Analytical and Bioanalytical Chemistry

, Volume 391, Issue 1, pp 117–134

Determination of marine biotoxins relevant for regulations: from the mouse bioassay to coupled LC-MS methods

Review

Abstract

The frequency of occurrence and intensity of harmful algal blooms (HABs) appear to be increasing on a global scale. Consequently, methods were established for the evaluation of possible hazards caused by the enrichment of algal toxins in the marine food chain. Different clinical types of algae-related poisoning have attracted scientific attention: paralytic shellfish poisoning (PSP), diarrhetic shellfish poisoning (DSP), and amnesic shellfish poisoning (ASP). In several countries fish specialties are consumed which may be contaminated with algal toxins typical for the respective region (e.g., ciguatera and tetrodotoxins). Bioassays are common methods for the determination of marine biotoxins. However, biological tests are not completely satisfactory, due to the low sensitivity and the absence of specialized variations. Moreover, there is growing resistance against the use of animal experiments. Therefore, many efforts have been made to determine algal toxins with chemical methods. In this context LC-MS methods replaced HPLC methods with optical detectors, allowing both effective seafood control and monitoring of phytoplankton in terms of the different groups of marine biotoxins.

Keywords

Marine biotoxins LC-MS/MS PSP toxins DSP toxins Domoic acid Tetrodotoxins Ciguatera 

References

  1. 1.
    Fernandez ML, Richard DJA, Cembella AD (2003) In vivo assays for phycotoxins. In: Hallegraeff G, Anderson DM, Cembella AD (eds) Manual on harmful marine microalgae. Intergovernmental Oceanographic Commission of UNESCO, Paris, ISBN 92-3-103871-0, p 349Google Scholar
  2. 2.
    Schantz EJ (1986) Chemistry and biology of saxitoxin and related toxins. Ann N Y Acad Sci 47:15–23Google Scholar
  3. 3.
    Luckas B, Hummert C, Oshima Y (2003) Analytical methods for paralytic shellfish poisons. In: Hallegraeff G, Anderson DM, Cembella AD (eds) Manual on harmful marine microalgae. Intergovernmental Oceanographic Commission of UNESCO, 7 Place de Fontenoy, 75352 Paris 07 SP, ISBN 92-3-103871-0, pp 191–209Google Scholar
  4. 4.
    Bates HA, Rapoport H (1975) A chemical assay for saxitoxin, the paralytic shellfish poison. J Agric Food Chem 23:237–239Google Scholar
  5. 5.
    Sullivan JJ, Wekell MM (1984) Determination of paralytic shellfish poisoning toxins by high pressure liquid chromatography. In: Ragelis EP (ed) Seafood toxins, ACS Symposium Series 262. American Chemical Society, Washington DC, pp 197–205Google Scholar
  6. 6.
    Luckas B (2000) Chemical analysis of PSP toxins. In: Botana LM (ed) Seafood and freshwater toxins: pharmacology, physiology and detection. Marcel Dekker, New York, ISBN 8247-8956-3, pp 173–186Google Scholar
  7. 7.
    Oshima Y, Sugino K, Yasumoto T (1989) Latest advances in HPLC analysis of paralytic shellfish toxins. In: Natori S, Hashimoto K, Ueno Y (eds) Mycotoxins and phycotoxins ′88. Elsevier, Amsterdam, pp 319–328Google Scholar
  8. 8.
    Diener M, Erler K, Hiller S, Christian B, Luckas B (2006) Determination of paralytic shellfish poisoning (PSP) toxins in dietary supplements by application of a new HPLC/FD method. Eur Food Res Technol 224:147–151Google Scholar
  9. 9.
    Jaime E, Hummert C, Hess P, Luckas B (2001) Ion-exchange separation of paralytic shellfish poisoning (PSP) toxins for high-performance liquid chromatography determination. J Chromatogr A 929:43–49Google Scholar
  10. 10.
    Quilliam MA (2003) The role of chromatography in the hunt for red tide toxins. J Chromatogr A 1000:527–548Google Scholar
  11. 11.
    Aversano CD, Hess P, Quilliam MA (2005) Hydrophilic interaction liquid chromatography-mass spectrometry for the analysis of paralytic shellfish poisoning (PSP) toxins. J Chromatogr A 1081:190–201Google Scholar
  12. 12.
