498
Views
32
CrossRef citations to date
0
Altmetric
Review Article

Microcystins: measuring human exposure and the impact on human health

&
Pages 639-649 | Received 12 Aug 2013, Accepted 03 Sep 2013, Published online: 08 Oct 2013

References

  • Backer LC, McNeel SV, Barber T, et al. (2010). Recreational exposure to microcystins during algal blooms in two California lakes. Toxicon 55:909–21
  • Bennett J., Klich M. (2003). Mycotoxins. Clin Microbiol Rev 16:497–516
  • Benson J, Hutt J, Rein K, et al. (2005). The toxicity of microcystin LR in mice following 7 days of inhalation exposure. Toxicon 45:691–8
  • Briand J-F, Jacquet S, Bernard C, Humbert J-F. (2003). Health hazards for terrestrial vertebrates from toxic cyanobacteria in surface water ecosystems. Vet Res 34:361–77
  • Burkholder JM. (2009). Harmful algal blooms. In: Likens GE, ed. Encyclopedia of Inland Waters. Oxford: Academic Press, 264–85
  • Carmichael W. (1992). Cyanobacteria secondary metabolites -- the Cyanotoxins. J Appl Bacteriol 72:445–59
  • Carmichael W, Azevedo S, An J, et al. (2001). Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environ Health Perspect 109:663–8
  • Carmichael WW, An J. (1999). Using an enzyme linked immunosorbent assay (ELISA) and a protein phosphatase inhibition assay for the detection of microcystins and nodularins. Nat Toxins 7:377–85
  • Chen J, Han FX, Wang F, et al. (2012). Accumulation and phytotoxicity of microcystin-LR in rice (Oryza sativa). Ecotox Environ Safe 76:193–9
  • Chen J, Xie P, Li L, Xu J. (2009). First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage. Toxicol Sci 108:81–9
  • Chen JG, Zhang SW. (2011). Liver cancer epidemic in China: past, present and future. Semin Cancer Biol 21:59–69
  • Chen T, Wang Q, Cui J, et al. (2005). Induction of apoptosis in mouse liver by microcystin-LR -- a combined transcriptomic, proteomic, and simulation strategy. Mol Cell Proteomics 4:958–74
  • Chen W, Jia Y, Li E, et al. (2012). Soil-based treatments of mechanically collected cyanobacterial blooms from Lake Taihu: efficiencies and potential risks. Environ Sci Technol 46:13370–6
  • Codd GA, Metcalf JS, Beattie KA. (1999). Retention of Microcystis aeruginosa and microcystin by salad lettuce (Lactuca sativa) after spray irrigation with water containing cyanobacteria. Toxicon 37:1181–5
  • de Figueiredo DR, Azeiteiro UM, Esteves SM, et al. (2004). Microcystin-producing blooms—a serious global public health issue. Ecotoxicol Environ Saf 59:151–63
  • de Magalhães VF, Soares RM, Azevedo SMFO. (2001). Microcystin contamination in fish from the Jacarepaguá Lagoon (Rio de Janeiro, Brazil): ecological implication and human health risk. Toxicon 39:1077–85
  • Devlin S, Meneely JP, Greer B, et al. (2013). Next generation planar waveguide detection of microcystins in freshwater and cyanobacterial extracts, utilising a novel lysis method for portable sample preparation and analysis. Anal Chim Acta 769:108–13
  • Dewes LJ, Sandrini JZ, Monserrat JM, Yunes JS. (2006). Biochemical and physiological responses after exposure to microcystins in the crab Chasmagnathus granulatus (Decapoda, Brachyura). Ecotoxicol Environ Saf 65:201–8
  • Falconer I. (1999). An overview of problems caused by toxic blue-green algae (cyanobacteria) in drinking and recreational water. Environ Toxicol 14:5–12
  • Falconer I. (2005). Is there a human health hazard from microcystins in the drinking water supply? Acta Hydrochim Hydrobiol 33:64–71
  • Falconer I, Burch MD, Steffensen DA, et al. (1994). Toxicity of the blue-green alga (cyanobacterium) Microcystis aeruginosa in drinking water to growing pigs, as an animal model for human injury and risk assessment. Environ Toxic Water 9:131–9
  • Falconer IR, Smith JV, Jackson ARB, et al. (1988). Oral toxicity of a bloom of the cyanobacterium Microcystis aeruginosa administered to mice over periods up to 1 year. J Toxicol Env Health 24:291–305
