State of the art on cyanotoxins in water and their behaviour towards chlorine.

The occurrence of cyanobacterial blooms is drastically increasing in temperate countries and drinking water resources are threatened. As a result, cyanotoxins should be considered in water treatment to protect human health. This study presents a state of the art on cyanotoxins in water and their behaviour towards chlorination, a common drinking water disinfection process. Chlorination efficiency on cyanotoxins alteration depends on pH, chlorine dose and oxidant nature. Microcystins and cylindrospermopsin are efficiently transformed by chlorine, with respectively 6 and 2 by-products identified. In addition, chlorination of microcystins and cylindrospermopsin is associated with a loss of acute toxicity. Even though they have been less investigated, saxitoxins and nodularins are also altered by chlorine. For these toxins, no by-products have been identified, but the chlorinated mixture does not show acute toxicity. On the contrary, the fact that anatoxin-a has a very slow reaction kinetics suggests that this toxin resists chlorination.

[1]  Vitor Vasconcelos,et al.  Toxicology and detection methods of the alkaloid neurotoxin produced by cyanobacteria, anatoxin-a. , 2007, Environment international.

[2]  Philip R. Cohen,et al.  Cyanobacterial microcystin‐LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants , 1990, FEBS letters.

[3]  G. Newcombe,et al.  Water treatment options for dissolved cyanotoxins , 2004 .

[4]  U. Azeiteiro,et al.  Microcystin-producing blooms--a serious global public health issue. , 2004, Ecotoxicology and environmental safety.

[5]  C. Bernard,et al.  Toxicological comparison of diverse Cylindrospermopsis raciborskii strains: Evidence of liver damage caused by a French C. raciborskii strain , 2003, Environmental toxicology.

[6]  J. Meriluoto,et al.  Oxidation of the cyanobacterial hepatotoxin microcystin-LR by chlorine dioxide: reaction kinetics, characterization, and toxicity of reaction products. , 2004, Environmental science & technology.

[7]  S. Gkelis,et al.  Diversity of hepatotoxic microcystins and bioactive anabaenopeptins in cyanobacterial blooms from Greek freshwaters , 2005, Environmental toxicology.

[8]  G. Klass,et al.  Decrease in toxicity of microcystins LA and LR in drinking water by ozonation. , 2006, Toxicon : official journal of the International Society on Toxinology.

[9]  S. Azevedo,et al.  Occurrence of saxitoxins and an anatoxin-a(s)-like anticholinesterase in a Brazilian drinking water supply , 2005 .

[10]  C. Scrimgeour,et al.  Identification of anatoxin-A in benthic cyanobacteria (blue-green algae) and in associated dog poisonings at Loch Insh, Scotland. , 1992, Toxicon : official journal of the International Society on Toxinology.

[11]  S. Carmeli,et al.  7-Epicylindrospermopsin, a toxic minor metabolite of the cyanobacterium Aphanizomenon ovalisporum from lake Kinneret, Israel. , 2000, Journal of natural products.

[12]  G. Shaw,et al.  Interaction of the cyanobacterial toxin cylindrospermopsin with the eukaryotic protein synthesis system. , 2008, Toxicon : official journal of the International Society on Toxinology.

[13]  D. Dietrich,et al.  Abundance and toxicity of Planktothrix rubescens in the pre-alpine Lake Ammersee, Germany , 2009 .

[14]  I. Chorus,et al.  Seasonal dynamics of cylindrospermopsin and cyanobacteria in two German lakes. , 2008, Toxicon : official journal of the International Society on Toxinology.

[15]  B. Neilan,et al.  Ecological and molecular investigations of cyanotoxin production. , 2001, FEMS microbiology ecology.

[16]  E. Viaggiu,et al.  Anatoxin‐a toxin in the cyanobacterium Planktothrix rubescens from a fishing pond in northern Italy , 2004, Environmental toxicology.

