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Biomonitoring of Heavy Metal(oid)s in the Residents of Abandoned Mining District in Northern Cyprus

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Abstract

Several heavy metal(oid)s are known mutagens and/or carcinogens. Exposure to these elements can lead to the development of malignancies. Gemikonagi, which is in the western part of Cyprus, was the hometown of mining operations. It is believed that the mining site is a significant heavy metal(oid) source for the environment and residents. In this biomonitoring study, a total of 60 blood samples from Gemikonagi region (n = 30) and from a control region located 40 km northeast from the mining site, Tepebasi (n = 30), and 5 soil samples from each region were collected to conduct heavy metal analysis using ICP-MS. To conduct genotoxicity analysis, alkaline comet assay and in vivo micronucleus assays were used. t test for independent samples and Mann-Whitney U tests were applied. Copper and iron were found to be enriched in Gemikonagi, while arsenic was found to be enriched in Tepebasi. Genotoxicity analyses demonstrated a statistically significant increase in parameters of micronuclei frequency (p value = 0.0001) and Comet Assay statistics upon exposure to some elements, such as arsenic (p value = 0.04) and copper (p value = 0.012). The results indicate that a general enrichment in heavy elements is not endemic to Gemikonagi, but a problem that might be generalized to the entirety of Cyprus.

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References

  1. Alkas FB, Shaban JA, Sukuroglu AA, Kurt MA, Battal D, Saygi S (2017) Monitoring and assessment of heavy metal/metalloid concentration by inductively coupled plasma mass spectroscopy (ICP-MS) method in Gonyeli Lake, Cyprus. Environ Monit Assess 189:516. https://doi.org/10.1007/s10661-017-6222-x

    Article  CAS  PubMed  Google Scholar 

  2. Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. In: Luch A (ed) Molecular, clinical and environmental toxicology. Experientia Supplementum, vol 101. Springer, Basel. https://doi.org/10.1007/978-3-7643-8340-4_6

  3. Nessa F, Khan SA, Abu Shawish KYI (2016) Lead, cadmium and nickel contents of some medicinal agents. Indian J Pharm Sci 78:111–119. https://doi.org/10.4103/0250-474X.180260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Kundi M, Waldherr M, Setayesh T et al (2016) Results of micronucleus assays with individuals who are occupationally and environmentally exposed to mercury, lead and cadmium. Mutat Res 770:119–139. https://doi.org/10.1016/J.MRREV.2016.04.002

    Article  Google Scholar 

  5. Rathnayake IVN, Megharaj M, Krishnamurti GSR, Bolan NS, Naidu R (2013) Heavy metal toxicity to bacteria–are the existing growth media accurate enough to determine heavy metal toxicity? Chemosphere 90:1195–1200. https://doi.org/10.1016/j.chemosphere.2012.09.036

    Article  CAS  PubMed  Google Scholar 

  6. Hartwig A (1994) Role of DNA repair inhibition in lead- and cadmium-induced genotoxicity: a review. Environ Health Perspect 102 Suppl:45–50. https://doi.org/10.1289/ehp.94102s345

    Article  Google Scholar 

  7. Hartwig A (1998) Carcinogenicity of metal compounds: possible role of DNA repair inhibition. Toxicol Lett 102–103:235–239. https://doi.org/10.1016/s0378-4274(98)00312-9

    Article  PubMed  Google Scholar 

  8. Zhang Z, Zhao X, Qin X (2017) Potential genotoxic and cytotoxicity of emamectin benzoate in human normal liver cells. Oncotarget 8:82185–82195. https://doi.org/10.18632/oncotarget.18988

    Article  PubMed  PubMed Central  Google Scholar 

  9. Morales ME, Derbes RS, Ade CM, Ortego JC, Stark J, Deininger PL, Roy-Engel AM (2016) Heavy metal exposure influences double strand break DNA repair outcomes. PLoS One 11:e0151367. https://doi.org/10.1371/journal.pone.0151367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. North Cyprus Online Ancient Names of Cyprus, Cyprus Names. http://www.northcyprusonline.com/North-Cyprus-Online-Ancient-Names.php. Accessed 2 Sep 2019

  11. Euromines (2012) Mining history of Cyprus - Copper mines | Euromines. http://www.euromines.org/news/newsletters/2-2012/mining-history-cyprus-copper-mines. Accessed 2 Sep 2019