  • Farmer PB. (2004). DNA and protein adducts as markers of genotoxicity. Toxicol Lett 149:3–9
  • Fawell JK, Mitchell RE, Everett DJ, Hill RE. (1999). The toxicity of cyanobacterial toxins in the mouse. Hum Exp Toxicol 18:162–7
  • Fernandes S, Welker M, Vasconcelos VM. (2009). Changes in the GST Activity of the Mussel Mytilus galloprovincialis during exposure and depuration of microcystins. J Exp Zool Part A 311A:226–30
  • Feurstein D, Holst K, Fischer A, Dietrich DR. (2009). Oatp-associated uptake and toxicity of microcystins in primary murine whole brain cells. Toxicol Appl Pharmacol 234:247–55
  • Feurstein D, Kleinteich J, Heussner AH, et al. (2010). Investigation of microcystin congener-dependent uptake into primary murine neurons. Environ Health Perspect 118:1370–5
  • Fu W-Y, Xu L-H, Yu Y-N. (2005). Proteomic analysis of cellular response to microcystins in human amnion FL cells. J Proteome Res 4:2207–15
  • Gehringer MM. (2004). Microcystin-LR and okadaic acid-induced cellular effects: a dualistic response. FEBS Lett 557:1–8
  • Giannuzzi L, Sedan D, Echenique R, Andrinolo D. (2011). An acute case of intoxication with cyanobacteria and cyanotoxins in recreational water in Salto Grande Dam, Argentina. Mar Drugs 9:2164–75
  • Gilroy D, Kauffman K, Hall R, et al. (2000). Assessing potential health risks from microcystin toxins in blue-green algae dietary supplements. Environ Health Perspect 108:435–9
  • Gong YY, Wilson S, Mwatha, JK, et al. (2012). Aflatoxin exposure may contribute to chronic hepatomegaly in Kenyan school children. Environ Health Perspect 120:893–6
  • Graham SF, Chevallier OP, Roberts D, et al. (2013). Investigation of the human brain metabolome to identify potential markers for early diagnosis and therapeutic targets of Alzheimer's disease. Anal Chem 85:1803–11
  • He J, Chen J, Wu L, et al. (2012). Metabolic response to oral microcystin-LR exposure in the rat by NMR-based metabonomic study. J Proteome Res 11:5934–46
  • Heinze R. (1999). Toxicity of the cyanobacterial toxin microcystin-LR to rats after 28 days intake with the drinking water. Environ Toxicol 14:57–60
  • Hereman TC, Bittencourt-Oliveira MDC. (2012). Bioaccumulation of microcystins in lettuce. J Phycol 48:1535–7
  • Hernandez JM, Lopez-Rodas V, Costas E. (2009). Microcystins from tap water could be a risk factor for liver and colorectal cancer: a risk intensified by global change. Med Hypotheses 72:539–40
  • Heussner AH, Mazija L, Fastner J, Dietrich DR. (2012). Toxin content and cytotoxicity of algal dietary supplements. Toxicol Appl Pharm 265:263–71
  • Hilborn E, Carmichael W, Yuan M, Azevedo S. (2005). A simple colorimetric method to detect biological evidence of human exposure to microcystins. Toxicon 46:218–21
  • Hilborn ED, Carmichael WW, Soares RM, et al. (2007). Serologic evaluation of human microcystin exposure. Environ Toxicol 22:459–63
  • Humpage A, Falconer I. (1999). Microcystin-LR and liver tumor promotion: effects on cytokinesis, ploidy, and apoptosis in cultured hepatocytes. Environ Toxicol 14:61–75
  • Ibeling BW, Chorus I. (2007). Accumulation of cyanobacterial toxins in freshwater “seafood” and its consequences for public health: a review. Environ Pollut 150:177–92
  • Imanishi S, Harada K-I. (2004). Proteomics approach on microcystin binding proteins in mouse liver for investigation of microcystin toxicity. Toxicon 43:651–9
  • Ito E, Kondo F, Terao K, Harada K. (1997). Neoplastic nodular formation in mouse liver induced by repeated intraperitoneal injections of microcystin-LR. Toxicon 35:1453–7
  • Jochimsen E, Carmichael W, An J, et al. (1998). Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N Engl J Med 338:873–8
