Environmental Science and Pollution Research

, Volume 26, Issue 11, pp 10961–10971 | Cite as

Genetic damage in human populations at mining sites in the upper basin of the San Jorge River, Colombia

  • Ángel Cruz-EsquivelEmail author
  • José Marrugo-Negrete
  • Clelia Calao-Ramos
Research Article


Contamination with mining wastes affects the environmental health and public, especially the human populations that live in these environments. The aim of this study was to evaluate the genotoxicity and levels of mercury (Hg) and arsenic (As) in blood samples from human populations exposed to mining activities in the upper basin of the San Jorge River. A total of 100 individuals participated in the study, 50 as an exposed group (Bocas de Ure = 15 individuals, Mina el Alacrán = 19 individuals, Torno Rojo = 16 individuals) and 50 individuals participated as the control group. Hg and As contents in blood samples were analyzed with atomic absorption spectrophotometry. A comet assay in peripheral blood lymphocytes and a micronucleus (MN) cytome assay (BMCyt) in exfoliated buccal cells were used to assess the effects of exposure to heavy metals on human communities located in mining areas. Higher concentrations of Hg and As were observed in human populations located in mining areas. The comet assay and BMCyt data revealed DNA damage and cell death in human communities located in mining areas. A positive association between blood arsenic and genetic damage was found. These data confirm the public health risk of the population near mining sites. Our findings suggest that populations that live at sites close to mining activities have high contents of heavy metals and genotoxic effects, representing a risk to human health.


Genotoxic Mercury Arsenic Mining Public health 



The authors wish to express their gratitude to the Administrative Department of Science, Technology and Innovation in Colombia, “Francisco José de Caldas” COLCIENCIAS code 1112-519-29083, contract number 223-2010; University of Córdoba; the Water Research Group, Environment and Applied Chemistry of the Chemistry Faculty of the University of Córdoba, Colombia; and all those who participated in the project implementation.

The authors are grateful to PhD Marcela Lopez Nigro, PhD Marta Ana Carballo, and PhD Fernanda Simoniello (Laboratory of Human Cytogenetics and Toxicology Genetics) for their generous contribution to and support of this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statements

The authors have complied with all ethical standards.


