[en] Vegetables and fruits can potentially accumulate cyanotoxins after water contaminated with cyanobacteria is used for irrigation. We developed and validated an analytical method to quantify eight microcystin congeners (MCs) and nodularin (NOD) using ultra high-performance liquid chromatography coupled with tandem mass spectrometry (UHPLC-MS/MS) in three different matrices. Strawberries, carrots and lettuce are selected as model matrices to represent the fruits/berries, leafy and root vegetables, sequentially. The validation of a UHPLC-MS/MS method in the strawberry matrix is novel. Matrix effects are observed in all three matrices. Our methodology uses matrix-matched calibration curves to compensate for the matrix effect. The implementation of our method on 103 samples, containing nine different sorts of fruits and vegetables from the Belgian market, showed no presence of MCs or NOD. However, the recoveries of our quality controls showed the effectiveness of our method, illustrating that the use of this method in future research or monitoring as well as in official food controls in fruit and vegetable matrices is valid.
Disciplines :
Food science Chemistry Public health, health care sciences & services
Author, co-author :
Van Hassel, Wannes ; Université de Liège - ULiège > Integrative Biological Sciences (InBioS)
Masquelier, Julien
Andjelkovic, Mirjana
Rajkovic, Andreja
Language :
English
Title :
Towards a Better Quantification of Cyanotoxins in Fruits and Vegetables: Validation and Application of an UHPLC-MS/MS-Based Method on Belgian Products
Publication date :
20 October 2022
Journal title :
Separations
eISSN :
2297-8739
Publisher :
MDPI AG
Special issue title :
Development of Highly Efficient Separation-Based Analytical Methods for Food Integrity Assurance
H2020 - 965173 - Imptox - AN INNOVATIVE ANALYTICAL PLATFORM TO INVESTIGATE THE EFFECT AND TOXICITY OF MICRO AND NANO PLASTICS COMBINED WITH ENVIRONMENTAL CONTAMINANTS ON THE RISK OF ALLERGIC DISEASE IN PRECLINICAL AND CLINICAL
Name of the research project :
SP 21/5 CYANTIR 1
Funders :
FPS Health Federal Public Service Health, Food Chain Safety and Environment [BE] EU - European Union [BE]
Falconer I.R. Buckley T. Runnegar M.T.C. Biological Half-Life, Organ Distribution and Excretion of 125I-Labelled Toxic Peptide from the Blue-Green Alga Microcystis aeruginosa Aust. J. Biol. Sci. 1986 39 17 21 10.1071/BI9860017 3096266
Mahmood N.A. Carmichael W.W. Anatoxin-a(s), an Anticholinesterase from the Cyanobacterium Anabaena Flos-Aquae NRC-525-17 Toxicon 1987 25 1221 1227 10.1016/0041-0101(87)90140-1
Mahmood N.A. Carmichael W.W. Paralytic Shellfish Poisons Produced by the Freshwater Cyanobacterium Aphanizomenon Flos-Aquae NH-5 Toxicon 1986 24 175 186 10.1016/0041-0101(86)90120-0
Namikoshi M. Rinehart K.L. Sakai R. Stotts R.R. Dahlem A.M. Beasley V.R. Carmichael W.W. Evans W.R. Identification of 12 Hepatotoxins from a Homer Lake Bloom of the Cyanobacteria Microcystis Aeruginosa, Microcystis Viridis, and Microcystis Wesenbergii: Nine New Microcystins J. Org. Chem. 1992 57 866 872 10.1021/jo00029a016