  • Karlsson K, Spoof L, Meriluoto J. (2005). Quantitative LC-ESI-MS analyses of microcystins and nodularin-R in animal tissue - matrix effects and method validation. Environ Toxicol 20: 381–9
  • Kaya K, Sano T, Inoue H, Takagi H. (2001). Selective determination of total normal microcystin by colorimetry, LC/UV detection and/or LC/MS. Anal Chim Acta 450:73–80
  • Kondo F, Ii Y, Oka H, et al. (1992). Formation, characterization, and toxicity of the glutathione and cysteine conjugates of toxic heptapeptide microcystins. Chem Res Toxicol 5:591–6
  • Kondo F, Matsumoto H, Yamada S, et al. (1996). Detection and identification of metabolites of microcystins formed in vivo in mouse and rat livers. Chem Res Toxicol 9:1355–9
  • Lance E, Neffling M, Gerard C, et al. (2010). Accumulation of free and covalently bound microcystins in tissues of Lymnaea stagnalis (Gastropoda) following toxic cyanobacteria or dissolved microcystin-LR exposure. Environ Poll 158:674–80
  • Lawton LA, Chambers H, Edwards C, et al. (2010). Rapid detection of microcystins in cells and water. Toxicon 55:973–8
  • Li G, Yan W, Qiao Q, et al. (2012). Global effects of subchronic treatment of microcystin-LR on rat splenetic protein levels. J Proteomics 77:383–93
  • Li Y, Chen J, Zhao Q, et al. (2011). 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 119:1483–8
  • Lin JR, Chu FS. (1994). Kinetics of distribution of microcystin LR in serum and liver cytosol of mice: an immunochemical analysis. J Agric Food Chem 42:1035–40
  • Mackintosh R, Dalby K, Campbell D, et al. (1995). The cyanobacterial toxin microcystin binds covalently to cysteine-273 on protein phosphatase-1. FEBS Lett 371:236–40
  • Malécot M, Marie A, Puiseux-Dao S, Edery M. (2011). iTRAQ-based proteomic study of the effects of microcystin-LR on medaka fish liver. Proteomics 11:2071–8
  • Malécot M, Mezhoud K, Marie A, et al. (2009). Proteomic study of the effects of microcystin-LR on organelle and membrane proteins in medaka fish liver. Aquat Toxicol 94:153–61
  • Mankiewicz-Boczek J, Palus J, Gagala I, et al. (2011). Effects of microcystins-containing cyanobacteria from a temperate ecosystem on human lymphocytes culture and their potential for adverse human health effects. Harmful Algae 10:356–65
  • Masson P, Spagou K, Nicholson JK, Want EJ. (2011). Technical and biological variation in UPLC-MS-based untargeted metabolic profiling of liver extracts: application in an experimental toxicity study on galactosamine. Anal Chem 83:1116–23
  • McDermott CM, Nho CW, Howard W, Holton B. (1998). The cyanobacterial toxin, microcystin-LR, can induce apoptosis in a variety of cell types. Toxicon 36:1981–96
  • McElhiney J, Lawton L. (2005). Detection of the cyanobacterial hepatotoxins microcystins. Toxicol Appl Pharmacol 203:219–30
  • McElhiney J, Lawton L, Leifert C. (2001). Investigations into the inhibitory effects of microcystins on plant growth, and the toxicity of plant tissues following exposure. Toxicon 39:1411–20
  • Messineo V, Bogialli S, Melchiorre S, et al. (2009). Cyanobacterial toxins in Italian freshwaters. Limnologica – Ecol Manage Inland Waters 39:95–106
  • Mezhoud K, Bauche, AL, Chateau-Joubert S, et al. (2008a). Proteomic and phosphoproteomic analysis of cellular responses in medaka fish (Oryzias latipes) following oral gavage with microcystin-LR. Toxicon 51:1431–9
  • Mezhoud K, Praseuth D, Puiseux-Dao S, et al. (2008b). Global quantitative analysis of protein expression and phosphorylation status in the liver of the medaka fish (Oryzias latipes) exposed to microcystin-LR I. Balneation study. Aquat Toxicol 86:166–75
  • Mohamed ZA, Al Shehri AM. (2009). Microcystins in groundwater wells and their accumulation in vegetable plants irrigated with contaminated waters in Saudi Arabia. J Hazard Mater 172:310–5
  • Mooney KM, Hamilton JTG, Floyd SD, et al. (2011). Initial studies on the occurrence of cyanobacteria and microcystins in Irish lakes. Environ Toxicol 26:566–70
