Inter-species variability of okadaic acid group toxicity in relation to the content of fatty acids detected in different marine vectors

References

• Alarcan J, Biré R, Le Hégarat L, Fessard V. 2018. Mixtures of lipophilic phycotoxins: exposure data and toxicological assessment. Mar Drugs. 16:46. doi:10.3390/md16020046
   Web of Science ®Google Scholar
• Alves TP, Schramm MA, Lao P, Pinto TO, Mafra LL. 2018. Interannual variability in Dinophysis spp. abundance and toxin accumulation in farmed mussels (Perna perna) in a subtropical estuary. Environ Monit Assess. 190:329.
   PubMed Web of Science ®Google Scholar
• Alves-de-Souza C, Varela D, Contreras C, de La Iglesia P, Fernández P, Hipp B, Hernández C, Riobo P, Reguera B, Franco JM, et al. 2014. Seasonal variability of Dinophysis spp. and Protoceratium reticulatum associated to lipophilic shellfish toxins in a strongly stratified Chilean fjord. Deep-Sea Research II. 101:152–162.
   Web of Science ®Google Scholar
• [AOAC] AOAC International. 2012. Official Method 948.15. Fat (crude) in seafood. Acid hydrolysis method. In: Official methods of analysis of AOAC international. 19th ed. Gaithersburg (MD): AOAC International. p. 1–23.
   Google Scholar
• Basti L, Suzuki T, Uchida H, Kamiyama T, Nagai S. 2018. Thermal acclimation affects growth and lipophilic toxin production in a strain of cosmopolitan harmful alga dinophysis acuminata. Harmful Algae. 73:119–128.
   PubMed Web of Science ®Google Scholar
• Behrenfeld MJ, Boss ES. 2014. Resurrecting the ecological underpinnings of ocean plankton blooms. Annu Rev Mar Sci. 6:167–194.
   PubMed Web of Science ®Google Scholar
• Ben-Gharbia H, Kéfi-Daly Yahia O, Amzil Z, Chomérat N, Abadie E, Masseret E, Sibat M, Zmerli Triki H, Nouri H, Laabi M. 2016. Toxicity and growth assessments of three thermophilic benthic dinoflagellates (Ostreopsis cf. ovata, Prorocentrum lima and Coolia monotis) developing in the southern Mediterranean basin. Toxins. 8:297. doi:10.3390/toxins8100297
   Web of Science ®Google Scholar
• Blanco J, Mariño C, Martín H, Acosta CP. 2007. Anatomical distribution of diarrhetic shellfish poisoning (DSP) toxins in the mussel Mytilus galloprovincialis. Toxicon. 50:1011–1018.
   PubMed Web of Science ®Google Scholar
• Botana LM. 2016. Toxicological perspective on climate change: aquatic toxins. Chem Res Toxicol. 29:619−625.
   PubMed Web of Science ®Google Scholar
• Botana LM, Hess P, Munday R, Nathalie A, De Grasse SL, Feeley M, Suzuki T, van der Berg M, Fattori V, Garrido Gamarra E, et al. 2017. Derivation of toxicity equivalency factors for marine biotoxins associated with bivalve molluscs. Trends Food Sci Technol. 50:15–24.
   Google Scholar
• Botelho MJ, Vale C, Joaquim S, Costa ST, Soares F, Roque C, Matias D. 2018. Combined effect of temperature and nutritional regime on the elimination of the lipophilic toxin okadaic acid in the naturally contaminated wedge shell Donax trunculus. Chemosphere. 190:166–173.
   PubMed Web of Science ®Google Scholar
• Cerdal G, Wolff M. 1993. Feeding ecology of the crab Cancer polyodon in La Herradura Bay, northern Chile. II. Food spectrum and prey consumption. Mar Ecol Prog Ser. 100:119–125.
   Web of Science ®Google Scholar
• Chen T, Xu X, Wei J, Chen J, Miu R, Huang L, Zhou X, Fu Y, Yan R, Wang Z, et al. 2013. Food-borne disease outbreak of diarrhetic shellfish poisoning due to toxic mussel consumption: the first recorded outbreak in China. PLoS One. 8:65049. doi:10.1371/journal.pone.0065049
   Web of Science ®Google Scholar
• Chong J, Sepúlveda K, Ibáñez CM. 2006. Temporal variation in the diet of the red ling, Genypterus chilensis (Guichenot, 1881) in the coast off Talcahuano, Chile (36º32’S – 36º45’S). Revista de Biologi´a Marina y Oceanografi´a. 41:195–202.