    Diener M, Erler K, Christian B, Luckas B (2007) Application of a new zwitterionic hydrophilic interaction chromatography column for determination of paralytic shellfish poisoning toxins. J Sep Sci 30:1821–1826Google Scholar
  13. 13.
    Yasumoto T, Murata M (1985) Diarrhetic shellfish toxins. Tetrahedron 41:1019–1025Google Scholar
  14. 14.
    Quilliam MA (2003) Chemical methods for lipophilic shellfish toxins. In: Hallegraeff G, Anderson DM, Cembella AD (eds) Manual on harmful marine microalgae. Intergovernmental oceanographic commission of UNESCO, Paris, ISBN 92-3-103871-0, pp 211–245Google Scholar
  15. 15.
    Suzuki T, Ota H, Yamasaki M (1999) Direct evidence of transformation of dinophysistoxin-1 to 7-O-acyl-dinophysistoxin-1 (dinophysistoxin-3) in the scallop Patinopecten yessoensis. Toxicon 37:187–198Google Scholar
  16. 16.
    EC (2002) Commission decision 2002/225/EC of 15. March 2002 laying down detailed rules for the implementation of Council Directive 91/492/EEC as regards the maximum levels and the methods of analysis of certain marine biotoxins in bivalve molluscs, echinoderms, tunicates and marine gastropods. Off J Eur Comm L75:62–64Google Scholar
  17. 17.
    James KJ, Bishop AG, Carmody EP, Kelly SS (2000) Detection methods for okadaic acid and analogues. In: Botana LM (ed) Seafood and freshwater toxins: pharmacology, physiology and detection. Marcel Dekker, New York, ISBN 8247-8956-3, pp 217–238Google Scholar
  18. 18.
    Vale P, Sampayo MAM (2002) First confirmation of human diarrhoeic poisoning by okadaic esters after ingestion of razor clams (Solen marginatus) and green crabs (Carcinus maenas) in Aveiro lagoon, Portugal and detection of okadaic acid esters in phytoplankton. Toxicon 40:989–996Google Scholar
  19. 19.
    Suzuki T, Beuzenberg V, Mackenzie L, Quilliam MA (2004) Discovery of okadaic acid esters in the toxic dinoflagellate Dinophysis acuta from New Zealand using liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 18:1131–1138Google Scholar
  20. 20.
    Suzuki T, Beuzenberg V, Mackenzie L, Quilliam, MA (2003) Liquid chromatography-mass spectrometry of spiroketal stereoisomers of pectenotoxins and the analysis of novel pectenotoxins isomers in the toxic dinoflagellate Dinophysis acuta from New Zealand. J Chromatogr A 992:141–150Google Scholar
  21. 21.
    EC (2004) Regulation (EC) No. 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. Off J Eur Commun Annex III, Sect VII, Chap V, 2. L 226 pp 60–61Google Scholar
  22. 22.
    Miles CO, Wilkins AL, Samdal IA, Sandvik M, Petersen D, Quilliam MA, Naustvoll LJ, Rundberget T, Torgensen T, Hovgaard P, Jensen DJ, Cooney JM (2004) A novel pectenotoxin, PTX-12, in Dinophysis spp. and shellfish from Norway. Chem Res Toxicol 17:1423–1433Google Scholar
  23. 23.
    Miles CO, Wilkins AL, Munday R, Dines MH, Hawkes AD, Briggs LR, Sandvik M, Jensen DJ, Cooney JM, Holland PT, Quilliam MA, MacKenzie AL, Beuzenberg V, Towers NR (2004) Isolation of pectenotoxin-2 seco acid, and preliminary assessment of their acute toxicities. Toxicon 43:1–9Google Scholar
  24. 24.
    Suzuki T, Mackenzie L, Stirling D, Adamson J (2001) Pectenotoxin-2 seco acid: A toxin converted from pectenotoxin-2 by the New Zealand Greenshell mussel Perna canalicus. Toxicon 39:507–514Google Scholar
  25. 25.
    Miles CO, Wilkins AL, Hawkes AD, Jensen DJ, Selwood AI, Beuzenberg V, Mackenzie AL, Cooney JM, Holland PT (2006) Isolation and identification of pectenotoxins-13 and -14 from Dinophysis acuta in New Zealand. Toxicon 48:152–159Google Scholar
  26. 26.
