[en] Cyanotoxins have gained global public interest due to their potential to bioaccumulate in food, which threatens human health. Bloom formation is usually enhanced under Mediterranean, subtropical and tropical climates which are the dominant climate types in developing countries. In this context, we present an up-to-date overview of cyanotoxins (types, toxic effects, analysis, occurrence, and mitigation) with a special focus on their contamination in (sea)food from all the developing countries in Africa, Asia, and Latin America as this has received less attention. A total of 65 publications have been found (from 2000 until October 2021) reporting the contamination by one or more cyanotoxins in seafood and edible plants (five papers). Only Brazil and China conducted more research on cyanotoxin contamination in food in comparison to other countries. The majority of research focused on the detection of microcystins using different analytical methods. The detected levels mostly surpassed the provisional tolerable daily intake limit set by the World Health Organization, indicating a real risk to the exposed population. Assessment of cyanotoxin contamination in foods from developing countries still requires further investigations by conducting more survey studies, especially the simultaneous detection of multiple categories of cyanotoxins in food.
Precision for document type :
Review article
Disciplines :
Pharmacy, pharmacology & toxicology Food science
Author, co-author :
Abdallah, Mohamed Fathi ; UGent - Universiteit Gent [BE] > Faculty of Bioscience Engineering > Department of Food Technology, Safety and Health
Van Hassel, Wannes H R ; Sciensano, Chemical and Physical Health Risks, Organic Contaminants and Additives, Leuvensesteenweg 17, 3080 Tervuren, Belgium
Andjelkovic, Mirjana ; Sciensano Research Institute, Chemical and Physical Health Risks, Risk and Health Impact Assessment, Ju-liette Wytsmanstreet 14, 1050 Brussels, Belgium
Wilmotte, Annick ; BCCM/ULC Cyanobacteria Collection, InBios-Centre for Protein Engineering, Université de Liège, 4000 Liège, Belgium
Rajkovic, Andreja ; Department of Food Technology, Safety and Health, Faculty of Bioscience Engineering, Ghent University, 9000 Ghent, Belgium
Language :
English
Title :
Cyanotoxins and Food Contamination in Developing Countries: Review of Their Types, Toxicity, Analysis, Occurrence and Mitigation Strategies.
Acknowledgments: The APC was funded by VLIRUOS Global Minds Grant 2021’ (AF-CYSTIN-milk project) from Ghent University. The work presented here is part of collective research effort done in the lab of Andreja Rajkovic regarding health impacts of foodborne and waterborne exposure to pathogens, toxins and contaminants.This work received funding from (1) the Ghent University Special Research Fund (BOF), grant number BOF20/PDO/032 which is a postdoctoral mandate awarded to M.F.A., (2) VLIRUOS Global Minds Grant 2021? (AF-CYSTIN-milk project) from Ghent University awarded to M.F.A., and (3) Cyantir project (www.cyantir.ugent.be) which is funded by Federal Public Service. Health, Food chain safety and Environment in Belgium and provides PhD scholarship to W.H.R.V.H. The Cyantir project is coordinated by A.R. Both M.A. (Senior Research Scientist at Sciensano) and A.W. (Senior Research Associate of the FRS-FNRS) are partners in Cyantir project.
Merel, S.; Walker, D.; Chicana, R.; Snyder, S.; Baurès, E.; Thomas, O. State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ. Int. 2013, 59, 303–327. [CrossRef] [PubMed]
Buratti, F.M.; Manganelli, M.; Vichi, S.; Stefanelli, M.; Scardala, S.; Testai, E.; Funari, E. Cyanotoxins: Producing organisms, occurrence, toxicity, mechanism of action and human health toxicological risk evaluation. Arch. Toxicol. 2017, 91, 1049–1130. [CrossRef]
Chen, J.; Zhang, D.; Xie, P.; Wang, Q.; Ma, Z. Simultaneous determination of microcystin contaminations in various vertebrates (fish, turtle, duck and water bird) from a large eutrophic Chinese lake, Lake Taihu, with toxic Microcystis blooms. Sci. Total Environ. 2009, 407, 3317–3322. [CrossRef] [PubMed]
Žegura, B.; Štraser, A.; Filipič, M. Genotoxicity and potential carcinogenicity of cyanobacterial toxins—A review. Mutat. Res. Rev. Mutat. Res. 2011, 727, 16–41. [CrossRef]
El-Shehawy, R.; Gorokhova, E.; Fernández-Piñas, F.; del Campo, F.F. Global warming and hepatotoxin production by cyanobacte-ria: What can we learn from experiments? Water Res. 2012, 46, 1420–1429. [CrossRef]
Testai, E.; Scardala, S.; Vichi, S.; Buratti, F.M.; Funari, E. Risk to human health associated with the environmental occurrence of cyanobacterial neurotoxic alkaloids anatoxins and saxitoxins. Crit. Rev. Toxicol. 2016, 46, 385–419. [CrossRef]
Reichwaldt, E.S.; Ghadouani, A. Effects of rainfall patterns on toxic cyanobacterial blooms in a changing climate: Between simplistic scenarios and complex dynamics. Water Res. 2012, 46, 1372–1393. [CrossRef] [PubMed]
Wang, H.; Xu, C.; Liu, Y.; Jeppesen, E.; Svenning, J.C.; Wu, J.; Zhang, W.; Zhou, T.; Wang, P.; Nangombe, S.; et al. From unusual suspect to serial killer: Cyanotoxins boosted by climate change may jeopardize megafauna. Innovation 2021, 2, 100092. [CrossRef]
Rastogi, R.P.; Madamwar, D.; Incharoensakdi, A. Bloom dynamics of cyanobacteria and their toxins: Environmental health impacts and mitigation strategies. Front. Microbiol. 2015, 6, 1–22. [CrossRef] [PubMed]
Zurawell, R.W.; Chen, H.; Burke, J.M.; Prepas, E.E. Hepatotoxic cyanobacteria: A review of the biological importance of microcystins in freshwater environments. J. Toxicol. Environ. Health Part B Crit. Rev. 2005, 8, 1–37. [CrossRef] [PubMed]
Neilan, B.A.; Pearson, L.A.; Muenchhoff, J.; Moffitt, M.C.; Dittmann, E. Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environ. Microbiol. 2013, 15, 1239–1253. [CrossRef] [PubMed]
Gutiérrez-Praena, D.; Jos, Á.; Pichardo, S.; Moreno, I.M.; Cameán, A.M. Presence and bioaccumulation of microcystins and cylindrospermopsin in food and the effectiveness of some cooking techniques at decreasing their concentrations: A review. Food Chem. Toxicol. 2013, 53, 139–152. [CrossRef]
Massey, I.Y.; Yang, F.; Ding, Z.; Yang, S.; Guo, J.; Tezi, C.; Al-Osman, M.; Kamegni, R.B.; Zeng, W. Exposure routes and health effects of microcystins on animals and humans: A mini-review. Toxicon 2018, 151, 156–162. [CrossRef]
Malbrouck, C.; Kestemont, P. Effects of microcystins on fish. Environ. Toxicol. Chem. 2006, 25, 72–86. [CrossRef]
Ferrão-Filho, A.D.S.; Kozlowsky-Suzuki, B. Cyanotoxins: Bioaccumulation and effects on aquatic animals. Mar. Drugs 2011, 9, 2729–2772. [CrossRef]
Nielsen, M.C.; Jiang, S.C. Can cyanotoxins penetrate human skin during water recreation to cause negative health effects? Harmful Algae 2020, 98, 101872. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