   Google Scholar
• Chun-Hung Lee T, Long-Yan Fong F, Ho KC, Wang-Fat Lee F. 2016. The mechanism of diarrhetic shellfish poisoning toxin production in Prorocentrum spp.: physiological and molecular perspectives. Toxins. 8:272. doi:10.3390/toxins8100272
   Web of Science ®Google Scholar
• Díaz P, Molinet C, Cáceres M, Valle-Levinson A. 2011. Seasonal and intratidal distribution of Dinophysis spp. in a Chilean fjord. Harmful Algae. 10:155–164.
   Web of Science ®Google Scholar
• Díaz PA, Ruiz-Villarreal M, Pazos Y, Moita T, Reguera B. 2016. Climate variability and Dinophysis acuta blooms in an upwelling system. Harmful Algae. 53:145–159.
   PubMed Web of Science ®Google Scholar
• Duinker A, Bergslien M, Ø S, Olseng CD, Svardal A. 2007. The effect of size and age on depuration rates of diarrhetic shellfish toxins (DST) in mussels (Mytilus edulis L.). Harmful Algae. 6:288–300.
   Web of Science ®Google Scholar
• [EFSA] European Food Safety Authority. 2008. Marine biotoxins in shellfish – okadaic acid and analogues – scientific opinion of the panel on contaminants in the food chain. Efsa J. 589:1–62.
   Google Scholar
• [EFSA] European Food Safety Authority. 2009. European Food Safety Authority. Marine biotoxins in shellfish – summary on regulated marine biotoxins. Scientific opinion of the panel on contaminants in the food chain. Efsa J. 1306:1–23.
   Google Scholar
• EFSA Panel on Contaminants in the Food Chain (CONTAM). 2010. Statement on further elaboration of the consumption figures of 400 g shellfish meat on the basis of new consumption data. Efsa J. 1706:1–20.
   Google Scholar
• Escalera L, Pazos Y, Doval MD, Reguera B. 2012. A comparison of integrated and discrete depth sampling for monitoring toxic species of Dinophysis. Mar Pollut Bull. 64:106–113.
   PubMed Web of Science ®Google Scholar
• [EURLMB] European Union Reference Laboratory for Marine Biotoxins. 2015. EU-harmonised standard operating procedure for determination of lipophilic marine biotoxins in molluscs by LC-MS/MS. Version. 5. [accessed 2016 Feb 4]. http://www.aecosan.msssi.gob.es/AECOSAN/docs/documentos/laboratorios/LNRBM/ARCHIVO2EU-Harmonised-SOP-LIPO-LCMSMS_Version5.pdf
   Google Scholar
• European Commission. 2011. Commission Regulation (EU) No. 15/2011 of 10 January 2011 amending regulation (EC) No. 2074/2005 as regards recognized testing methods for detecting marine biotoxins in live bivalve molluscs. Off J Eur Union. L 6/3: p.1–15. 11. 01.11.
   Google Scholar
• [FAO] Food and Agriculture Organization of the United Nations. 2016. The state of world fisheries and aquaculture (SOFIA) FAO. Rome (Italy): Contributing to food security and nutrition for all. ISBN 978-92-5-109185-2; p. 200
   Google Scholar
• Farrell H, Gentien P, Fernand L, Lunven M, Reguera B, González-Gil S, Raine R. 2012. Scales characterising a high density thin layer of Dinophysis acuta Ehrenberg and its transport within a coastal jet. Harmful Algae. 15:36–46.
   Web of Science ®Google Scholar
• Fernandez B, Campillo JA, Martinez-Gomez C, Benedicto J. 2010. Antioxidant responses in gills of mussel (Mytilus galloprovincialis) as biomarkers of environmental stress along the Spanish Mediterranean coast. Aquatic Toxicology. 99:186–197.
   PubMed Web of Science ®Google Scholar
• Furumochi S, Onoda T, Cho Y, Fuwa H, Sasaki M, Yotsu-Yamashita M, Konoki K. 2016. Effect of carbon chain length in acyl coenzyme A on the efficiency of enzymatic transformation of okadaic acid to 7-O-acyl okadaic acid. Bioorg Med Chem Lett. 26:2992–2996.
   PubMed Web of Science ®Google Scholar
• García C, Contreras HR. 2014. Effects of both paralytic shellfish toxins and diarrhetic shellfish toxins in human poisoning: toxicity, distribution and biotransformation. In: Hay RM, editor. Shellfish human consumption, health implications and conservation concerns. 1 ed. Vol. 1. New York (NY): Nova Science Publishers; p. 345–384. ISBN 978–1–63321–195–7.
