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Substantial Evidences Indicate That Inorganic Arsenic Is a Genotoxic Carcinogen: a Review

  • Roy, Jinia Sinha (Molecular Genetics Division, CSIR-Indian Institute of Chemical Biology) ;
  • Chatterjee, Debmita (Molecular Genetics Division, CSIR-Indian Institute of Chemical Biology) ;
  • Das, Nandana (Molecular Genetics Division, CSIR-Indian Institute of Chemical Biology) ;
  • Giri, Ashok K. (Molecular Genetics Division, CSIR-Indian Institute of Chemical Biology)
  • Received : 2018.08.12
  • Accepted : 2018.09.07
  • Published : 2018.10.15

Abstract

Arsenic is one of the most toxic environmental toxicants. More than 150 million people worldwide are exposed to arsenic through ground water contamination. It is an exclusive human carcinogen. Although the hallmarks of arsenic toxicity are skin lesions and skin cancers, arsenic can also induce cancers in the lung, liver, kidney, urinary bladder, and other internal organs. Arsenic is a non-mutagenic compound but can induce significant cytogenetic damage as measured by chromosomal aberrations, sister chromatid exchanges, and micronuclei formation in human systems. These genotoxic end points are extensively used to predict genotoxic potentials of different environmental chemicals, drugs, pesticides, and insecticides. These cytogenetic end points are also used for evaluating cancer risk. Here, by critically reviewing and analyzing the existing literature, we conclude that inorganic arsenic is a genotoxic carcinogen.

Keywords

References

  1. Polya, D. and Charlet, L. (2009) Environmental science: rising arsenic risk? Nat. Geosci., 2, 383-384. https://doi.org/10.1038/ngeo537
  2. Ghosh, P., Basu, A., Mahata, J., Basu, S., Sengupta, M., Das, J.K., Mukherjee, A., Sarkar, A.K., Mondal, L., Ray, K. and Giri, A.K. (2006) Cytogenetic damage and genetic variants in the individuals susceptible to arsenic-induced cancer through drinking water. Int. J. Cancer, 118, 2470-2478. https://doi.org/10.1002/ijc.21640
  3. Ghosh, P., Banerjee, M., De Chaudhuri, S., Chowdhury, R., Das, J.K., Mukherjee, A., Sarkar, A.K., Mondal, L., Baidya, K., Sau, T.J., Banerjee, A., Basu, A., Chaudhuri, K., Ray, K. and Giri, A.K. (2007) Comparison of health effects between individuals with and without skin lesions in the population exposed to arsenic through drinking water in West Bengal, India. J. Expo. Sci. Environ. Epidemiol., 17, 215-223. https://doi.org/10.1038/sj.jes.7500510
  4. Reichard, J.F., Schnekenburger, M. and Puga, A. (2007) Long term low-dose arsenic exposure induces loss of DNA methylation. Biochem. Biophys. Res. Commun., 352, 188-192. https://doi.org/10.1016/j.bbrc.2006.11.001
  5. Coppin, J.F., Qu, W. and Waalkes, M.P. (2008) Interplay between cellular methyl metabolism and adaptive efflux during oncogenic transformation from chronic arsenic exposure in human cells. J. Biol. Chem., 283, 19342-19350. https://doi.org/10.1074/jbc.M802942200
  6. Noma, K.I., Allis, C.D. and Grewal, S.I. (2001) Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science, 293, 1150-1155. https://doi.org/10.1126/science.1064150
  7. Banerjee, M., Banerjee, N., Bhattacharjee, P., Mondal, D., Lythgoe, P.R., Martinez, M., Pan, J., Polya, D.A. and Giri, A.K. (2013) High arsenic in rice is associated with elevated genotoxic effects in humans. Sci. Rep., 3, 2195. https://doi.org/10.1038/srep02195
  8. Paul, S., Banerjee, N., Chatterjee, A., Sau, T.J., Das, J.K., Mishra, P.K., Chakrabarti, P., Bandyopadhyay, A. and Giri, A.K. (2014) Arsenic-induced promoter hypomethylation and over-expression of ERCC2 reduces DNA repair capacity in humans by non-disjunction of the ERCC2-Cdk7 complex. Metallomics, 6, 864-873. https://doi.org/10.1039/c3mt00328k
  9. Liou, S.H., Lung, J.C., Chen, Y.H., Yang, T., Hsieh, L.L., Chen, C.J. and Wu, T.N. (1999) Increased chromosome-type chromosome aberration frequencies as biomarkers of cancer risk in a blackfoot endemic area. Cancer Res., 59, 1481-1484.