[17]  W. Carmichael,et al.  Microcystin analysis in human sera and liver from human fatalities in Caruaru, Brazil 1996. , 2006, Toxicon : official journal of the International Society on Toxinology.

[18]  Jussi Meriluoto,et al.  Oxidation of microcystins by permanganate: reaction kinetics and implications for water treatment. , 2007, Water research.

[19]  Ho-Dong Park,et al.  Hepatotoxic microcystins and neurotoxic anatoxin‐a in cyanobacterial blooms from Korean lakes , 1998 .

[20]  G. Shaw,et al.  Chlorination for degrading saxitoxins (paralytic shellfish poisons) in water , 2003, Environmental technology.

[21]  C. Bernard,et al.  Health hazards for terrestrial vertebrates from toxic cyanobacteria in surface water ecosystems. , 2003, Veterinary research.

[22]  A. Humpage,et al.  Preliminary evidence for in vivo tumour initiation by oral administration of extracts of the blue‐green alga Cylindrospermopsis raciborskii containing the toxin cylindrospermopsin , 2001, Environmental toxicology.

[23]  F. Pomati,et al.  The genetics and genomics of cyanobacterial toxicity. , 2008, Advances in experimental medicine and biology.

[24]  Daniel W. Smith,et al.  Cyanobacteria toxins and the current state of knowledge on water treatment options: a review , 2004 .

[25]  G. Newcombe,et al.  Ozonation of NOM and algal toxins in four treated waters. , 2001, Water research.

[26]  A. Rejeb,et al.  Seasonal occurrence and toxicity of Microcystis spp. and Oscillatoria tenuis in the Lebna Dam, Tunisia. , 2008, Water research.

[27]  Jamie Bartram,et al.  SAFE LEVELS AND SAFE PRACTICES , 1999 .

[28]  G. Shaw,et al.  Degradation of the cyanobacterial toxin cylindrospermopsin, from Cylindrospermopsis raciborskii, by chlorination. , 2000, Toxicon : official journal of the International Society on Toxinology.

[29]  I. Chorus,et al.  Occurrence of the cyanobacterial toxin cylindrospermopsin in northeast Germany , 2007, Environmental toxicology.

[30]  I. Falconer.  Tumor promotion and liver injury caused by oral consumption of cyanobacteria , 1991 .

[31]  Huijuan Liu,et al.  Cyanobacteria and their toxins in Guanting Reservoir of Beijing, China. , 2008, Journal of hazardous materials.

[32]  M. Teixeira,et al.  Microcystins removal by nanofiltration membranes , 2005 .

[33]  Winn-Jung Huang,et al.  Adsorption of microcystin-LR by three types of activated carbon. , 2007, Journal of hazardous materials.

[34]  Judy A Westrick.  Cyanobacterial toxin removal in drinking water treatment processes and recreational waters. , 2008, Advances in experimental medicine and biology.

[35]  A. Humpage,et al.  Cylindrospermopsin‐induced protein synthesis inhibition and its dissociation from acute toxicity in mouse hepatocytes , 2003, Environmental toxicology.

[36]  S. Oishi,et al.  Simultaneous production of homoanatoxin-a, anatoxin-a, and a new non-toxic 4-hydroxyhomoanatoxin-a by the cyanobacterium Raphidiopsis mediterranea Skuja. , 2003, Toxicon : official journal of the International Society on Toxinology.

[37]  H. Naegeli,et al.  Identification of a microcystin in benthic cyanobacteria linked to cattle deaths on alpine pastures in Switzerland , 1997 .

[38]  A. Bourke,et al.  An outbreak of hepato-enteritis (the Palm Island mystery disease) possibly caused by algal intoxication , 1983 .

[39]  D. Dietrich,et al.  Microcystin-LR toxicodynamics, induced pathology, and immunohistochemical localization in livers of blue-green algae exposed rainbow trout (oncorhynchus mykiss). , 2000, Toxicological sciences : an official journal of the Society of Toxicology.