Welker M. Brunke M. Preussel K. Lippert I. von Döhren H. Diversity and Distribution of Microcystis (Cyanobacteria) Oligopeptide Chemotypes from Natural Communities Studied by Single-Colony Mass Spectrometry Microbiology (Reading) 2004 150 1785 1796 10.1099/mic.0.26947-0
Edwards C. Beattie K.A. Scrimgeour C.M. Codd G.A. Identification of Anatoxin-A in Benthic Cyanobacteria (Blue-Green Algae) and in Associated Dog Poisonings at Loch Insh, Scotland Toxicon 1992 30 1165 1175 10.1016/0041-0101(92)90432-5
Harada K.I. Ohtani I. Iwamoto K. Suzuki M. Watanabe M.F. Watanabe M. Terao K. Isolation of Cylindrospermopsin from a Cyanobacterium Umezakia Natans and Its Screening Method Toxicon 1994 32 73 84 10.1016/0041-0101(94)90023-X
Dahlmann J. Rühl A. Hummert C. Liebezeit G. Carlsson P. Granéli E. Different Methods for Toxin Analysis in the Cyanobacterium Nodularia Spumigena (Cyanophyceae) Toxicon 2001 39 1183 1190 10.1016/S0041-0101(00)00256-7
Testai E. Buratti F.M. Funari E. Manganelli M. Vichi S. Arnich N. Fessard V. Sialehaamoa A. Review and Analysis of Occurrence, Exposure and Toxicity of Cyanobacteria Toxins in Food EFSA Extern. Sci. Rep. 2016 13 998E 10.2903/sp.efsa.2016.EN-998
Abdallah M.F. Van Hassel W.H.R. Andjelkovic M. Wilmotte A. Rajkovic A. Cyanotoxins and Food Contamination in Developing Countries: Review of Their Types, Toxicity, Analysis, Occurrence and Mitigation Strategies Toxins 2021 13 786 10.3390/toxins13110786
Mantzouki E. Lürling M. Fastner J. de Senerpont Domis L. Wilk-Wo´zniak E. Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins Toxins 2018 10 156 10.3390/toxins10040156 29652856
Mazur-Marzec H. Sutryk K. Kobos J. Hebel A. Hohlfeld N. Błaszczyk A. Toruńska A. Kaczkowska M.J. Łysiak-Pastuszak E. Kraśniewski W. et al. Occurrence of Cyanobacteria and Cyanotoxin in the Southern Baltic Proper. Filamentous Cyanobacteria versus Single-Celled Picocyanobacteria Hydrobiologia 2013 701 235 252 10.1007/s10750-012-1278-7
MacKintosh C. Beattie K.A. Klumpp S. Cohen P. Codd G.A. Cyanobacterial Microcystin-LR Is a Potent and Specific Inhibitor of Protein Phosphatases 1 and 2A from Both Mammals and Higher Plants FEBS Lett. 1990 264 187 192 10.1016/0014-5793(90)80245-E
Runnegar M.T. Kong S. Berndt N. Protein Phosphatase Inhibition and in Vivo Hepatotoxicity of Microcystins Am. J. Physiol. -Gastrointest. Liver Physiol. 1993 265 G224 G230 10.1152/ajpgi.1993.265.2.G224 8396333
Fischer A. Hoeger S.J. Stemmer K. Feurstein D.J. Knobeloch D. Nussler A. Dietrich D.R. The Role of Organic Anion Transporting Polypeptides (OATPs/SLCOs) in the Toxicity of Different Microcystin Congeners in Vitro: A Comparison of Primary Human Hepatocytes and OATP-Transfected HEK293 Cells Toxicol. Appl. Pharmacol. 2010 245 9 20 10.1016/j.taap.2010.02.006
Feurstein D. Holst K. Fischer A. Dietrich D.R. Oatp-Associated Uptake and Toxicity of Microcystins in Primary Murine Whole Brain Cells Toxicol. Appl. Pharmacol. 2009 234 247 255 10.1016/j.taap.2008.10.011
Hawkins P.R. Chandrasena N.R. Jones G.J. Humpage A.R. Falconer I.R. Isolation and Toxicity of Cylindrospermopsis Raciborskii from an Ornamental Lake Toxicon 1997 35 341 346 10.1016/S0041-0101(96)00185-7
Antunes J.T. Leão P.N. Vasconcelos V.M. Cylindrospermopsis Raciborskii: Review of the Distribution, Phylogeography, and Ecophysiology of a Global Invasive Species Front Microbiol. 2015 6 473 10.3389/fmicb.2015.00473