  1. Agency for toxic substances and disease (2007) Registry toxicological profile for arsenic. Department of Health and Human Services, Public Health Service. Atlanta ATSDR, pp 558Google Scholar
  2. Alonso D, Latorre S, Castillo E, Brandão P (2014) Environmental occurrence of arsenic in Colombia: a review. Environ Pollut 186:272–281. CrossRefGoogle Scholar
  3. Amorim M, Mergler D, Bahia M, Dubeau H, Miranda D, Lebel J, Burbano RR, Lucotte M (2000) Cytogenetic damage related to low levels of methylmercury contamination in the Brazilian Amazon. An Acad Bras Cienc 72:497–507CrossRefGoogle Scholar
  4. APHA (1995) Standard methods for the examination of water and wastewater,, DC 19th edn. American Public Health Association, Washington, DCGoogle Scholar
  5. Arrifano GPF, Martín-Doimeadios RCR, Jiménez-Moreno M, Fernández-Trujillo S, Augusto-Oliveira M, Souza-Monteiro JR, Macchi BM, Alvarez-Leite JI, do Nascimento JLM, Amador MT, Santos S, Ribeiro-Dos-Santos Â, Silva-Pereira LC, Oriá RB, Crespo-Lopez ME (2018) Genetic susceptibility to neurodegeneration in Amazon: apolipoprotein E genotyping in vulnerable populations exposed to mercury. Front Genet 9:285. CrossRefGoogle Scholar
  6. Beyersmann D, Hartwig A (2008) Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch Toxicol 82(8):493–512. CrossRefGoogle Scholar
  7. Bonassi S, Fenech M, Lando C, Lin YP, Ceppi M, Chang WP, Holland N, KirschVolders M, Zeiger E, Ban S, Barale R, Bigatti MP, Bolognesi C, Jia C, Di Giorgio M, Ferguson LR, Fucic A, Lima OG, Hrelia P, Krishnaja AP, Lee TK, Migliore L, Mikhalevich L, Mirkova E, Mosesso P, Müller WU, Odagiri Y, Scarffi MR, Szabova E, Vorobtsova I, Vral A, Zijno A (2001) Human micronucleus project: international database comparison for results with the cytokinesis-block micronucleus assay in human lymphocytes: i. Effect of laboratory protocol, scoring criteria, and host factors on the frequency of micronuclei. Environ Mol Mutagen 37:31–45CrossRefGoogle Scholar
  8. Calao C, Marrugo-Negrete J (2015) Efectos genotóxicos en población humana asociados a metales pesados en la región de La Mojana, Colombia. 2013. Biomédica 35:139–151. CrossRefGoogle Scholar
  9. Collins AR, Oscoz AA, Brunborg G, Gaivão I, Giovannelli L, Kruszewski M, Smith C, Stetina S (2008) The comet assay: topical issues. Mutagenesis 23:143–151CrossRefGoogle Scholar
  10. Crespo M, Lima A, Herculano A, Rodríguez R, Martin J (2007) Methylmercury genotoxicity: a novel effect in human cell lines of the central nervous system. Environ Int 33:141–146CrossRefGoogle Scholar
  11. Crespo-López M, Macêdo GL, Pereira SI, Arrifano GP, Picanço-Diniz DL, do Nascimento JL, Herculano AM (2009) Mercury and human genotoxicity: critical considerations and possible molecular mechanisms. Pharmacol Res 60(4):212–220. CrossRefGoogle Scholar
  12. Da Silva J, Moraes CR, Heuser VD, Andrade VM, Silva FR, Kvitko K, Emmel V, Rohr P, Bordin DL, Andreazza AC, Salvador M, Henriques JA, Erdtmann B (2008) Evaluation of genetic damage in a Brazilian population occupationally exposed to pesticides and its correlation with polymorphisms in metabolizing genes. Mutagenesis 23(5):415–422. CrossRefGoogle Scholar
  13. Espitia-Perez L, Sosa MQ, Salcedo-Arteaga S, Leon-Mejia G, Hoyos-Giraldo LS, Brango, H, Henriques JA (2016) Polymorphisms in metabolism and repair genes affects DNA damage caused by open-cast coal mining exposure. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 808:38–51Google Scholar
  14. Florea AM, Yamoah EN, Dopp E (2005) Intracellular calcium disturbances induced by arsenic and its methylated derivatives in relation to genomic damage and apoptosis induction. Environ Health Perspect 113:659–664CrossRefGoogle Scholar
  15. Gajski G, Gerić M, Oreščanin V, Garaj-Vrhovac V (2018) Cytokinesis-block micronucleus cytome assay parameters in peripheral blood lymphocytes of the general population: contribution of age, sex, seasonal variations and lifestyle factors. Ecotoxicol Environ Saf 148:561–570CrossRefGoogle Scholar
  16. Gamiño S, Gonzalez C, Gonsebatt ME, Monroy-Fernández MG (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 35:37–51CrossRefGoogle Scholar
  17. Gracia L, Marrugo-Negrete J, Alvis E (2010) Contaminación por mercurio en humanos y peces en el municipio de Ayapel, Córdoba, Colombia, 2009. Rev Fac Nac Salud Pública 28(2):118–124Google Scholar
  18. Grover P, Banu BS, Devi KD, Begum S (2001) In vivo genotoxic effects of mercuric chloride in rat peripheral blood leucocytes using comet assay. Toxicology 167:191–197CrossRefGoogle Scholar
  19. Guillamet E, Creis A, Ponti J (2004) In vitro DNA damage by arsenic compounds in human lymphoblastoid cell line (TK6) assessed by the alkaline comet assay. Mutagenesis 19:129–135CrossRefGoogle Scholar
  20. Halliwel B (2007) Oxidative stress and cancer: have we moved forward? Biochem J 401:1–11CrossRefGoogle Scholar
  21. Idrovo A, Rivero-Rubio C, Amaya-Castellanos C (2017) Perception of pollution and arsenic in hair of indigenous living near a ferronickel open-pit mine (Córdoba, Colombia): public health case report. Rev Univ Ind Santander Salud 49(1):115–123. Google Scholar
  22. International Agency for Research on Cancer (IARC) (2012) Arsenic, metals, fibers, and dusts. IARC Monogr Eval Carcinog Risks Hum 100:41–93Google Scholar
  23. IOMC (2008) Guiance for identifying populations at risk from mercury exposure. Inter-Organization Programme for the Sound Management of Chemicals. Accessed 10 Oct 2018
