florida red tide (Karenia brevis): Natural chemical stressors in South Florida coastal ecosystems. Ecotoxicology 2008, 17, 623–631. [Google Scholar] [CrossRef] [PubMed]
- Steidinger, K.A.; Landsberg, J.H.; Flewelling, L.J.; Kikpatrick, B.A. Toxic dinoflagellates. In Oceans and Human Health: Rosks and Remedies from the Seas; Walsh, P.J., Smith, S., Fleming, L., Solo-Gabriele, H., Gerwick, W.I., Eds.; Elsevier: New York, NY, USA, 2008. [Google Scholar]
- Pierce, R.H.; Henry, M.S.; Blum, P.C.; Hamel, S.L.; Kirkpatrick, B.; Cheng, Y.S.; Zhou, Y.; Irvin, C.M.; Naar, J. Brevetoxin composition in water and marine aerosols along a Florida beach: Assessing potential human exposure to marine biotoxins. Harmful Algae 1995, 4, 965–972. [Google Scholar] [CrossRef]
- Fleming, L.E.; Kirkpatrick, B.; Backer, L.C.; Bean, J.A.; Wanner, A.; Dalpra, D.; Tamer, R.; Zalas, J.; Cheng, Y.-S.; Pierce, R.; et al. Initial evaluation of the effects of aerosolized Florida red tide toxins (brevetoxins) in persons with Asthma. Environ. Health Perspect. 2005, 113, 650–657. [Google Scholar]
- Zaias, J.; Fleming, L.E.; Baden, D.G.; Abraham, W.M. Repeated exposure to aerosolized brevetoxin-3 induced prolonged airway hyperresponsiveness and lung inflammation in sheep. Inhal. Toxicol. 2011, 23, 205–211. [Google Scholar] [CrossRef] [PubMed]
- Otero, A.; Chapela, M.J.; Atanassova, M.; Cabado, A.G. Phycotoxin biotransformation, shellfish detoxification and industrial application. In New Trends in Marine and Freshwater Toxins; Cabado, A.G., Vieites, J.M., Eds.; Nova Science Publishers: New York, NY, USA, 2012. [Google Scholar]
- Dickey, R.; Jester, E.; Granade, R.; Mowdy, D.; Moncreiff, C.; Rebarchik, D.; Robl, M.; Musser, S.; Poli, M. Monitoring brevetoxins during a Gymnodinium breve red tide: Comparison of sodium channel specific cytotoxicity assay and mouse bioassay for determination of neurotoxic shellfish toxins in shellfish extracts. Nat. Toxins 1999, 7, 157–165. [Google Scholar] [CrossRef] [PubMed]
- Leverone, J.R.; Shumway, S.E.; Blake, N.J. Comparative effects of the toxic dinoflagellate CKarenia brevis on clearance rates in juveniles of four bivalve molluscs from Florida, USA. Toxicon 2007, 49, 634–645. [Google Scholar] [CrossRef] [PubMed]
- Echevarria, M.; Naar, J.P.; Tomas, C.; Pawlik, J.R. Effects of Karenia brevis on clearance rates and bioaccumulation of brevetoxins in benthic suspension feeding invertebrates. Aquat. Toxicol. 2012, 106, 85–94. [Google Scholar] [CrossRef] [PubMed]
- Brand, L.E.; Campbell, L.; Bresnan, E. Karenia: The biology and ecology of a toxic genus. Harmful Algae 2012, 14, 156–178. [Google Scholar] [CrossRef]
- Davidson, K.; Miller, P.I.; Wilding, T.; Shutler, J.; Bresnan, E.; Kennington, K.; Swan, S. A large and prolonged bloom of Karenia mikimotoi in Scottish waters in 2006. Harmful Algae 2009, 8, 349–361. [Google Scholar] [CrossRef]
- Silke, J.; O’Beirn, F.; Cronin, M. Marenia mikimotoi: An Exceptional Dinoflagellate Bloom in Western Irish Waters, Summer 2005; Marine Environment and Health Series, No. 21, 2005; Marine Institute: Galway, UK, 2005. [Google Scholar]
- Satake, M.; Shoji, M.; Oshima, Y.; Naoki, H.; Fujita, T.; Yasumoto, T. Gymnocin-A, a cytotoxic polyether from the notorious red tide dinoflagellate, Gymnodinium mikimotoi. Tetrahedron Lett. 2002, 43, 5829–5832. [Google Scholar] [CrossRef]
- MacKenzie, L.; Rhodes, L.L.; Till, D.; Chang, F.H.; Kaspar, H.; Haywood, A.; Kapa, J.; Walker, B. A Gymnodinium. sp. bloom and the contamination of shellfish with lipid soluble toxins in New Zealand, January–April 1993. In Harmful Marine Algal Blooms; Lassus, P., Erard, E., Gentien, P., Marcaillou, C., Eds.; Lavoisier Science Publishers: Paris, France, 1995; pp. 795–800. [Google Scholar]
- Hallegraeff, G.; Bolch, C.J. Transport of toxic dinoflagellate cysts via ships’ ballast water. Mar. Poll Bull. 1991, 22, 27–30. [Google Scholar] [CrossRef]
