Analytical and Bioanalytical Chemistry

, Volume 397, Issue 5, pp 1655–1671 | Cite as

Comparison of analytical tools and biological assays for detection of paralytic shellfish poisoning toxins

Review

Abstract

The paralytic shellfish poisoning toxins (PSTs) were, as their name suggests, discovered as a result of human poisoning after consumption of contaminated shellfish. More recently, however, the same toxins have been found to be produced by freshwater cyanobacteria. These organisms have worldwide distribution and are common in our sources of drinking water, thus presenting another route of potential human exposure. However, the regulatory limits for PSTs in drinking water are considerably lower than in shellfish. This has increased the need to find alternatives to the mouse bioassay, which, apart from being ethically questionable, does not have a limit of detection capable of detecting the PSTs in water at the regulated concentrations. Additionally, the number of naturally occurring PSTs has grown substantially since saxitoxin was first characterised, markedly increasing the analytical challenge of this group of compounds. This paper summarises the development of chromatographic, toxicity, and molecular sensor binding methodologies for detection of the PSTs in shellfish, cyanobacteria, and water contaminated by these toxins. It then summarises the advantages and disadvantages of their use for particular applications. Finally it recommends some future requirements that will contribute to their improvement for these applications.

Keywords

Saxitoxin Gonyautoxin C-toxin Dinoflagellate Cyanobacteria Drinking water Bioassay ELISA HPLC LC–MS PSTs 

Notes

Acknowledgements

We thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for a post-doctoral research fellowship supporting the visit of VFM to the laboratory of ARH.

References

  1. 1.
    Kao CY (1993) In: Falconer I (ed) Algal toxins in seafood and drinking water. Academic Press Limited, LondonGoogle Scholar
  2. 2.
    Llewellyn LE, Dodd M, Robertson A, Ericson G, de Koning C, Negri AP (2002) Post-mortem analysis of samples from a human victim of a fatal poisoning caused by the xanthid crab, Zosimus aeneus. Toxicon 40:1463–1469Google Scholar
  3. 3.
    Li R, Carmichael WW, Liu Y, Watanabe MM (2000) Taxonomic re-evaluation of Aphanizomenon flos-aquae NH-5 based on morphology and 16S rRNA sequences. Hydrobiologia 438:99–105Google Scholar
  4. 4.
    McBarron EJ, Walker RI, Gardner I, Walker KH (1975) Toxicity to livestock of the blue-green alga Anabaena circinalis. Aust Vet J 51:587–588Google Scholar
  5. 5.
    Humpage AR, Rositano J, Bretag AH, Brown R, Baker PD, Nicholson BC, Steffensen DA (1994) Paralytic shellfish poisons from Australian cyanobacterial blooms. Aust J Mar Freshwat Res 45:761–771Google Scholar
  6. 6.
    Negri A, Jones GJ, Blackburn S, Oshima Y, Onodera H (1997) Effect of culture and bloom development and of storage on paralytic shellfish poisons in the cyanobacterium Anabaena circinalis. J Phycol 33:26–35Google Scholar
  7. 7.
    Negri A, Llewellyn L, Doyle J, Webster N, Frampton D, Blackburn S (2003) Paralytic shellfish toxins are restricted to few species among Australia's taxonomic diversity of cultured microalgae. J Phycol 39:663–667Google Scholar
  8. 8.
    Velzeboer RMA, Baker PD, Rositano J, Heresztyn T, Codd GA, Raggett SL (2000) Geographical patterns of occurrence and composition of saxitoxins in the cyanobacterial genus Anabaena (Nostocales, Cyanophyta) in Australia. Phycologia 39:395–407CrossRefGoogle Scholar
  9. 9.
    Lagos N, Onodera H, Zagatto PA, Andrinolo D, Azevedo S, Oshima Y (1999) The first evidence of paralytic shellfish toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon 37:1359–1373Google Scholar
  10. 10.
    Molica R, Onodera H, Garcia C, Rivas M, Andrinolo D, Nascimento S, Meguro H, Oshima Y, Azevedo S, Lagos N (2002) Toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii (Cyanophyceae) isolated from Tabocas reservoir in Caruaru, Brazil, including demonstration of a new saxitoxin analogue. Phycologia 41:606–611Google Scholar
  11. 11.