  24. Kim NS, Lee BK (2010) Blood total mercury and fish consumption in the Korean general population in KNHANES III, 2005. Sci Total Environ 408:4841–4847. CrossRefGoogle Scholar
  25. León-Mejía G, Espitía L, Hoyos L (2010) Assessment of DNA damage in coal open-cast mining workers using the cytokinesis-blocked micronucleus test and the comet assay. Sci Total Environ 409(4):686–691. CrossRefGoogle Scholar
  26. León-Mejía G, Espitia L, Hoyos LS, Da Silva J, Hartmann A, Henriques JA, Quintana M (2011) Assessment of DNA damage in coal open-cast mining workers using the cytokinesis-blocked micronucleus test and the comet assay. Sci Total Environ 409:686–691. CrossRefGoogle Scholar
  27. León-Mejía G, Quintana M, Debastiani R, Dias J, Espitia-Pérez L, Hartmann A, Henriques JA, Da Silva J (2014) Genetic damage in coal miners evaluated by buccal micronucleus cytome assay. Ecotoxicol Environ Saf 107:133–139. CrossRefGoogle Scholar
  28. Madrid G, Gracia L, Marrugo-Negrete J (2011) Genotóxicidad de metales pesados (Hg, Zn, Cu, Pb y Cd) asociado a explotaciones mineras en pobladores de la cuenca del río San Jorge del Departamento de Córdoba, Colombia. Rev Assoc Col Cienc 23:103–111Google Scholar
  29. Marrugo-Negrete J, Benitez LN, Olivero-Verbel J (2008) Distribution of mercury in several environmental compartments in an aquatic ecosystem impacted by gold mining in Northern Colombia. Arch Environ Contam Toxicol 55(2):305–316. CrossRefGoogle Scholar
  30. Marrugo-Negrete J, Benítez LN, Olivero-Verbel J, Lans E, Vazquez F (2010) Spatial and seasonal mercury distribution in the Ayapel Marsh, Mojana region, Colombia. Int J Environ Res Public Health 20(6):451–459. CrossRefGoogle Scholar
  31. Marrugo-Negrete J, Urango-Cardenas I, Burgos S, Díez S (2014) Atmospheric deposition of heavy metals in the mining area of the San Jorge river basin, Colombia. Air Qual Atmos Health 7(4):577–588. CrossRefGoogle Scholar
  32. Marrugo-Negrete J, Pinedo J, Diez S (2015) Geochemistry of mercury in tropical swamps impacted by gold mining. Chemosphere 134:44–51. CrossRefGoogle Scholar
  33. Nersesyan A, Kundi M, Waldherr M (2016) Results of micronucleus assays with individuals who are occupationally and environmentally exposed to mercury, lead and cadmium. Mutat Res Rev Mutat Res 770:119–139CrossRefGoogle Scholar
  34. Patra M, Sharma A (2002) Relative efficacy of Allium cepa and Allium sativum in anaphase-telophase test screening metal genotoxicity. Biologia 57:409–414Google Scholar
  35. Rashed MN, (2010) Monitoring of contaminated toxic and heavy metals, from mine tailings through age accumulation, in soil and some wild plants at Southeast Egypt. J Hazard Mater 178(1–3):739–746Google Scholar
  36. Robins NA, Hagan NA (2012) Mercury production and use in colonial Andean silver production: emissions and health implications. Environ Health Perspect 120(5):627–631. CrossRefGoogle Scholar
  37. Roy P, Mukherjee A, Giri S (2016) Evaluation of genetic damage in tobacco and arsenic exposed population of Southern Assam, India using buccal cytome assay and comet assay. Ecotoxicol Environ Saf 124:169–176. CrossRefGoogle Scholar
  38. Silva L, Cardoso P, Leite D, Bahia M, Bastos W, Smith M, Burbano RR (2005) Cytotoxicity and genotoxicity of low doses of mercury chloride and methylmercury chloride on human lymphocytes in vitro. Braz J Med Biol Res 38:901–907CrossRefGoogle Scholar
  39. Singh NP, McCoy MT, Tice RR (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175(1):184–191. CrossRefGoogle Scholar
  40. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336CrossRefGoogle Scholar
  41. Sysalova J, Spevackova V (2003) A study of sample mineralization methods for arsenic analysis of blood and urine by hydride generation and graphite furnace atomic absorption spectrometry. Cent Eur J Chem 1:108–120Google Scholar
  42. Tchounwou B, Yedjou C, Platolla A, Sutton D (2012) Heavy metal toxicity and the environment. Mol Clin Environ Toxicol 101:133–164. CrossRefGoogle Scholar
  43. Thomas N, Holland C, Bolognesi M, Bolognesi C, Kirsch-Volders M, Bonassi S, Zeiger E, Knasmueller S, Fenech M (2009) Buccal micronucleus cytome assay. Nat Protoc 4(6):825–837. CrossRefGoogle Scholar
  44. Tolbert P, Shy C, Allen J (1992) Micronuclei and other anomalies in buccal smears: methods development. Mutat Res 271(1):69–77. CrossRefGoogle Scholar
  45. Unidad de Planeación Minero-Energética (UPME) (2014) Indicadores de la minería en Colombia (Version preliminar). Bogota D.E. UPME. In:
  46. USGS (2006) World Coal Quality Inventory: Colombia. Cap 5 World Coal Quality Inventory: Colombia. United States Geological Survey. Accessed 02 Oct 2018
  47. World Health Organization (WHO) (2008) UNEP United Nations Environment Programme, IOMC Inter-Organization Programme for the Sound Management of Chemicals. Guidance for identifying populations at risk from mercury exposureGoogle Scholar
  48. Yáñez L, García-Nieto E, Rojas E (2003) DNA damage in blood cells from children exposed to arsenic and lead in a mining area. Environ Res 93(3):231–240. CrossRefGoogle Scholar
  49. Martín-Crespo T,  Gómez-Ortiz D, Martín-Velázquez S, Martínez-Pagán P, De Ignacio C, Lillo J, Faz A (2018) Geoenvironmental characterization of unstable abandoned mine tailings combining geophysical and geochemical methods (Cartagena-La Union district, Spain). Eng Geol 232:135–146Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Water, Applied and Environmental Chemistry GroupUniversity of CórdobaMonteríaColombia
  2. 2.Laboratory Toxicology and Environmental ManagementUniversity of CórdobaMonteríaColombia

Personalised recommendations