    Wilkins AL, Rehmann N, Torgersen T, Rundberget T, Keogh M, Petersen D, Hess P, Rise F, Miles CO (2006) Identification of fatty acid esters of pectenotoxin-2 seco acid in blue mussels (Mytilus edulis) from Ireland. J Agric Food Chem 54:5672–5678Google Scholar
  27. 27.
    Miles CO, Wilkins AL, Hawkes AD, Selwood AI, Jensen DJ, Cooney JM, Beuzenberg V, MacKenzie AL (2006) Identification of 45-hydroxy-46,47-dinoryessotoxin, 44-oxo-45,46,47-trinoryessotoxin, and 9-methyl-42,43,45,46,47,55-heptanor-38-en-41-oxo-yessotoxin, and partial characterization of some minor yessotoxin, from Protoceratium reticulatum. Toxicon 47:229–240Google Scholar
  28. 28.
    Satake M, Eiki K, Ichimura T, Ota S, Sekiguchi K, Oshima Y (2006) Structure of 45,46,47-trinorhomoyessotoxin, a new yessotoxin analog, from Protoceratium reticulatum which represents the first detection of a homoyessotoxin analog in Japan. Harmful Algae 5:731–735Google Scholar
  29. 29.
    Cañás IR, Hamilton B, Amandi MF, Furey A, James KJ (2004) Nano liquid chromatography with hybrid quadrupole time-of-flight mass spectrometry for the determination of yessotoxin in marine phytoplankton. J Chromatogr A 1056:253–256Google Scholar
  30. 30.
    Suzuki T, Horie Y, Koike K, Satake M, Oshima Y, Iwataki M, Yoshimatsu S (2007) Yessotoxin analogues in several strains of Protoceratium reticulatum in Japan determined by liquid chromatography-hybrid triple quadrupole/linear ion trap mass spectrometry. J Chromatogr A 1142:172–177Google Scholar
  31. 31.
    Ciminiello P, Dell’Aversano C, Fattorusso E, Forino M, Magno S, Poletti R (2002) Direct detection of yessotoxin an its analogues by liquid chromatography coupled with electrospray ion trap mass spectrometry. J Chromatogr A 968:61–69Google Scholar
  32. 32.
    Finch SC, Wilkins AL, Hawkes AD, Jensen DJ, MacKenzie AL, Beuzenberg V, Quilliam MA, Olseng CD, Samdal IA, Aasen J, Selwood AI, Cooney JM, Sandvik M, Miles CO (2005) Isolation and identification of (44-R,S)-44,55-dihydroxy yessotoxin from Protoceratium reticulatum, and its occurrence in extracts of shellfish from New Zealand, Norway and Canada. Toxicon 46:160–170Google Scholar
  33. 33.
    Samdal IA, Aasen JAB, Briggs LR, Dahl E, Miles CO (2005) Comparison of ELISA and LC-MS analyses for yessotoxins in blue mussels (Mytilus edulis). Toxicon 46:7–15Google Scholar
  34. 34.
    Miles CO, Samdal IA, Aasen JAG, Jensen DJ, Quilliam MA, Petersen D, Briggs LM, Wilkins AL, Rise F, Cooney JM, MacKenzie AL (2005) Evidence for numerous analogs of yessotoxin in Protoceratium reticulatum. Harmful Algae 4:1075–1091Google Scholar
  35. 35.
    Rhodes L, McNabb P, de Salas M, Briggs L, Beuzenberg V, Gladstone M (2006) Yessotoxin production by Gonyaulax spinifera. Harmful Algae 5:148–155Google Scholar
  36. 36.
    Ciminiello P, Dell’Aversano C, Fattorusso E, Forino M, Magno S, Guerrini F, Pistocchi R, Boni L (2003) Complex yessotoxins profile in Protoceratium reticulatum from north-western Adriatic sea revealed by LC-MS analysis. Toxicon 42:7–14Google Scholar
  37. 37.
    Amandi MF, Furey A, Lehane M, Ramstad H, James KJ (2002) Liquid chromatography with electrospray ion-trap mass spectrometry for the determination of yessotoxins in shellfish. J Chromatogr A 976:329–334Google Scholar
  38. 38.