[40]  I. Xagoraraki,et al.  Inactivation Kinetics of the Cyanobacterial Toxin Microcystin-LR by Free Chlorine , 2006 .

[41]  M. Saker,et al.  Cattle mortality attributed to the toxic cyanobacterium Cylindrospermopsis raciborskii in an outback region of North Queensland , 1999 .

[42]  J. Białczyk,et al.  Sensitised decomposition of microcystin-LR using UV radiation. , 2004, Journal of photochemistry and photobiology. B, Biology.

[43]  J. Meriluoto,et al.  Oxidation of MC-LR and -RR with chlorine and potassium permanganate: toxicity of the reaction products. , 2008, Water research.

[44]  G. Codd,et al.  Cyanobacterial toxins: risk management for health protection. , 2005, Toxicology and applied pharmacology.

[45]  K. James,et al.  Anatoxin-a in Irish freshwater and cyanobacteria, determined using a new fluorimetric liquid chromatographic method. , 1997, Toxicon : official journal of the International Society on Toxinology.

[46]  S. Byth,et al.  PALM ISLAND MYSTERY DISEASE , 1980, The Medical journal of Australia.

[47]  J. T. Turner,et al.  Ecology of harmful algae , 2006 .

[48]  W. Preiser,et al.  Fatal microcystin intoxication in haemodialysis unit in Caruaru, Brazil , 1998, The Lancet.

[49]  Jamie Bartram,et al.  Toxic Cyanobacteria in Water: a Guide to Their Public Health Consequences, Monitoring and Management Chapter 2. Cyanobacteria in the Environment 2.1 Nature and Diversity 2.1.1 Systematics , 2022 .

[50]  M. Gage,et al.  The cyanobacterial toxin, cylindrospermopsin, induces fetal toxicity in the mouse after exposure late in gestation. , 2007, Toxicon.

[51]  I. Chorus,et al.  Concentrations of particulate and dissolved cylindrospermopsin in 21 Aphanizomenon-dominated temperate lakes. , 2007, Toxicon : official journal of the International Society on Toxinology.

[52]  W. Carmichael,et al.  Isolation and identification of the cyanotoxin cylindrospermopsin and deoxy-cylindrospermopsin from a Thailand strain of Cylindrospermopsis raciborskii (Cyanobacteria). , 2001, Toxicon : official journal of the International Society on Toxinology.

[53]  A. Quesada,et al.  Anatoxin‐a occurrence and potential cyanobacterial anatoxin‐a producers in Spanish reservoirs 1 , 2007 .

[54]  K. James,et al.  Sensitive determination of anatoxin-a, homoanatoxin-a and their degradation products by liquid chromatography with fluorimetric detection. , 1998, Journal of chromatography. A.

[55]  V. Paul.  Global warming and cyanobacterial harmful algal blooms. , 2008, Advances in experimental medicine and biology.

[56]  S. Carmeli,et al.  IDENTIFICATION OF CYLINDROSPERMOPSIN IN APHANIZOMENON OVALISPORUM (CYANOPHYCEAE) ISOLATED FROM LAKE KINNERET, ISRAEL 1 , 1997 .

[57]  W. Carmichael,et al.  Serologic evaluation of human microcystin exposure , 2007, Environmental toxicology.

[58]  J. Fawell,et al.  The toxicity of cyanobacterial toxins in the mouse: I Microcystin-LR , 1999, Human & experimental toxicology.

[59]  W. Carmichael,et al.  Human Fatalities from Cyanobacteria: Chemical and Biological Evidence for Cyanotoxins , 2001 .

[60]  M. Fenech,et al.  Micronucleus induction and chromosome loss in transformed human white cells indicate clastogenic and aneugenic action of the cyanobacterial toxin, cylindrospermopsin. , 2000, Mutation research.