   Google Scholar
• García C, Oyaneder-Terrazas J, Contreras C, Del Campo M, Torres R, Contreras HR. 2016. Determination of the toxic variability of lipophilic biotoxins in marine bivalve and gastropod tissues treated with an industrial canning process. Food Addit Contam: Part A. 33:1711–1727.
   PubMed Web of Science ®Google Scholar
• García C, Oyaneder-Terrazas J, Contreras HR. 2018. Instrumental methods for detection of lipophilic marine toxins in endemic species from pacific austral fjords. In: Cano Carmona E, editor. Endemic species. 1 ed. Vol. 1. London (UK): IntechOpen. p. 1–34. doi:10.5772/intechopen.82438.
   Google Scholar
• Garcia C, Oyaneder-Terrazas J, Figueroa D, Díaz C, Mora R, Contreras HR. Oxidative effects in aquatic organisms exposed to lipophilic marine biotoxins. In: Kovács A, Nagy P, editors. Advances in marine biology. Vol. 1. 1 ed. New York (NY): Nova Science Publishers; 2017. p. 91–135. ISBN 978–1–53612–749–2.
   Google Scholar
• García C, Pérez F, Contreras C, Figueroa D, Barriga A, López-Rivera A, Araneda OF, Contreras HR. 2015. Saxitoxins and okadaic acid group: accumulation and distribution in invertebrate marine vectors from Southern Chile. Food Addit Contam: Part A. 32:984–1002.
   PubMed Web of Science ®Google Scholar
• García C, Rodriguez-Unda N, Contreras C, Barriga A, Lagos N. 2012. Lipophilic toxin profiles detected in farmed and benthic mussels populations from the most relevant production zones in Southern Chile. Food Addit Contam: Part A. 29:1011–1020.
   PubMed Web of Science ®Google Scholar
• García C, Seguel M, Uribe JC. 2013. Dynamics of toxic dinoflagellates’ blooms in the austral pacific region: distribution, toxicity and impact on aquaculture. In: Tobias RD, Lariree VM, editors. Dinoflagellates: biology, geographical distribution and economic importance. 1 ed. Vol. 1. New York (NY): Nova Science Publishers; p. 1–56. ISBN 978–1–62948–237–8.
   Google Scholar
• García C, Truan D, Lagos M, Santelices JP, Díaz JC, Lagos N. 2005. Metabolic transformation of dinophysistoxin-3 into dinophysistoxin-1 causes human intoxication by consumption of O-acyl-derivatives dinophysistoxins contaminated shellfish. J Toxicol Sci. 30:287–296.
   PubMedGoogle Scholar
• Glibert PM, Allen JI, Artioli J, Beusen A, Bouwman L, Harle J, Holmes R, Holt J. 2014. Vulnerability of coastal ecosystems to changes in harmful algal bloom distribution in response to climate change: projections based on model analysis. Glob Chang Biol. 20:3845–3858.
   PubMed Web of Science ®Google Scholar
• Hashimoto S, Nishimura K, Takahashi K, Itabashi Y. 2011. Evaluation of the possibility that free fatty acids cause false-positive result in diarrhetic shellfish poisoning mouse bioassay in actual use. Shokuhin Eiseigaku Zasshi. 52:194–198.
   PubMed Web of Science ®Google Scholar
• Hoppenrath M, Chomérat N, Horiguchi T, Schweikert M, Nagahama Y, Murray S. 2013. Taxonomy and phylogeny of the benthic Prorocentrum species (Dinophyceae)—a proposal and review. Harmful Algae. 27:1–28.
   Web of Science ®Google Scholar
• Hossen V, Jourdan-Da Silva N, Guillois-Becel Y, Marchal J, Krys S. 2009. Food poisoning outbreaks linked to mussels contaminated with okadaic acid and ester dinophysistoxin-3 in France, June 2009. Euro Surveill. 16. p. 1–7.
   Google Scholar
• Hu T, LeBlanc P, Burton IW, Walter JA, McCarron P, Melanson JE, Strangman WK, Wright JLC. 2017. Sulfated diesters of okadaic acid and DTX-1: self-protective precursors of diarrhetic shellfish poisoning (DSP) toxins. Harmful Algae. 63:85–93.
   PubMed Web of Science ®Google Scholar
• Jørgensen K, Cold U, Fischer K. 2008. Accumulation and depuration of okadaic acid esters in the European green crab (Carcinus maenas) during a feeding study. Toxicon. 51:468–472.