  10. Rossner, P., Boffetta, P., Ceppi, M., Bonassi, S., Smerhovsky, Z., Landa, K., Juzova, D. and Sram, R.J. (2005) Chromosomal aberrations in lymphocytes of healthy subjects and risk of cancer. Environ. Health Perspect., 113, 517. https://doi.org/10.1289/ehp.6925
  11. Ghosh, P., Banerjee, M., De Chaudhuri, S., Das, J.K., Sarma, N., Basu, A. and Giri, A.K. (2007) Increased chromosome aberration frequencies in the Bowen's patients compared to non-cancerous skin lesions individuals exposed to arsenic. Mutat. Res., 632, 104-110. https://doi.org/10.1016/j.mrgentox.2007.05.005
  12. Yamanaka, K., Hoshino, M., Okamoto, M., Sawamura, R., Hasegawa, A. and Okada, S. (1990) Induction of DNA damage by dimethylarsine, a metabolite of inorganic arsenics, is for the major part likely due to its peroxyl radical. Biochem. Biophys. Res. Commun., 168, 58-64. https://doi.org/10.1016/0006-291X(90)91674-H
  13. Ghosh, P., Basu, A., Singh, K.K. and Giri, A.K. (2008) Evaluation of cell types for assessment of cytogenetic damage in arsenic exposed population. Mol. Cancer., 7, 45. https://doi.org/10.1186/1476-4598-7-45
  14. Basu, A., Ghosh, P., Das, J.K., Banerjee, A., Ray, K. and Giri, A.K. (2004) Micronuclei as biomarkers of carcinogen exposure in populations exposed to arsenic through drinking water in West Bengal, India: a comparative study in three cell types. Cancer Epidemiol. Biomarkers Prev., 13, 820-827.
  15. Smith, A.H., Hopenhayn-Rich, C., Warner, M., Biggs, M.L., Moore, L. and Smith, M.T. (1993) Rationale for selecting exfoliated bladder cell micronuclei as potential biomarkers for arsenic genotoxicity. J. Toxicol. Environ. Health, 40, 223-234. https://doi.org/10.1080/15287399309531790
  16. Cohen, S.M., Chowdhury, A. and Arlond, L.L. (2016) Inorganic arsenic: a non genotoxic carcinogen. J. Environ. Sci. (China), 49, 28-37. https://doi.org/10.1016/j.jes.2016.04.015
  17. Kligerman, A. (2013) Arsenic Is A Genotoxic Carcinogen. Env. Mutagenesis Geneomics Society Meeting (2013 Sep 21-25), Monterey, CA.
  18. Hei, T.K., Liu, S.X. and Waldren, C. (1998) Mutagenicity of arsenic in mammalian cells: role of reactive oxygen species. Proc. Natl. Acad. Sci. U.S.A., 95, 8103-8107. https://doi.org/10.1073/pnas.95.14.8103
  19. Marchiset-Ferlay, N., Savanovitch, C. and Sauvant-Rochat, M.P. (2012) What is the best biomarker to assess arsenic exposure via drinking water? Environ. Int., 39, 150-171. https://doi.org/10.1016/j.envint.2011.07.015
  20. Faita, F., Cori, L., Bianchi, F. and Andreassi, M.G. (2013) Arsenic-induced genotoxicity and genetic susceptibility to arsenic-related pathologies. Int. J. Environ. Res. Public Health, 10, 1527-1546. https://doi.org/10.3390/ijerph10041527
  21. Paul, S., Bhattacharjee, P., Mishra, P.K., Chatterjee, D., Biswas, A., Deb, D., Ghosh, A., Mazumder, D.G. and Giri, A.K. (2013) Human urothelial micronucleus assay to assess genotoxic recovery by reduction of arsenic in drinking water: a cohort study in West Bengal, India. Biometals, 26, 855-862. https://doi.org/10.1007/s10534-013-9652-0
  22. Mo, J., Xia, Y., Wade, T.J., Schmitt, M., Le, X.C., Dang, R. and Mumford, J.L. (2006) Chronic arsenic exposure and oxidative stress: OGG1 expression and arsenic exposure, nail seleniumand skin hyperkeratosis in Inner Mongolia. Environ. Health Perspect., 114, 835-841. https://doi.org/10.1289/ehp.8723