Corbel, S.; Mougin, C.; Bouaïcha, N. Cyanobacterial toxins: Modes of actions, fate in aquatic and soil ecosystems, phytotoxicity and bioaccumulation in agricultural crops. Chemosphere 2014, 96, 1–15. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
Bittencourt-Oliveira, M.d.C.; Cordeiro-Araújo, M.K.; Chia, M.A.; Arruda-Neto, J.D.d.T.; Oliveira, Ê.T.d.; dos Santos, F. Lettuce irrigated with contaminated water: Photosynthetic effects, antioxidative response and bioaccumulation of microcystin congeners. Ecotoxicol. Environ. Saf. 2016, 128, 83–90. [CrossRef]
Zhang, Y.; Whalen, J.K.; Sauvé, S. Phytotoxicity and bioconcentration of microcystins in agricultural plants: Meta-analysis and risk assessment. Environ. Pollut. 2021, 272, 115966. [CrossRef]
Testai, E.; Buratti, F.M.; Funari, E.; Manganelli, M.; Vichi, S.; Arnich, N.; Biré, R.; Fessard, V.; Sialehaamoa, A. Review and analysis of occurrence, exposure and toxicity of cyanobacteria toxins in food. EFSA Supporting Publ. 2017, 13, 1–309. [CrossRef]
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. [CrossRef]
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. [CrossRef]
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. [CrossRef]
Giannuzzi, L.; Sedan, D.; Echenique, R.; Andrinolo, D. An acute case of intoxication with cyanobacteria and cyanotoxins in recreational water in Salto Grande Dam, Argentina. Mar. Drugs 2011, 9, 2164–2175. [CrossRef] [PubMed]
Vidal, F.; Sedan, D.; D’Agostino, D.; Cavalieri, M.L.; Mullen, E.; Parot Varela, M.M.; Flores, C.; Caixach, J.; Andrinolo, D. Recreational exposure during algal bloom in carrasco beach, uruguay: A liver failure case report. Toxins 2017, 9, 267. [CrossRef]
Metcalf, J.S.; Richer, R.; Cox, P.A.; Codd, G.A. Cyanotoxins in desert environments may present a risk to human health. Sci. Total Environ. 2012, 421–422, 118–123. [CrossRef] [PubMed]
Azevedo, S.M.F.O.; Carmichael, W.W.; Jochimsen, E.M.; Rinehart, K.L.; Lau, S.; Shaw, G.R.; Eaglesham, G.K. Human intoxication by microcystins during renal dialysis treatment in Caruaru-Brazil. Toxicology 2002, 181–182, 441–446. [CrossRef]
Van Apeldoorn, M.E.; Van Egmond, H.P.; Speijers, G.J.A.; Bakker, G.J.I. Toxins of cyanobacteria. Mol. Nutr. Food Res. 2007, 51, 7–60. [CrossRef] [PubMed]
Wood, R. Acute animal and human poisonings from cyanotoxin exposure—A review of the literature. Environ. Int. 2016, 91, 276–282. [CrossRef]
Kaebernick, M.; Neilan, B.A. Ecological and molecular investigations of cyanotoxin production. FEMS Microbiol. Ecol. 2006, 35, 1–9. [CrossRef]
De Figueiredo, D.R.; Azeiteiro, U.M.; Esteves, S.M.; Gonçalves, F.J.M.; Pereira, M.J. Microcystin-producing blooms–A serious global public health issue. Ecotoxicol. Environ. Saf. 2004, 59, 151–163. [CrossRef] [PubMed]
Aráoz, R.; Molgó, J.; Tandeau de Marsac, N. Neurotoxic cyanobacterial toxins. Toxicon 2010, 56, 813–828. [CrossRef] [PubMed]
Berry, J.P. Cyanobacterial Toxins as Allelochemicals with Potential Applications as Algaecides, Herbicides and Insecticides. Mar. Drugs 2008, 6, 117–146. [CrossRef]
Demuez, M.; González-Fernández, C.; Ballesteros, M. Algicidal microorganisms and secreted algicides: New tools to induce microalgal cell disruption. Biotechnol. Adv. 2015, 33, 1615–1625. [CrossRef]
Rastogi, R.P.; Sinha, R.P.; Incharoensakdi, A. The cyanotoxin-microcystins: Current overview. Rev. Environ. Sci. Biotechnol. 2014, 13, 215–249. [CrossRef]
Díez-Quijada, L.; Prieto, A.I.; Guzmán-Guillén, R.; Jos, A.; Cameán, A.M. Occurrence and toxicity of microcystin congeners other than MC-LR and MC-RR: A review. Food Chem. Toxicol. 2019, 125, 106–132. [CrossRef] [PubMed]
Bouaïcha, N.; Miles, C.O.; Beach, D.G.; Labidi, Z.; Djabri, A.; Benayache, N.Y.; Nguyen-Quang, T. Structural diversity, characterization and toxicology of microcystins. Toxins 2019, 11, 714. [CrossRef]
Massey, I.Y.; Yang, F. A mini review on microcystins and bacterial degradation. Toxins 2020, 12, 268. [CrossRef]
Díez-Quijada, L.; Puerto, M.; Gutiérrez-Praena, D.; Llana-Ruiz-Cabello, M.; Jos, A.; Cameán, A.M. Microcystin-RR: Occurrence, content in water and food and toxicological studies. A review. Environ. Res. 2019, 168, 467–489. [CrossRef]
Wang, Z.; Li, G.; Wu, Q.; Liu, C.; Shen, J.Z.; Yan, W. Microcystin-LR exposure induced nephrotoxicity by triggering apoptosis in female zebrafish. Chemosphere 2019, 214, 598–605. [CrossRef]
Hinojosa, M.G.; Gutiérrez-Praena, D.; Prieto, A.I.; Guzmán-Guillén, R.; Jos, A.; Cameán, A.M. Neurotoxicity induced by microcystins and cylindrospermopsin: A review. Sci. Total Environ. 2019, 668, 547–565. [CrossRef] [PubMed]
Nasri, H.; El Herry, S.; Bouaïcha, N. First reported case of turtle deaths during a toxic Microcystis spp. bloom in Lake Oubeira, Algeria. Ecotoxicol. Environ. Saf. 2008, 71, 535–544. [CrossRef] [PubMed]
Mohamed, Z.; Ahmed, Z.; Bakr, A.; Hashem, M.; Alamri, S. Detection of free and bound microcystins in tilapia fish from Egyptian fishpond farms and its related public health risk assessment. J. Verbrauch. Lebensm. 2020, 15, 37–47. [CrossRef]
Chen, J.; Xie, P. Tissue distributions and seasonal dynamics of the hepatotoxic microcystins-LR and-RR in two freshwater shrimps, Palaemon modestus and Macrobrachium nipponensis, from a large shallow, eutrophic lake of the subtropical China. Toxicon 2005, 45, 615–625. [CrossRef] [PubMed]
Mohamed, Z.A.; Carmichael, W.W.; Hussein, A.A. Estimation of microcystins in the freshwater fish Oreochromis niloticus in an Egyptian fish farm containing a Microcystis bloom. Environ. Toxicol. 2003, 18, 137–141. [CrossRef] [PubMed]
Freitas de Magalhães, V.; Moraes Soares, R.; Azevedo, S.M.F.O. Microcystin contamination in fish from the Jacarepaguá Lagoon (Rio de Janeiro, Brazil): Ecological implication and human health risk. Toxicon 2001, 39, 1077–1085. [CrossRef]
Zamora-Barrios, C.A.; Nandini, S.; Sarma, S.S.S. Bioaccumulation of microcystins in seston, zooplankton and fish: A case study in Lake Zumpango, Mexico. Environ. Pollut. 2019, 249, 267–276. [CrossRef]
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-contaminatedwater in the growth, mineral content, and contamination of spinacia oleracea and lactuca sativa. Toxins 2019, 11, 624. [CrossRef]
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. [CrossRef]
Cordeiro-Araújo, M.K.; Chia, M.A.; Arruda-Neto, J.D.d.T.; Tornisielo, V.L.; Vilca, F.Z.; Bittencourt-Oliveira, M.d.C. Microcystin-LR bioaccumulation and depuration kinetics in lettuce and arugula: Human health risk assessment. Sci. Total Environ. 2016, 566–567, 1379–1386. [CrossRef]
IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. IARC monographs on the evaluation of carcinogenic risks to humans. Ingested nitrate and nitrite, and cyanobacterial peptide toxins. Int. Agency Res. Cancer 2010, 94, 1–412.