    James KJ, Bishop AG, Furey A (2000) New toxins on the horizon. In: Botana LM (ed) Seafood and freshwater toxins: pharmacology, physiology and detection. Marcel Dekker, New York, ISBN 8247-8956-3, pp 693–714Google Scholar
  39. 39.
    James KJ, Furey A, Lehane M, Ramstad H, Aune T, Hovgaard P, Morris S, Higman W, Satake M, Yasumoto T (2002) First evidence of an extensive northern European distribution of azaspiracid poisoning (AZP) toxins in shellfish. Toxicon 40:909–915Google Scholar
  40. 40.
    Brombacher S, Edmonds S, Volmer DA (2002) Studies on azapsiracids biotoxins. II. Mass spectral behaviour and structural elucidation of azaspiracid analogues. Rapid Commun Mass Spectrom 16:2306–2316Google Scholar
  41. 41.
    James KJ, Sierra MD, Lehane M, Magdalena AB, Furey A (2003) Detection of five new hydroxyl analogues of azaspiracids in shellfhish using multiple tandem mass spectrometry. Toxicon 41:277–283Google Scholar
  42. 42.
    Vale P (2004) Is there a risk of human poisoning by azaspiracids from shellfish harvested at the Portuguese coast? Toxicon 44:943–947Google Scholar
  43. 43.
    Magdalena AB, Lehane M, Krys S, Fernández ML, Furey A, James KJ (2003) The first identification of azaspiracids in shellfish from France and Spain. Toxicon 42:105–108Google Scholar
  44. 44.
    James KJ, Moroney C, Roden C, Satake M, Yasumonto T, Lehane M, Furey A (2003) Ubiquitous ‘benign’ alga emerges as the cause of shellfish contamination responsible for the human toxic syndrome, azaspiracid poisoning. Toxicon 41:145–151Google Scholar
  45. 45.
    Hess P, Nguyen L, Aasen J, Keogh M, Kilcoyne J, McCarron P, Aune T (2005) Tissue distribution, effects of cooking and parameters affecting the extraction of azaspiracids from mussels, Mytilus edulis, prior to analysis by liquid chromatography coupled to mass spectrometry. Toxicon 46:62–71Google Scholar
  46. 46.
    Draisci R, Palleschi L, Ferretti E, Furey A, James KJ, Satake M, Yasumoto T (2000) Development of a method for the identification of azaspiracid in shellfish by liquid chromatography-tandem mass spectrometry. J Chromatogr A 871:13–21Google Scholar
  47. 47.
    Lehane M, Sáez MJF, Magdalena AB, Cañás IR, Sierra MD, Hamilton B, Furey A, James KJ (2004) Liquid chromatography-multiple tandem mass spectrometry for the determination of ten azaspiracids, including hydroxyl analogues in shellfish. J Chromatogr A 1024:63–70Google Scholar
  48. 48.
    Quilliam MA, Wright JLC (1989) The amnesic shellfish poisoning mystery. Anal Chem 81:1053–1060Google Scholar
  49. 49.
    Todd ECD (1993) Domoic acid and amnesic shellfish poisoning-a review. J Food Prot 56:69–83Google Scholar
  50. 50.
    James KJ, Gillman M, Amandi MF, López-Rivera A, Puente PF, Lehane M, Mitrovic S, Furey A (2005) Amnesic shellfish poisoning toxins in bivalve molluscs in Ireland. Toxicon 46:852–858Google Scholar
  51. 51.
    Lawrence JF, Lau VP, Cleroux C, Lewis D (1994) Comparison of UV absorption and electrospray mass-spectrometry for the high-performance liquid chromatographic determination of domoic acid in shellfish and biological samples. J Chromatogr A 659:119–126Google Scholar
  52. 52.
    Hummert C, Reichelt M, Luckas B (1997) Automatic HPLC-UV Determination of domoic acid in mussels and algae. Chromatographia 45:284–288Google Scholar
  53. 53.
    Furey A, Lehane M, Gillman M, Fernandez-Puente P, James KJ (2001) Determination of domoic acid in shellfish by liquid chromatography with electrospray ionization and multiple tandem mass spectrometry. J Chromatogr A 938:167–174Google Scholar
  54. 54.
    López-Rivera A, Suárez-Isla BA, Eilers PP, Beaudry CG, Hall S, Amandi MF, Furey A, James KJ (2005) Improved high-performance liquid chromatographic method for the determination of domoic acid and analogues in shellfish: effect of pH. Anal Bioanal Chem 381:1540–1545Google Scholar
  55. 55.