  23. Bach, J., Peremarti, J., Annangi, B., Marcos, R. and Hernandez, A. (2015) Reduced cellular DNA repair capacity after environmentally relevant arsenic exposure. Influence of Ogg1 deficiency. Mutat. Res., 779, 144-151. https://doi.org/10.1016/j.mrfmmm.2015.07.004
  24. Moore, M.M., Harrington-Brock, K. and Doerr, C.L. (1997) Relative genotoxic potency of arsenic and its methylated metabolites. Mutat. Res., 386, 279-290. https://doi.org/10.1016/S1383-5742(97)00003-3
  25. Tian, D., Ma, H., Feng, Z., Xia, Y., Le, X.C., Ni, Z., Allen, J., Collins, B., Schreinemachers, D. and Mumford, J.L. (2001) Analyses of micronuclei in exfoliated epithelial cells from individuals chronically exposed to arsenic via drinking water in inner Mongolia, China. J. Toxicol. Environ. Health Part A, 64, 473-484. https://doi.org/10.1080/152873901753215939
  26. Sun, H.J., Rathinasabapathi, B., Wu, B., Luo, J., Pu, L.P. and Ma, L.Q. (2014) Arsenic and selenium toxicity and their interactive effects in humans. Environ. Int., 69, 148-158. https://doi.org/10.1016/j.envint.2014.04.019
  27. Petres, J., Baron, D. and Hagedorn, M. (1977) Effects of arsenic cell metabolism and cell proliferation: cytogenetic and biochemical studies. Environ. Health Perspect., 19, 223-227. https://doi.org/10.1289/ehp.7719223
  28. Nakamuro, K. and Sayato, Y. (1981) Comparative studies of chromosomal aberration induced by trivalent and pentavalent arsenic. Mutat. Res., 88, 73-80. https://doi.org/10.1016/0165-1218(81)90091-4
  29. Vega, L., Gonsebatt, M.E. and Ostrosky-Wegman, P. (1995) Aneugenic effect of sodium arsenite on human lymphocytes in vitro: an individual susceptibility effect detected. Mutat. Res., 334, 365-373. https://doi.org/10.1016/0165-1161(95)90074-8
  30. Ramirez, P., Eastmond, D.A., Laclette, J.P. and Ostrosky-Wegman, P. (1997) Disruption of microtubule assembly and spindle formation as a mechanism for the induction of aneuploid cells by sodium arsenite and vanadium pentoxide. Mutat. Res., 386, 291-298. https://doi.org/10.1016/S1383-5742(97)00018-5
  31. Huang, R.Y., Jan, K.Y. and Lee, T.C. (1987) Posttreatment with sodium arsenite is coclastogenic in log phase but not in stationary phase. Hum. Genet., 75, 159-162. https://doi.org/10.1007/BF00591079
  32. Huang, R.N., Ho, I.C., Yih, L.H. and Lee, T.C. (1995) Sodium arsenite induces chromosome endoreduplication and inhibits protein phosphatase activity in human fibroblasts. Environ. Mol. Mutagen., 25, 188-196. https://doi.org/10.1002/em.2850250304
  33. Oya-Ohta, Y., Kaise, T. and Ochi, T. (1996) Induction of chromosomal aberrations in cultured human fibroblasts by inorganic and organic arsenic compounds and the different roles of glutathione in such induction. Mutat. Res., 357, 123-129. https://doi.org/10.1016/0027-5107(96)00092-9
  34. Yih, L.H. and Lee, T.C. (1999) Effects of exposure protocols on induction of kinetochore-plus and-minus micronuclei by arsenite in diploid human fibroblasts. Mutat. Res., 440, 75-82. https://doi.org/10.1016/S1383-5718(99)00008-X
  35. Jiang, X., Chen, C., Zhao, W. and Zhang, Z. (2013) Sodium arsenite and arsenic trioxide differently affect the oxidative stress, genotoxicity and apoptosis in A549 cells: an implication for the paradoxical mechanism. Environ. Toxicol. Pharmacol., 36, 891-902. https://doi.org/10.1016/j.etap.2013.08.002
  36. Hu, Y., Zhao, W., Chen, C., Jiang, X. and Zhang, Z. (2014) Research on the sodium arsenite and arsenic trioxide induced proliferation and apoptosis effects on human hepatocyte. Wei Sheng Yan Jiu, 43, 203-209.