Zheng, C.; Zeng, H.; Lin, H.; Wang, J.; Feng, X.; Qiu, Z.; Chen, J.A.; Luo, J.; Luo, Y.; Huang, Y.; et al. Serum microcystin levels positively linked with risk of hepatocellular carcinoma: A case-control study in southwest China. Hepatology 2017, 66, 1519–1528. [CrossRef]
Liu, W.; Wang, L.; Zheng, C.; Liu, L.; Wang, J.; Li, D.; Tan, Y.; Zhao, X.; He, L.; Shu, W. Microcystin-LR increases genotoxicity induced by aflatoxin B1 through oxidative stress and DNA base excision repair genes in human hepatic cell lines. Environ. Pollut. 2018, 233, 455–463. [CrossRef]
Zhou, L.; Yu, H.; Chen, K. Relationship between microcystin in drinking water and colorectal cancer. Biomed. Environ. Sci. 2002, 15, 166–171. [PubMed]
Pan, C.; Zhang, L.; Meng, X.; Qin, H.; Xiang, Z.; Gong, W.; Luo, W.; Li, D.; Han, X. Chronic exposure to microcystin-LR increases the risk of prostate cancer and induces malignant transformation of human prostate epithelial cells. Chemosphere 2021, 263, 128295. [CrossRef]
Gehringer, M.M.; Adler, L.; Roberts, A.A.; Moffitt, M.C.; Mihali, T.K.; Mills, T.J.T.; Fieker, C.; Neilan, B.A. Nodularin, a cyanobacterial toxin, is synthesized in planta by symbiotic Nostoc sp. ISME J. 2012, 6, 1834–1847. [CrossRef]
Chen, Y.; Shen, D.; Fang, D. Nodularins in poisoning. Clin. Chim. Acta 2013, 425, 18–29. [CrossRef] [PubMed]
Galanti, L.N.; Amé, M.V.; Wunderlin, D.A. Accumulation and detoxification dynamic of cyanotoxins in the freshwater shrimp Palaemonetes argentinus. Harmful Algae 2013, 27, 88–97. [CrossRef]
Krienitz, L.; Ballot, A.; Kotut, K.; Wiegand, C.; Pütz, S.; Metcalf, J.S.; Codd, G.A.; Stephan, P. Contribution of hot spring cyanobacteria to the mysterious deaths of Lesser Flamingos at Lake Bogoria, Kenya. FEMS Microbiol. Ecol. 2003, 43, 141–148. [CrossRef]
Becker, V.; Ihara, P.; Yunes, J.S.; Huszar, V.L.M. Occurrence of anatoxin-a(s) during a bloom of Anabaena crassa in a water-supply reservoir in southern Brazil. J. Appl. Phycol. 2010, 22, 235–241. [CrossRef]
Cook, W.O.; Beasley, V.R.; Dahlem, A.M.; Dellinger, J.A.; Harlin, K.S.; Carmichael, W.W. Comparison of effects of anatoxin-a(s) and paraoxon, physostigmine and pyridostigmine on mouse brain cholinesterase activity. Toxicon 1988, 26, 750–753. [CrossRef]
Ohtani, I.; Moore, R.E.; Runnegar, M.T.C. Cylindrospermopsin: A Potent Hepatotoxin from the Blue-Green Alga Cylindrospermopsis raciborskii. J. Am. Chem. Soc. 1992, 114, 7941–7942. [CrossRef]
Rzymski, P.; Poniedziałek, B. In search of environmental role of cylindrospermopsin: A review on global distribution and ecology of its producers. Water Res. 2014, 66, 320–337. [CrossRef]
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. [CrossRef]
Yang, Y.; Yu, G.; Chen, Y.; Jia, N.; Li, R. Four decades of progress in cylindrospermopsin research: The ins and outs of a potent cyanotoxin. J. Hazard. Mater. 2021, 406, 124653. [CrossRef]
Bouvy, M.; Falcão, D.; Marinho, M.; Pagano, M.; Moura, A. Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought. Aquat. Microb. Ecol. 2000, 23, 13–27. [CrossRef]
Chellappa, N.T.; Mederios Costa, M.A. Dominant and co-existing species of Cyanobacteria from a Eutrophicated reservoir of Rio Grande do Norte State, Brazil. Acta Oecol. 2003, 24, S3–S10. [CrossRef]
Briand, J.F.; Leboulanger, C.; Humbert, J.F.; Bernard, C.; Dufour, P. Cylindrospermopsis raciborskii (Cyanobacteria) invasion at mid-latitudes: Selection, wide physiological tolerance, or global warming? J. Phycol. 2004, 40, 231–238. [CrossRef]
Mohamed, Z.A.; Bakr, A. Concentrations of cylindrospermopsin toxin in water and tilapia fish of tropical fishponds in Egypt, and assessing their potential risk to human health. Environ. Sci. Pollut. Res. 2018, 25, 36287–36297. [CrossRef] [PubMed]
Costa, I.A.S.; Azevedo, S.M.F.O.; Senna, P.A.C.; Bernardo, R.R.; Costa, S.M.; Chellappa, N.T. Occurrence of toxin-producing cyanobacteria blooms in a Brazilian semiarid reservoir. Braz. J. Biol. 2006, 66, 211–219. [CrossRef]
Berry, J.P.; Jaja-Chimedza, A.; Dávalos-Lind, L.; Lind, O. Apparent bioaccumulation of cylindrospermopsin and paralytic shellfish toxins by finfish in lake catemaco (Veracruz, Mexico). Food Addit. Contam. Part A Chem. Anal. Control. Expo. Risk Assess. 2012, 29, 314–321. [CrossRef]
De La Cruz, A.A.; Hiskia, A.; Kaloudis, T.; Chernoff, N.; Hill, D.; Antoniou, M.G.; He, X.; Loftin, K.; O’Shea, K.; Zhao, C.; et al. A review on cylindrospermopsin: The global occurrence, detection, toxicity and degradation of a potent cyanotoxin. Environ. Sci. Process. Impacts 2013, 15, 1979–2003. [CrossRef]
Bittencourt-Oliveira, M.d.C.; Piccin-Santos, V.; Kujbida, P.; Moura, A.d.N. Cylindrospermopsin in Water Supply Reservoirs in Brazil Determined by Immunochemical and Molecular Methods. J. Water Resour. Prot. 2011, 3, 349–355. [CrossRef]
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. [CrossRef]
Hercog, K.; Štern, A.; Maisanaba, S.; Filipič, M.; Žegura, B. Plastics in cyanobacterial blooms—Genotoxic effects of binary mixtures of cylindrospermopsin and bisphenols in HepG2 cells. Toxins 2020, 12, 219. [CrossRef]