    Hess P, Morris S, Stobo LA, Brown NA, McEvoy JDG, Kennedy G, Young PB, Slattery D, McGovern E, McMahon T, Gallacher S (2005) LC-UV and LC-MS methods for the determination of domoic acid. Trends Anal Chem 24:358–367Google Scholar
  56. 56.
    Tor ER, Puschner B, Whitehead WE (2003) Rapid determination of domoic acid in serum and urine by liquid chromatography-electrospray tandem mass spectrometry. J Agric Food Chem 51:1791–1796Google Scholar
  57. 57.
    Yokoo A (1950) Chemical studies on globefish poison. J Chem Soc Japan 71:590–593Google Scholar
  58. 58.
    Woodward RB (1964) The structure of tetrodotoxin. Pure Appl Chem 9:49CrossRefGoogle Scholar
  59. 59.
    Goto T, Kishi Y, Takahashi S, Hirata Y (1965) Tetrodotoxin. Tetrahedron 21:2059–2061Google Scholar
  60. 60.
    Yasumoto T, Murata M (1993) Marine Toxins Chem Rev 93:1897–1909Google Scholar
  61. 61.
    Shoji YS, Yamashita MY, Miyazawa T, Yasumoto T (2001) Electrospray ionization mass spectrometry of tetrodotoxin and its analogs: liquid chromatography/mass spectrometry, tandem mass spectrometry, and liqid chromatography/tandem mass spectrometry. Anal Biochem 290:10–17Google Scholar
  62. 62.
    Yotsu-Yamashita M (2001) Chemistry of puffer fish toxin. J Toxicol Toxin Rev 20:51–66Google Scholar
  63. 63.
    Pires OR, Sebben A, Schwartz EF, Morales RAV, Bloch C, Schwartz CA (2005) Further report of the occurrence of tetrodotoxin and new analogues in the Anuran family Brachycephalidae. Toxicon 45:73–79Google Scholar
  64. 64.
    Yotsu-Yamashita M, Mebs D, Flachsenberger W (2007) Distribution of tetrodotoxin in the body of the blue-ringed octopus (Hapalochlaena maculosa). Toxicon 49:410–412Google Scholar
  65. 65.
    Diener M, Christian B, Ahmed S, Luckas B (2007) Determination of tetrodotoxin and its analogs in the puffer fish Takifugu oblongus from Bangladesh by hydrophilic interaction chromatography and mass spectrometric detection. Anal Bioanal Chem. DOI 10.1007/100216-007-1602-7
  66. 66.
    Simidu U, Noguchi T, Hwang DF, Shida Y, Hashimoto K (1987) Marine bacteria which produce tetrodotoxin. Appl Environ Microbiol 53:1714–1715Google Scholar
  67. 67.
    Kodama M, Shimizu H, Sato S, Ogata T, Terao K (1995) The infection of bacteria in the liver cells of toxic puffer-a possible cause for organisms to be made toxic by tetrodotoxin in association with bacteria. In: Lassus P, Arzul G, Erard-LeDenn E, Gentien P, Marcaillou-LeBaut C (eds) Harmful marine algal blooms. Lavoisier, Paris, ISBN 1-898298-11-4, pp 457–462Google Scholar
  68. 68.
    Lee MJ, Jeong DY, Kim WS, Kim HD, Kim CH, Park WW, Park YH, Kim KS, Kim HM, Kim DS (2000) A tetrodotoxin-producing Vibrio strain, LM-1, from the puffer fish Fugu vermicularis radiatus. Appl Environ Microbiol 66:1698–1701Google Scholar
  69. 69.
    Mosher HS, Fuhrman FA (1984) Occurrence and origin of tetrodotoxin. In: Ragelis EP (ed) Seafood toxins. ACS, Washington DC, pp 333–334Google Scholar
  70. 70.
    Yasumoto T, Fukui M, Sasaki K, Sugiyama K (1995) Determinations of marine toxins in food. J Assoc Off Anal Chem Intern 78:574–582Google Scholar
  71. 71.
    Nakamura M, Oshima Y, Yasumoto T (1984) Occurrence of saxitoxin in puffer fish. Toxicon 22:381–385Google Scholar
  72. 72.
