Confirmation of pinnatoxins and spirolides in shellfish and passive samplers from Catalonia (Spain) by liquid chromatography coupled with triple quadrupole and high-resolution hybrid tandem mass spectrometry

Marine Drugs

Volumn 12, Issue 6, 2014, Pages 3706-3732

  García Altares, María ^a   Casanova, Alexis ^a   Bane, Vaishali ^b   Diogeǹe, Jorge ^a   Furey, Ambrose ^b   De La Iglesia, Pablo ^a  

^a Marine and Continental Waters Program   (Spain)

^b Munster Technological University   (Ireland)

Author keywords

High resolution mass spectrometry; Mediterranean sea; Orbitrap FT MS; Pinnatoxins; Spirolides; Triple quadrupole mass spectrometry

Indexed keywords

13 DESMETHYL SPIROLIDE; PINNATOXIN DERIVATIVE; PINNATOXIN G; SHELLFISH TOXIN; SPIROLIDE DERIVATIVE; UNCLASSIFIED DRUG; ALKALOID; IMINE; SPIRO COMPOUND; SPIROLIDE I;

ANALYTICAL EQUIPMENT; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETER; MEDITERRANEAN SEA; MUSSEL; NONHUMAN; OPTICAL RESOLUTION; OYSTER; QUADRUPOLE MASS SPECTROMETRY; REACTION TIME; SAMPLER; SCREENING TEST; SOLID PHASE ADSORPTION TOXIN TRACKING DEVICE; SPAIN; TANDEM MASS SPECTROMETRY; TOXIN ANALYSIS; TOXIN STRUCTURE; ANIMAL; BIVALVE; ISOLATION AND PURIFICATION; METABOLISM; PROCEDURES; REPRODUCIBILITY; SHELLFISH; STANDARD; VALIDATION STUDY;

ALKALOIDS; ANIMALS; BIVALVIA; CHROMATOGRAPHY, LIQUID; IMINES; MEDITERRANEAN SEA; OSTREIDAE; REFERENCE STANDARDS; REPRODUCIBILITY OF RESULTS; SHELLFISH; SPAIN; SPIRO COMPOUNDS; TANDEM MASS SPECTROMETRY;

EID: 84903535585     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12063706     Document Type: Article

References (74)