Lee, J.; Lee, S.; Jiang, X. Cyanobacterial Toxins in Freshwater and Food: Important Sources of Exposure to Humans. Annu. Rev. Food Sci. Technol. 2017, 8, 281–304. [CrossRef] [PubMed]
Pichardo, S.; Cameán, A.M.; Jos, A. In vitro toxicological assessment of cylindrospermopsin: A review. Toxins 2017, 9, 402. [CrossRef] [PubMed]
Griffiths, D.J.; Saker, M.L. The Palm Island mystery disease 20 years on: A review of research on the cyanotoxin cylindrosper-mopsin. Environ. Toxicol. 2003, 18, 78–93. [CrossRef] [PubMed]
Wiese, M.; D’Agostino, P.M.; Mihali, T.K.; Moffitt, M.C.; Neilan, B.A. Neurotoxic alkaloids: Saxitoxin and its analogs. Mar. Drugs 2010, 8, 2185–2211. [CrossRef] [PubMed]
Cusick, K.D.; Sayler, G.S. An overview on the marine neurotoxin, saxitoxin: Genetics, moleculartargets, methods of detection and ecological functions. Mar. Drugs 2013, 11, 991–1018. [CrossRef]
Thottumkara, A.P.; Parsons, W.H.; Du Bois, J. Saxitoxin. Angew. Chem. Int. Ed. 2014, 53, 5760–5784. [CrossRef] [PubMed]
Etheridge, S.M. Paralytic shellfish poisoning: Seafood safety and human health perspectives. Toxicon 2010, 56, 108–122. [CrossRef] [PubMed]
Galvão, J.A.; Oetterer, M.; Bittencourt-Oliveira, M.d.C.; Gouvêa-Barros, S.; Hiller, S.; Erler, K.; Luckas, B.; Pinto, E.; Kujbida, P. Saxitoxins accumulation by freshwater tilapia (Oreochromis niloticus) for human consumption. Toxicon 2009, 54, 891–894. [CrossRef]
Berry, J.P.; Lind, O. First evidence of “paralytic shellfish toxins” and cylindrospermopsin in a Mexican freshwater system, Lago Catemaco, and apparent bioaccumulation of the toxins in “tegogolo” snails (Pomacea patula catemacensis). Toxicon 2010, 55, 930–938. [CrossRef]
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. [CrossRef]
Durai, P.; Batool, M.; Choi, S. Structure and effects of cyanobacterial lipopolysaccharides. Mar. Drugs 2015, 13, 4217–4230. [CrossRef]
Bláhová, L.; Adamovský, O.; Kubala, L.; Švihálková Šindlerová, L.; Zounková, R.; Bláha, L. The isolation and characterization of lipopolysaccharides from Microcystis aeruginosa, a prominent toxic water bloom forming cyanobacteria. Toxicon 2013, 76, 187–196. [CrossRef]
Turner, A.D.; Waack, J.; Lewis, A.; Edwards, C.; Lawton, L. Development and single-laboratory validation of a UHPLC-MS/MS method for quantitation of microcystins and nodularin in natural water, cyanobacteria, shellfish and algal supplement tablet powders. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2018, 1074–1075, 111–123. [CrossRef]
Roy-Lachapelle, A.; Vo Duy, S.; Munoz, G.; Dinh, Q.T.; Bahl, E.; Simon, D.F.; Sauvé, S. Analysis of multiclass cyanotoxins (microcystins, anabaenopeptins, cylindrospermopsin and anatoxins) in lake waters using on-line SPE liquid chromatography high-resolution Orbitrap mass spectrometry. Anal. Methods 2019, 11, 5289–5300. [CrossRef]
Tran, N.H.; Li, Y.; Reinhard, M.; Goh, K.C.; Sukarji, N.H.B.; You, L.; He, Y.; Gin, K.Y.H. Quantification of cylindrospermopsin, anatoxin-a and homoanatoxin-a in cyanobacterial bloom freshwater using direct injection/SPE coupled with UPLC-MS/MS. Sci. Total. Environ. 2020, 731, 139014. [CrossRef] [PubMed]
Kumar, P.; Rautela, A.; Kesari, V.; Szlag, D.; Westrick, J.; Kumar, S. Recent developments in the methods of quantitative analysis of microcystins. J. Biochem. Mol. Toxicol. 2020, 34, e22582. [CrossRef]
Xu, X.; Zhu, B.; Liu, Z.; Wang, F.; Liang, J. Simultaneous determination of eight microcystins in fish by PRiME pass-through cleanup and online solid phase extraction coupled to ultra high performance liquid chromatography-tandem mass spectrometry. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2019, 1125, 121709. [CrossRef]
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. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
Qian, Z.Y.; Li, Z.G.; Ma, J.; Gong, T.-t.; Xian, Q.M. Analysis of trace microcystins in vegetables using matrix solid-phase dispersion followed by high performance liquid chromatography triple-quadrupole mass spectrometry detection. Talanta 2017, 173, 101–106. [CrossRef]
Massey, I.Y.; Wu, P.; Wei, J.; Luo, J.; Ding, P.; Wei, H.; Yang, F. A mini-review on detection methods of microcystins. Toxins 2020, 12, 641. [CrossRef]
Geis-Asteggiante, L.; Lehotay, S.J.; Fortis, L.L.; Paoli, G.; Wijey, C.; Heinzen, H. Development and validation of a rapid method for microcystins in fish and comparing LC-MS/MS results with ELISA. Anal. Bioanal. Chem. 2011, 401, 2617–2630. [CrossRef]
Parker, C.H.; Stutts, W.L.; Degrasse, S.L. Development and Validation of a Liquid Chromatography-Tandem Mass Spectrometry Method for the Quantitation of Microcystins in Blue-Green Algal Dietary Supplements. J. Agric. Food Chem. 2015, 63, 10303–10312. [CrossRef]
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. [CrossRef]
Díez-Quijada Jiménez, L.; Guzmán-Guillén, R.; Cătunescu, G.M.; Campos, A.; Vasconcelos, V.; Jos, Á.; Cameán, A.M. A new method for the simultaneous determination of cyanotoxins (Microcystins and Cylindrospermopsin) in mussels using SPE-UPLC-MS/MS. Environ. Res. 2020, 185, 109284. [CrossRef]