[61]  M. Quilliam,et al.  First report of the cyanobacterial toxin cylindrospermopsin in New Zealand. , 2001, Toxicon : official journal of the International Society on Toxinology.

[62]  Peter K. J. Robertson,et al.  PHYSICO-CHEMICAL TREATMENT METHODS FOR THE REMOVAL OF MICROCYSTINS (CYANOBACTERIAL HEPATOTOXINS) FROM POTABLE WATERS , 1999 .

[63]  GEORGE FRANCIS,et al.  Poisonous Australian Lake , 1878, Nature.

[64]  Z. Mohamed.  Toxic cyanobacteria and cyanotoxins in public hot springs in Saudi Arabia. , 2008, Toxicon : official journal of the International Society on Toxinology.

[65]  Elke Dittmann,et al.  Cyanobacterial toxins--occurrence, biosynthesis and impact on human affairs. , 2006, Molecular nutrition & food research.

[66]  P. Henriksen,et al.  Confirmation of anatoxin-a(s), in the cyanobacterium Anabaena lemmermannii, as the cause of bird kills in Danish lakes. , 1997, Toxicon : official journal of the International Society on Toxinology.

[67]  Michael D. Burch,et al.  Destruction of cyanobacterial peptide hepatotoxins by chlorine and chloramine , 1994 .

[68]  U. von Gunten,et al.  Reactions of chlorine with inorganic and organic compounds during water treatment-Kinetics and mechanisms: a critical review. , 2008, Water research.

[69]  S. Suzuki,et al.  Stability of microcystins from cyanobacteria--II. Effect of UV light on decomposition and isomerization. , 1995, Toxicon : official journal of the International Society on Toxinology.

[70]  B. Dale,et al.  Climate Change and Harmful Algal Blooms , 2006 .

[71]  A. Humpage,et al.  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 , 2003, Environmental toxicology.

[72]  D. Dietrich,et al.  Guidance values for microcystins in water and cyanobacterial supplement products (blue-green algal supplements): a reasonable or misguided approach? , 2005, Toxicology and applied pharmacology.

[73]  G. Shaw,et al.  Deoxycylindrospermopsin, an analog of cylindrospermopsin from Cylindrospermopsis raciborskii , 1999 .

[74]  J. Burns.  Toxic cyanobacteria in Florida waters. , 2008, Advances in experimental medicine and biology.

[75]  G. Eaglesham,et al.  Cylindrospermopsin occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii (Cyanobacteria) isolates. , 2003, Toxicon : official journal of the International Society on Toxinology.

[76]  W. Carmichael,et al.  Use of a colorimetric protein phosphatase inhibition assay and enzyme linked immunosorbent assay for the study of microcystins and nodularins. , 1994, Toxicon : official journal of the International Society on Toxinology.

[77]  W. Carmichael,et al.  Sublethal exposure from microcystins to renal insufficiency patients in Rio de Janeiro, Brazil , 2006, Environmental toxicology.

[78]  J. Bartram,et al.  HUMAN HEALTH ASPECTS , 1999 .

[79]  Claudia Wiegand,et al.  Cyanobacterial toxins in Lake Baringo, Kenya , 2003 .

[80]  J. Fastner,et al.  First occurrence of cylindrospermopsin in freshwater in France , 2009, Environmental toxicology.

[81]  Geoffrey A. Codd,et al.  HARMFUL CYANOBACTERIA From mass mortalities to management measures , 2005 .

[82]  Judy A. Westrick,et al.  Manager to Manager -- Everything a Manager Should Know about Algal Toxins but Was Afraid to Ask (PDF) , 2003 .

[83]  H. Fromme,et al.  Occurrence of cyanobacterial toxins—microcystins and anatoxin‐a—in Berlin water bodies with implications to human health and regulations , 2000 .

[84]  D. Dietrich,et al.  Effect of ozonation on the removal of cyanobacterial toxins during drinking water treatment. , 2002, Environmental health perspectives.