    Humpage AR, Ledreux A, Fanok S, Bernard C, Briand JF, Eaglesham G, Papageorgiou J, Nicholson B, Steffensen D (2007) Application of the neuroblastoma assay for paralytic shellfish poisons to neurotoxic freshwater cyanobacteria: Interlaboratory calibration and comparison with other methods of analysis. Environ Toxicol Chem 26:1512–1519Google Scholar
  12. 12.
    Bowling LC (1994) Occurrence and possible causes of a severe cyanobacterial bloom in Lake Cargelico, New South Wales. Aust J Mar Freshwat Res 45:737–745Google Scholar
  13. 13.
    Ferrão-Filho AS, Soares MC, Rocha MIA, Magalhães VF, Azevedo SMFO (2009) Florações de cianobactérias tóxicas no reservatório do Funil: dinâmica sazonal e Consequências para o zooplâncton. Oecol Bras 13(2):346–365Google Scholar
  14. 14.
    Jones GJ, Negri A (1997) Persistence and degradation of the cyanobacterial paralytic shellfish poisons (PSPs) in freshwaters. Water Res 31:525–533Google Scholar
  15. 15.
    Negri AP, Jones GJ (1995) Bioaccumulation of paralytic shellfish poisoning (PSP) toxins from the cyanobacterium Anabaena circinalis by the freshwater mussel Alathyria condola. Toxicon 33:667–678Google Scholar
  16. 16.
    Baker PD, Humpage AR (1994) Toxicity associated with commonly occurring cyanobacteria in surface waters of the Murray-Darling Basin, Australia. Aust J Mar Freshwat Res 45:773–786Google Scholar
  17. 17.
    Carmichael WW, Evans WR, Yin QQ, Bell P, Moczydlowski E (1997) Evidence for paralytic shellfish poisons in the freshwater cyanobacterium Lyngbya wollei (Farlow ex Gomont) comb. nov. Appl Environ Microbiol 63:3104–3110Google Scholar
  18. 18.
    Pomati F, Sacchi S, Rossetti C, Giovannardi S, Onodera H, Oshima Y, Neilan BA (2000) The freshwater cyanobacterium Planktothrix sp FP1: molecular identification and detection of paralytic shellfish poisoning toxins. J Phycol 36:553–562Google Scholar
  19. 19.
    Liu YM, Chen W, Li DH, Shen YW, Liu YD, Song LR (2006) Analysis of paralytic shellfish toxins in Aphanizomenon DC-1 from Lake Dianchi, China. Environ Toxicol 21:289–295Google Scholar
  20. 20.
    Pereira P, Li RH, Carmichael WW, Dias E, Franca S (2004) Taxonomy and production of paralytic shellfish toxins by the freshwater cyanobacterium Aphanizomenon gracile LMECYA40. Eur J Phycol 39:361–368Google Scholar
  21. 21.
    Pereira P, Onodera H, Andrinolo D, Franca S, Araujo F, Lagos N, Oshima Y (2000) Paralytic shellfish toxins in the freshwater cyanobacterium Aphanizomenon flos-aquae, isolated from Montargil reservoir, Portugal. Toxicon 38:1689–1702Google Scholar
  22. 22.
    Kaas H, Henriksen P (2000) Saxitoxins (PSP toxins) in Danish lakes. Water Res 34:2089–2097Google Scholar
  23. 23.
    Rapala J, Robertson A, Negri AP, Berg KA, Tuomi P, Lyra C, Erkomaa K, Lahti K, Hoppu K, Lepisto L (2005) First report of saxitoxin in Finnish lakes and possible associated effects on human health. Environ Toxicol 20:331–340Google Scholar
  24. 24.
    Kellmann R, Michali TK, Neilan BA (2008) Identification of a Saxitoxin biosynthesis gene with a history of frequent horizontal gene transfers. J Mol Evol 67:526–538Google Scholar
  25. 25.
    Bouvy M, Molica R, Oliveira S, Marinho M, Beker B (1999) Dynamics of a toxic cyanobacterial bloom (Cylindrospermopsis raciboskii) in a shallow reservoir in the semi-arid region of northeast Brazil. Aquat Microb Ecol 20:285–297Google Scholar
  26. 26.
    Komárková J, Laudares-Silva R, Senna PAC (1999) Extreme morphology of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in the Lagoa do Peri, a freshwater coastal lagoon, Santa Catarina, Brazil. Algol Stud 94:207–222Google Scholar
  27. 27.