  • Mooney MH, Le Bizec B, Elliott CT. (2009). Combining biomarker screening and mass-spectrometric analysis to detect hormone abuse in cattle. TRAC 28:665–75
  • Nishiwaki-Matsushima R, Ohta T, Nishiwaki S, et al. (1992). Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. J Cancer Res Clin Oncol 118:420–4
  • Oberholster PJ, Myburgh JG, Govender D, et al. (2009). Identification of toxigenic Microcystis strains after incidents of wild animal mortalities in the Kruger National Park, South Africa. Ecotoxicol Environ Saf 72:1177–82
  • Paerl HW, Paul VJ. (2012). Climate change: links to global expansion of harmful cyanobacteria. Water Res 46:1349–63
  • Pearson L, Mihali T, Moffitt M, et al. (2010). On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Marine Drugs 8:1650–80
  • Pflugmacher S, Wiegand C, Oberemm A, et al. (1998). Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: the first step of detoxication. Biochim Biophys Acta-Gen Subj 1425:527–33
  • Piñeiro C, Cañas B, Carrera M. (2010). The role of proteomics in the study of the influence of climate change on seafood products. Food Res Int 43:1791–802
  • Pinel G, Weigel S, Antignac J-P, et al. (2010). Targeted and untargeted profiling of biological fluids to screen for anabolic practices in cattle. TRAC 29:1269–80
  • Poste AE, Hecky RE, Guildford SJ. (2011). Evaluating microcystin exposure risk through fish consumption. Environ Sci Technol 45:5806–11
  • Pouria S, de Andrade A, Barbosa J, et al. (1998). Fatal microcystin intoxication in haemodialysis unit in Caruaru, Brazil. Lancet 352:21–6
  • Qiu T, Xie P, Guo L, Zhang D. (2009). Plasma biochemical responses of the planktivorous filter-feeding silver carp (Hypophthalmichthys molitrix) and bighead carp (Aristichthys nobilis) to prolonged toxic cyanobacterial blooms in natural waters. Environ Toxicol Phar 27:350–6
  • Repavich W, Sonzogni W, Standridge J, et al. (1990). Cyanobacteria (Blue-Green-Algae) in Wisconsin Waters - acute and chronic toxicity. Water Res 24:225–31
  • Robinson NA, Miura GA, Matson CF, et al. (1989). Characterization of chemically tritiated microcystin-LR and its distribution in mice. Toxicon 27:1035–42
  • Robinson NA, Pace JG, Matson CF, et al. (1991). Tissue distribution, excretion and hepatic biotransformation of microcystin-LR in mice. J Pharmacol Exp Ther 256:176–82
  • Runnegar M, Berndt N, Kong S, et al. (1995a). In-vivo and in-vitro binding of microcystin to protein phosphatase-1 and phosphatase-2a. Biochem Biophys Res Commun 216:162–9
  • Runnegar M, Berndt N, Kaplowitz N. (1995b). Microcystin uptake and inhibition of protein phosphatases -- effects of chemoprotectants and self-inhibition in relation to known hepatic transporters. Toxicol Appl Pharmacol 134:264–72
  • Runnegar MTC, Falconer IR. (1982). The in vivo and in vitro biological effects of the peptide hepatotoxin from the blue-green alga Microcystis aeruginosa. S Afr J Sci 78:363–6
  • Runnegar MTC, Gerdes RG, Falconer IR. (1991). The uptake of the cyanobacterial hepatotoxin microcystin by isolated rat hepatocytes. Toxicon 29:43–51
  • Schmidt CW. (2006). Signs of the times – biomarkers in perspective. Environ Health Perspect 114:A700–5
  • Sedan D, Giannuzzi L, Rosso L, et al. (2013). Biomarkers of prolonged exposure to microcystin-LR. Toxicon 68:9–17
  • Soares R, Yuan M, Servaites J, et al. (2006). Sublethal exposure from microcystins to renal insufficiency patients in Rio de Janeiro, Brazil. Environ Toxicol 21:95–103
  • Turner P, Gammie A, Hollinrake K, Codd G. (1990). Pneumonia associated with contact with cyanobacteria. Br Med J 300:1440–1
  • Turner PC, Gong YY, Pourshams A, et al. (2012). A pilot survey for Fusarium mycotoxin biomarkers in women from Golestan, Northern Iran. World Mycotoxin J 5:195–9