  12. Lee SS, Lim JE, El-Azeem SAMA et al (2013) Heavy metal immobilization in soil near abandoned mines using eggshell waste and rapeseed residue. Environ Sci Pollut Res 20:1719–1726. https://doi.org/10.1007/s11356-012-1104-9

    Article  CAS  Google Scholar 

  13. Baycu G, Tolunay D, Ozden H, Csatari I, Karadag S, Agba T, Rognes SE (2015) An abandoned copper mining site in Cyprus and assessment of metal concentrations in plants and soil. Int J Phytoremediation 17:622–631. https://doi.org/10.1080/15226514.2014.922929

    Article  CAS  PubMed  Google Scholar 

  14. Zhao X, Li Z, Wang D, Li J, Zou B, Tao Y, Lei L, Qiao F, Huang J (2019) Assessment of residents’ total environmental exposure to heavy metals in China. Sci Rep 9:16386. https://doi.org/10.1038/s41598-019-52649-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Eaton A, Franson M (2005) Standard methods for the examination of water & wastewater. American Public Health Association, Washington, DC

    Google Scholar 

  16. Araldi RP, dos Santos MO, Barbon FF, Manjerona BA, Meirelles BR, de Oliva Neto P, da Silva PI Jr, dos Santos L, Camargo ICC, de Souza EB (2018) Analysis of antioxidant, cytotoxic and mutagenic potential of Agave sisalana Perrine extracts using Vero cells, human lymphocytes and mice polychromatic erythrocytes. Biomed Pharmacother 98:873–885. https://doi.org/10.1016/J.BIOPHA.2018.01.022

    Article  CAS  PubMed  Google Scholar 

  17. Mayo Clinic Laboratories (2017) HMDB - Clinical: Heavy Metals Screen with Demographics, Blood. https://www.mayocliniclabs.com/test-catalog/Clinical+and+Interpretive/39183. Accessed 2 Sep 2019

  18. Atsdr Toxicological profile for chromium

  19. Agency for Toxic Substances & Disease Control (2004) Agency for Toxic Substances & Disease Registry (ATSDR) - Public Health Statement: Copper. https://www.atsdr.cdc.gov/phs/phs.asp?id=204&tid=37. Accessed 2 Sep 2019

  20. Bodek I, Lyman W, Reehl WF, Roseblatt DH (1988) Environmental organic chemistry. Pergamon Press, New York

    Google Scholar 

  21. WHO Regional Office for Europe (2000) Chapter 6.10 Nickel. Copenhagen

  22. Chapter 6.12 Vanadium general description

  23. Agency for Toxic Substances & Disease Registry (2012) Agency for Toxic Substances & Disease Registry (ATSDR) - Toxicological Profile: Manganese. https://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=102&tid=23. Accessed 2 Sep 2019

  24. Mayo Clinic Laboratories (2017) ASB - Clinical: Arsenic, Blood. https://www.mayocliniclabs.com/test-catalog/Clinical+and+Interpretive/8645. Accessed 10 Jun 2020

  25. Medlineplus.gov (2019) Chromium - blood test: MedlinePlus Medical Encyclopedia. https://medlineplus.gov/ency/article/003359.htm. Accessed 10 Jun 2020

  26. University of Rochester MC (2017) Total Copper (Blood) - Health Encyclopedia - University of Rochester Medical Center. https://www.urmc.rochester.edu/encyclopedia/content.aspx?contenttypeid=167&contentid=total_copper_blood. Accessed 10 Jun 2020

  27. Mayo Clinic (2017) Hemoglobin test - Mayo Clinic. https://www.mayoclinic.org/tests-procedures/hemoglobin-test/about/pac-20385075. Accessed 2 Sep 2019

  28. Atsdr 2. Relevance to Public Health 2.1 Background and environmental exposures to nickel in the United States

  29. Atsdr ToxGuide for vanadium

  30. Atsdr 1 Manganese 2. Relevance to Public Health 2.1 Background and environmental exposures to manganese in the United States

  31. Kocadal K, Alkas FB, Battal D, Saygi S (2020) Cellular pathologies and genotoxic effects arising secondary to heavy metal exposure: a review. Hum Exp Toxicol 39:3–13

    Article  CAS  Google Scholar 

  32. Dhawan A, Bajpayee M, Parmar D (2009) Comet assay: a reliable tool for the assessment of DNA damage in different models. Cell Biol Toxicol 25:5–32

