Abstract
Chlordecone (CLD) is a chlorinated hydrocarbon insecticide, now classified as a persistent organic pollutant. Several studies have previously reported that chronic exposure to CLD leads to hepatotoxicity, neurotoxicity, raises early child development and pregnancy complications, and increases the risk of liver and prostate cancer. In situ chemical reduction (ISCR) has been identified as a possible way for the remediation of soils contaminated by CLD. In the present study, the objectives were (i) to evaluate the genotoxicity and the mutagenicity of two CLD metabolites formed by ISCR, CLD-5a-hydro, or CLD-5-hydro (5a- or 5- according to CAS nomenclature; CLD-1Cl) and tri-hydroCLD (CLD-3Cl), and (ii) to explore the angiogenic properties of these molecules. Mutagenicity and genotoxicity were investigated using the Ames’s technique on Salmonella typhimurium and the in vitro micronucleus micromethod with TK6 human lymphoblastoid cells. The proangiogenic properties were evaluated on the in vitro capillary network formation of human primary endothelial cells. Like CLD, the dechlorinated derivatives of CLD studied were devoid of genotoxic and mutagenic activity. In the assay targeting angiogenic properties, significantly lower microvessel lengths formed by endothelial cells were observed for the CLD-3Cl-treated cells compared to the CLD-treated cells for two of the three tested concentrations. These results suggest that dechlorinated CLD derivatives are devoid of mutagenicity and genotoxicity and have lower proangiogenic properties than CLD.
Similar content being viewed by others
References
Achard R, Cabidoche Y-M, Caron A et al. (2007) Contamination des racines et tubercules cultivés sur sol pollué par la chlordécone aux Antilles. Cah PRAM 45–50. http://agritrop.cirad.fr/547718/1/document_547718.pdf. Accessed November 18th 2016
Ames BN, Mccann J, Yamasaki E (1975) Methods for detecting carcinogens and mutagens with the salmonella/mammalian-microsome mutagenicity test. Mutat Res 31:347–364
Badach H, Nazimek T, Kaminski R, Turski W (2000) Organochlorine pesticides concentration in the drinking water from regions of extensive agriculture in Poland. Ann Agric Environ Med AAEM 7:25–28
Belghit H, Colas C, Bristeau S et al (2015) Liquid chromatography–high-resolution mass spectrometry for identifying aqueous chlordecone hydrate dechlorinated transformation products formed by reaction with zero-valent iron. Int J Environ Anal Chem 95:93–105. doi:10.1080/03067319.2014.994615
Bjørge C, Brunborg G, Wiger R et al (1996) A comparative study of chemically induced DNA damage in isolated human and rat testicular cells. Reprod Toxicol Elmsford N 10:509–519
Borenfreund E, Babich H, Martin-Alguacil N (1988) Comparisons of two in vitro cytotoxicity assays-the neutral red (NR) and tetrazolium MTT tests. Toxicol Vitro Int J Publ Assoc BIBRA 2:1–6
Bryant JD, Wilson JT (2003) In-situ chemical oxidation-reduction and precipitation of heavy metals in soils and groundwater. United States Patent US6623646 B2
Cabidoche Y-M, Achard R, Cattan P et al (2009) long-term pollution by chlordecone of tropical volcanic soils in the French West Indies: a simple leaching model accounts for current residue. Environ Pollut Barking Essex 157:1697–1705. doi:10.1016/j.envpol.2008.12.015
Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473:298–307. doi:10.1038/nature10144
Carver RA, Griffith FD (1979) Determination of kepone dechlorination products in finfish, oysters, and crustaceans. J Agric Food Chem 27:1035–1037
Clere N, Lauret E, Malthiery Y et al (2012) Estrogen receptor alpha as a key target of organochlorines to promote angiogenesis. Angiogenesis 15:745–760. doi:10.1007/s10456-012-9288-7
Clostre F, Lesueur-Jannoyer M, Cadiboche Y-M (2010) Rémédiation à la pollution par la chlordécone aux Antilles. Cah PRAM 9–10. http://www.observatoire-eau-martinique.fr/les-outils/base-documentaire/conclusions-de-l2019atelier-abremediation-a-la-pollution-par-la-chlordecone-aux-antillesbb. Accessed November 18th 2016