Haddad, S.P.; Bobbitt, J.M.; Taylor, R.B.; Lovin, L.M.; Conkle, J.L.; Chambliss, C.K.; Brooks, B.W. Determination of microcystins, nodularin, anatoxin-a, cylindrospermopsin, and saxitoxin in water and fish tissue using isotope dilution liquid chromatography tandem mass spectrometry. J. Chromatogr. A 2019, 1599, 66–74. [CrossRef]
Greer, B.; Maul, R.; Campbell, K.; Elliott, C.T. Detection of freshwater cyanotoxins and measurement of masked microcystins in tilapia from Southeast Asian aquaculture farms. Anal. Bioanal. Chem. 2017, 409, 4057–4069. [CrossRef] [PubMed]
Romera-García, E.; Helmus, R.; Ballesteros-Gómez, A.; Visser, P.M. Multi-class determination of intracellular and extracellular cyanotoxins in freshwater samples by ultra-high performance liquid chromatography coupled to high resolution mass spectrometry. Chemosphere 2021, 274, 129770. [CrossRef]
Di Pofi, G.; Favero, G.; Nigro Di Gregorio, F.; Ferretti, E.; Viaggiu, E.; Lucentini, L. Multi-residue Ultra Performance Liquid Chromatography-High resolution mass spectrometric method for the analysis of 21 cyanotoxins in surface water for human consumption. Talanta 2020, 211, 120738. [CrossRef] [PubMed]
Roy-Lachapelle, A.; Solliec, M.; Bouchard, M.F.; Sauvé, S. Detection of cyanotoxins in algae dietary supplements. Toxins 2017, 9, 76. [CrossRef]
Bogialli, S.; Bortolini, C.; Di Gangi, I.M.; Di Gregorio, F.N.; Lucentini, L.; Favaro, G.; Pastore, P. Liquid chromatography-high resolution mass spectrometric methods for the surveillance monitoring of cyanotoxins in freshwaters. Talanta 2017, 170, 322–330. [CrossRef] [PubMed]
Yang, R.; Song, D.; Fang, S.; Liu, Y.; Zhou, X.; Long, F.; Zhu, A. Development of novel portable and reusable fiber optical chemiluminescent biosensor and its application for sensitive detection of microcystin-LR. Biosens. Bioelectron. 2018, 121, 27–33. [CrossRef]
Vogiazi, V.; De La Cruz, A.; Mishra, S.; Shanov, V.; Heineman, W.R.; Dionysiou, D.D. A Comprehensive Review: Development of Electrochemical Biosensors for Detection of Cyanotoxins in Freshwater. ACS Sens. 2019, 4, 1151–1173. [CrossRef] [PubMed]
Modley, L.A.S.; Rampedi, I.T.; Avenant-Oldewage, A.; Mhuka, V.; Nindi, M.; Van Dyk, C. Microcystin concentrations and liver histopathology in Clarias gariepinus and Oreochromis mossambicus from three impacted rivers flowing into a hyper-eutrophic freshwater system: A pilot study. Environ. Toxicol. Pharmacol. 2019, 71, 103222. [CrossRef]
Nyakairu, G.W.A.; Nagawa, C.B.; Mbabazi, J. Assessment of cyanobacteria toxins in freshwater fish: A case study of Murchison Bay (Lake Victoria) and Lake Mburo, Uganda. Toxicon 2010, 55, 939–946. [CrossRef]
Semyalo, R.; Rohrlack, T.; Naggawa, C.; Nyakairu, G.W. Microcystin concentrations in Nile tilapia (Oreochromis niloticus) caught from Murchison Bay, Lake Victoria and Lake Mburo: Uganda. Hydrobiologia 2010, 638, 235–244. [CrossRef]
Amrani, A.; Nasri, H.; Azzouz, A.; Kadi, Y.; Bouaïcha, N. Variation in cyanobacterial hepatotoxin (microcystin) content of water samples and two species of fishes collected from a shallow lake in Algeria. Arch. Environ. Contam. Toxicol. 2014, 66, 379–389. [CrossRef] [PubMed]
Zewde, T.W.; Johansen, J.A.; Kifle, D.; Demissie, T.B.; Hansen, J.H.; Tadesse, Z. Concentrations of microcystins in the muscle and liver tissues of fish species from Koka reservoir, Ethiopia: A potential threat to public health. Toxicon 2018, 153, 85–95. [CrossRef] [PubMed]
Simiyu, B.M.; Oduor, S.O.; Rohrlack, T.; Sitoki, L.; Kurmayer, R. Microcystin content in phytoplankton and in small fish from eutrophic nyanza gulf, Lake Victoria, Kenya. Toxins 2018, 10, 275. [CrossRef]
Nchabeleng, T.; Cheng, P.; Oberholster, P.J.; Botha, A.M.; Smit, W.J.; Luus-Powell, W.J. Microcystin-LR equivalent concentrations in fish tissue during a postbloom Microcystis exposure in Loskop Dam, South Africa. Afr. J. Aquat. Sci. 2014, 39, 459–466. [CrossRef]
Humpage, A.R.; Falconer, I.R. Oral toxicity of the cyanobacterial toxin cylindrospermopsin in male Swiss albino mice: Determination of no observed adverse effect level for deriving a drinking water guideline value. Environ. Toxicol. 2003, 18, 94–103. [CrossRef]
Kotut, K.; Ballot, A.; Krienitz, L. Toxic cyanobacteria and their toxins in standing waters of Kenya: Implications for water resource use. J. Water Health 2006, 4, 233–245. [CrossRef]
Zewde, T.W.; Kifle, D.; Johansen, J.A.; Demissie, T.B.; Hansen, J.H.; Tadesse, Z. Cyanobacterial abundance and microcystins in water, seston and fish tissues in Lake Hora-Arsedi (Ethiopia). Afr. J. Aquat. Sci. 2020, 45, 475–485. [CrossRef]
Mchau, G.J. Cyanotoxins Occurrence in Drinking Waters and Risk of Exposure to Human in Ukerewe District Mwanza, Tanzania. Ph.D. Dissertation, The Nelson Mandela African Institution of Science and Technology, Arusha, Tanzania, 2020.
Mchau, G.J.; Makule, E.; Machunda, R.; Gong, Y.Y.; Kimanya, M. Harmful algal bloom and associated health risks among users of Lake Victoria freshwater: Ukerewe Island, Tanzania. J. Water Health 2019, 17, 826–836. [CrossRef] [PubMed]
Chen, J.; Xie, P. Accumulation of hepatotoxic microcystes in freshwater mussels, aquatic insect larvae and oligochaetes in a large, shallow eutrophic lake (Lake Chaohu) of subtropical China. Fresenius Environ. Bull. 2008, 17, 849–854.