1. Guéret, S.; Brimble, M. Spiroimine shellfish poisoning (SSP) and the spirolide family of shellfish toxins: Isolation, structure, biological activity and synthesis. Nat. Prod. Rep. 2010, 27, 1350-1366.
2. Otero, A.; Chapela, M.-J.; Atanassova, M.; Vieites, J.M.; Cabado, A.G. Cyclic imines: Chemistry and mechanism of action: A review. Chem. Res. Toxicol. 2011, 24, 1817-1829.
3. Kita, M.; Ohishi, N.; Washida, K.; Kondo, M.; Koyama, T.; Yamada, K.; Uemura, D. Symbioimine and neosymbioimine, amphoteric iminium metabolites from the symbiotic marine dinoflagellate Symbiodinium sp. Bioorg. Med. Chem. 2005, 13, 5253-5258. (Pubitemid 41039986)
4. Selwood, A.I.; Wilkins, A.L.; Munday, R.; Shi, F.; Rhodes, L.L.; Holland, P.T. Portimine: A bioactive metabolite from the benthic dinoflagellate Vulcanodinium rugosum. Tetrahedron Lett. 2013, 54, 4705-4707.
5. Duroure, L.; Jousseaume, T.; Aráoz, R.; Barré, E.; Retailleau, P.; Chabaud, L.; Molgó, J.; Guillou, C. 6,6-Spiroimine analogs of (-)-gymnodimine A: Synthesis and biological evaluation on nicotinic acetylcholine receptors. Org. Biomol. Chem. 2011, 9, 8112-8118.
6. Hu, T.; Curtis, J.M.; Oshima, Y.; Quilliam, M.A.; Walter, J.A.; Watson-Wright, W.M.; Wright, J.L.C. Spirolides B and D, two novel macrocycles isolated from the digestive glands of shellfish. J. Chem. Soc. Chem. Commun. 1995, doi:10.1039/C39950002159.
7. Hu, T.; Burton, I.; Cembella, A.; Curtis, J.; Quilliam, M.; Walter, J.; Wright, J.; Walker, J. Characterization of spirolides a, c, and 13-desmethyl c, new marine toxins isolated from toxic plankton and contaminated shellfish. J. Nat. Prod. 2001, 64, 308-312.
8. Sleno, L.; Windust, A.J.; Volmer, D.A. Structural study of spirolide marine toxins by mass spectrometry: Part I. Fragmentation pathways of 13-desmethyl spirolide C by collision-induced dissociation and infrared multiphoton dissociation mass spectrometry. Anal. Bioanal. Chem. 2004, 378, 969-976. (Pubitemid 40890209)
9. Hu, T.; Curtis, J.; Walter, J.; Wright, J.; Walker, J. Characterization of biologically inactive spirolides E and F: Identification of the spirolide pharmacophore. Tetrahedron Lett. 1996, 37, 7671-7674.
10. MacKinnon, S.; Walter, J.; Quilliam, M.; Cembella, A.; LeBlanc, P.; Burton, I.; Hardstaff, W.; Lewis, N. Spirolides Isolated from Danish Strains of the Toxigenic Dinoflagellate Alexandrium ostenfeldii. J. Nat. Prod. 2006, 69, 8-12.
11. Roach, J.S.; LeBlanc, P.; Lewis, N.I.; Munday, R.; Quilliam, M.A.; MacKinnon, S.L. Characterization of a dispiroketal spirolide subclass from Alexandrium ostenfeldii. J. Nat. Prod. 2009, 72, 1237-1240.
12. Ciminiello, P.; Dell'Aversano, C.; Fattorusso, E.; Forino, M.; Grauso, L.; Tartaglione, L.; Guerrini, F.; Pistocchi, R. Spirolide toxin profile of adriatic Alexandrium ostenfeldii cultures and structure elucidation of 27-hydroxy-13,19-didesmethyl spirolide C. J. Nat. Prod. 2007, 70, 1878-1883.
13. Sleno, L.; Chalmers, M.; Chamorro, M.; Windust, A. Structural study of spirolide marine toxins by mass spectrometry. Part II. Mass spectrometric characterization of unknown spirolides and related compounds in a cultured phytoplankton extract. Anal. Bioanal. Chem. 2004, 378, 977-986.
14. Ciminiello, P.; Dell'aversano, C.; Iacovo, E.D.; Fattorusso, E.; Forino, M.; Grauso, L.; Tartaglione, L.; Guerrini, F.; Pezzolesi, L.; Pistocchi, R. Characterization of 27-hydroxy-13-desmethyl spirolide C and 27-oxo-13,19- didesmethyl spirolide C. Further insights into the complex Adriatic Alexandrium ostenfeldii toxin profile. Toxicon 2010, 56, 1327-1333.