    Yasumura D, Oshima Y, Yasumoto T, Alcala AC, Alcala LC (1986) Tetrodotoxin and paralytic shellfish toxins in Philippine crabs. Agric Biol Chem 50:593–598Google Scholar
  73. 73.
    Nakashima K, Arakawa O, Taniyama S, Nonaka M, Takatani T, Yamamori K, Fuchi Y, Noguchi T (2004) Occurrence of saxitoxins as a major toxin in the ovary of a marine puffer Arothron firmamentum. Toxicon 43:207–212Google Scholar
  74. 74.
    Onoue Y, Noguchi T, Nagashima Y, Hashimoto K, Kanoh S, Ito M, Tsukada K (1983) Separation of tetrodotoxin and paralytic shellfish poisons by high-performance liquid chromatography with a fluorimetric detection using o-phthaldialdehyde. J Chromatogr 257:373–379Google Scholar
  75. 75.
    Gawley RE, Shanmugasundaram M, Thorne JB, Tarkka RM (2005) Selective detection of saxitoxin over tetrodotoxin using acridinylmethyl crown ether chemosensor. Toxicon 45:783–787Google Scholar
  76. 76.
    Yasumoto T, Michishita T (1985) Fluorimetric determination of tetrodotoxin by high-performance liquid chromatography. Agric Biol Chem 49:3077–3089Google Scholar
  77. 77.
    Nagashima Y, Maruyama J, Noguchi T, Hashimoto K (1987) Analysis of paralytic shellfish poison and tetrodotoxin by ion-pairing high-performance liquid chromatography. Nippon Suisan Gakkaishi 53:819–823Google Scholar
  78. 78.
    Quilliam MA, Thomson BA, Scott GJ, Siu KWM (1989) Ion-spray mass spectrometry of marine neutrotoxins. Rapid Comm Mass Spectrom 3:145–150Google Scholar
  79. 79.
    Horie M, Kobayashi S, Shimizu N, Nakazawa H (2002) Determination of tetrodotoxin in puffer-fish by liquid chromatography-electrospray ionization mass spectrometry. Analyst 127:755–759Google Scholar
  80. 80.
    Jang J, Yotsu-Yamashita M (2006) Distribution of tetrodotoxin, saxitoxin, and their analogs among tissues of the puffer fish Fugu pardalis. Toxicon 48:980–987Google Scholar
  81. 81.
    Nakagawa T, Jang J, Yotsu-Yamashita M (2006) Hydrophilic interaction liquid chromatography-electrospray ionization mass spectrometry of tetrodotoxin and its analogs. Anal Biochem 352:142–144Google Scholar
  82. 82.
    EC (2004) Regulation (EC) No. 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. Off J Eur Commun Annex III, Sect VII, Chap V, E L 226: p 68Google Scholar
  83. 83.
    Guzman-Perez SE, Park DL (2000) Ciguatera toxins: Chemistry and detection. In: Botana LM (ed) Seafood and freshwater toxins: pharmacology, physiology and detection. Marcel Dekker, New York, ISBN 8247-8956-3, pp 401–418Google Scholar
  84. 84.
    Capra MF, Cameron J (1987) Ciguatera poisoning: pharmacology and pathology. Report to the Fishing Industries Research Committee, Department of Primary Industries, Canberra, 1987Google Scholar
  85. 85.
    Lewis RJ, Sellin M (1992) Multiple ciguatoxins in the flesh of fish. Toxicon 30:915–919Google Scholar
  86. 86.
    Scheuer PJ, Takahashi W, Tsutsumi J, Yoshida T (1967) Ciguatoxin: Isolation and chemical nature. Science 155:1267–1268Google Scholar
  87. 87.
    Murata M, Legrand AM, Ishibashi Y, Fukui M, Yasumoto T (1989) Structure of ciguatoxin and its congener. J Am Chem Soc 111:8929–8931Google Scholar
  88. 88.
    Sperr AE, Doucette GJ (1996) Variation in growth rate and Ciguatera toxin production among geographically distinct isolates of Gambierdiscus toxicus. In: Yasumoto T, Oshima Y, Fukuyo Y (eds) Harmful and Toxic Algal Blooms. Intergovernmental Oceanographic Commission , UNESCO, Paris, pp 309–312Google Scholar
  89. 89.