  37. Zanzoni, F. and Jung, E.G. (1980) Arsenic elevates the sister chromatid exchange (SCE) rate in human lymphocytes in vitro. Arch. Dermatol. Res., 267, 91-95. https://doi.org/10.1007/BF00416927
  38. Nordenson, I., Sweins, A. and Beckman, L. (1981) Chromosome aberrations in cultured human lymphocytes exposed to trivalent and pentavalent arsenic. Scand. J. Work Environ. Health, 7, 277-281. https://doi.org/10.5271/sjweh.2551
  39. Wen, W.N., Lieu, T.L., Chang, H.J., Wuu, S.W., Yau, M.L. and Jan, K.Y. (1981) Baseline and sodium arsenite-induced sister chromatid exchanges in cultured lymphocytes from patients with Blackfoot disease and healthy persons. Hum. Genet., 59, 201-203.
  40. Crossen, P.E. (1983) Arsenic and SCE in human lymphocytes. Mutat. Res., 119, 415-419. https://doi.org/10.1016/0165-7992(83)90194-X
  41. Sahu, R.K., Katsifis, S.P., Kinney, P.L. and Christie, N.T. (1989) Effects of nickel sulfate, lead sulfateand sodium arsenite alone and with UV light on sister chromatid exchanges in cultured human lymphocytes. Mol. Toxicol., 2, 129-136.
  42. Wiencke, J.K. and Yager, J.W. (1992) Specificity of arsenite in potentiating cytogenetic damage induced by the DNA crosslinking agent diepoxybutane. Environ. Mol. Mutagen., 19, 195-200 https://doi.org/10.1002/em.2850190303
  43. Yager, J.W. and Wiencke, J.K. (1993) Enhancement of chromosomal damage by arsenic: implications for mechanism. Environ. Health Perspect., 101, 79-82.
  44. Jha, A.N., Noditi, M., Nilsson, R. and Natarajan, A.T. (1992) Genotoxic effects of sodium arsenite on human cells. Mutat. Res., 284, 215-221. https://doi.org/10.1016/0027-5107(92)90005-M
  45. Hartmann, A. and Speit, G. (1994) Comparative investigations of the genotoxic effects of metals in the single cell gel (SCG) assay and the sister chromatid exchange (SCE) test. Environ. Mol. Mutagen., 23, 299-305. https://doi.org/10.1002/em.2850230407
  46. Rasmussen, R.E. and Menzel, D.B. (1997) Variation in arsenic-induced sister chromatid exchange in human lymphocytes and lymphoblastoid cell lines. Mutat. Res., 386, 299-306. https://doi.org/10.1016/S1383-5742(97)00010-0
  47. Schaumloffel, N. and Gebel, T. (1998) Heterogeneity of the DNA damage provoked by antimony and arsenic. Mutagenesis, 13, 281-286. https://doi.org/10.1093/mutage/13.3.281
  48. Colognato, R., Coppede, F., Ponti, J., Sabbioni, E. and Migliore, L. (2007) Genotoxicity induced by arsenic compounds in peripheral human lymphocytes analysed by cytokinesis-block micronucleus assay. Mutagenesis, 22, 255-261. https://doi.org/10.1093/mutage/gem010
  49. Avani, G. and Rao, M.V. (2007) Genotoxic effects in human lymphocytes exposed to arsenic and vitamin A. Toxicol. In Vitro, 21, 626-631. https://doi.org/10.1016/j.tiv.2006.12.010
  50. Sordo, M., Herrera, L.A., Ostrosky-Wegman, P. and Rojas, E. (2001) Cytotoxic and genotoxic effects of As, MMA and DMA on leukocytes and stimulated human lymphocytes. Teratog., Carcinog. Mutagen., 21, 249-260. https://doi.org/10.1002/tcm.1013
  51. Guillamet, E., Creus, A., Ponti, J., Sabbioni, E., Fortaner, S. and Marcos, R. (2004) In vitro DNA damage by arsenic compounds in a human lymphoblastoid cell line (TK6) assessed by the alkaline Comet assay. Mutagenesis, 19, 129-135. https://doi.org/10.1093/mutage/geh005