- Chang, F.H.; Chiswell, S.M.; Uddstrom, M.J. Occurrence and distribution of Karenia brevisulcata (Dinophyceae) during the 1998 summer toxic outbreaks on the central east coast of New Zealand. Phycologia 2001, 40, 215–222. [Google Scholar] [CrossRef]
- Holland, P.T.; Shi, F.; Satake, M. Novel toxins produced by the dinoflagellate Karenia brevisulcata. Harmful Algae 2012, 13, 47–57. [Google Scholar] [CrossRef]
- Suzuki, R.; Irie, R.; Harntaweesup, Y.; Tachibana, K.; Holland, P.T.; Harwood, D.T.; Shi, F.; Beuzenberg, V.; Itoh, Y.; Pascal, S.; et al. Brevisulcatic acids, marine ladder-frame polyethers from the red tide dinoflagellate Karenia brevisulcate in New Zealand. Org. Lett. 2014, 16, 5850. [Google Scholar]
- Harwood, D.T.; Shi, F.; Satake, M.; Holland, P.T. A sensitive LC-MS/MS assay for brevisulcenal and brevisulcatic acid toxins produced by the dinoflagellate Karenia brevisculcata. Toxicon 2014, 84, 19–27. [Google Scholar] [CrossRef] [PubMed]
- Satake, M. Novel toxins from the New Zealand red tide dinoflagellate Karenia brevisulcata. In Proceedings of the International Conference on Harmful Algae, Wellington, New Zealand, 27–31 October 2014.
- Bresnan, E.; Marine Scotland, Aberdeen, Aberdeenshire, UK. Personal Communication, 2013.
- Haywood, A.J.; Steidinger, K.A.; Truby, E.W.; Bergquist, P.R.; Bergquist, P.L.; Adamson, J.; Mackenzie, L. Comparative morphology and molecular phylogenetic analysis of three new species of the genus Karenia (Dinophyceae) from New Zealand. J. Phycol. 2004, 40, 165–179. [Google Scholar] [CrossRef]
- Fraga, S.; Sanchez, F.J. Toxic and potentially toxic dinoflagellates found in Galician Rias (NW Spain). In Toxic Dinoflagellates; Anderson, D.M., White, A.D., Baden, D.G., Eds.; Elsevier Science Publishers: New York, NY, USA, 1985; pp. 51–54. [Google Scholar]
- Fukuyo, Y.; Takano, H.; Chihara, M.; Matsuoka, K. Red Tide Organisms in Japan—An Illustrated Taxonomic Guide; Uchida Rokakuho: Tokyo, Japan, 1990. [Google Scholar]
- Davidson, K.; Gowen, R.; Tett, P.; Bresnan, E.; Harrison, P.J.; McKinney, A.; Milligan, S.; Mills, D.K.; Silke, J.; Crooks, A.M. Harmful algal blooms: How strong is the evidence that nutrient ratios and forms influence their occurrence? Est. Coast. Shelf Sci. 2012, 115, 399–413. [Google Scholar] [CrossRef]
- Gowen, R.J.; Tett, P.; Bresnan, E.; Davidson, K.; McKinney, A.; Milligan, S.; Mills, D.K.; Silke, J.; Gordon, A.; Crooks, A.M. Anthropogenic nutrient enrichment and blooms of harmful micro-algae. Oceanogr. Mar. Biol. 2012, 50, 65–126. [Google Scholar]
- Smayda, T.J. Harmful Algal Bloom Communities in Scottish Coastal Waters: Relationship to Fish Farming and Regional Comparisons—A Review. The Scottish Government, 2005. Available online: http://www.scotland.gov.uk/Resource/Doc/92174/0022031.pdf (accessed on 2 March 2015).
- MacDonald, E.M.; Davidson, R.D. The Occurrence of Harmful Algae in Ballast Water Discharges to Scottish Ports and the Effects of Mid-Water Exchange in Regional Seas. In Proceedings of the 8th International Conference on Harmful Algae; Reguera, B., Blanco, J., Fernandez, M.L., Wyatt, T., Eds.; IOC of UNESCO: Vigo, Spain, 1998; pp. 200–223. [Google Scholar]
- Hamer, J.P.; Lucas, I.A.N.; McCollin, T.S. Harmful dinoflagellate resting cysts in ships’ ballast tank sediments: Potential for introduction into English and Welsh waters. Phycologia 2001, 40, 246–255. [Google Scholar] [CrossRef]
- Roy, S.; Parerteau, M.; Casas-Monroy, O.; Rochon, A. Coastal ship traffic: A significant introduction vector for potentially harmful dinoflagellates in eastern Canada. Can. J. Fish. Aquat. Sci. 2012, 69, 627–644. [Google Scholar] [CrossRef]
- ICES, 2010. In Report of the Workshop on Harmful Phyto-Plankton that Could Potentially be Trans-Ported or Introduced by Ballast Water (WKHABAL); ICES CM 2010/ACOM: 67; ICES: Copenhagen, Denmark, 2010.