  • Turner PC, Rothwell JA, White KL, et al. (2008). Urinary deoxynivalenol is correlated with cereal intake in individuals from the United Kingdom. Environ Health Perspect 116:21–5
  • Ueno Y, Nagata S, Tsutsumi T, et al. (1996). Detection of microcystins, a blue-green algal hepatotoxin, in drinking water sampled in Haimen and Fusui, endemic areas of primary liver cancer in China, by highly sensitive immunoassay. Carcinogenesis 17:1317–21
  • Van Der Westhuizen L, Shephard GS, Burger HM, et al. (2011). Fumonisin B1 as a urinary biomarker of exposure in a maize intervention study among South African subsistence farmers. Cancer Epidem Biomar 20:483–9
  • Vasconcelos V. (1995). Uptake and Depuration of the Heptapeptide Toxin Microcystin-LR in Mytilus-Galloprovincialis. Aquat Toxicol 32:227–37
  • Vasconcelos V, Martins A, Vale M, et al. (2010). First report on the occurrence of microcystins in planktonic cyanobacteria from Central Mexico. Toxicon 56:425–31
  • Vasconcelos VM, Sivonen K, Evans WR, et al. (1996). Hepatotoxic microcystin diversity in cyanobacterial blooms collected in Portuguese freshwaters. Water Res 30:2377–84
  • Vichi S, Lavorini P, Funari E, et al. (2012). Contamination by Microcystis and microcystins of blue-green algae food supplements (BGAS) on the Italian market and possible risk for the exposed population. Food Chem Toxicol 50:4493–9
  • Vinogradova T, Danaher M, Baxter A, et al. (2011). Rapid surface plasmon resonance immunobiosensor assay for microcystin toxins in blue-green algae food supplements. Talanta 84:638–43
  • Wang M, Chan LL, Si M, et al. (2010a). Proteomic analysis of hepatic tissue of Zebrafish (Danio rerio) experimentally exposed to chronic microcystin-LR. Toxicol Sci 113:60–9
  • Wang M, Wang D, Lin L, Hong H. (2010b). Protein profiles in zebrafish (Danio rerio) brains exposed to chronic microcystin-LR. Chemosphere 81:716–24
  • WHO (World Health Organization). (1999a). Cyanobacterial toxins. In: Chorus I, Bartram J, eds. Toxic Cyanobacteria in water – a guide to their public health consequences, monitoring and management. London: E&FN Spon, 55–124
  • WHO (World Health Organization). (1999b). Safe levels and safe practices. In: Chorus I, Bartram J, eds. Toxic cyanobacteria in water – a guide to their public health consequences, monitoring and management. London: E&FN Spon, 161–82
  • WHO (World Health Organization) International Agency for Research on Cancer. (2010). IARC monographs on the evaluation of carcinogenic risks to humans, ingested nitrate and nitrite, and cyanobacterial peptide toxins, Lyon, France, Vol. 94
  • Wood SA, Heath MW, Holland PT, et al. (2010). Identification of a benthic microcystin-producing filamentous cyanobacterium (oscillatoriales) associated with a dog poisoning in New Zealand. Toxicon 55:897--903
  • Yen H, Lin T, Liao P. (2011). Simultaneous detection of nine cyanotoxins in drinking water using dual solid-phase extraction and liquid chromatography-mass spectrometry. Toxicon 58:209–18
  • Yu H, Jang A, Kim LH, et al. (2011). Bead-based competitive fluorescence immunoassay for sensitive and rapid diagnosis of cyanotoxin risk in drinking water. Environ Sci Technol 45:7804–11
  • Yuan M, Carmichael WW, Hilborn ED. (2006). Microcystin analysis in human sera and liver from human fatalities in Caruaru, Brazil 1996. Toxicon 48:627–40
  • Zeck A, Weller MG, Bursill D, Niessner R. (2001). Generic microcystin immunoassay based on monoclonal antibodies against Adda. Analyst 126:2002–7
  • Zegura B, Sedmak B, Filipič M. (2003). Microcystin-LR induces oxidative DNA damage in human hepatoma cell line HepG2. Toxicon 41:41–8
  • Zhou L, Yu H, Chen K. (2002). Relationship between microcystin in drinking water and colorectal cancer. Biomed Environ Sci 15:166–71

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.