  52. Yedjou, C.G. and Tchounwou, P.B. (2007) In-vitro cytotoxic and genotoxic effects of arsenic trioxide on human leukemia (HL-60) cells using the MTT and alkaline single cell gel electrophoresis (Comet) assays. Mol. Cell. Biochem., 301, 123-130. https://doi.org/10.1007/s11010-006-9403-4
  53. Stevens, J.J., Graham, B., Walker, A.M., Tchounwou, P.B. and Rogers, C. (2010) The effects of arsenic trioxide on DNA synthesis and genotoxicity in human colon cancer cells. Int. J. Environ. Res. Public Health, 7, 2018-2032. https://doi.org/10.3390/ijerph7052018
  54. Salazar, A.M., Sordo, M. and Ostrosky-Wegman, P. (2009) Relationship between micronuclei formation and p53 induction. Mutat. Res., 672, 124-128. https://doi.org/10.1016/j.mrgentox.2008.10.015
  55. Alarifi, S., Ali, D., Alkahtani, S., Siddiqui, M.A. and Ali, B.A. (2013) Arsenic trioxide-mediated oxidative stress and genotoxicity in human hepatocellular carcinoma cells. Onco Targets Ther., 6, 75-84.
  56. Graham, B., Stevens, J., Wells, P., Sims, J., Rogers, C., Leggett, S.S., Ekunwe, S. and Ndebele, K. (2014) Enhancement of arsenic trioxide-mediated changes in human induced pluripotent stem cells (IPS) Int. J. Environ. Res. Public Health, 11, 7524-7536. https://doi.org/10.3390/ijerph110707524
  57. Xie, H., Huang, S., Martin, S. and Wise, J.P. (2014) Arsenic is cytotoxic and genotoxic to primary human lung cells. Mutat. Res., 760, 33-41. https://doi.org/10.1016/j.mrfmmm.2013.12.002
  58. Petres, J., Schmid-Ullrich, K. and Wolf, U. (1970) Chromosomenaberrationen an menschlichen Lymphozyten bei chronischen Arsenschäden. Dtsch. Med. Wochenschr., 95, 79-80. https://doi.org/10.1055/s-0028-1108414
  59. Nordenson, I., Salmonsson, S., Brun, E. and Beckman, G. (1979) Chromosome aberrations in psoriatic patients treated with arsenic. Hum. Genet., 48, 1-6. https://doi.org/10.1007/BF00273266
  60. Burgdorf, W., Kurvink, K. and Cervenka, J. (1977) Elevated sister chromatid exchange rate in lymphocytes of subjects treated with arsenic. Hum. Genet., 36, 69-72. https://doi.org/10.1007/BF00390438
  61. Ostrosky-Wegman, P., Gonsebatt, M.E., Montero, R., Vega, L., Barba, H., Espinosa, J., Palao, A., Cortinas, C., Garcia-Vargas, G., Del Razo, L.M. and Cebrian, M. (1991) Lymphocyte proliferation kinetics and genotoxic findings in a pilot study on individuals chronically exposed to arsenic in Mexico. Mutat. Res., 250, 477-482. https://doi.org/10.1016/0027-5107(91)90204-2
  62. Vig, B.K., Figueroa, M.L., Cornforth, M.N. and Jenkins, S.H. (1984) Chromosome studies in human subjects chronically exposed to arsenic in drinking water. Am. J. Ind. Med., 6, 325-338. https://doi.org/10.1002/ajim.4700060503
  63. Beckman, G., Beckman, L. and Nordenson, I. (1977) Chromosome aberrations in workers exposed to arsenic. Environ. Health Perspect., 19, 145-146. https://doi.org/10.1289/ehp.7719145
  64. Nordenson, I., Beckman, G., Beckman, L. and Nordstrom, S. (1978) Occupational and environmental risks in and around a smelter in northern Sweden: II. Chromosomal aberrations in workers exposed to arsenic. Hereditas, 88, 47-50.