    Falconer IR (2005) Cyanobacterial toxins of drinking water supplies: cylindrospermopsins and microcystins. CRC Press, Boca Raton, FloridaGoogle Scholar
  28. 28.
    Humpage AR (2008) In: Hudnell HK (ed) Proceedings of the Interagency, International Symposium on Cyanobacterial Harmful Algal Blooms (ISOC_HAB): state of the science and research needs. Advances in experimental medicine & biology. Springer, New YorkGoogle Scholar
  29. 29.
    Oshima Y (1995) Postcolumn derivatization liquid chromatographic method for paralytic shellfish toxins. J AOAC Int 78:528–532Google Scholar
  30. 30.
    Shimizu Y (2000) In: Botana LM (ed) Seafood and freshwater toxins: pharmacology, physiology and detection. New York, Marcel Dekker IncGoogle Scholar
  31. 31.
    Wekell JC, Hurst J, Lefebvre KA (2004) The origin of the regulatory limits for PSP and ASP toxins in shellfish. J Shellfish Res 23:927–930Google Scholar
  32. 32.
    Schantz EJ, Mold JD, Stanger DW, Shavel J, Riel FJ, Bowden JP, Lynch JM, Wiler RS, Riegel B, Sommer H (1957) Paralytic Shellfish Poison. VI. A procedure for the isolation and purification of the poison from toxic clam and mussel tissues. J Am Chem Soc 79:5230–5235Google Scholar
  33. 33.
    Wong JL, Oesterlin R, Rapoport H (1971) The structure of Saxitoxin. J Am Chem Soc 93:7344–7345Google Scholar
  34. 34.
    AOAC (1959) AOAC Official methods of analysis, chapter 49, 18th edn. Natural Toxins, AOAC International, Gaithersburg, MD, USAGoogle Scholar
  35. 35.
    McFarren EF (1959) Report on collaborative studies of the bioassay for paralytic shellfish poison. Journal of the Association of Official Analytical Chemists 42:263–271Google Scholar
  36. 36.
    AOAC (2005) AOAC official methods of analysis, chapter 49, 18th edn. Natural Toxins, AOAC International, Gaithersburg, MD, USAGoogle Scholar
  37. 37.
    Hess P, Grune B, Anderson DB, Aune T, Botana LM, Caricato P, van Egmond HP, Halder M, Hall S, Lawrence JF, Moffat C, Poletti R, Richmond J, Rossini GP, Seamer C, Vilageliu JS (2006) Three Rs approaches in marine biotoxin testing - The report and recommendations of a joint ECVAM/DG SANCO workshop (ECVAM workshop 55). Atla-Alternatives to Laboratory Animals 34:193–224Google Scholar
  38. 38.
    Campas M, Prieto-Simon B, Marty JL (2007) Biosensors to detect marine toxins: assessing seafood safety. Talanta 72:884–895Google Scholar
  39. 39.
    Fitzgerald DJ, Cunliffe DA, Burch MD (1999) Development of health alerts for cyanobacteria and related toxins in drinking-water in South Australia. Environ Toxicol 14:203–209Google Scholar
  40. 40.
    ADWG (2004) Australian Drinking Water Guidelines. http://www.nhmrc.gov.au/publications/synopses/eh19syn.htm
  41. 41.
    BDWG (2004) Brazilian drinking water guidelines: PORTARIA Nº 518/GM -25 march 2004. http://dtr2001.saude.gov.br/sas/PORTARIAS/Port2004/GM/GM-518.htm
  42. 42.
    NZDWG (2005) Guidelines for drinking water quality management for New Zealand. http://www.moh.govt.nz/moh.nsf/0/5A25BF765B400911CC25708F0002B5A8/$File/appendix1-mavs.pdf
  43. 43.
    Llewellyn LE, Doyle J, Jellett J, Barrett R, Alison C, Bentz C, Quilliam M (2001) Measurement of paralytic shellfish toxins in molluscan extracts: comparison of the microtitre plate saxiphilin and sodium channel radioreceptor assays with mouse bioassay, HPLC analysis and a commercially available cell culture assay. Food Addit Contam 18:970–980Google Scholar
  44. 44.
    Bates HA, Rapoport H (1975) A chemical assay for saxitoxin, the paralytic shellfish poison. J Agric Food Chem 23:237–239Google Scholar
  45. 45.