- Hallegraeff, G.M. Ocean climate change, phytoplankton community responses, and harmful algal blooms: A formidable predictive challenge. J. Phycol. 2010, 46, 220–235. [Google Scholar] [CrossRef]
- Bresnan, E.; Fernand, L.; Davidson, K.; Edwards, M.; Milligan, S.; Gowan, R.; Silke, J.; Kröger, S.; Raine, R. Climate Change impacts on Harmful Algal Blooms (HABs) in MCCIP Annual Report Card 2010. pp. 2010–2011. MCCIP Science Review. Available online: www.mccip.org.uk/arc (accessed on 2 March 2015).
- Bresnan, E.; Davidson, K.; Edwards, M.; Fernand, L.; Gowen, R.; Hall, A.; Kennington, K.; Milligan, S.; Raine, R.; Silke, J. Harmful Algal Blooms Marine Climate Change Impact Partnership Report Card. 2013.
- Eppley, R.W. Temperature and phytoplankton growth in the sea. Fish. Bull. 1972, 70, 1063–1085. [Google Scholar]
- Edwards, M.; Richardson, J. Impact of climate change on marine pleagic phenology and trophic mismatch. Nature 2004, 430, 881–884. [Google Scholar] [CrossRef] [PubMed]
- Paredes, I.; Rietjens, I.M.C.M.; Vietes, J.M.; Cabado, A.G. Update of risk assessments of main marine biotoxins in the European Union. Toxicon 2011, 58, 336–354. [Google Scholar] [CrossRef] [PubMed]
- Plakas, S.M.; Jester, E.L.E.; El Said, K.R.; Granade, H.R.; Abraham, A.; Dickey, R.W.; Scott, P.S.; Flewelling, L.; Henry, M.; Blum, P.; et al. Monitoring of brevetoxins in the Kareina brevis bloom-exposed Eastern oyster (Crassostrea virginica). Toxicon 2008, 52, 32–38. [Google Scholar] [PubMed]
- Landsberg, J.H. The effects of harmful algal blooms on aquatic organisms. Rev. Fish. Sci. 2002, 10, 113–390. [Google Scholar] [CrossRef]
- Carmen Louzao, M.; Lago, J.; Ferreira, M.; Alfonso, A. Advances in knowledge of phycotoxins, new information about their toxicology and consequences on European legislation. In New Trends in Marine and Freshwater Toxins; Cabado, A.G., Vieites, J.M., Eds.; Nova Publishers: New York, NY, USA, 2012; pp. 149–202. [Google Scholar]
- Anderson, P. Design and Implementation of Some Harmful Algal Monitoring Systems IOC Technical Series No. 44; UNESCO: Paris, France, 1996. [Google Scholar]
- Karlson, B.; Cusack, C.; Bresnan, E. Microscopic and Molecular Methods for Quantitative Phytoplankton Analysis; IOC Manuals and Guides, No. 55. (IOC/2010/MG/55); UNESCO: Paris, France, 2012. [Google Scholar]
- Sekar, R.; Fuchs, B.M.; Amann, R.; Pernthaler, J. Flow sorting of marine bacterioplankton after fluorescence In situ hybridization. Appl. Environ. Micro 2004, 70, 6210–6219. [Google Scholar] [CrossRef]
- Kalyuzhnaya, M.G.; Zabinbsky, R.; Bowerman, S.; Baker, D.R.; Lidstrom, M.E.; Chistoserdova, L. Fluorescence in situ hybridization-flow cytometry-cell sorting-based method for separation and enrichment of type I and type II methanotroph populations. Appl. Environ. Micro 2006, 72, 4293–4301. [Google Scholar] [CrossRef]
- Eckford-Soper, L.K.; Davidson, K.; Bresnan, E. Identification and quantification of toxic and non-toxic strains of the harmful dinoflagellate Alexandrium tamarense using fluorescence in situ hybridization and flow cytometry. Limnol. Oceanogr. Methods 2013, 11, 540–548. [Google Scholar] [CrossRef]
- Buskey, E.; Hyall, C.J. Use of the FlowCAM for semi-automated recognition and enumeration of red tide cells (Karenia brevis) in natural plankton samples. Harmful Algae 2006, 5, 685–692. [Google Scholar] [CrossRef]
- Campbell, L.; Henricks, D.W.; Olson, R.J.; Sosik, H. Continuous automated imaging-in-flow cytometry for detection and early warning of Karenia brevis blooms in the Gulf of Mexico. Environ. Sci. Pollut. Res. 2013, 20, 6896–6902. [Google Scholar] [CrossRef]