  65. Hu, G.G. (1989) Investigation of protective effect of selenium on genetic materials among workers exposed to arsenic. Zhonghua Yu Fang Yi Xue Za Zhi, 23, 286-288.
  66. Nilsson, R., Jha, A.N., Zaprianov, Z. and Natarajan, A.T. (1993) Chromosomal aberrations in humans exposed to arsenic in the Srednogorie area, Bulgaria. Fresen. Environ. Bull., 2, 59-64.
  67. Lerda, D. (1994) Sister-chromatid exchange (SCE) among individuals chronically exposed to arsenic in drinking water. Mutat. Res., 312, 111-120. https://doi.org/10.1016/0165-1161(94)90015-9
  68. Warner, M.L., Moore, L.E., Smith, M.T., Kalman, D.A., Fanning, E. and Smith, A.H. (1994) Increased micronuclei in exfoliated bladder cells of individuals who chronically ingest arsenic-contaminated water in Nevada. Cancer Epidemiol. Biomarkers Prev., 3, 583-590.
  69. Dulout, F.N., Grillo, C.A., Seoane, A.I., Maderna, C.R., Nilsson, R., Vahter, M., Darroudi, F. and Natarajan, A.T. (1996) Chromosomal aberrations in peripheral blood lymphocytes from native Andean women and children from northwestern Argentina exposed to arsenic in drinking water. Mutat. Res., 370, 151-158. https://doi.org/10.1016/S0165-1218(96)00060-2
  70. Moore, L.E., Warner, M.L., Smith, A.H., Kalman, D.A. and Smith, M.T. (1996) Use of the fluorescent micronucleus assay to detect the genotoxic effects of radiation and arsenic exposure in exfoliated human epithelial cells. Environ. Mol. Mutagen., 27, 176-184. https://doi.org/10.1002/(SICI)1098-2280(1996)27:3<176::AID-EM2>3.0.CO;2-D
  71. Moore, L.E., Smith, A.H., Hopenhayn-Rich, C., Biggs, M.L., Kalman, D.A. and Smith, M.T. (1997) Micronuclei in exfoliated bladder cells among individuals chronically exposed to arsenic in drinking water. Cancer Epidemiol. Biomarkers Prev., 6, 31-36.
  72. Biggs, M.L., Kalman, D.A., Moore, L.E., Hopenhayn-Rich, C., Smith, M.T. and Smith, A.H. (1997) Relationship of urinary arsenic to intake estimates and a biomarker of effect, bladder cell micronuclei. Mutat. Res., 386, 185-195. https://doi.org/10.1016/S1383-5742(97)00012-4
  73. Gonsebatt, M.E., Vega, L., Salazar, A.M., Montero, R., Guzman, P., Blas, J., Del Razo, L.M., Garcia-Vargas, G., Albores, A., Cebrian, M.E. and Kelsh, M. (1997) Cytogenetic effects in human exposure to arsenic. Mutat. Res., 386, 219-228. https://doi.org/10.1016/S1383-5742(97)00009-4
  74. Mäki-Paakkanen, J., Kurttio, P., Paldy, A. and Pekkanen, J. (1998) Association between the clastogenic effect in peripheral lymphocytes and human exposure to arsenic through drinking water. Environ. Mol. Mutagen., 32, 301-313. https://doi.org/10.1002/(SICI)1098-2280(1998)32:4<301::AID-EM3>3.0.CO;2-I
  75. Martinez, V., Creus, A., Venegas, W., Arroyo, A., Beck, J.P., Gebel, T.W., Surralles, J. and Marcos, R. (2004) Evaluation of micronucleus induction in a Chilean population environmentally exposed to arsenic. Mutat. Res., 564, 65-74. https://doi.org/10.1016/j.mrgentox.2004.07.008
  76. Martinez, V., Creus, A., Venegas, W., Arroyo, A., Beck, J.P., Gebel, T.W., Surralles, J. and Marcos, R. (2005) Micronuclei assessment in buccal cells of people environmentally exposed to arsenic in northern Chile. Toxicol. Lett., 155, 319-327. https://doi.org/10.1016/j.toxlet.2004.10.007