15. Aasen, J.; Hardstaff, W.; Aune, T.; Quilliam, M.A. Discovery of fatty acid ester metabolites of spirolide toxins in mussels from Norway using liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2006, 20, 1531-1537.
16. Rundberget, T.; Aasen, J.; Selwood, A.; Miles, C. Pinnatoxins and spirolides in Norwegian blue mussels and seawater. Toxicon 2011, 58, 700-711.
17. Selwood, A.; Miles, C.; Wilkins, A.; van Ginkel, R.; Munday, R.; Rise, F.; McNabb, P. Isolation, structural determination and acute toxicity of pinnatoxins E, F and G. J. Agric. Food Chem. 2010, 58, 6532-6542.
18. McCarron, P.; Rourke, W.; Hardstaff, W.; Pooley, B.; Quilliam, M. Identification of pinnatoxins and discovery of their fatty acid ester metabolites in mussels (Mytilus edulis) from eastern Canada. J. Agric. Food Chem. 2012, 60, 1437-1446.
19. Uemura, D.; Chou, T.; Haino, T.; Nagatsu, A.; Fukuzawa, S.; Zheng, S.-Z.; Chen, H.-S. Pinnatoxin A: A toxic amphoteric macrocycle from the Okinawan bivalve Pinna muricata. J. Chem. Soc. 1995, 117, 1155-1156.
20. Takada, N.; Umemura, N.; Suenaga, K.; Chou, T.; Nagatsu, A.; Haino, T.; Yamada, K.; Uemura, D. Pinnatoxins B and C, the most toxic components in the pinnatoxin series from the Okinawan bivalve Pinna muricata. Tetrahedron Lett. 2001, 42, 3491-3494. (Pubitemid 32385746)
21. Hellyer, S.; Selwood, A.; Rhodes, L.; Kerr, S. Marine algal pinnatoxins E and F cause neuromuscular block in an in vitro hemidiaphragm preparation. Toxicon 2011, 58, 693-699.
22. Bourne, Y.; Radic, Z.; Aráoz, R.; Talley, T.T.; Benoit, E.; Servent, D.; Taylor, P.; Molgó, J.; Marchot, P.; Radiæ, Z. Structural determinants in phycotoxins and AChBP conferring high affinity binding and nicotinic AChR antagonism. Proc. Natl. Acad. Sci. USA 2010, 107, 6076-6081.
23. Hauser, T.A.; Hepler, C.D.; Kombo, D.C.; Grinevich, V.P.; Kiser, M.N.; Hooker, D.N.; Zhang, J.; Mountfort, D.; Selwood, A.; Akireddy, S.R.; et al. Comparison of acetylcholine receptor interactions of the marine toxins, 13-desmethylspirolide C and gymnodimine. Neuropharmacology 2012, 62, 2238-2249.
24. Marrouchi, R.; Rome, G.; Kharrat, R.; Molgò, J.; Benoit, E. Analysis of the action of gymnodimine-A and 13-desmethyl spirolide C on the mouse neuromuscular system in vivo . Toxicon 2013, 75, 27-34.
25. Rhodes, L.; Smith, K.; Selwood, A.; McNabb, P.; Munday, R.; Molenaar, S. Dinoflagellate Vulcanodinium rugosum identified as the causative organism of pinnatoxins in Australia, New Zealand and Japan. Phycologia 2011, 50, 624-628.
26. Haywood, A.; 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. (Pubitemid 38241648)
27. Kremp, A.; Tahvanainen, P.; Litaker, W.; Krock, B.; Suikkanen, S.; Leaw, C.P.; Tomas, C. Phylogenetic relationships, morphological variation, and toxin patterns in the Alexandrium ostenfeldii (Dinophyceae) complex: Implications for species boundaries and identities. J. Phycol. 2014, 50, 81-100.
28. Cembella, A.; Lewis, N.; Quilliam, M. The marine dinoflagellate Alexandrium ostenfeldii (Dinophyceae) as the causative organism of spirolide shellfish toxins. Phycologia 2000, 39, 67-74. (Pubitemid 30121488)
29. Touzet, N.; Franco, J.M.; Raine, R. Morphogenetic diversity and biotoxin composition of Alexandrium (Dinophyceae) in Irish coastal waters. Harmful Algae 2008, 7, 782-797.
30. Tomas, C.; van Wagoner, R.; Tatters, A.; White, K.; Hall, S.; Wright, J. Alexandrium peruvianum (Balech and Mendiola) Balech and Tangen a new toxic species for coastal North Carolina. Harmful Algae 2012, 17, 54-63.