Merel S. Villarín M.C. Chung K. Snyder S. Spatial and Thematic Distribution of Research on Cyanotoxins Toxicon 2013 76 118 131 10.1016/j.toxicon.2013.09.008
Hoeger S.J. Shaw G. Hitzfeld B.C. Dietrich D.R. Occurrence and Elimination of Cyanobacterial Toxins in Two Australian Drinking Water Treatment Plants Toxicon 2004 43 639 649 10.1016/j.toxicon.2004.02.019
Clemente Z. Busato R.H. Oliveira Ribeiro C.A. Cestari M.M. Ramsdorf W.A. Magalhães V.F. Wosiack A.C. Silva de Assis H.C. Analyses of Paralytic Shellfish Toxins and Biomarkers in a Southern Brazilian Reservoir Toxicon 2010 55 396 406 10.1016/j.toxicon.2009.09.003 19778550
Ballot A. Fastner J. Lentz M. Wiedner C. First Report of Anatoxin-a-Producing Cyanobacterium Aphanizomenon Issatschenkoi in Northeastern Germany Toxicon 2010 56 964 971 10.1016/j.toxicon.2010.06.021 20615427
Codd G.A. Metcalf J.S. Beattie K.A. Retention of Microcystis Aeruginosa and Microcystin by Salad Lettuce (Lactuca Sativa) after Spray Irrigation with Water Containing Cyanobacteria Toxicon 1999 37 1181 1185 10.1016/S0041-0101(98)00244-X
Chen J. Song L. Dai J. Gan N. Liu Z. Effects of Microcystins on the Growth and the Activity of Superoxide Dismutase and Peroxidase of Rape (Brassica Napus L.) and Rice (Oryza Sativa L.) Toxicon 2004 43 393 400 10.1016/j.toxicon.2004.01.011
Pflugmacher S. Wiegand C. Beattie K.A. Krause E. Steinberg C.E.W. Codd G.A. Uptake, Effects, and Metabolism of Cyanobacterial Toxins in the Emergent Reed Plant Phragmites Australis (CAV.) Trin. Ex Steud Environ. Toxicol. Chem. 2001 20 846 852 10.1002/etc.5620200421
McElhiney J. Lawton L.A. Leifert C. Investigations into the Inhibitory Effects of Microcystins on Plant Growth, and the Toxicity of Plant Tissues Following Exposure Toxicon 2001 39 1411 1420 10.1016/S0041-0101(01)00100-3
Järvenpää S. Lundberg-Niinistö C. Spoof L. Sjövall O. Tyystjärvi E. Meriluoto J. Effects of Microcystins on Broccoli and Mustard, and Analysis of Accumulated Toxin by Liquid Chromatography–Mass Spectrometry Toxicon 2007 49 865 874 10.1016/j.toxicon.2006.12.008
Li Y.-W. Zhan X.-J. Xiang L. Deng Z.-S. Huang B.-H. Wen H.-F. Sun T.-F. Cai Q.-Y. Li H. Mo C.-H. Analysis of Trace Microcystins in Vegetables Using Solid-Phase Extraction Followed by High Performance Liquid Chromatography Triple-Quadrupole Mass Spectrometry J. Agric. Food Chem. 2014 62 11831 11839 10.1021/jf5033075
Prieto A.I. Guzmán-Guillén R. Díez-Quijada L. Campos A. Vasconcelos V. Jos Á. Cameán A.M. Validation of a Method for Cylindrospermopsin Determination in Vegetables: Application to Real Samples Such as Lettuce (Lactuca Sativa L.) Toxins 2018 10 63 10.3390/toxins10020063
Manubolu M. Lee J. Riedl K.M. Kua Z.X. Collart L.P. Ludsin S.A. Optimization of Extraction Methods for Quantification of Microcystin-LR and Microcystin-RR in Fish, Vegetable, and Soil Matrices Using UPLC–MS/MS Harmful Algae 2018 76 47 57 10.1016/j.hal.2018.04.009
Díez-Quijada L. Guzmán-Guillén R. Prieto Ortega A.I. Llana-Ruíz-Cabello M. Campos A. Vasconcelos V. Jos Á. Cameán A.M. New Method for Simultaneous Determination of Microcystins and Cylindrospermopsin in Vegetable Matrices by SPE-UPLC-MS/MS Toxins 2018 10 406 10.3390/toxins10100406 30297653