- Smith, K.F.; de Salas, M.; Adamson, J.; Rhodes, L.L. Rapid and accurate identification by real-time PCR of biotoxin-producing dinoflagellates from the family gymnodiniaceae. Mar. Drugs 2014, 12, 1361–1376. [Google Scholar] [CrossRef] [PubMed]
- Ishizaka, J.; Kitaura, Y.; Touke, Y.; Sasaki, H.; Tanaka, A.; Murakami, H.; Suzuki, T.; Matsuoka, K.; Nakata, H. Satellite detection of red tide in Ariake Sound 1998–2201. J. Oceanogr. 2006, 62, 37–45. [Google Scholar] [CrossRef]
- Shutler, J.D.; Davidson, K.; Miller, P.I.; Swan, S.C.; Grant, M.G.; Bresnan, E. An adaptive approach to detect high biomass algal blooms from EO chlorophyll-a data in support of harmful algal bloom monitoring. Remote Sens. Lett. 2012, 3, 101–110. [Google Scholar] [CrossRef]
- Kurekin, A.A.; Miller, P.I.; van der Woerd, H.J. Satellite discrimination of Karenia mikimotoi and Phaeocystis harmful algal blooms in European coastal waters: Merged classification of ocean colour data. Harmful Algae 2014, 31, 163–176. [Google Scholar] [CrossRef]
- Stumpf, R.P.; Tomlinson, M.C.; Calkins, J.A.; Kirkpatrick, B.; Fisher, K.; Nierenberg, K.; Currier, R.; Wynne, T.T. Skill assessment for an operational algal bloom forecast system. J. Mar. Syst. 2009, 76, 151–161. [Google Scholar] [CrossRef] [PubMed]
- Hess, P.; Amzil, Z.; Belin, C.; Compère, C.; Lassus, P.; Ménesguen, A. Evolution of European monitoring systems for shellfish toxins—An increased need for the surveillance of phytoplankton. In Proceedings of the 14th International Conference on Harmful Algae, Heraklion Crete, Greek, 2012.
- Richardson, Greek; Pinckney, J.L. Monitoring of the toxic dinoflagellate Karenia brevis using gyroxanthin-based detection methods. J. Appl. Phycol. 2004, 16, 315–328. [Google Scholar] [CrossRef]
- Salas, M.F.; de Bolch, C.J.S.; Botes, L.; Nash, G.; Wright, S.W.; Hallegraeff, G.M. Takayama gen. nov (Gymnodiniales, Dinophyceae), a new genus of unarmored dinoflagellates with sigmoid apical grooves, including the description of two new species. J. Phycol. 2003, 39, 1233–1246. [Google Scholar]
- Salas, M.F.; de Bolch, C.J.S.; Hallegraeff, G.M. Karlodinium australe sp. nov. (Gymnodiniales, Dinophyceae), a new potentially ichthyotoxic unarmoured dinoflagellate from lagoonal habitats of south-eastern Australia. Phycologia 2005, 44, 640–650. [Google Scholar]
- Kirkpatrick, G.J.; Millie, D.; Moline, M.A.; Schofield, O. Optical discrimination of a phytoplankton species in natural mixed populations. Limnol. Oceanogr. 2000, 45, 467–471. [Google Scholar] [CrossRef]
- Robbins, I.C.; Kirkpatrick, G.J.; Blackwell, S.M.; Hillier, J.; Knight, C.A.; Moline, M.A. Improved monitoring of HABs using autonomous underwater vehicles (AUV). Harmful Algae 2006, 5, 749–761. [Google Scholar] [CrossRef]
- Wong, C.K.; Hung, P.; Kam, K.M. Development of an ICR mouse bioassay for toxicity evaluation in neurotoxic poisoning toxins-contaminated shellfish. Biomed. Environ. Sci. 2013, 26, 346–364. [Google Scholar] [PubMed]
- Stewart, I.; McLeod, C. The laboratory mouse in routine food safety testing for marine algal biotoxins and harmful algal bloom toxin research: Past, present and future. J. AOAC Intl. 2014, 97, 356–372. [Google Scholar] [CrossRef]
- Munday, R.; Reeve, J. Risk assessment of shellfish toxins. Toxins 2012, 5, 2109–2137. [Google Scholar] [CrossRef]