31. Van Wagoner, R.M.; Misner, I.; Tomas, C.R.; Wright, J.L.C. Occurrence of 12-methylgymnodimine in a spirolide-producing dinoflagellate Alexandrium peruvianum and the biogenetic implications. Tetrahedron Lett. 2011, 52, 4243-4246.
32. Zheng, S.; Huang, F.; Chen, S.; Tan, X.; Zuo, J.; Peng, J.; Xie, R. The isolation and bioactivities of pinnatoxin. Chin. J. Mar. Drugs 1990, 33, 33-35.
33. Rhodes, L.; Smith, K.; Selwood, A.; McNabb, P.; Molenaar, S.; Munday, R.R.; Wilkinson, C.; Hallegraeff, G. Production of pinnatoxins E, F and G by scrippsielloid dinoflagellates isolated from Franklin Harbour, South Australia. N. Z. J. Mar. Freshw. Res. 2011, 45, 703-709.
34. Hess, P.; Abadie, E.; Hervè, F.; Berteaux, T.; Séchet, V.; Aráoz, R.; Molgó, J.; Zakarian, A.; Sibat, M.; Rundberget, T.; et al . Pinnatoxin G is responsible for atypical toxicity in mussels (Mytilus galloprovincialis) and clams (Venerupis decussata) from Ingril, a French Mediterranean lagoon. Toxicon 2013, 75, 16-26.
35. Álvarez, G.; Uribe, E.; Ávalos, P.; Mariño, C.; Blanco, J.; Alvarez, G.; Avalos, P. First identification of azaspiracid and spirolides in Mesodesma donacium and Mulinia edulis from Northern Chile. Toxicon 2010, 55, 638-641.
36. Amzil, Z.; Sibat, M.; Royer, F.; Masson, N.; Abadie, E. Report on the first detection of pectenotoxin-2, spirolide-a and their derivatives in French shellfish. Mar. Drugs 2007, 5, 168-179.
37. Ciminiello, P.; Dell'Aversano, C.; Fattorusso, E.; Magno, S.; Tartaglione, L.; Cangini, M.; Pompei, M.; Guerrini, F.; Boni, L.; Pistocchi, R. Toxin profile of Alexandrium ostenfeldii (Dinophyceae) from the Northern Adriatic Sea revealed by liquid chromatography-mass spectrometry. Toxicon 2006, 47, 597-604.
38. Gribble, K.; Keafer, B.; Quilliam, M.; Cembella, A.; Kulis, D.; Manahan, A.; Anderson, D. Distribution and toxicity of Alexandrium ostenfeldii (Dinophyceae) in the Gulf of Maine, USA. Deep Sea Res. Part II 2005, 52, 2745-2763. (Pubitemid 41659369)
39. MacKinnon, S.; Cembella, A.; Burton, I.; Lewis, N.; LeBlanc, P.; Walter, J. Biosynthesis of 13-desmethyl spirolide C by the dinoflagellate Alexandrium ostenfeldii. J. Org. Chem. 2006, 71, 8724-8731. (Pubitemid 44721942)
40. Villar-González, A.; Rodríguez-Velasco, M.L.; Ben-Gigirey, B.; Botana, L.M.; González, A.V.; Villar González, A. First evidence of spirolides in Spanish shellfish. Toxicon 2006, 48, 1068-1074.
41. Biré, R.; Krys, S.; Frémy, J.-M.; Dragacci, S.; Stirling, D.; Kharrat, R. First evidence on occurrence of gymnodimine in clams from Tunisia. J. Nat. Toxins 2002, 11, 269-275. (Pubitemid 36029231)
42. Ciminiello, P.; Dell'Aversano, C.; Fattorusso, E.; Forino, M.; Tartaglione, L.; Boschetti, L.; Rubini, S.; Cangini, M.; Pigozzi, S.; Poletti, R. Complex toxin profile of Mytilus galloprovincialis from the Adriatic sea revealed by LC-MS. Toxicon 2010, 55, 280-288.
43. Satta, C.T.; Anglès, S.; Lugliè, A.; Guillén, J.; Sechi, N.; Camp, J.; Garcés, E. Studies on dinoflagellate cyst assemblages in two estuarine Mediterranean bays: A useful tool for the discovery and mapping of harmful algal species. Harmful Algae 2013, 24, 65-79.
44. European Food Safety Authority (EFSA), Panel on Contaminants in the Food Chain (CONTAM). Scientific Opinion on marine biotoxins in shellfish-Cyclic imines (spirolides, gymnodimines, pinnatoxins and pteriatoxins). EFSA J. 2010, 8, 1628-1667.