Chen, J.; Xie, P.; Zhang, D.; Ke, Z.; Yang, H. In situ studies on the bioaccumulation of microcystins in the phytoplanktivorous silver carp (Hypophthalmichthys molitrix) stocked in Lake Taihu with dense toxic Microcystis blooms. Aquaculture 2006, 261, 1026–1038. [CrossRef]
Chen, J.; Xie, P. Seasonal dynamics of the hepatotoxic microcystins in various organs of four freshwater bivalves from the large eutrophic Lake Taihu of subtropical China and the risk to human consumption. Environ. Toxicol. 2005, 20, 572–584. [CrossRef]
Chen, J.; Xie, P.; Zhang, D.; Lei, H. In situ studies on the distribution patterns and dynamics of microcystins in a biomanipulation fish–bighead carp (Aristichthys nobilis). Environ. Pollut. 2007, 147, 150–157. [CrossRef]
Peng, L.; Tang, Q.; Gu, J.; Lei, L.; Chen, W.; Song, L. Seasonal variation of microcystins and their accumulation in fish in two large shallow lakes of China. Ecotoxicology 2020, 29, 790–800. [CrossRef] [PubMed]
Zhang, D.; Xie, P.; Liu, Y.; Qiu, T. Transfer, distribution and bioaccumulation of microcystins in the aquatic food web in Lake Taihu, China, with potential risks to human health. Sci. Total Environ. 2009, 407, 2191–2199. [CrossRef] [PubMed]
Jia, J.; Luo, W.; Lu, Y.; Giesy, J.P. Bioaccumulation of microcystins (MCs) in four fish species from Lake Taihu, China: Assessment of risks to humans. Sci. Total Environ. 2014, 487, 224–232. [CrossRef]
Jiang, Y.; Xie, P.; Nie, Y. Concentration and bioaccumulation of cyanobacterial bioactive and odorous metabolites occurred in a large, shallow chinese lake. Bull. Environ. Contam. Toxicol. 2014, 93, 643–648. [CrossRef] [PubMed]
Jiang, Y.; Yang, Y.; Wu, Y.; Tao, J.; Cheng, B. Microcystin Bioaccumulation in Freshwater Fish at Different Trophic Levels from the Eutrophic Lake Chaohu, China. Bull. Environ. Contam. Toxicol. 2017, 99, 69–74. [CrossRef]
Jing, M.; Lin, D.; Lin, J.; Li, Q.; Yan, H.; Feng, X. Mercury, microcystins and Omega-3 polyunsaturated fatty acids in farmed fish in eutrophic reservoir: Risk and benefit assessment. Environ. Pollut. 2021, 270, 116047. [CrossRef] [PubMed]
Peng, L.; Liu, Y.; Chen, W.; Liu, L.; Kent, M.; Song, L. Health risks associated with consumption of microcystin-contaminated fish and shellfish in three Chinese lakes: Significance for freshwater aquacultures. Ecotoxicol. Environ. Saf. 2010, 73, 1804–1811. [CrossRef] [PubMed]
Zhang, D.; Deng, X.; Xie, P.; Chen, J.; Guo, L. Risk assessment of microcystins in silver carp (Hypophthalmichthys molitrix) from eight eutrophic lakes in China. Food Chem. 2013, 140, 17–21. [CrossRef] [PubMed]
Gurbuz, F.; Uzunmehmetoğlu, O.Y.; Diler, Ö.; Metcalf, J.S.; Codd, G.A. Occurrence of microcystins in water, bloom, sediment and fish from a public water supply. Sci. Total Environ. 2016, 562, 860–868. [CrossRef]
Akcaalan, R.; Köker, L.; Oğuz, A.; Spoof, L.; Meriluoto, J.; Albay, M. First report of cylindrospermopsin production by two cyanobacteria (Dolichospermum mendotae and Chrysosporum ovalisporum) in Lake Iznik, Turkey. Toxins 2014, 6, 3173–3186. [CrossRef] [PubMed]
Koker, L.; Akcaalan, R.; Oguz, A.; Gaygusuz, O.; Kose, C.A.; Gucver, S.; Karaaslan, Y.; Albay, M.; Kinaci, C. Distribution of toxic cyanobacteria and cyanotoxins in Turkish waterbodies. J. Environ. Prot. Ecol. 2017, 18, 425–432.
Singh, S.; Asthana, R.K. Assessment of microcystin concentration in carp and catfish: A case study from Lakshmikund Pond, Varanasi, India. Bull. Environ. Contam. Toxicol. 2014, 92, 687–692. [CrossRef]
Rezaitabar, S.; Esmaili Sari, A.; Bahramifar, N.; Ramezanpour, Z. Transfer, tissue distribution and bioaccumulation of microcystin LR in the phytoplanktivorous and carnivorous fish in Anzali wetland, with potential health risks to humans. Sci. Total Environ. 2017, 575, 1130–1138. [CrossRef]
Ruangrit, K.; Peerapornpisal, Y.; Pekkoh, J.; Whangchai, N. Microcystin Accumulation in Nile Tilapia, Oreochromis niloticus and Giant Freshwater Prawns, Macrobrachium rosenbergii in Green Water System Cultivation. Int. J. Geosci. 2013, 4, 60–63. [CrossRef]
Ruangrit, K.; Whangchai, N.; Pekkoh, J.; Ruangyuttikarn, W.; Peerapornpisal, Y. First report on microcystins contamination in giant freshwater prawn (Macrobrachium rosenbergii) and Nile tilapia (Tilapia nilotica) cultured in earthen ponds. Int. J. Agric. Biol. 2011, 13, 1025–1028.
Pham, T.L.; Shimizu, K.; Dao, T.S.; Motoo, U. First report on free and covalently bound microcystins in fish and bivalves from Vietnam: Assessment of risks to humans. Environ. Toxicol. Chem. 2017, 36, 2953–2957. [CrossRef] [PubMed]
Trung, B.; Dao, T.S.; Faassen, E.; Lürling, M. Cyanobacterial blooms and microcystins in Southern Vietnam. Toxins 2018, 10, 471. [CrossRef]
Bi, X.; Dai, W.; Wang, X.; Dong, S.; Zhang, S.; Zhang, D.; Wu, M. Microcystins distribution, bioaccumulation, and Microcystis genotype succession in a fish culture pond. Sci. Total Environ. 2019, 688, 380–388. [CrossRef] [PubMed]
Zhang, H.j.; Zhang, J.-y.; Hong, Y.; Chen, Y. xu Evaluation of organ distribution of microcystins in the freshwater phytoplanktivo-rous fish Hypophthalmichthys molitrix. J. Zhejiang Univ. Sci. B 2007, 8, 116–120. [CrossRef]
Ni, W.; Zhang, J.; Luo, Y. Microcystin accumulation in bighead carp (Aristichthys nobilis) during a Microcystis-dominated bloom and risk assessment of the dietary intake in a fish pond in China. Environ. Sci. Pollut. Res. 2017, 24, 8894–8902. [CrossRef] [PubMed]
Zhang, J.; Wang, Z.; Song, Z.; Xie, Z.; Li, L.; Song, L. Bioaccumulation of microcystins in two freshwater gastropods from a cyanobacteria-bloom plateau lake, Lake Dianchi. Environ. Pollut. 2012, 164, 227–234. [CrossRef] [PubMed]
Xie, L.; Xie, P.; Guo, L.; Li, L.; Miyabara, Y.; Park, H.D. Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China. Environ. Toxicol. 2005, 20, 293–300. [CrossRef]
Ruangsomboon, S.; Yongmanitchai, W.; Taveekijakarn, P.; Ganmanee, M. Cyanobacterial composition and microcystin accumulation in catfish pond. Chiang Mai J. Sci. 2014, 41, 27–38.