    Bates HA, Kostriken R, Rapoport H (1978) A chemical assay for saxitoxin. Improvements and modifications. J Agric Food Chem 26:252–254Google Scholar
  46. 46.
    Bordner J, Thiessen WE, Bates HA, Rapoport H (1975) The structure of a crystalline derivative of saxitoxin. The structure of saxitoxin. J Am Chem Soc 97:6008–6012Google Scholar
  47. 47.
    Buckley LJ, Ikawa M, Sasner JJJ (1976) Isolation of Gonyaulax tamarensis toxins from Soft Shell Clams (Mya arenaria) and a Thin-Layer Chromatographic-Fluorimetric method for their detection. J Agric Food Chem 24:107–111Google Scholar
  48. 48.
    Schantz EJ, Ghazarossian VE, Schnoes HK, Strong FM, Springer JP, Pezzanite JO, Clardy J (1975) The Structure of Saxitoxin. J Am Chem Soc 97:1238–1239Google Scholar
  49. 49.
    Shimizu Y, Alam M, Oshima Y, Fallon WE (1975) Presence of four toxins in red tide infested clams and cultured Gonyaulax tamarensis cells. Biochem Biophys Res Commun 66:731–737Google Scholar
  50. 50.
    Shimizu Y, Buckley LJ, Alam M, Oshima Y, Fallon WE, Kasai H, Miura I, Gullo VP, Nakanishi K (1976) Structures of Gonyautoxin II and III from the East Coast toxic Dinoflagellate Gonyaulax tamarensis. J Am Chem Soc 98:5414–5416Google Scholar
  51. 51.
    Ghazarossian VE, Schantz EJ, Schonoes HK, Strong FM (1976) A biologically active acid hydrolysis product of saxitoxin. Biochem Biophys Res Commun 68:776–780Google Scholar
  52. 52.
    Oshima Y, Buckley LJ, Alam M, Shimizu Y (1977) Heterogeneity of paralytic shellfish poisons. Three new toxins from cultured Gonyaulax tamarensis cells, Mya arenaria and Saxidomus giganteus. Comparative Biochemistry and Physiology D-Genomics & Proteomics 57C:31–34Google Scholar
  53. 53.
    Shimizu Y, Hsu C, Fallon WE, Oshima Y, Miura I, Nakanishi K (1978) Structure of Neosaxitoxin. J Am Chem Soc 100:6791–6793Google Scholar
  54. 54.
    Sullivan JJ, Iwaoka WT (1983) High pressure liquid chromatographic determination of toxins associated with paralytic shellfish poisoning. Journal of the Association of Official Analytical Chemists 66:297–303Google Scholar
  55. 55.
    Oshima Y, Hasegawa M, Yasumoto T, Hallegraeff G, Blackburn SI (1987) Dinoflagellate Gymnodinium catenatum as the source of paralytic shellfish toxins in Tasmanian shellfish. Toxicon 25:1105–1111Google Scholar
  56. 56.
    Franco JM, Fernández-Vila P (1993) Separation of paralytic shellfish toxins by reversed phase high performance liquid chromatography, with postcolumn reaction and fluorimetric detection. Chromatographia 35:613–620Google Scholar
  57. 57.
    Onodera, H, Oshima, Y, Watanabe, MF, Watanabe, M, Bolch, CJ, Blackburn, S, Yasumoto, T (1996) In: Yasumoto, T, Oshima, Y, Fukuyo, Y (ed) Harmful and toxic algal blooms. Proceedings of the Seventh International Conference on Toxic Phytoplankton, Sendai, Japan, 12-16 July 1995, Intergovernmental Oceanographic Commission of UNESCOGoogle Scholar
  58. 58.
    Leão JM, Gago A, Rodríguez-Vázquez JA, Aguete EC, Omil MM, Comesaña M (1998) Solid-phase extraction and high-performance liquid chromatography procedures for the analysis of paralytic shellfish toxins. J Chromatogr 798:131–136Google Scholar
  59. 59.
    Bire R, Krys S, Fremy JM, Dragacci S (2003) Improved solid-phase extraction procedure in the analysis of paralytic shellfish poisoning toxins by liquid chromatography with fluorescence detection. J Agric Food Chem 51:6386–6390Google Scholar
  60. 60.
    Ravn H, Anthoni U, Christophersen C, Nielsen PH, Oshima Y (1995) Standardized extraction method for paralytic shellfish toxins in phytoplankton. J Appl Phycol 7:589–594Google Scholar
  61. 61.