- Wang, Z.; El Said, K.R.; Plakas, S.M.; Dickey, R.W. Sample preparation methods for analysis of brevetoxins in oysters by LC-MS. In Harmful Algae 2002. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography and Intergovernmental Oceanographic Commission of UNESCO; Steidinger, K.A., Landsberg, J.H., Tomas, C.R., Vargo, G.A., Eds.; UNESCO: St. Petersburg, FL, USA, 2004; pp. 300–302. [Google Scholar]
- Plakas, S.M.; Wang, Z.; El Said, K.R.; Jester, E.L.E.; Granade, H.R.; Flewelling, L.; Scott, P.S.; Dickey, R.W. Brevetoxin metabolism and elimination in the Eastern oyster (Crassostrea virginica) after controlled exposures to Karenia brevis. Toxicon 2004, 44, 677–685. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Plakas, S.M.; El Said, K.R.; Jester, E.L.E.; Granade, H.R.; Dickey, R.W. LC/MS analysis of brevetoxin metabolites in the Eastern oyster (Crassostrea virginica). Toxicon 2004, 43, 455–465. [Google Scholar] [CrossRef] [PubMed]
- Abraham, A.; Plakas, S.M.; Wang, Z.H.; Jester, E.L.E.; El Said, K.R.; Granade, H.R.; Henry, M.S.; Blum, P.C.; Pierce, R.H.; Dickey, R.W. Characterisation of polar brevetoxin derivatives isolated from Karenia. brevis cultures and natural blooms. Toxicon 2006, 48, 104–115. [Google Scholar]
- Nozawa, A.; Tsuji, K.; And Ishida, H. Implication of brevetoxin B1 and PbTx-3 in neurotoxic shellfish poisoning in New Zealand by isolation and quantitative determination with liquid chromatography tandem mass spectrometry. Toxicon 2003, 42, 91–103. [Google Scholar] [CrossRef] [PubMed]
- Poli, M.A.; Musser, S.M.; Dickey, R.; Eilers, P.; Hall, S. Neurotoxic shellfish poisoning and brevetoxin metabolites: A case study from Florida. Toxicon 2000, 38, 981–983. [Google Scholar] [CrossRef] [PubMed]
- Pierce, R.H.; Henry, M.S.; Blum, P.C.; Lyons, J.; Cheng, Y.S.; Yazzie, D. Brevetoxin concentrations in marine aerosol: Human exposure levels during a Karenia brevis harmful algal bloom. Bull. Environ. Contam. Toxicol. 2003, 70, 161–165. [Google Scholar] [CrossRef] [PubMed]
- Dickey, R.W.; Bencasth, F.A.; Granade, H.R.; Lewis, R.J. Liquid chromatographic mass spectrometric methods for the determination of marine polyether toxins. Bull. Exotic Pathol. Soc. 1992, 85, 514–515. [Google Scholar]
- Shea, D. Analysis of brevetoxins by micellar electrokinetic capillary chromatography and laser-induced fluorescence detection. Electrophoresis 1997, 18, 277–283. [Google Scholar] [CrossRef] [PubMed]
- Baden, D.G.; Bourdelais, A.J.; Jacocks, H.; Michelliza, S.; Naar, J. Natural and derivative brevetoxins: Historical background, multiplicity and effects. Environ. Health Perspect. 2005, 113, 621–625. [Google Scholar] [CrossRef] [PubMed]
- Plakas, S.M.; Elsaid, K.R.; Jester, E.L.E.; Granade, H.R.; Musser, S.M.; Dickey, R.W. Confirmation of brevetoxin metabolism in the Eastern oyster (Crassostrea Virginia) by controlled exposures to pure toxins and to Karenia brevis cultures. Toxicon 2002, 40, 721–729. [Google Scholar] [CrossRef] [PubMed]
- Ishida, H.; Nozawa, A.; Nukaya, H.; Tsuji, K. Comparative concentrations of brevetoxins PbTx-2, PbTx-3, BTX-B1 and BTX-B5 in cockle, Austrovenus stutchburyi, greenshell mussel, Perna canaliculus, and Pacific oyster, Crassostrea gigas, involved neurotoxic shellfish poisoning in New Zealand. Toxicon 2004, 43, 779–789. [Google Scholar] [CrossRef] [PubMed]
- Hua, Y.; Lu, W.; Henry, M.; Pierce, R.; Cole, R.B. On-line high-performance liquid chromatography-electrospray ionisation mass spectrometry for the determinatino of brevetoxins in “red tide” algae. Anal. Chem. 1995, 67, 1815–1823. [Google Scholar] [CrossRef] [PubMed]