Lee S. Jiang X. Manubolu M. Riedl K. Ludsin S.A. Martin J.F. Lee J. Fresh Produce and Their Soils Accumulate Cyanotoxins from Irrigation Water: Implications for Public Health and Food Security Food Res. Int. 2017 102 234 245 10.1016/j.foodres.2017.09.079 29195944
Crush J.R. Briggs L.R. Sprosen J.M. Nichols S.N. Effect of Irrigation with Lake Water Containing Microcystins on Microcystin Content and Growth of Ryegrass, Clover, Rape, and Lettuce Environ. Toxicol. 2008 23 246 252 10.1002/tox.20331 18214908
Mohamed Z.A. Al Shehri A.M. Microcystins in Groundwater Wells and Their Accumulation in Vegetable Plants Irrigated with Contaminated Waters in Saudi Arabia J. Hazard. Mater. 2009 172 310 315 10.1016/j.jhazmat.2009.07.010
Hereman T.C. Bittencourt-Oliveira M.d.C. Bioaccumulation of Microcystins in Lettuce J. Phycol. 2012 48 1535 1537 10.1111/jpy.12006
Levizou E. Statiris G. Papadimitriou T. Laspidou C.S. Kormas K.A. Lettuce Facing Microcystins-Rich Irrigation Water at Different Developmental Stages: Effects on Plant Performance and Microcystins Bioaccumulation Ecotoxicol. Environ. Saf. 2017 143 193 200 10.1016/j.ecoenv.2017.05.037
do Bittencourt-Oliveira M.C. Cordeiro-Araújo M.K. Chia M.A. Arruda-Neto J.D.d.T. de Oliveira Ê.T. dos Santos F. Lettuce Irrigated with Contaminated Water: Photosynthetic Effects, Antioxidative Response and Bioaccumulation of Microcystin Congeners Ecotoxicol. Environ. Saf. 2016 128 83 90 10.1016/j.ecoenv.2016.02.014
Cordeiro-Araújo M.K. Chia M.A. de Arruda-Neto J.D.T. Tornisielo V.L. Vilca F.Z. do Bittencourt-Oliveira M.C. Microcystin-LR Bioaccumulation and Depuration Kinetics in Lettuce and Arugula: Human Health Risk Assessment Sci. Total Environ. 2016 566–567 1379 1386 10.1016/j.scitotenv.2016.05.204
Cordeiro-Araújo M.K. Chia M.A. Bittencourt-Oliveira M.d.C. Potential Human Health Risk Assessment of Cylindrospermopsin Accumulation and Depuration in Lettuce and Arugula Harmful Algae 2017 68 217 223 10.1016/j.hal.2017.08.010
Llana-Ruiz-Cabello M. Jos A. Cameán A. Oliveira F. Barreiro A. Machado J. Azevedo J. Pinto E. Almeida A. Campos A. et al. Analysis of the Use of Cylindrospermopsin and/or Microcystin-Contaminated Water in the Growth, Mineral Content, and Contamination of Spinacia Oleracea and Lactuca Sativa Toxins 2019 11 624 10.3390/toxins11110624
Machado J. Campos A. Vasconcelos V. Freitas M. Effects of Microcystin-LR and Cylindrospermopsin on Plant-Soil Systems: A Review of Their Relevance for Agricultural Plant Quality and Public Health Environ. Res. 2017 153 191 204 10.1016/j.envres.2016.09.015 27702441
Levizou E. Papadimitriou T. Papavasileiou E. Papadimitriou N. Kormas K.A. Root Vegetables Bioaccumulate Microcystins-LR in a Developmental Stage-Dependent Manner under Realistic Exposure Scenario: The Case of Carrot and Radish Agric. Water Manag. 2020 240 106274 10.1016/j.agwat.2020.106274
Chen J. Han F.X. Wang F. Zhang H. Shi Z. Accumulation and Phytotoxicity of Microcystin-LR in Rice (Oryza Sativa) Ecotoxicol. Environ. Saf. 2012 76 193 199 10.1016/j.ecoenv.2011.09.022 22036264
Wijewickrama M.M. Manage P.M. Accumulation of Microcystin-LR in Grains of Two Rice Varieties (Oryza Sativa L.) and a Leafy Vegetable, Ipomoea Aquatica Toxins 2019 11 432 10.3390/toxins11080432 31344839