    Indrasena WM, Gill TA (2000) Storage stability of paralytic shellfish poisoning toxins. Food Chem 71:71–77Google Scholar
  62. 62.
    Lawrence JF, Menard C (1991) Liquid chromatographic determination of paralytic shellfish poisons in shellfish after prechromatographic oxidation. Journal of the Association of Official Analytical Chemists 74:1006–1012Google Scholar
  63. 63.
    Lawrence JF, Menard C, Charbonneau CF, Hall S (1991) A study of ten toxins associated with paralytic shellfish poison using prechromatographic oxidation and liquid chromatography with fluorescence detection. Journal of the Association of Official Analytical Chemists 74:404–409Google Scholar
  64. 64.
    Lawrence JF, Ménard C, Cleroux C (1995) Evaluation of prechromatographic oxidation for liquid chromatographic determination of paralytic shellfish poisons in shellfish. J AOAC Int 78:514–520Google Scholar
  65. 65.
    Lawrence JF, Wong B, Menard C (1996) Determination of decarbamoyl saxitoxin and its analogues in shellfish by prechromatographic oxidation and liquid chromatography with fluorescence detection. J AOAC Int 79:1111–1115Google Scholar
  66. 66.
    Gago-Martinez A, Moscoso SA, Martins JML, Vazquez JAR, Niedzwiadek B, Lawrence JF (2001) Effect of pH on the oxidation of paralytic shellfish poisoning toxins for analysis by liquid chromatography. J Chromatogr 905:351–357Google Scholar
  67. 67.
    Lawrence JF, Niedzwiadek B, Menard C (2005) Quantitative determination of paralytic shellfish poisoning toxins in shellfish using prechromatographic oxidation and liquid chromatography with fluorescence detection: Collaborative study. J AOAC Int 88:1714–1732Google Scholar
  68. 68.
    Vale P, Sampayo MAD (2001) Determination of paralytic shellfish toxins in Portuguese shellfish by automated pre-column oxidation. Toxicon 39:561–571Google Scholar
  69. 69.
    Cianca RCC, Pallares MA, Barbosa RD, Adan LV, Martins JML, Gago-Martinez A (2007) Application of precolumn oxidation HPLC method with fluorescence detection to evaluate saxitoxin levels in discrete brain regions of rats. Toxicon 49:89–99Google Scholar
  70. 70.
    Ben-Gigirey B, Rodriguez-Velasco ML, Villar-Gonzalez A, Botana LM (2007) Influence of the sample toxic profile on the suitability of a high performance liquid chromatography method for official paralytic shellfish toxins control. J Chromatogr 1140:78–87Google Scholar
  71. 71.
    Turner AD, Norton DM, Hatfield RG, Morris S, Reese AR, Algoet M, Lees DN (2009) Refinement and extension of AOAC method 2005.06 to include additional toxins in mussels: single-laboratory validation. J AOAC Int 92:190–207Google Scholar
  72. 72.
    He HZ, Li HB, Jiang Y, Chen F (2005) Determination of paralytic shellfish poisoning toxins in cultured microalgae by high-performance liquid chromatography with fluorescence detection. Anal Bioanal Chem 383:1014–1017Google Scholar
  73. 73.
    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
  74. 74.
    Rourke WA, Murphy CJ, Pitcher G, van de Riet JM, Burns BG, Thomas KM, Quilliam MA (2008) Rapid postcolumn methodology for determination of paralytic shellfish toxins in shellfish tissue. J AOAC Int 91:589–597Google Scholar
  75. 75.
    Quilliam MA (1998) Phycotoxins. J AOAC Int 81:142–151Google Scholar
  76. 76.
    Dell'Aversano C, Eaglesham GK, Quilliam MA (2004) Analysis of cyanobacterial toxins by hydrophilic interaction liquid chromatography-mass spectrometry. J Chromatogr 1028:155–164Google Scholar
  77. 77.
    Jaime E, Hummert C, Hess P, Luckas B (2001) Determination of paralytic shellfish poisoning toxins by high-performance ion-exchange chromatography. J Chromatogr 929:43–49Google Scholar
  78. 78.
    Dell’Aversano C, Hess P, Quilliam MA (2005) Hydrophilic interaction liquid chromatography-mass spectrometry for the analysis of Paralytic Shellfish Poisoning (PSP) toxins. J Chromatogr 1081:190–201Google Scholar
  79. 79.