45. Perry, R.H.; Cooks, R.G.; Noll, R.J. Orbitrap Mass Spectrometry: Instrumentation, ion motion and applications. Mass Spectrom. Rev. 2008, 27, 661-699.
46. Makarov, A.; Denisov, E.; Lange, O. Dynamic Range of Mass Accuracy in LTQ Orbitrap Hybrid Mass Spectrometer. J. Am. Soc. Mass Spectrom. 2006, 17, 3-8.
47. Gerssen, A.; Mulder, P.P.J.; de Boer, J. Screening of lipophilic marine toxins in shellfish and algae: Development of a library using liquid chromatography coupled to Orbitrap mass spectrometry. Anal. Chim. Acta 2011, 685, 176-185.
48. Blay, P.; Hui, J.P.M.; Chang, J.; Melanson, J.E. Screening for multiple classes of marine biotoxins by liquid chromatography-high-resolution mass spectrometry. Anal. Bioanal. Chem. 2011, 400, 577-585.
49. Domènech, A.; Cortés-Francisco, N.; Palacios, O.; Franco, J.M.; Riobó, P.; Llerena, J.J.; Vichi, S.; Caixach, J. Determination of lipophilic marine toxins in mussels. Quantification and confirmation criteria using high resolution mass spectrometry. J. Chromatogr. A 2014, 1328, 16-25.
50. Kaufmann, A.; Walker, S. Evaluation of the interrelationship between mass resolving power and mass error tolerances for targeted bioanalysis using liquid chromatography coupled to high-resolution mass spectrometry. Rapid Commun. Mass Spectrom. 2012, 27, 347-356.
51. Van der Heeft, E.; Bolck, Y.J.C.; Beumer, B.; Nijrolder, A.W.J.M.; Stolker, A.A.M.; Nielen, M.W.F. Full-Scan Accurate Mass Selectivity of Ultra-Performance Liquid Chromatography Combined with Time-of-Flight and Orbitrap Mass Spectrometry in Hormone and Veterinary Drug Residue Analysis. J. Am. Soc. Mass Spectrom. 2009, 20, 451-463.
52. Kaufmann, A.; Walker, S. Post-run target screening strategy for ultra high performance liquid chromatography coupled to Orbitrap based veterinary drug residue analysis in animal urine. J. Chromatogr. A 2013, 1292, 104-110.
53. Kaufmann, A.; Walker, S. Accuracy of relative isotopic abundance and mass measurements in a single-stage orbitrap mass spectrometer. Rapid Commun. Mass Spectrom. 2012, 26, 1081-1090.
54. Xu, Y.; Heilier, J.F.; Madalinski, G.; Genin, E.; Ezan, E.; Tabet, J.C.; Junot, C. Evaluation of accurate mass and relative isotopic abundance measurements in the LTQ-Orbitrap mass spectrometer for further metabolomics database building. Anal. Chem. 2010, 82, 5490-5501.
55. De la Iglesia, P.; McCarron, P.; Diogène, J.; Quilliam, M.A. Discovery of gymnodimine fatty acid ester metabolites in shellfish using liquid chromatography/mass spectrometry. Rapid Commun. Mass Spectrom. 2013, 27, 643-653.
56. European Commission. 2002/657/EC: Commission Decision of 12 August 2002 implementing Council Directive 96/23/EC concerning the performance of analytical methods and the interpretation of results. Off. J. Eur. Union. 2002, L221, 8-36.
57. Stolker, A.A.M.; Linders, S.H.M.A.; van Ginkel, L.A.; Brinkman, U.A.T. Application of the revised EU criteria for the confirmation of anabolic steroids in meat using GC-MS. Anal. Bioanal. Chem. 2004, 378, 1313-1321. (Pubitemid 40877729)
58. García-Altares, M.; Diogène, J.; de la Iglesia, P. The implementation of liquid chromatography tandem mass spectrometry for the official control of lipophilic toxins in seafood: Single-laboratory validation under four chromatographic conditions. J. Chromatogr. A 2013, 1275, 48-60.
59. De Zeeuw, R. Substance identification: The weak link in analytical toxicology. J. Chromatogr. B 2004, 811, 3-12. (Pubitemid 39348842)