Corbel S. Mougin C. Nélieu S. Delarue G. Bouaïcha N. Evaluation of the Transfer and the Accumulation of Microcystins in Tomato (Solanum Lycopersicum Cultivar MicroTom) Tissues Using a Cyanobacterial Extract Containing Microcystins and the Radiolabeled Microcystin-LR (14C-MC-LR) Sci. Total Environ. 2016 541 1052 1058 10.1016/j.scitotenv.2015.10.004
Romero-Oliva C.S. Contardo-Jara V. Block T. Pflugmacher S. Accumulation of Microcystin Congeners in Different Aquatic Plants and Crops – A Case Study from Lake Amatitlán, Guatemala Ecotoxicol. Environ. Saf. 2014 102 121 128 10.1016/j.ecoenv.2014.01.031
Peuthert A. Chakrabarti S. Pflugmacher S. Uptake of Microcystins-LR and -LF (Cyanobacterial Toxins) in Seedlings of Several Important Agricultural Plant Species and the Correlation with Cellular Damage (Lipid Peroxidation) Environ. Toxicol. 2007 22 436 442 10.1002/tox.20266
Xiang L. Li Y.-W. Wang Z.-R. Liu B.-L. Zhao H.-M. Li H. Cai Q.-Y. Mo C.-H. Li Q.X. Bioaccumulation and Phytotoxicity and Human Health Risk from Microcystin-LR under Various Treatments: A Pot Study Toxins 2020 12 523 10.3390/toxins12080523
Chen J. Dai J. Zhang H. Wang C. Zhou G. Han Z. Liu Z. Bioaccumulation of Microcystin and Its Oxidative Stress in the Apple (Malus Pumila) Ecotoxicology 2010 19 796 803 10.1007/s10646-009-0456-5
Corbel S. Bouaïcha N. Nélieu S. Mougin C. Soil Irrigation with Water and Toxic Cyanobacterial Microcystins Accelerates Tomato Development Env. Chem. Lett. 2015 13 447 452 10.1007/s10311-015-0518-2
Haida M. El Khalloufi F. Mugani R. Redouane E.M. Campos A. Vasconcelos V. Oudra B. Effects of Irrigation with Microcystin-Containing Water on Growth, Physiology, and Antioxidant Defense in Strawberry Fragaria Vulgaris under Hydroponic Culture Toxins 2022 14 198 10.3390/toxins14030198 35324694
Gutiérrez-Praena D. Campos A. Azevedo J. Neves J. Freitas M. Guzmán-Guillén R. Cameán A.M. Renaut J. Vasconcelos V. Exposure of Lycopersicon Esculentum to Microcystin-LR: Effects in the Leaf Proteome and Toxin Translocation from Water to Leaves and Fruits Toxins 2014 6 1837 1854 10.3390/toxins6061837 24921194
Van Hassel W.H.R. Huybrechts B. Masquelier J. Wilmotte A. Andjelkovic M. Development, Validation and Application of a Targeted LC-MS Method for Quantification of Microcystins and Nodularin: Towards a Better Characterization of Drinking Water Water 2022 14 1195 10.3390/w14081195
Van Hassel W.H.R. Ahn A.-C. Huybrechts B. Masquelier J. Wilmotte A. Andjelkovic M. LC-MS/MS Validation and Quantification of Cyanotoxins in Algal Food Supplements from the Belgium Market and Their Molecular Origins Toxins 2022 14 513 10.3390/toxins14080513
Van Hassel W.H.R. Andjelkovic M. Durieu B. Marroquin V.A. Masquelier J. Huybrechts B. Wilmotte A. A Summer of Cyanobacterial Blooms in Belgian Waterbodies: Microcystin Quantification and Molecular Characterizations Toxins 2022 14 61 10.3390/toxins14010061
P.O. of the E. Union, CELEX1, 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 (Text with EEA Relevance) (Notified under Document Number C(2002) 3044) Available online: http://op.europa.eu/en/publication-detail/-/publication/ed928116-a955-4a84-b10a-cf7a82bad858/language-en (accessed on 30 November 2020)