    Dell'Aversano C, Walter JA, Burton IW, Stirling DJ, Fattorusso E, Quilliam MA (2008) Isolation and structure elucidation of new and unusual saxitoxin analogues from mussels. J Nat Prod 71:1518–1523Google Scholar
  80. 80.
    Diener M, Erler K, Christian B, Luckas B (2007) Application of a new zwitterionic hydrophillic interaction chromatography column for determination of paralytic shellfish poisoning toxins. J Sep Sci 30:1821–1826Google Scholar
  81. 81.
    Turrell E, Stobo L, Lacaze JP, Piletsky S, Piletska E (2008) Optimization of hydrophilic interaction liquid chromatography/mass spectrometry and development of solid-phase extraction for the determination of paralytic shellfish poisoning toxins. J AOAC Int 91:1372–1386Google Scholar
  82. 82.
    Llewellyn LE (2007) Predictive toxinology: an initial foray using calculated molecular descriptors to describe toxicity using saxitoxins as a model. Toxicon 50:901–913Google Scholar
  83. 83.
    Usup G, Leaw CP, Cheah MY, Ahmad A, Ng BK (2004) Analysis of paralytic shellfish poisoning toxin congeners by a sodium channel receptor binding assay. Toxicon 44:37–43Google Scholar
  84. 84.
    Rastogi SC (2003) Cell and molecular biology, 2nd edn. New Age International (P) Limited, Noida, IndiaGoogle Scholar
  85. 85.
    Kogure K, Tamplin ML, Simidu U, Colwell RR (1989) In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides: biology, environmental science and toxicology. Elsevier, New York, NY, USAGoogle Scholar
  86. 86.
    Jellett JF, Marks LJ, Stewart JE, Dorey ML, Watson-Wright W, Lawrence JF (1992) Paralytic shellfish poison (saxitoxin family) bioassays: automated endpoint determination and standardization of the in vitro tissue culture bioassay, and comparison with the standard mouse bioassay. Toxicon 30:1143–1156Google Scholar
  87. 87.
    Manger RL, Leja LS, Lee SY, Hungerford JM, Hokama Y, Dickey RW, Granade HR, Lewis R, Yasumoto T, Wekell MM (1995) Detection of sodium channel toxins - directed cytotoxicity assays of purified ciguatoxins, brevetoxins, saxitoxins, and seafood extracts. J AOAC Int 78:521–527Google Scholar
  88. 88.
    Manger RL, Leja LS, Lee SY, Hungerford JM, Wekell MM (1993) Tetrazolium-based cell bioassay for neurotoxins active on voltage-sensitive sodium channels: Semiautomated assay for saxitoxins, brevetoxins, and ciguatoxins. Anal Biochem 214:190–194Google Scholar
  89. 89.
    Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63Google Scholar
  90. 90.
    Manger RL, Leja LS, Lee SY, Hungerford JM, Kirkpatrick MA, Yasumoto T, Wekell MM (2003) Detection of paralytic shellfish poison by rapid cell bioassay: antagonism of voltage-gated sodium channel active toxins in vitro. J AOAC Int 86:540–543Google Scholar
  91. 91.
    Jellett J, Stewart JE, Laycock MV (1995) Toxicological evaluation of saxitoxin, neosaxitoxin, gontautoxin II, gonyautoxin II plus III, and decarbomoylsaxitoxin with the mouse neuroblastoma cell bioassay. Toxicol In Vitro 9:57–65Google Scholar
  92. 92.
    Dechraoui MYB, Ramsdell JS (2003) Type B brevetoxins show tissue selectivity for voltage-gated sodium channels: comparison of brain, skeletal muscle and cardiac sodium channels. Toxicon 41:919–927Google Scholar
  93. 93.
    Teste V, Briand JF, Nicholson BC, Puiseux-Dao S (2002) Comparison of changes in toxicity during growth of Anabaena circinalis (cyanobacteria) determined by mouse neuroblastoma bioassay and HPLC. J Appl Phycol 14:399–407Google Scholar
  94. 94.
    Okumura M, Tsuzuki H, Tomita B (2005) A rapid detection method for paralytic shellfish poisoning toxins by cell bioassay. Toxicon 46:93–98Google Scholar
  95. 95.