  77. Sampayo-Reyes, A., Hernandez, A., El-Yamani, N., Lopez-Campos, C., Mayet-Machado, E., Rincon-Castañeda, C.B., Limones-Aguilar, M.D.L., Lopez-Campos, J.E., de Leon, M.B., Gonzalez-Hernandez, S. and Hinojosa-Garza, D. (2010) Arsenic induces DNA damage in environmentally exposed Mexican children and adults. Influence of GSTO1 and AS3MT polymorphisms. Toxicol. Sci., 117, 63-71. https://doi.org/10.1093/toxsci/kfq173
  78. Mahata, J., Basu, A., Ghoshal, S., Sarkar, J.N., Roy, A.K., Poddar, G., Nandy, A.K., Banerjee, A., Ray, K., Natarajan, A.T. and Nilsson, R. (2003) Chromosomal aberrations and sister chromatid exchanges in individuals exposed to arsenic through drinking water in West Bengal, India. Mutat. Res., 534, 133-143. https://doi.org/10.1016/S1383-5718(02)00255-3
  79. Basu, A., Mahata, J., Roy, A.K., Sarkar, J.N., Poddar, G., Nandy, A.K., Sarkar, P.K., Dutta, P.K., Banerjee, A., Das, M. and Ray, K. (2002) Enhanced frequency of micronuclei in individuals exposed to arsenic through drinking water in West Bengal, India. Mutat. Res., 516, 29-40. https://doi.org/10.1016/S1383-5718(02)00014-1
  80. Basu, A., Som, A., Ghoshal, S., Mondal, L., Chaubey, R.C., Bhilwade, H.N., Rahman, M.M. and Giri, A.K. (2005) Assessment of DNA damage in peripheral blood lymphocytes of individuals susceptible to arsenic induced toxicity in West Bengal, India. Toxicol. Lett., 159, 100-112. https://doi.org/10.1016/j.toxlet.2005.05.001
  81. Yañez, L., Garcia-Nieto, E., Rojas, E., Carrizales, L., Mejia, J., Calderon, J., Razo, I. and Diaz-Barriga, F. (2003) DNA damage in blood cells from children exposed to arsenic and lead in a mining area. Environ. Res., 93, 231-240. https://doi.org/10.1016/j.envres.2003.07.005
  82. Paiva, L., Marcos, R., Creus, A., Coggan, M., Oakley, A.J. and Board, P.G. (2008) Polymorphism of glutathione transferase Omega 1 in a population exposed to a high environmental arsenic burden. Pharmacogenet. Genomics, 18, 1-10. https://doi.org/10.1097/FPC.0b013e3282f29663
  83. Dastgiri, S., Mosaferi, M., Fizi, M.A., Olfati, N., Zolali, S., Pouladi, N. and Azarfam, P. (2010) Arsenic exposure, dermatological lesions, hypertensionand chromosomal abnormalities among people in a rural community of northwest Iran. J. Health Popul. Nutr., 28, 14-22.
  84. Bartolotta, S.A., Pacskowski, M.G., Hick, A. and Carballo, M.A. (2011) Micronuclei assay in exfoliated buccal cells from individuals exposed to arsenic in Argentina. Arch. Environ. Contam. Toxicol., 61, 337-343. https://doi.org/10.1007/s00244-010-9607-1
  85. Gamino-Gutierrez, S.P., Gonzalez-Perez, C.I., Gonsebatt, M.E. and Monroy-Fernandez, M.G. (2013) Arsenic and lead contamination in urban soils of Villa de la Paz (Mexico) affected by historical mine wastes and its effect on children's health studied by micronucleated exfoliated cells assay. Environ. Geochem. Health, 35, 37-51. https://doi.org/10.1007/s10653-012-9469-8
  86. Chatterjee, D., Adak, S., Banerjee, N., Bhattacharjee, P., Bandyopadhyay, A.K. and Giri, A.K. (2018) Evaluation of health effects, genetic damage and telomere length in children exposed to arsenic in West Bengal, İndia. Mutat. Res., doi:10.1016/j.mrgentox.2018.06.012/.

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  1. Perspectives on trace chemical safety and chemophobia: risk communication and risk management pp.1087-2620, 2019, https://doi.org/10.1080/15287394.2019.1575625