Dallaire R, Muckle G, Rouget F et al (2012) Cognitive, visual, and motor development of 7-month-old Guadeloupean infants exposed to chlordecone. Environ Res 118:79–85. doi:10.1016/j.envres.2012.07.006
Delfosse V, Grimaldi M, Cavaillès V et al (2014) Structural and functional profiling of environmental ligands for estrogen receptors. Environ Health Perspect 122:1306–1313. doi:10.1289/ehp.1408453
End DW, Carchman RA, Dewey WL (1981) Neurochemical correlates of chlordecone neurotoxicity. J Toxicol Environ Health 8:707–718. doi:10.1080/15287398109530107
Faroon O, Kueberuwa S, Smith L, DeRosa C (1995) ATSDR evaluation of health effects of chemicals. II. Mirex and chlordecone: health effects, toxicokinetics, human exposure, and environmental fate. Toxicol Ind Health 11:1–203
Fenech M, Chang WP, Kirsch-Volders M et al (2003) HUMN project: detailed description of the scoring criteria for the cytokinesis-block micronucleus assay using isolated human lymphocyte cultures. Mutat Res 534:65–75
Fintz M (2009) L’autorisation du Chlordécone en France 1968–1981, Rapport AFSSET; http://www.observatoire-pesticides.fr/upload/bibliotheque/457291400429630296486151015810/autorisation_chlordecone_france__1968_1981.pdf. Accessed January 3rd, 2017
Hammond B, Katzenellenbogen BS, Krauthammer N, McConnell J (1979) Estrogenic activity of the insecticide chlordecone (kepone) and interaction with uterine estrogen receptors. Proc Natl Acad Sci U S A 76:6641–6645
Heath CW (1978) Environmental pollutants and the epidemiology of cancer. Environ Health Perspect 27:7–10
Ikegwuonu FI, Mehendale HM (1991) Biochemical assessment of the genotoxicity of the in vitro interaction between chlordecone and carbon tetrachloride in rat hepatocytes. J Appl Toxicol JAT 11:303–310
Joly PB (2010) La saga du chlordécone aux Antilles françaises. Reconstruction chronologique 1968–2008. Rapport INRA Sens; http://www.observatoire-pesticides.fr/upload/bibliotheque/852173530783222242256849728077/saga_chlordecone_antilles_francaises_1968_2008.pdf. Accessed January 3rd, 2017
Kadhel P, Monfort C, Costet N et al (2014) Chlordecone exposure, length of gestation, and risk of preterm birth. Am J Epidemiol 179:536–544. doi:10.1093/aje/kwt313
Kim S-C, Yang JE, Ok YS et al (2010) Accelerated Metolachlor degradation in soil by Zerovalent iron and compost amendments. Bull Environ Contam Toxicol 84:459–464. doi:10.1007/s00128-010-9963-6
Mahon G, Green M, Middleton B et al (1989) Analysis of data from microbial colony assays. In: Kirkland DJ (ed) UKEMS sub-committee on guidelines for mutagenicity testing report: part III statistical evaluation of mutagenicity test data. Cambridge University Press, Cambridge, New York, pp 26–65
Maron DM, Ames BN (1983) Revised methods for the salmonella mutagenicity test. Mutat Res 113:173–215
Mouvet C, Dictor M-C, Bristeau S et al (2016a) Remediation by chemical reduction in laboratory mesocosms of three chlordecone-contaminated tropical soils. Environ Sci Pollut Res Int. doi:10.1007/s11356-016-7582-4
Mouvet C, Collet B, Gaude JM et al. (2016b) Décontamination par In Situ Chemical Reduction d’un nitisol et d’un sol alluvionnaire pollués par la chlordécone. Résultats physico-chimiques et agronomiques. Rapport final. BRGM/RP-65462-FR, 188p., 61 ill., 61 tabl., 1 ann. http://infoterre.brgm.fr/rapports/RP-58704-FR.pdf. Accessed October 7th 2016
Mouvet C, Crouzet C, Bristeau S et al. (2016c) Sorption et désorption de la chlordécone et de deux de ses produits de dégradation formés par déchloration réductive. Rapport final. BRGM/RP-65357-FR, 34p., 6 fig., 10 tabl. http://infoterre.brgm.fr/rapports/RP-65357-FR.pdf. Accessed October 7th 2016
Multigner L, Kadhel P, Rouget F et al (2016) Chlordecone exposure and adverse effects in French West Indies populations. Environ Sci Pollut Res Int 23:3–8. doi:10.1007/s11356-015-4621-5