    Louzao MC, Vieytes MR, Baptista de Sousa JM, Leira F, Botana LM (2000) A fluorimetric method based on changes in membrane potential for screening paralytic shellfish toxins in mussels. Anal Biochem 289:246–250Google Scholar
  96. 96.
    Louzao MC, Vieytes MR, Cabado AG, de Sousa J, Botana LM (2003) A fluorimetric microplate assay for detection and quantitation of toxins causing paralytic shellfish poisoning. Chem Res Toxicol 16:433–438Google Scholar
  97. 97.
    Manger R, Woodle D, Berger A, Hungerford J (2007) Flow cytometric detection of saxitoxins using fluorescent voltage-sensitive dyes. Anal Biochem 366:149–155Google Scholar
  98. 98.
    Vieytes MR, Cabado AG, Alfonso A, Louzao C, Botana A, Botana L (1993) Solid-phase radioreceptor assay for paralytic shellfish toxins. Anal Biochem 211:87–93Google Scholar
  99. 99.
    Doucette GJ, Logan MM, Ramsdell JS, Van Dolah FM (1997) Development and preliminary validation of a microtiter plate-based receptor binding assay for paralytic shellfish poisoning toxins. Toxicon 35:625–636Google Scholar
  100. 100.
    Ruberu SR, Liu YG, Wong CT, Perera SK, Langlois GW, Doucette GJ, Powell CL (2003) Receptor binding assay for paralytic shellfish poisoning toxins: optimization and interlaboratory comparison. J AOAC Int 86:737–745Google Scholar
  101. 101.
    Llewellyn L, Negri A, Quilliam M (2004) High affinity for the rat brain sodium channel of newly discovered hydroxybenzoate saxitoxin analogues from the dinoflagellate Gymnodinium catenatum. Toxicon 43:101–104Google Scholar
  102. 102.
    Llewellyn L, Moczydlowski E (1994) Characterization of saxitoxin binding to saxiphilin, a relative of the transferrin family that displays pH-dependent ligand binding. Biochemistry 33:12312–12322Google Scholar
  103. 103.
    Llewellyn LE, Doyle J (2001) Microtitre plate assay for paralytic shellfish toxins using saxiphilin: gauging the effects of shellfish extract matrices, salts and pH upon assay performance. Toxicon 39:217–224Google Scholar
  104. 104.
    Llewellyn LE, Doyle J, Negri AP (1998) A high-throughput, microtiter plate assay for paralytic shellfish poisons using the saxitoxin-specific receptor, saxiphilin. Anal Biochem 261:51–56Google Scholar
  105. 105.
    Negri A, Llewellyn L (1998) Comparative analyses by HPLC and the sodium channel and saxiphilin H-3-saxitoxin receptor assays for paralytic shellfish toxins in crustaceans and molluscs from tropical North West Australia. Toxicon 36:283–298Google Scholar
  106. 106.
    Llewellyn LE, Negri AP, Doyle J, Baker PD, Beltran EC, Neilan BA (2001) Radioreceptor assays for sensitive detection and quantitation of saxitoxin and its analogues from strains of the freshwater cyanobacterium, Anabaena circinalis. Environ Sci Technol 35:1445–1451Google Scholar
  107. 107.
    Usleber E, Dietrich R, Burk C, Schneider E, Martlbauer E (2001) Immunoassay methods for paralytic shellfish poisoning toxins. J AOAC Int 84:1649–1656Google Scholar
  108. 108.
    Chu FS, Hsu KH, Huang X, Barrett R, Allison C (1996) Screening of paralytic shellfish poisoning toxins in naturally occurring samples with different direct competitive enzyme-linked immunosorbent assays. J Agric Food Chem 44:4043–4047Google Scholar
  109. 109.
    Kawatsu K, Hamano Y, Sugiyama A, Hashizume K, Noguchi T (2002) Development and application of an enzyme immunoassay based on a monoclonal antibody against gonyautoxin components of paralytic shellfish poisoning toxins. J Food Prot 65:1304–1308Google Scholar
  110. 110.
    Garthwaite I, Ross KM, Miles CO, Briggs LR, Towers NR, Borrell T, Busby P (2001) Integrated enzyme-linked immunosorbent assay screening system for amnesic, neurotoxic, diarrhetic, and paralytic shellfish poisoning toxins found in New Zealand. J AOAC Int 84:1643–1648Google Scholar
  111. 111.