    Lewis RJ, Sellin M, Poli MA, Norton RS, MacLeod JK, Sheil MM (1991) Purification and characterization of ciguatoxins from Moray Eel (Lycodontis javanicus, Muraenidae). Toxicon 29:1115–1127Google Scholar
  90. 90.
    Gaboa PM, Park DL, Fremy JM (1992) Extraction and purification of toxic fractions from barracuda (Sphyraena barracuda) implicated in ciguatera poisoning. In: Tosteson TR (ed) Proceedings of the 3rd international conference on ciguatera fish poisoning. Polyscience, Quebec, pp 13–24Google Scholar
  91. 91.
    Lewis RJ, Molgo J, Adams DJ (2000) Ciguatera toxins: Pharmacology of toxins involved in ciguatera and related fish poisoning. In: Botana LM (ed) Seafood and freshwater toxins: pharmacology, physiology and detection. Marcel Dekker, New York, ISBN 8247-8956-3 pp 419–447Google Scholar
  92. 92.
    Park DL (1994) Evolution of methods for assessing ciguatera toxins in fish. Rev Environ Contam Toxicol 136:1–20Google Scholar
  93. 93.
    Vernoux JP, Lahlou N, Magras LP, Greaux JB (1985) Chick feeding test: a simple system to detect ciguatoxin. Acta tropica 42:235–240Google Scholar
  94. 94.
    Chungue E, Bagnis RA, Parc E (1984) The use of the mosquito (Aedes aegypti) to detect ciguatoxin in surgeonfishes (Ctenochaetus striatus). Toxicon 22:161–164Google Scholar
  95. 95.
    Hokama Y (1985) A rapid simplified enzyme immunoassay stick test for the detection of ciguatoxin and related polyethers from fish tissues. Toxicon 23:939–946Google Scholar
  96. 96.
    Hokama Y, Asahina AY, Hong TWP, Shang ES, Miyahara JT (1990) Evaluation of the stick enzyme immunoassay in Carnax sp. and Seriola dumerili associated with ciguatera. J Clin Lab Anal 4:363–366Google Scholar
  97. 97.
    Park DL (1995) Detection of ciguatera and diarrheic shellfish toxins in finfish and shellfish with ciguatect kit. J Assoc Off Anal Chem Intern 78:533–537Google Scholar
  98. 98.
    EC (2004) Regulation (EC) No. 854/2004 of the European Parliament and of the Council of 29. April 2004 laying down specific rules for the organisation of official controls on products of animal origin intended for human consumption. Off J Eur Commun Annex III, Chap II, G L 226: p123Google Scholar
  99. 99.
    Pottier I, Hamilton B, Jones A, Lewis RJ, Vernoux JP (2003) Identification of slow and fast-acting toxins in a highly ciguatoxic barracuda (Sphyraena barracuda) by HPLC/MS and radiolabelled ligand binding. Toxicon 42:663–672Google Scholar
  100. 100.
    Bottein Dechraoui MY, Tiedeken JA, Persad R, Wang Z, Granade HR, Dickey RW, Ramsdell JS (2005) Use of two detection methods to discriminate ciguatoxins from brevetoxins: application to great barracuda from Florida Keys. Toxicon 46:261–270Google Scholar
  101. 101.
    Chateau-Degat M-L, Chinain M, Cerf N, Gingras S, Hubert B, Dewailly È (2005) Seawater temperature, Gambierdiscus spp. variability and incidence of ciguatera poisoning in French Polynesia. Harmful Algae 4:1053–1062Google Scholar
  102. 102.
    Hamilton B, Hurbungs M, Jones A, Lewis RJ (2002) Multiple ciguatoxins present in Indian ocean reef fish. Toxicon 40:1347–1353Google Scholar
  103. 103.
    Pottier I, Vernoux J-P, Jones A, Lewis RJ (2002) Characterisation of multiple Caribbean ciguatoxins and congeners in individual specimens of horse-eye jack (Caranx latus) by high-performance liquid chromatography/mass spectrometry. Toxicon 40:929–939Google Scholar
  104. 104.
    Hamilton B, Hurbungs M, Vernoux J-P, Jones A, Lewis RJ (2002) Isolation and characterisation of Indian ocean ciguatoxin. Toxicon 40:685–693Google Scholar
  105. 105.