[85]  G. Shaw,et al.  Toxicological aspects of treatment to remove cyanobacterial toxins from drinking water determined using the heterozygous P53 transgenic mouse model. , 2003, Toxicon : official journal of the International Society on Toxinology.

[86]  S. Hrudey,et al.  Adsorption of microcystin-LR by activated carbon and removal in full scale water treatment , 1996 .

[87]  W. Carmichael,et al.  Human intoxication by microcystins during renal dialysis treatment in Caruaru-Brazil. , 2002, Toxicology.

[88]  Jussi Meriluoto,et al.  Kinetics of reactions between chlorine and the cyanobacterial toxins microcystins. , 2005, Water research.

[89]  H. Galal-Gorchev.  Chlorine in Water Disinfection , 1996 .

[90]  W. Carmichael,et al.  Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR , 2005, Journal of Cancer Research and Clinical Oncology.

[91]  D. Dietrich,et al.  Cyanobacterial toxins: removal during drinking water treatment, and human risk assessment. , 2000, Environmental health perspectives.

[92]  C. Saint,et al.  Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii , 2001, Environmental toxicology.

[93]  Lise,et al.  LIVER FAILURE AND DEATH AFTER EXPOSURE TO MICROCYSTINS AT A HEMODIALYSIS CENTER IN BRAZIL LIVER FAILURE AND DEATH AFTER EXPOSURE TO MICROCYSTINS AT A HEMODIALYSIS CENTER IN BRAZIL , 2000 .

[94]  Inhibition of plant protein synthesis by the cyanobacterial hepatotoxin, cylindrospermopsin. , 2004, FEMS microbiology letters.

[95]  Lionel Ho,et al.  Differences in the chlorine reactivity of four microcystin analogues. , 2006, Water research.

[96]  H. V. van Egmond,et al.  Toxins of cyanobacteria. , 2007, Molecular nutrition & food research.

[97]  R. Vijayaraghavan,et al.  Comparative toxicity evaluation of cyanobacterial cyclic peptide toxin microcystin variants (LR, RR, YR) in mice. , 2003, Toxicology.

[98]  Jussi Meriluoto,et al.  First observation of cylindrospermopsin in Anabaena lapponica isolated from the boreal environment (Finland) , 2006, Environmental toxicology.

[99]  J. Burkholder,et al.  Occurrence of Cyanobacterial Harmful Algal Blooms Workgroup report. , 2008, Advances in experimental medicine and biology.

[100]  I. Chorus,et al.  Removal of cyanotoxins by ultrafiltration and nanofiltration , 2006 .

[101]  R M Dawson,et al.  The toxicology of microcystins. , 1998, Toxicon : official journal of the International Society on Toxinology.

[102]  A. Humpage,et al.  Cyanobacterial (blue‐green algal) toxins in water supplies: Cylindrospermopsins , 2006, Environmental toxicology.

[103]  G. Shaw,et al.  Toxicology and risk assessment of freshwater cyanobacterial (blue-green algal) toxins in water. , 2000, Reviews of environmental contamination and toxicology.

[104]  M. Saker,et al.  The Palm Island mystery disease 20 years on: A review of research on the cyanotoxin cylindrospermopsin , 2003, Environmental toxicology.

[105]  G. Shaw,et al.  Stability of cylindrospermopsin, the toxin from the cyanobacterium, Cylindrospermopsis raciborskii: Effect of pH, temperature, and sunlight on decomposition , 1999 .

[106]  S. Wood,et al.  First report of homoanatoxin-a and associated dog neurotoxicosis in New Zealand. , 2007, Toxicon : official journal of the International Society on Toxinology.

[107]  P. Pendleton,et al.  Microcystin-LR Adsorption by Activated Carbon. , 2001, Journal of colloid and interface science.

[108]  J. Meriluoto,et al.  Oxidation of the cyanobacterial hepatotoxin microcystin-LR by chlorine dioxide: influence of natural organic matter. , 2006, Environmental science & technology.