   PubMed Web of Science ®Google Scholar
• Konoki K, Onoda T, Watanabe R, Cho Y, Kaga S, Suzuki T, Yotsu-Yamashita M. 2013. In vitro acylation of okadaic acid in the presence of various bivalves’ extracts. Mar Drugs. 11:300–315. doi:10.3390/md11020300
   PubMed Web of Science ®Google Scholar
• Lindahl O, Lundve B, Johansen M. 2007. Toxicity of Dinophysis spp. in relation to population density and environmental conditions on the Swedish west coast. Harmful Algae. 6:218–231.
   Web of Science ®Google Scholar
• Mafra LL, Lopes D, Bonilauri VC, Uchida H, Suzuki T. 2015. Persistent contamination of octopuses and mussels with lipophilic shellfish toxins during spring Dinophysis blooms in a subtropical estuary. Mar Drugs. 13:3920–3935. doi:10.3390/md13063920
   PubMed Web of Science ®Google Scholar
• Matsushima R, Uchida H, Nagai S, Watanabe R, Kamio M, Nagai H, Kaneniwa M, Suzuki T. 2015. Assimilation, accumulation, and metabolism of dinophysistoxins (DTXs) and pectenotoxins (PTXs) in the several tissues of Japanese scallop Patinopecten yessoensis. Toxins. 7:5141–5154. doi:10.3390/toxins7124870
   PubMed Web of Science ®Google Scholar
• Minsal. 2010. Report program of surveillance of harmful algal blooms (HABs) in Chile. Santiago (Chile): Gobierno de Chile; p. 1–28.
   Google Scholar
• Moroño A, Arévalo F, Fernández ML, Maneiro J, Pazos Y, Salgado C, Blanco J. 2003. Accumulation and transformation of DSP toxins in mussels Mytilus galloprovincialis during a toxic episode caused by Dinophysis acuminata. Aquatic Toxicology. 62:269–280.
   PubMed Web of Science ®Google Scholar
• Munday R, Reeve J. 2013. Risk assessment of shellfish toxins. Toxins. 5:2109–2137. doi:10.3390/toxins5112109
   PubMed Web of Science ®Google Scholar
• Oyaneder-Terrazas J, Contreras HR, García C. 2017. Prevalence, variability and bioconcentration of saxitoxin-group in different marine species present in the food chain. Toxins. 9(6):190.
   Web of Science ®Google Scholar
• Pazos AJ, Sanchez JL, Roman G, Perez-Parallé M, Abad M. 2003. Seasonal changes in lipid classes and fatty acid composition in the digestive gland of Pecten maximus. Comp Biochem Physiol B. 134:367–380.
   PubMed Web of Science ®Google Scholar
• Prego-Faraldo MV, Valdiglesias V, Méndez J, Eirín-López JM. 2013. Okadaic acid meet and greet: an insight into detection methods, response strategies and genotoxic effects in marine invertebrates. Mar Drugs. 11:2829–2845. doi:10.3390/md11082829
   PubMed Web of Science ®Google Scholar
• Rasmussen SA, Andersen AJC, Andersen NG, Nielsen KF, Hansen PJ, Ostenfeld Larsen T. 2016. Chemical diversity, origin, and analysis of phycotoxins. J Nat Prod. 79:662−673.
   PubMed Web of Science ®Google Scholar
• Reguera B, Riobó P, Rodríguez F, Díaz PA, Pizarro G, Paz B, Franco JM, Blanco J. 2014. Dinophysis toxins: causative organisms, distribution and fate in shellfish. Mar Drugs. 12:394–461. doi:10.3390/md12010394
   PubMed Web of Science ®Google Scholar
• Reguera B, Velo-Suárez L, Raine R, Gil Park M. 2012. Harmful Dinophysis species: a review. Harmful Algae. 14:87–106.
   Web of Science ®Google Scholar
• Rossignoli AE, Blanco J. 2008. Cellular distribution of okadaic acid in the digestive gland of Mytilus galloprovincialis (Lamarck, 1819). Toxicon. 52:957–959.
   PubMed Web of Science ®Google Scholar
• Rossignoli AE, Blanco J. 2010. Subcellular distribution of okadaic acid in the digestive gland of Mytilus galloprovincialis: first evidences of lipoprotein binding to okadaic acid. Toxicon. 55:221–226.
   PubMed Web of Science ®Google Scholar
• Rossignoli AE, Fernández D, Acosta CP, Blanco J. 2011b. Microencapsulation of okadaic acid as a tool for studying the accumulation of DSP toxins in mussels. Mar Environ Res. 71:91–93.
   PubMed Web of Science ®Google Scholar
• Rossignoli AE, Fernández D, Regueiro J, Mariño C, Blanco J. 2011a. Esterification of okadaic acid in the mussel Mytilus galloprovincialis. Toxicon. 57:712–720.