    Article  CAS  Google Scholar 

  33. Battal D, Aktas A, Sungur MA et al (2013) In vivo genotoxicity assessment of sertraline by using alkaline comet assay and the cytokinesis-block micronucleus assay. Basic Clin Pharmacol Toxicol 113:n/a–n/a. https://doi.org/10.1111/bcpt.12095

    Article  CAS  Google Scholar 

  34. Heddle JA, Cimino MC, Hayashi M, Romagna F, Shelby MD, Tucker JD, Vanparys P, MacGregor JT (1991) Micronuclei as an index of cytogenetic damage: past, present, and future. Environ Mol Mutagen 18:277–291. https://doi.org/10.1002/em.2850180414

    Article  CAS  PubMed  Google Scholar 

  35. Barkett MO, Akün E (2018) Heavy metal contents of contaminated soils and ecological risk assessment in abandoned copper mine harbor in Yedidalga, Northern Cyprus. Environ Earth Sci 77. https://doi.org/10.1007/s12665-018-7556-6

  36. University of Rochester Medical center (2019) Total Copper (Blood) - Health Encyclopedia - University of Rochester Medical Center. https://www.urmc.rochester.edu/encyclopedia/content.aspx?contenttypeid=167&contentid=total_copper_blood. Accessed 2 Sep 2019

  37. Agency for Toxic Substances & Disease Registry (2005) Agency for Toxic Substances & Disease Registry (ATSDR) - Toxicological Profile: Nickel. https://www.atsdr.cdc.gov/ToxProfiles/tp.asp?id=245&tid=44. Accessed 2 Sep 2019

  38. Babich H, Stotzky G (1983) Synergism between nickel and copper in their toxicity to microbes: mediation by pH. Ecotoxicol Environ Saf 7:576–587. https://doi.org/10.1016/0147-6513(83)90017-9

    Article  CAS  PubMed  Google Scholar 

  39. di Bucchianico S, Gliga AR, Åkerlund E, Skoglund S, Wallinder IO, Fadeel B, Karlsson HL (2018) Calcium-dependent cyto- and genotoxicity of nickel metal and nickel oxide nanoparticles in human lung cells. Part Fibre Toxicol 15:32. https://doi.org/10.1186/s12989-018-0268-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Prá D, Franke SIR, Giulian R, Yoneama ML, Dias JF, Erdtmann B, Henriques JAP (2008) Genotoxicity and mutagenicity of iron and copper in mice. BioMetals 21:289–297. https://doi.org/10.1007/s10534-007-9118-3

    Article  CAS  PubMed  Google Scholar 

  41. Valko M, Morris H, Cronin M (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208. https://doi.org/10.2174/0929867053764635

    Article  CAS  PubMed  Google Scholar 

  42. Shi C, Xie S, Jia J (2008) The study of a new method to determine copper ion by square-wave voltammetry-extraction iodometry at the liquid/liquid interfaces. J Autom Methods Manag Chem 2008:453429–453425. https://doi.org/10.1155/2008/453429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Christou A, Theologides CP, Costa C, Kalavrouziotis IK, Varnavas SP (2017) Assessment of toxic heavy metals concentrations in soils and wild and cultivated plant species in Limni abandoned copper mining site, Cyprus. J Geochem Explor 178:16–22. https://doi.org/10.1016/J.GEXPLO.2017.03.012

    Article  CAS  Google Scholar 

  44. USEPA (United States Environmental Protection Agency) (2009) Regional Screening Levels Table

  45. Yukselen MA (2002) Characterization of heavy metal contaminated soils in Northern Cyprus. Environ Geol 42:597–603. https://doi.org/10.1007/s00254-002-0556-5

    Article  CAS  Google Scholar 

  46. Akun ME (2020) Heavy metal contamination and remediation of water and soil with case studies from Cyprus, heavy metal toxicity in public health. In: Nduka JK and Rashed MN (eds) IntechOpen. https://doi.org/10.5772/intechopen.90060

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Funding

This work was supported by Near East University, Department of Scientific Research Projects (BAP), Grant Number: SAG-2017-01-36.

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Correspondence to Dilek Battal.

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Kocadal, K., Alkas, F.B., Ulutas, O.K. et al. Biomonitoring of Heavy Metal(oid)s in the Residents of Abandoned Mining District in Northern Cyprus. Biol Trace Elem Res 199, 3667–3676 (2021). https://doi.org/10.1007/s12011-020-02520-1

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