[109]  O. Thomas,et al.  Ms identification of microcystin-LR chlorination by-products. , 2009, Chemosphere.

[110]  Tapan Chakrabarti,et al.  Methods for determining microcystins (peptide hepatotoxins) and microcystin-producing cyanobacteria. , 2006, Water research.

[111]  H. Zhang,et al.  Identification of microcystins in waters used for daily life by people who live on Tai Lake during a serious cyanobacteria dominated bloom with risk analysis to human health , 2009, Environmental toxicology.

[112]  I. Falconer,et al.  Health effects associated with controlled exposures to cyanobacterial toxins. , 2008, Advances in experimental medicine and biology.

[113]  Ian Stewart,et al.  Chapter 28: Cyanobacterial poisoning in livestock, wild mammals and birds – an overview , 2008 .

[114]  M. D. G. Teixeira,et al.  Gastroenteritis epidemic in the area of the Itaparica Dam, Bahia, Brazil. , 1993, Bulletin of the Pan American Health Organization.

[115]  L. Krienitz,et al.  Contribution of hot spring cyanobacteria to the mysterious deaths of Lesser Flamingos at Lake Bogoria, Kenya. , 2003, FEMS microbiology ecology.

[116]  H. Kenneth Hudnell,et al.  Cyanobacterial harmful algal blooms: state of the science and research needs. Proceedings of the Interagency, International Symposium on Cyanobacterial Harmful Algal Blooms (ISOC-HAB). , 2008, Advances in Experimental Medicine and Biology.

[117]  S. Carmeli,et al.  Uracil Moiety is Required for Toxicity of the Cyanobacterial Hepatotoxin Cylindrospermopsin , 2001, Journal of toxicology and environmental health. Part A.

[118]  W. Carmichael,et al.  Detection of an anatoxin-a(s)-like anticholinesterase in natural blooms and cultures of cyanobacteria/blue-green algae from Danish lakes and in the stomach contents of poisoned birds. , 1997, Toxicon : official journal of the International Society on Toxinology.

[119]  A. Negri,et al.  Persistence and degradation of cyanobacterial paralytic shellfish poisons (PSPs) in freshwaters , 1997 .

[120]  J. Meriluoto,et al.  Selective oxidation of key functional groups in cyanotoxins during drinking water ozonation. , 2007, Environmental science & technology.

[121]  M. Watanabe,et al.  Hepatotoxin (microcystin) and neurotoxin (anatoxin-a) contained in natural blooms and strains of cyanobacteria from Japanese freshwaters. , 1993, Natural toxins.

[122]  E. Rodríguez,et al.  Kinetics of the oxidation of cylindrospermopsin and anatoxin-a with chlorine, monochloramine and permanganate. , 2007, Water research.

[123]  A. Ledreux,et al.  First report in a river in France of the benthic cyanobacterium Phormidium favosum producing anatoxin-a associated with dog neurotoxicosis. , 2005, Toxicon : official journal of the International Society on Toxinology.

[124]  T. Kull,et al.  Oxidative elimination of cyanotoxins: comparison of ozone, chlorine, chlorine dioxide and permanganate. , 2007, Water research.

[125]  H. Nakazawa,et al.  Stability of microcystins from cyanobacteria--IV. Effect of chlorination on decomposition. , 1997, Toxicon : official journal of the International Society on Toxinology.

[126]  G. Newcombe,et al.  Treatment options for the saxitoxin class of cyanotoxins , 2002 .

[127]  Manuel J. Rodríguez,et al.  Chlorinated disinfection by-products in drinking water according to source, treatment, season, and distribution location , 2007 .

[128]  W. Carmichael,et al.  Evidence for paralytic shellfish poisons in the freshwater cyanobacterium Lyngbya wollei (Farlow ex Gomont) comb. nov , 1997, Applied and environmental microbiology.