- Hua, Y.; Lu, W.; Henry, M.S.; Pierce, R.H.; Cole, R.B. On-line chromatography-electrospray ionisation mass spectrometry for determination of the brevetoxin profile in natural “red tide” algae blooms. J. Chrom. A 1996, 750, 115–125. [Google Scholar] [CrossRef]
- Hua, Y.; Cole, R.N. Electrospray ionisation tandem mass spectrometry for structural elucidation of protonated brevetoxins in red tide algae. Anal. Chem. 2000, 72, 376–383. [Google Scholar] [CrossRef] [PubMed]
- Ishida, H.; Nozawa, A.; Nukaya, H.; Rhodes, L.; McNabb, P.; Holland, P.T.; Tsuji, K. Brevetoxin metabolism in shellfish associated with neurotoxic shellfish poisoning. In Mycotoxins and Phycotoxins: Advances in Determination, Toxicology and Exposure Management; Njapau, H., Trujillo, S., van Egmond, H., Park, D.L., Eds.; Wageningen Academic: Wageningen, The Netherlands, 2006; pp. 297–307. [Google Scholar]
- Ishida, H.; Nozawa, A.; Nukaya, H.; Rhodes, L.; McNabb, P.; Holland, P.T.; Tsuji, K. Confirmation of brevetoxin metabolism in cockle, Austrovenus stutchburyi, and greenshell mussel, Perna canaliculus, associated with New Zealand neurotoxic shellfish poisoning, by controlled exposure to Karenia brevis culture. Toxicon 2004, 43, 701–712. [Google Scholar] [CrossRef] [PubMed]
- McNabb, P.; Rhodes, L.; Selwood, A. Results of analyses for brevetoxins and pinnatoxins in Rangaunu Harbour oysters, 1993–2008. Prepared for NZ Food Safety Authority. Cawthron 2008, 1453, 18. [Google Scholar]
- Wang, Z.; Cole, R.B. Enhanced collision-induced decomposition efficiency and unravelling of fragmentation pathways for anionic adducts of brevetoxins in negative ion electrospray mass spectrometry. Anal. Chem. 2009, 81, 8826–8838. [Google Scholar] [CrossRef] [PubMed]
- Dickey, R.W.; Plakas, S.M.; Jester, E.L.E.; El Said, K.R.; Johannessen, J.N.; Flewelling, L.J.; Scott, P.; Hammond, D.G.; van Dolah, F.M.; Leighfield, T.A.; et al. Multi-laboratory study of five methods for the determination of brevetoxins in shellfish tissue extracts. In Harmful Algae 2002; Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO; Steidinger, K.A., Landsberg, J.H., Thomas, C.R., Vargo, G.A., Eds.; UNESCO: St. Petersburg, FL, USA, 2004; pp. 300–302. [Google Scholar]
- Mead, R.N.; Probst, E.E.; Helms, J.R.G.; Brooks Avery, G.; Kieber, R.J.; Skrabal, S.A. Enhanced detection of the algal toxin PbTx-2 in marine waters by atmospheric pressure chemical ionization mass spectrometry rapid commun. Mass Spectrom. 2014, 28, 2455–2460. [Google Scholar]
- Selwood, A.I.; van Ginkel, R.; Wilkins, A.L.; Munday, R.; Ramsdell, J.S.; Jensen, D.J.; Cooney, J.M.; Miles, C.O. Semisynthesis of S-desoxybrevetoxin-B2 and brevetoxin-B2, and assessment of their acute toxicities. Chem. Res. Toxicol. 2008, 21, 944–950. [Google Scholar] [CrossRef] [PubMed]
- Selwood, A.I.; Cawthron Institute, Nelson, New Zealand. Personal Communication, 2013.
- McNabb, P. OVerview of ten years experience using LCMS for biotoxin monitoring. In Proceedings of the Marine and Freshwater Toxin Symposium, Baiona, Spain, May 2011.
- McNabb, P.; Selwood, A.I.; van Ginkel, R.; Boundy, M.; Holland, P.T. Determination of brevetoxins in shellfish by LC/MS/MS: Single laboratory validation. J. AOAC Int. 2012, 95, 1097–1105. [Google Scholar] [CrossRef] [PubMed]
- Harwood, D.T. Karenia brevisulcata toxins: A threat to New Zealand aquaculture? In Proceedings of the International Conference on Harmful Algae, Wellington, New Zealand, October 2014.