60. Lehotay, S.; Mastovska, K.; Amirav, A.; Fialkov, A.; Martos, P.; Kok, A.; Fernández-Alba, A. Identification and confirmation of chemical residues in food by chromatography-mass spectrometry and other techniques. TrAC Trends Anal. Chem. 2008, 27, 1070-1090.
61. Mol, H.; Zomer, P.; De Koning, M. Qualitative aspects and validation of a screening method for pesticides in vegetables and fruits based on liquid chromatography coupled to full scan high resolution (Orbitrap) mass spectrometry. Anal. Bioanal. Chem. 2012, 403, 2891-2908.
62. Nielen, M.W.F.; van Engelen, M.C.; Zuiderent, R.; Ramaker, R. Screening and confirmation criteria for hormone residue analysis using liquid chromatography accurate mass time-of-flight, Fourier transform ion cyclotron resonance and orbitrap mass spectrometry techniques. Anal. Chim. Acta 2007, 586, 122-129.
63. Gerssen, A.; Mulder, P.; McElhinney, M.A.; de Boer, J. Liquid chromatography-tandem mass spectrometry method for the detection of marine lipophilic toxins under alkaline conditions. J. Chromatogr. A 2009, 1216, 1421-1430.
64. Community Reference Laboratory on Marine Biotoxins. In Interlaboratory Validation Study of the EU-Harmonised SOP-LIPO-LC-MS/MS; EURLMB: Vigo, Spain, 2011; Version 4.
65. Mountfort, D.O.; Suzuki, T.; Truman, P. Protein phosphatase inhibition assay adapted for determination of total DSP in contaminated mussels. Toxicon 2000, 39, 383-390. (Pubitemid 30649087)
66. MacKenzie, L.A. In situ passive solid-phase adsorption of micro-algal biotoxins as a monitoring tool. Curr. Opin. Biotechnol. 2002, 21, 326-331.
67. Caillaud, A.; de la Iglesia, P.; Barber, E.; Eixarch, H.; Mohammad-Noor, N.; Yasumoto, T.; Diogène, J. Monitoring of dissolved ciguatoxin and maitotoxin using solid-phase adsorption toxin tracking devices: Application to Gambierdiscus pacificus in culture. Harmful Algae 2011, 10, 433-446.
68. Gerssen, A.; van Olst, E.; Mulder, P.; de Boer, J. In-house validation of a liquid chromatography tandem mass spectrometry method for the analysis of lipophilic marine toxins in shellfish using matrix-matched calibration. Anal. Bioanal. Chem. 2010, 397, 3079-3088.
69. Tran, J.C.; Doucette, A.A. Cyclic Polyamide Oligomers Extracted from Nylon 66 Membrane Filter Disks as a Source of Contamination in Liquid Chromatography/Mass Spectrometry. J. Am. Soc. Mass Spectrom. 2006, 17, 652-656.
70. Keller, B.O.; Sui, J.; Young, A.B.; Whittal, R.M. Interferences and contaminants encountered in modern mass spectrometry. Anal. Chim. Acta 2008, 627, 71-81.
71. Taverniers, I.; de Loose, M.; van Bockstaele, E. Trends in quality in the analytical laboratory. II. Analytical method validation and quality assurance. TrAC Trends Anal. Chem. 2004, 23, 535-552.
72. IUPAC Compendium of Chemical Terminology. In The Gold Book, 2nd ed.; McNaught, A.D., Wilkinson, A., Eds.; Blackwell Scientific Publications: Oxford, UK, 1997.
73. Fassel, V.A. International Union of Pure and Applied Chemistry. Analytical Chemistry Division. Commission on Spectrochemical and Other Optical Procedures for Analysis. Nomenclature, symbols, units and their usage in spectrochemical analysis. II. Data interpretation. (Rules approved 1975). Anal. Chem. 1976, 48, 2294.
74. Corley, J. Best practices in establishing detection and quantification limits for pesticide residues in foods. In Handbook of Residue Analytical Methods for Agrochemicals; Lee, P.W., Aizawa, H., Barefoot, A.C., Murphy, J.J., Eds.; Wiley & Sons: New York, NY, USA, 2003.