Whangchai, N.; Wanno, S.; Gutierrez, R.; Kannika, K.; Promna, R.; Iwami, N.; Itayama, T. Accumulation of microcystins in water and economic fish in Phayao Lake, and fish ponds along the Ing River tributary in Chiang Rai, Thailand. Agric. Sci. 2013, 4, 52–56. [CrossRef]
Lin, H.; Liu, W.; Zeng, H.; Pu, C.; Zhang, R.; Qiu, Z.; Chen, J.A.; Wang, L.; Tan, Y.; Zheng, C.; et al. Determination of Environmental Exposure to Microcystin and Aflatoxin as a Risk for Renal Function Based on 5493 Rural People in Southwest China. Environ. Sci. Technol. 2016, 50, 5346–5356. [CrossRef]
Greer, B.; Meneely, J.P.; Elliott, C.T. Uptake and accumulation of Microcystin-LR based on exposure through drinking water: An animal model assessing the human health risk. Sci. Rep. 2018, 8, 4913. [CrossRef]
Calado, S.L.d.M.; Santos, G.S.; Leite, T.P.B.; Wojciechowski, J.; Nadaline, M.; Bozza, D.C.; de Magalhães, V.F.; Cestari, M.M.; Prodocimo, V.; Silva de Assis, H.C. Depuration time and sublethal effects of microcystins in a freshwater fish from water supply reservoir. Chemosphere 2018, 210, 805–815. [CrossRef]
Oliveira, N.B.; Schwartz, C.A.; Bloch, C.; Paulino, L.; Pires, O.R. Bioacumulation of cyanotoxins in hypophthalmichthys molitrix (silver carp) in paranoá lake, Brasilia-DF, Brazil. Bull. Environ. Contam. Toxicol. 2013, 90, 308–313. [CrossRef]
Deblois, C.P.; Aranda-Rodriguez, R.; Giani, A.; Bird, D.F. Microcystin accumulation in liver and muscle of tilapia in two large Brazilian hydroelectric reservoirs. Toxicon 2008, 51, 435–448. [CrossRef]
Chellappa, N.T.; Chellappa, S.L.; Chellappa, S. Harmful Phytoplankton Blooms and Fish Mortality in a eutrophicated reservoir of Northeast Brazil. Braz. Arch. Biol. Technol. 2008, 51, 833–841. [CrossRef]
Magalhães, V.F.; Marinho, M.M.; Domingos, P.; Oliveira, A.C.; Costa, S.M.; Azevedo, L.O.; Azevedo, S.M.F.O. Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brasil, RJ). Toxicon 2003, 42, 289–295. [CrossRef]
Berry, J.P.; Lee, E.; Walton, K.; Wilson, A.E.; Bernal-Brooks, F. Bioaccumulation of microcystins by fish associated with a persistent cyanobacterial bloom in Lago de Patzcuaro (Michoacan, Mexico). Environ. Toxicol. Chem. 2011, 30, 1621–1628. [CrossRef]
Cazenave, J.; Wunderlin, D.A.; Bistoni, M.D.L.Á.; Amé, M.V.; Krause, E.; Pflugmacher, S.; Wiegand, C. Uptake, tissue distribution and accumulation of microcystin-RR in Corydoras paleatus, Jenynsia multidentata and Odontesthes bonariensis: A field and laboratory study. Aquat. Toxicol. 2005, 75, 178–190. [CrossRef]
Amé, M.V.; Galanti, L.N.; Menone, M.L.; Gerpe, M.S.; Moreno, V.J.; Wunderlin, D.A. Microcystin-LR,-RR,-YR and-LA in water samples and fishes from a shallow lake in Argentina. Harmful Algae 2010, 9, 66–73. [CrossRef]
De Bock, M.F.S.; Moraes, G.S.d.O.; Almeida, R.G.d.S.; Vieira, K.D.d.S.; Santoro, K.R.; Bicudo, Á.J.d.A.; Molica, R.J.R. Exposure of Nile Tilapia (Oreochromis niloticus) Fingerlings to a Saxitoxin-Producing Strain of Raphidiopsis (Cylindrospermopsis) raciborskii (Cyanobacterium) Reduces Growth Performance and Increases Mortality Rate. Environ. Toxicol. Chem. 2020, 39, 1409–1420. [CrossRef]
Hauser-Davis, R.A.; Lavradas, R.T.; Lavandier, R.C.; Rojas, E.G.A.; Guarino, A.W.S.; Ziolli, R.L. Accumulation and toxic effects of microcystin in tilapia (Oreochromis niloticus) from an eutrophic Brazilian lagoon. Ecotoxicol. Environ. Saf. 2015, 112, 132–136. [CrossRef] [PubMed]
WHO. Guidelines for Drinking-Water Quality, 3rd ed.; WHO: Geneva, Switzerland, 2008; Volume 1, ISBN 9789241547611.
WHO. Cyanobacterial toxins: Microcystin-LR in Drinking-water. In WHO Guidelines for Drinking-Water Quality; WHO: Geneva, Switzerland, 2003; pp. 95–110.
World Health Organization. Cyanobacterial Toxins: Microcystins; WHO: Geneva, Switzerland, 2020.
World Health Organization. Cyanobacterial Toxins: Cylindrospermopsins; WHO: Geneva, Switzerland, 2020.
World Health Organization. Cyanobacterial Toxins: Saxitoxins; WHO: Geneva, Switzerland, 2020.
World Health Organization. Cyanobacterial Toxins: Anatoxin-a and Analogues; WHO: Geneva, Switzerland, 2020.
The European Parliament and the Council of the European Union Directive (EU). 2020/2184, EU (revised) Drinking Water Directive. Annex 1. Part B. Off. J. Eur. Communities 2020, 2019, 35.
Aguilera, A.; Haakonsson, S.; Martin, M.V.; Salerno, G.L.; Echenique, R.O. Bloom-forming cyanobacteria and cyanotoxins in Argentina: A growing health and environmental concern. Limnologica 2018, 69, 103–114. [CrossRef]
Copetti, D.; Finsterle, K.; Marziali, L.; Stefani, F.; Tartari, G.; Douglas, G.; Reitzel, K.; Spears, B.M.; Winfield, I.J.; Crosa, G.; et al. Eutrophication management in surface waters using lanthanum modified bentonite: A review. Water Res. 2015, 97, 162–174. [CrossRef]
Wu, H.; Wei, G.; Tan, X.; Li, L.; Li, M. Species-dependent variation in sensitivity of Microcystis species to copper sulfate: Implication in algal toxicity of copper and controls of blooms. Sci. Rep. 2017, 7, 40393. [CrossRef] [PubMed]
Zamyadi, A.; Greenstein, K.E.; Glover, C.M.; Adams, C.; Rosenfeldt, E.; Wert, E.C. Impact of hydrogen peroxide and copper sulfate on the delayed release of microcystin. Water 2020, 12, 1105. [CrossRef]
Li, X.; Chen, S.; Zeng, J.; Chabi, K.; Song, W.; Xian, X.; Yu, X. Impact of chlorination on cell inactivation, toxin release and degradation of cyanobacteria of development and maintenance stage. Chem. Eng. J. 2020, 397, 125378. [CrossRef]
Matthijs, H.C.P.; Visser, P.M.; Reeze, B.; Meeuse, J.; Slot, P.C.; Wijn, G.; Talens, R.; Huisman, J. Selective suppression of harmful cyanobacteria in an entire lake with hydrogen peroxide. Water Res. 2012, 46, 1460–1472. [CrossRef] [PubMed]
Roegner, A.F.; Brena, B.; González-Sapienza, G.; Puschner, B. Microcystins in potable surface waters: Toxic effects and removal strategies. J. Appl. Toxicol. 2014, 34, 441–457. [CrossRef]
Abbas, T.; Kajjumba, G.W.; Ejjada, M.; Masrura, S.U.; Marti, E.J.; Khan, E.; Jones-lepp, T.L. Recent advancements in the removal of cyanotoxins from water using conventional and modified adsorbents—A contemporary review. Water 2020, 12, 2756. [CrossRef]