- Bottein Dechraoui, M-Y.; Tiedeken, J.A.; Persad, R.; Wang, Z.; Granade, H.R.; Dickey, R.W.; Ramsdell, J.S. Use of two detection methods to discriminate ciguatoxins from brevetoxins: Application to great barracuda from Florida Keys. Toxicon 2005, 46, 261–270. [Google Scholar] [CrossRef] [PubMed]
- Manger, R.L.; Leja, L.S.; Lee, S.Y.; Hungerford, J.M.; Wekell, M.M. Tetrazolium-based cell bioassay for neurotoxins active on voltage-sensitive sodium channels: Semiautomated assay for saxitoxins, brevetoxins, and ciguatoxins. Anal. Biochem. 1993, 214, 190–194. [Google Scholar]
- Murata, K.; Satake, M.; Naoki, H.; Kaspar, H.F.; Yasumoto, T. Isolation and structure of a new brevetoxin analog, brevetoxin B2, from greenshell mussels from New Zealand. Tetrahedron 1998, 54, 735–742. [Google Scholar] [CrossRef]
- Campas, M.; Prieto-Simon, B.; Marty, J.-L. Biosensors to detect marine toxins: Assessing seafood safety. Talanta 2007, 72, 884–895. [Google Scholar] [CrossRef] [PubMed]
- Bottein Dechraoui, M.-Y.; Maucher Fuquay, J.; Munday, R.; Selwood, A.I.; van Ginkel, R.; Miles, C.O.; Loader, J.I.; Wilkins, A.L.; Ramsdell, J.S. Bioassay methods for detection of N-palmitoylbrevetoxin-B2 (BTX-B4). Toxicon 2010, 55, 497–506. [Google Scholar] [CrossRef] [PubMed]
- Manger, R.; Woodle, D.; Berger, A.; Dickey, R.W.; Jester, E.; Yasumoto, T.; Lewis, R.; Hawryluk, T.; Hungerford, J. Flow cytometric-membrane potential detection of sodium channel active marine toxins: Application to ciguatoxins in fish muscle and feasibility of automating saxitoxin detection. J. AOAC Int. 2014, 97, 229–306. [Google Scholar]
- McCall, J.R.; Elliott, E.A.; Bourdelais, A.J. A new cytotoxicity assay for brevetoxins using fluorescence microscopy. Mar. Drugs 2014, 12, 4868–4882. [Google Scholar] [CrossRef] [PubMed]
- Trainer, V.L.; Poli, M.A. Assays for dinoflagellate toxins, specifically brevetoxin, ciguatoxin and saxitoxin. In Animal Toxins: Facts and Protocols; Rochat, H., Marin-Eauclaire, M.F., Eds.; Birkhauser Verlag: Basel, Switzerland, 2000; pp. 1–19. [Google Scholar]
- Bottein Dechraoui, M.-Y.; Wang, Z.; Ramsdell, J.S. Intrinsic potency of synthetically prepared brevetoxin cysteine metabolites BTX-B2 and desocyBTX-B2. Toxicon 2007, 50, 825–834. [Google Scholar] [CrossRef] [PubMed]
- AOAC Official Method 2011.27 Paralytic Shellfish Toxins (PSTs) in Shellfish. Receptor Binding Assay. First Action 2011; AOAC International: Gaithersburg, MD, USA, 2011.
- Whitney, P.L.; Delgado, J.A.; Baden, D.G. Complex behaviour of marine animal tissue extracts in the competitive binding assay of brevetoxins with rat brain synaptosomes. Nat. Toxins 1997, 5, 193–200. [Google Scholar] [CrossRef] [PubMed]
- Van Dolah, F.M.; Finley, E.L.; Haynes, G.J.; Doucette, G.J.; Moeller, P.D.; Ramsdell, J.S. Development of rapid and sensitive high throughput pharmacologic assays for marine phycotoxins. Nat. Toxins 1994, 2, 189–196. [Google Scholar] [CrossRef] [PubMed]
- McCall, J.R.; Jacocks, H.M.; Baden, D.G.; Bourdelais, A.J. Development of a competitive fluorescence-based synaptosomes binding assay for brevetoxins. Harmful Algae 2012, 19, 85–91. [Google Scholar] [CrossRef] [PubMed]
- McCall, J.R.; Jacocks, H.M.; Niven, S.C.; Poli, M.A.; Baden, D.G.; Bourdelais, A.J. Development and utilization of a competitive fluorescence-based receptor binding assay for site 5 voltage gated sodium channel ligands brevetoxin and ciguatoxin. J. AOAC Int. 2014, 97, 307–315. [Google Scholar] [CrossRef] [PubMed]
- Trainer, V.L.; Baden, D.G. An enzyme immunoassay for the detection of Florida red tide brevetoxins. Toxicon 1991, 29, 1387–1394. [Google Scholar] [CrossRef] [PubMed]
- Poli, M.A.; Hewetson, J.F. Antibody production and development of a radioimmunoassay for the PbTx-2 type brevetoxins. In Ciguatera: Proceedings of the Third International Conference on Ciguatera; Tosteson, T.R., Ed.; Polyscience Publications: Morin Heights, QC, Canada, 1992; pp. 115–127. [Google Scholar]
- Poli, M.A. Detection of brevetoxins in the twenty-first century. In Seafood and Freshwater Toxins: Pharmacology, Physiology and Detection, 2nd ed.; Botana, L.M., Ed.; CRC Press: Boca Raton, FL, USA, 2008; pp. 551–558. [Google Scholar]
- Campbell, K.; Vilarino, N.; Botana, L.M.; Elliot, C.T. A European perspective on progress in moving away from the mouse bioassay for marine-toxin analysis. Trends Anal. Chem. 2011, 30, 239–253. [Google Scholar] [CrossRef]
- Naar, J.; Bourdelais, A.; Tomas, C.; Kubanek, J.; Whitney, P.L.; Flewelling, L.; Steidinger, K.; Lancaster, J.; Baden, D.G. A competitive ELISA to detect brevetoxins from Karenia brevis (formerly Gymnodinium breve) in seawater, shellfish and mammalian body fluid. Environ. Health Perspect. 2002, 110, 179–185. [Google Scholar] [CrossRef] [PubMed]
- Maucher, J.M.; Briggs, L.R.; Podmore, C.; Ramsdell, J.S. Optimisation of blood collection card method/ELISA for monitoring exposure of bottlenose dolphin to brevetoxin-producing red tides. Environ. Sci. Technol. 2007, 41, 563–567. [Google Scholar] [CrossRef] [PubMed]
- ISSC. Interstate Shellfish Sanitation Conference. In Proceedings of the Summary of Action 2009 Biennial Meeting, Manchester, NH, USA, 17–23 October 2009.