   PubMed Web of Science ®Google Scholar
• Seguel M, Sfeir A. 2010. Distribution of marine toxins and cysts of dinoflagellates in western channels of the region of Aysén. Cienc Tecnol. 33:43–55.
   Google Scholar
• Sernapesca. 2015. Health program of bivalve molluscs for export. Valparaiso: Chile; p. 1–69.
   Google Scholar
• Smith JL, Tong M, Fux E, Anderson DM. 2012. Toxin production, retention, and extracellular release by Dinophysis acuminata during extended stationary phase and culture decline. Harmful Algae. 19:125–132.
   Web of Science ®Google Scholar
• Suzuki H. 2012. Susceptibility of different mice strains to okadaic acid, a diarrhetic shellfish poisoning toxin. Food Addit Contam: Part A. 29:1307–1310. doi:10.1080/19440049.2012.685892
   PubMed Web of Science ®Google Scholar
• Suzuki H. 2014. Influence of body weight of mice on the susceptibility to okadaic acid, a diarrhetic shellfish poisoning toxin. Food Addit Contam: Part A. 31:719–722.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Yoshizawa R, Kawamura T, Yamasaki M. 1996. Interference of free fatty acids from the hepatopancreas of mussels with the mouse bioassay for shellfish toxins. Lipids. 31:641–645.
   PubMed Web of Science ®Google Scholar
• Svensson S, FöRlin L. 2004. Analysis of the importance of lipid breakdown for elimination of okadaic acid (diarrhetic shellfish toxin) in mussels, Mytilus edulis: results from a field study and a laboratory experiment. Aquatic Toxicology. 66:405–418.
   PubMed Web of Science ®Google Scholar
• Taylor M, McIntyre L, Ritson M, Stone J, Bronson R, Bitzikos O, Rourke W, Galanis E. 2013. Outbreak of diarrhetic shellfish poisoning associated with mussels, British Columbia, Canada. Mar Drugs. 11:1669–1676.
   PubMed Web of Science ®Google Scholar
• Tor Nielsen L, Juel Hansen P, Krock B, Vismann B. 2016. Accumulation, transformation and breakdown of DSP toxins from the toxic dinoflagellate Dinophysis acuta in blue mussels, Mytilus edulis. Toxicon. 117:84–93.
   PubMed Web of Science ®Google Scholar
• Tor Nielsen L, Krock B, Hansen PJ. 2013. Production and excretion of okadaic acid, pectenotoxin-2 and a novel dinophysistoxin from the DSP-causing marine dinoflagellate Dinophysis acuta – effects of light, food availability and growth phase. Harmful Algae. 23:34–45.
   Web of Science ®Google Scholar
• Torgersen T, Lindegarth S, Ungfors A, Sandvik M. 2008. Profiles and levels of fatty acid esters of okadaic acid group toxins and pectenotoxins during toxin depuration, part I: brown crab (Cancer pagurus). Toxicon. 52:407–417.
   PubMed Web of Science ®Google Scholar
• Turner AD, Goya AB. 2016. Comparison of four rapid test kits for the detection of okadaic acid- group toxins in bivalve shellfish from Argentina. Food Control. 59:829–840.
   Web of Science ®Google Scholar
• Turner JT. 2014. Planktonic marine copepods and harmful algae. Harmful Algae. 32::81–93.
   Web of Science ®Google Scholar
• Vasconcelos V, Azevedo J, Silva M, Ramos V. 2010. Effects of marine toxins on the reproduction and early stages development of aquatic organisms. Mar Drugs. 8:59–79.
   PubMed Web of Science ®Google Scholar
• Visciano P, Schirone M, Berti M, Milandri A, Tofalo R, Suzzi G. 2016. Marine biotoxins: occurrence, toxicity, regulatory limits and reference methods. Front Microbiol. 7:1051. doi:10.3389/fmicb.2016.01051
   PubMed Web of Science ®Google Scholar
• Yap CK, Hatta Y, Edward FB, Tan SG. 2008. Distribution of heavy metal concentrations (Cd, Cu, Ni, Fe and Zn) in the different soft tissues and shells of wild mussels Perna viridis collected from Bagan Tiang and Kuala Kedah. Malays Appl Biol. 37:1–10.
   Google Scholar
• Zamorano R, Marín M, Cabrera F, Figueroa D, Contreras C, Barriga A, Lagos N, García C. 2013. Determination of the variability of both hydrophilic and lipophilic toxins in endemic wild bivalves and carnivorous gastropods from the southern part of Chile. Food Addit Contam: Part A. 30:1660–1677.
   PubMed Web of Science ®Google Scholar