    Cordova JL, Jamett A, Aguayo J, Faure MT, Villarroel O, Cardenas L (2001) An in vitro assay to detect paralytic shellfish poison. J Shellfish Res 20:55–61Google Scholar
  112. 112.
    Laycock MV, Donovan MA, Easy DJ (2009) Sensitivity of lateral flow tests to mixtures of saxitoxins and applications to shellfish and phytoplankton monitoring. Toxicon In Press: doi: 10.1016/j.toxicon.2009.10.014
  113. 113.
    Laycock MV, Jellett JF, Belland ER, Bishop PC, Thériault BL, Russell-Tattrie AL, Quilliam MA, Cembella AD, Richards RC (2000) In: Hallegraeff GM, Blackburn SI, Bolch LJ, Lewis RJ (eds) IX International Conference on Harmful Algal Blooms, Intergovernment Oceanographic Commission of UNESCO, Hobart, Tasmania, AustraliaGoogle Scholar
  114. 114.
    Costa PR, Baugh KA, Wright B, RaLonde R, Nance SL, Tatarenkova N, Etheridge SM, Lefebvre KA (2009) Comparative determination of paralytic shellfish toxins (PSTs) using five different toxin detection methods in shellfish species collected in the Aleutian Islands, Alaska. Toxicon 54:313–320Google Scholar
  115. 115.
    Inami GB, Crandall C, Csuti D, Oshiro M, Brenden RA (2004) Feasibility of reduction in use of the mouse bioassay: presence/absence screening for saxitoxin in frozen acidified mussel and oyster extracts from the coast of California with in vitro methods. J AOAC Int 87:1133–1142Google Scholar
  116. 116.
    Oshiro M, Pham L, Csuti D, Dodd M, Inami GB, Brenden RA (2006) Paralytic shellfish poisoning surveillance in California using the Jellett Rapid PSP test. Harmful Algae 5:69–73Google Scholar
  117. 117.
    Campbell K, Stewart LD, Doucette GJ, Fodey TL, Haughey SA, Vilarino N, Kawatsu K, Elliott CT (2007) Assessment of specific binding proteins suitable for the detection of paralytic shellfish poisons using optical biosensor technology. Anal Chem 79:5906–5914Google Scholar
  118. 118.
    Fonfria ES, Vilarino N, Campbell K, Elliott C, Haughey SA, Ben-Gigirey B, Vieites JM, Kawatsu K, Botana LM (2007) Paralytic shellfish poisoning detection by surface plasmon resonance-based biosensors in shellfish matrixes. Anal Chem 79:6303–6311Google Scholar
  119. 119.
    Gawley RE, Mao H, Haque MM, Thorne JB, Pharr JS (2007) Visible fluorescence chemosensor for saxitoxin. J Org Chem 72:2187–2191Google Scholar
  120. 120.
    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
  121. 121.
    Kele N, Orbulescu J, Calhoun TL, Gawley RE, Leblanc RM (2002) Coumaryl crown ether based chemosensors: Selective detection of saxitoxin in the presence of sodium and potassium ions. Tetrahedron Lett 43:4413–4416Google Scholar
  122. 122.
    Mao H, Thorne JB, Pharr JS, Gawley RE (2006) Effect of crown ether ring size on binding and fluorescence response to saxitoxin in anthracylmethyl monoazacrown ether chemosensors. Canadian Journal of Chemistry-Revue Canadienne De Chimie 84:1273–1279Google Scholar
  123. 123.
    Llewellyn LE, Bell PM, Moczydlowski EG (1997) Phylogenetic survey of soluble saxitoxin-binding activity in pursuit of the function and molecular evolution of saxiphilin, a relative of transferrin. Proc R Soc Lond B Biol Sci 264:891–902Google Scholar
  124. 124.
    Azanza MPV, Azanza RV, Ventura SR (2003) Varied assays for PSP toxins in heat shocked Philippine green mussels (Perna viridis). J Food Saf 23:249–261Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • A. R. Humpage
    • 1
  • V. F. Magalhaes
    • 2
  • S. M. Froscio
    • 1
  1. 1.Australian Water Quality CentreAdelaideAustralia
  2. 2.Universidade Federal do Rio de Janeiro, Instituto de Biofísica Carlos Chagas FilhoCCS - Bloco G - UFRJ - Ilha do FundãoRio de JaneiroBrasil

Personalised recommendations