Multigner L, Ndong JR, Giusti A et al (2010) Chlordecone exposure and risk of prostate cancer. J Clin Oncol Off J Am Soc Clin Oncol 28:3457–3462. doi:10.1200/JCO.2009.27.2153
Nesslany F, Simar-Meintières S, Ficheux H, Marzin D (2009) Aloe-emodin-induced DNA fragmentation in the mouse in vivo comet assay. Mutat Res 678:13–19. doi:10.1016/j.mrgentox.2009.06.004
OPECST (Office Parlementaire d’Evaluation des Choix Scientifiques et Technologiques; 2009). Rapport sur les impacts de l’utilisation de la Chlordécone et des pesticides aux Antilles : bilan et perspectives d’évolution, par M. Jean-Yves LE DÉAUT, député et Mme Catherine PROCACCIA, sénateur; http://www.senat.fr/rap/r08-487/r08-4871.pdf. Accessed January 3rd, 2017
Phillips TM, Lee H, Trevors JT, Seech AG (2004) Mineralization of hexachlorocyclohexane in soil during solid-phase bioremediation. J Ind Microbiol Biotechnol 31:216–222. doi:10.1007/s10295-004-0139-4
Phillips TM, Lee H, Trevors JT, Seech AG (2006) Full-scale in situ bioremediation of hexachlorocyclohexane-contaminated soil. J Chem Technol Biotechnol 81:289–298. doi:10.1002/jctb.1390
Phillips TM, Seech AG, Lee H, Trevors JT (2005) Biodegradation of hexachlorocyclohexane (HCH) by microorganisms. Biodegradation 16:363–392
PNAC (2008) Plan d’action chlordécone en Martinique et en Guadeloupe: rapport interministériel d’activité (année 2009). http://agriculture.gouv.fr/telecharger/63798?token=aa65f5b7b786198cd89d253f56c23541.pdf. Accessed October 7th 2016
Reuber MD (1979) The carcinogenicity kepone. J Environ Pathol Toxicol 2:671–686
Schoeny RS, Smith CC, Loper JC (1979) Non-mutagenicity for salmonella of the chlorinated hydrocarbons aroclor 1254, 1,2,4-trichlorobenzene, mirex and kepone. Mutat Res 68:125–132
Sirica AE, Wilkerson CS, Wu LL et al (1989) Evaluation of chlordecone in a two-stage model of hepatocarcinogenesis: a significant sex difference in the hepatocellular carcinoma incidence. Carcinogenesis 10:1047–1054
Soileau SD, Moreland DE (1983) Effects of chlordecone and its alteration products on isolated rat liver mitochondria. Toxicol Appl Pharmacol 67:89–99
Taylor JR (1982) Neurological manifestations in humans exposed to chlordecone and follow-up results. Neurotoxicology 3:9–16
UNEP/POPS/POPRC.3/10 (2007) Projet d’évaluation de la gestion des risques : chlordécone. http://www.pops.int/documents/meetings/poprc_3/meetingdocs/poprc3_doc/10/K0762894.F_POPS_POPRC_3_10.pdf. Accessed January 3rd, 2017
Woignier T, Fernandes P, Jannoyer-Lesueur M, Soler A (2012) Sequestration of chlordecone in the porous structure of an andosol and effects of added organic matter: an alternative to decontamination. Eur J Soil Sci 63:717–723. doi:10.1111/j.1365-2389.2012.01471.x
Woignier T, Fernandes P, Soler A et al (2013) Soil microstructure and organic matter: keys for chlordecone sequestration. J Hazard Mater 262:357–364. doi:10.1016/j.jhazmat.2013.08.070
Yang L, Zhou B, Zha J, Wang Z (2016) Mechanistic study of chlordecone-induced endocrine disruption: based on an adverse outcome pathway network. Chemosphere 161:372–381. doi:10.1016/j.chemosphere.2016.07.034
Acknowledgements
The results presented here were obtained through financing by the French Ministry of Environment, General Directorate for Risk Prevention (action F of the 2015 grant program MEDDE/BRGM).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare no competing financial interests.
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Legeay, S., Billat, PA., Clere, N. et al. Two dechlorinated chlordecone derivatives formed by in situ chemical reduction are devoid of genotoxicity and mutagenicity and have lower proangiogenic properties compared to the parent compound. Environ Sci Pollut Res 25, 14313–14323 (2018). https://doi.org/10.1007/s11356-017-8592-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-8592-6