- Abraham, A.; FDA, Dauphin Island, AL, USA. Personal communication, 2013.
- Rubio, F.; Abraxis, Warminster, PA, USA. Personal communication, 2013.
- Mouri, R.; Oishi, T.; Torikai, K.; Ujihara, S.; Matsumori, N.; Murata, M.; Oshima, Y. Surface plasmon resonance-based detection of ladder-shaped polyethers by inhibition detection method. Bioorg. Med. Chem. Lett. 2009, 19, 2824–2828. [Google Scholar] [CrossRef] [PubMed]
- Vilarino, N.; Fonfria, E.S.; Carmen Louzao, M.; Botana, L.M. Use of biosensors as alternatives to current regulatory methods for marine biotoxins. Sensors 2009, 9, 9414–9443. [Google Scholar] [CrossRef] [PubMed]
- Kreuzer, M.P.; Pravada, M.; O’Sullivan, C.K.; Guilbault, G.G. Novel electrochemical immunosensors for seafood toxin analysis. Toxicon 2002, 40, 1267–1274. [Google Scholar] [CrossRef] [PubMed]
- Kulagina, N.V.; Mikulski, C.M.; Gray, S.; Ma, W.; Doucette, G.J.; Ramsdell, J.S.; Pancrazio, J.J. Detection of marine toxins, brevetoxin-3 and saxitoxin, in seawater using neuronal networks. Environ. Sci. Technol. 2006, 40, 578–583. [Google Scholar] [CrossRef] [PubMed]
- Leao-Martins, J. Solid phase immunoaffinity extraction prior to LCMS of Brevetoxins. In Proceedings of the Marine and Freshwater Toxin Symposium, Baiona, Spain, May 2011.
- Plakas, S.; FDA, Dauphin Island, AL, USA. Personal Communication, 2013.
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Turner, A.D.; Higgins, C.; Davidson, K.; Veszelovszki, A.; Payne, D.; Hungerford, J.; Higman, W. Potential Threats Posed by New or Emerging Marine Biotoxins in UK Waters and Examination of Detection Methodology Used in Their Control: Brevetoxins. Mar. Drugs 2015, 13, 1224-1254. https://doi.org/10.3390/md13031224
Turner AD, Higgins C, Davidson K, Veszelovszki A, Payne D, Hungerford J, Higman W. Potential Threats Posed by New or Emerging Marine Biotoxins in UK Waters and Examination of Detection Methodology Used in Their Control: Brevetoxins. Marine Drugs. 2015; 13(3):1224-1254. https://doi.org/10.3390/md13031224
Chicago/Turabian StyleTurner, Andrew D., Cowan Higgins, Keith Davidson, Andrea Veszelovszki, Daniel Payne, James Hungerford, and Wendy Higman. 2015. "Potential Threats Posed by New or Emerging Marine Biotoxins in UK Waters and Examination of Detection Methodology Used in Their Control: Brevetoxins" Marine Drugs 13, no. 3: 1224-1254. https://doi.org/10.3390/md13031224
APA StyleTurner, A. D., Higgins, C., Davidson, K., Veszelovszki, A., Payne, D., Hungerford, J., & Higman, W. (2015). Potential Threats Posed by New or Emerging Marine Biotoxins in UK Waters and Examination of Detection Methodology Used in Their Control: Brevetoxins. Marine Drugs, 13(3), 1224-1254. https://doi.org/10.3390/md13031224