Drogui, P.; Daghrir, R.; Simard, M.C.; Sauvageau, C.; Blais, J.F. Removal of microcystin-LR from spiked water using either activated carbon or anthracite as filter material. Environ. Technol. 2012, 33, 381–391. [CrossRef] [PubMed]
Nasri, H.; Bouaïcha, N.; Harche, M.K. A new morphospecies of Microcystis sp. forming bloom in the cheffia dam (Algeria): Seasonal variation of microcystin concentrations in raw water and their removal in a full-scale treatment plant. Environ. Toxicol. 2007, 22, 347–356. [CrossRef] [PubMed]
Park, J.A.; Jung, S.M.; Choi, J.W.; Kim, J.H.; Hong, S.; Lee, S.H. Mesoporous carbon for efficient removal of microcystin-LR in drinking water sources, Nak-Dong River, South Korea: Application to a field-scale drinking water treatment plant. Chemosphere 2018, 193, 883–891. [CrossRef]
Shi, H.; Ding, J.; Timmons, T.; Adams, C. PH effects on the adsorption of saxitoxin by powdered activated carbon. Harmful Algae 2012, 19, 61–67. [CrossRef]
Bajracharya, A.; Liu, Y.L.; Lenhart, J.J. The influence of natural organic matter on the adsorption of microcystin-LR by powdered activated carbon. Environ. Sci. Water Res. Technol. 2019, 5, 256–267. [CrossRef]
Lian, L.; Cao, X.; Wu, Y.; Sun, D.; Lou, D. A green synthesis of magnetic bentonite material and its application for removal of microcystin-LR in water. Appl. Surf. Sci. 2014, 289, 245–251. [CrossRef]
Lee, J.; Walker, H.W. Adsorption of microcystin-Lr onto iron oxide nanoparticles. Colloids Surf. A Physicochem. Eng. Asp. 2011, 373, 94–100. [CrossRef]
He, X.; de la Cruz, A.A.; Hiskia, A.; Kaloudis, T.; O’Shea, K.; Dionysiou, D.D. Destruction of microcystins (cyanotoxins) by UV-254 nm-based direct photolysis and advanced oxidation processes (AOPs): Influence of variable amino acids on the degradation kinetics and reaction mechanisms. Water Res. 2015, 74, 227–238. [CrossRef]
Liu, X.; Chen, Z.; Zhou, N.; Shen, J.; Ye, M. Degradation and detoxification of microcystin-LR in drinking water by sequential use of UV and ozone. J. Environ. Sci. 2010, 22, 1897–1902. [CrossRef]
Chang, J.; Chen, Z.L.; Wang, Z.; Kang, J.; Chen, Q.; Yuan, L.; Shen, J.M. Oxidation of microcystin-LR in water by ozone combined with UV radiation: The removal and degradation pathway. Chem. Eng. J. 2015, 276, 97–105. [CrossRef]
Afzal, A.; Oppenländer, T.; Bolton, J.R.; El-Din, M.G. Anatoxin-a degradation by Advanced Oxidation Processes: Vacuum-UV at 172 nm, photolysis using medium pressure UV and UV/H2 O2 . Water Res. 2010, 44, 278–286. [CrossRef] [PubMed]
He, X.; Pelaez, M.; Westrick, J.A.; O’Shea, K.E.; Hiskia, A.; Triantis, T.; Kaloudis, T.; Stefan, M.I.; de la Cruz, A.A.; Dionysiou, D.D. Efficient removal of microcystin-LR by UV-C/H2 O2 in synthetic and natural water samples. Water Res. 2012, 46, 1501–1510. [CrossRef]
Chintalapati, P.; Mohseni, M. Degradation of cyanotoxin microcystin-LR in synthetic and natural waters by chemical-free UV/VUV radiation. J. Hazard. Mater. 2020, 381, 120921. [CrossRef] [PubMed]
Xie, G.; Hu, X.; Du, Y.; Jin, Q.; Liu, Y.; Tang, C.; Hu, X.; Li, G.; Chen, Z.; Zhou, D.; et al. Light-driven breakdown of microcystin-LR in water: A critical review. Chem. Eng. J. 2021, 417, 129244. [CrossRef]
Zhang, J.; Shi, H.; Liu, A.; Cao, Z.; Hao, J.; Gong, R. Identification of a new microcystin-degrading bacterium isolated from Lake Chaohu, China. Bull. Environ. Contam. Toxicol. 2015, 94, 661–666. [CrossRef] [PubMed]
Hu, L.; Zhang, F.; Liu, C.; Wang, M. Biodegradation of microcystins by Bacillus sp. Strain EMB. Energy Procedia 2012, 16, 2054–2059. [CrossRef]
Li, J.; Li, R.; Li, J. Current research scenario for microcystins biodegradation–A review on fundamental knowledge, application prospects and challenges. Sci. Total Environ. 2017, 595, 615–632. [CrossRef]
Guzmán-Guillén, R.; Prieto, A.I.; Moreno, I.; Soria, M.E.; Cameán, A.M. Effects of thermal treatments during cooking, microwave oven and boiling, on the unconjugated microcystin concentration in muscle of fish (Oreochromis niloticus). Food Chem. Toxicol. 2011, 49, 2060–2067. [CrossRef]
Guzmán-Guillén, R.; Maisanaba, S.; Prieto Ortega, A.I.; Valderrama-Fernández, R.; Jos, Á.; Cameán, A.M. Changes on cylindros-permopsin concentration and characterization of decomposition products in fish muscle (Oreochromis niloticus) by boiling and steaming. Food Control 2017, 77, 210–220. [CrossRef]
Prieto, A.I.; Guzmán-Guillén, R.; Valderrama-Fernández, R.; Jos, Á.; Cameán, A.M. Influence of cooking (Microwaving and broil-ing) on cylindrospermopsin concentration in muscle of nile tilapia (Oreochromis niloticus) and characterization of decomposition products. Toxins 2017, 9, 177. [CrossRef]
Meneely, J.P.; Elliott, C.T. Microcystins: Measuring human exposure and the impact on human health. Biomarkers 2013, 18, 639–649. [CrossRef]
Mchau, G.J.; Machunda, R.; Kimanya, M.; Makule, E.; Gong, Y.Y.; Mpolya, E.; Meneely, J.P.; Elliott, C.T.; Greer, B. First Report of the Co-occurrence of Cylindrospermopsin, Nodularin and Microcystins in the Freshwaters of Lake Victoria, Tanzania. Expo. Health 2021, 13, 185–194. [CrossRef]
Li, Y.; Chen, J.-a.; Zhao, Q.; Pu, C.; Qiu, Z.; Zhang, R.; Shu, W. A cross-sectional investigation of chronic exposure to microcystin in relationship to childhood liver damage in the three gorges reservoir region, China. Environ. Health Perspect. 2011, 119, 1483–1488. [CrossRef]
Metcalf, J.S.; Codd, G.A. Co-occurrence of cyanobacteria and cyanotoxins with other environmental health hazards: Impacts and implications. Toxins 2020, 12, 629. [CrossRef] [PubMed]
Guo, H.; Ji, J.; Wang, J.-S.; Sun, X. Co-contamination and interaction of fungal toxins and other environmental toxins. Trends Food Sci. Technol. 2020, 103, 162–178. [CrossRef]
Meneely, J.P.; Hajšlová, J.; Krska, R.; Elliott, C.T. Assessing the combined toxicity of the natural toxins, aflatoxin B1, fumonisin B1 and microcystin-LR by high content analysis. Food Chem. Toxicol. 2018, 121, 527–540. [CrossRef] [PubMed]