    Shumway SE, von Egmond HP, Hurst JW, Bean LL (1995) Management of shellfish resources. In: Hallegraeff GM, Anderson DM, Cembella AD (eds) Manual on harmful marine microalgae. IOC Manuals and Guides 33, UNESCO, Paris, pp 433–459Google Scholar
  106. 106.
    Reguera B, Campos MJ, Fraga S, Marino J, Bravo I (1991) The monitoring of harmful algal blooms in Galicia (NW Spain). In: Fremy JM (ed) Proceedings of symposium on marine biotoxins. CNEVA, Maisons-Alfort, pp 217–223Google Scholar
  107. 107.
    Anderson DM (1989) Toxic algal blooms and red tides, a global perspective. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides-biology environmental science and toxicology. Elsevier, New York, pp 11–16Google Scholar
  108. 108.
    van Egmond HP, Speijers GJA, van den Top HJ (1992) Current situation on worldwide regulations for marine phycotoxins. J Nat Toxins 1:67–85Google Scholar
  109. 109.
    Food and Drug Administration (1989) Compliance policy guide 7108.20 on paralytic shellfish poison in clams, mussels, oysters-fresh, frozen or Canned. FDA, Washington DC, 30 Nov 1989Google Scholar
  110. 110.
    National Shellfish Sanitation Program (NSSP) (1990) Manual of operations, part I: Sanitation of shellfish growing areas, 1990 revision. USDepartment of Health and Human Services, Public Health Service, Food and Drug Administration (FDA), Washington DC, C22–C24Google Scholar
  111. 111.
    Council of European Communities (1992) Council decision on reference laboratories for the monitoring of marine biotoxins. COM (92) 551 final. Brussels, 16 Dec 1992Google Scholar
  112. 112.
    EC (2004) Regulation (EC) No. 854/2004 of the European Parliament and of the Council of 29. April 2004 laying down specific rules for the organisation of official controls on products of animal origin intended for human consumption. Off J Eur Commun Annex II, Chap II, A-D L 226: pp 119–121Google Scholar
  113. 113.
    Hummert C, Rühl A, Reinhardt K, Gerdts G, Luckas B (2002) Simultaneous analysis of different algal toxins by LC-MS. Chromatographia 55:673–680Google Scholar
  114. 114.
    Dahlmann J, Budakowski WR, Luckas B (2003) Liquid chromatography-electrospray ionisation-mass spectrometry based method for the simultaneous determination of algal and cyanobacterial toxins in phytoplankton from marine waters and lakes followed by tentative structural elucidation of microcystins. J Chromatogr A 994:45–57Google Scholar
  115. 115.
    MacKenzie L, Holland P, McNabb P, Beuzenberg V, Selwood A, Suzuki T (2002) Complex toxin profiles in phytoplankton and Greenshell mussels (Perna canaliculus), revealed by LC-MS/MS analysis. Toxicon 40:1321–1330Google Scholar
  116. 116.
    Ciminiello P, Dell’Aversano C, Fattorusso E, Forino M, Magno S, Santelia F, Tsoukatou M (2006) Investigation of the toxin profile of Greek mussels Mytilus galloprovincialis by liquid chromatography-mass spectrometry. Toxicon 47:174–181Google Scholar
  117. 117.
    McNabb P, Selwood AI, Holland PT (2005) Multiresidue method for determination of algal toxins in shellfish: single-laboratory validation and interlaboratory study. J Anal Off Anal Chem Int 88:761–772Google Scholar
  118. 118.
    Suzuki T, Jin T, Shirota Y, Mitsuya T, Okumura Y, Kamiyama T (2005) Quantification of lipophilic toxins associated with diarrhetic shellfish poisoning in Japanese bivalves by liquid chromatography-mass spectrometry and comparison with mouse bioassay. Fisheries Sci 71:1370–1378Google Scholar
  119. 119.
    Botana LM (ed) (2007) Phycotoxins: chemistry and biochemistry. Blackwell, Ames, ISBN 978-0-8138-2700-1Google Scholar
  120. 120.
    Fux E, McMillan D, Bire R, Hess P (2007) Development of an ultra-performance liquid chromatography-mass spectrometry method for the detection of lipophilic marine toxins. J Chromatogr A 1157:273–280Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Institute for NutritionFriedrich-Schiller-University of JenaJenaGermany

Personalised recommendations