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Appraisal of Metal Imbalances in the Blood of Thyroid Cancer Patients in Comparison with Healthy Subjects

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Abstract

Cancer incidence and mortality rates have been increasing rapidly worldwide. A growing body of evidence revealed that exposure to trace metals is the most important aetiology for development of the cancer. Therefore, present study was intended to evaluate the imbalances in the concentrations of selected metals (Na, K, Ca, Mg, Sr, Li, Fe, Zn, Cu, Co, Mn, Ag, Cd, Cr, Ni and Pb) in the blood of newly diagnosed thyroid cancer patients in comparison with counterpart healthy subjects/controls. Concentrations of the metals were quantified by flame atomic absorption spectrometry by employing nitric acid/perchloric acid–based wet digestion method. Average concentrations of Pb (774.6 μg/dL), Cr (757.9 μg/dL), Cd (472.5 μg/dL) and Ni (360.5 μg/dL) were found to be significantly higher in the blood of cancer patients than controls. Correlation study and multivariate analysis showed strong mutual relationships among Fe-Cd-Ca-Mg-Pb, Co-Sr-Zn, Li-Ag-Na-K and Cu-Ni in the blood of thyroid cancer patients while Na-K-Fe-Co-Pb, Zn-Sr-Cr, Ca-Mg and Li-Ag-Cu-Ni exhibited strong mutual associations in the blood of healthy donors. Significant variations in the trace metal levels were observed with the age, gender, habitat, food habits and smoking habits of both donor groups. Metal levels also exhibited considerable disparities with the stages and types of thyroid cancer. Multivariate analysis of the metal data revealed significantly divergent apportionment of the metals in the blood of cancer patients compared with the healthy group.

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References

  1. Przybylik-Mazurek E, Zagrodzki P, Kuźniarz-Rymarz S, Hubalewska-Dydejczyk A (2014) Thyroid disorders—assessments of trace elements, clinical, and laboratory parameters. Biol Trace Elem Res 141(1–3):65–75

    Google Scholar 

  2. Qayyum MA, Shah MH (2014) Comparative assessment of selected metals in the scalp hair and nails of lung cancer patients and controls. Biol Trace Elem Res 158(3):305–322

    Article  PubMed  CAS  Google Scholar 

  3. Zhang F, Liu N, Wang X, Zhu L, Chai Z (2004) Study of trace elements in blood of thyroid disorder subjects before and after 131I therapy. Biol Trace Elem Res 97(2):125–133

    Article  CAS  PubMed  Google Scholar 

  4. Binkowski ŁJ, Rogoziński P, Roychoudhury S, Bruliński K, Kucharzewski M, Łaciak T, Massanyi P, Stawarz R (2015) Accumulation of metals in cancerous and healthy tissues of patients with lung cancer in southern Poland. J Environ Sci Health A Tox Hazard Subst Environ Eng 50(1):9–15

    Article  CAS  PubMed  Google Scholar 

  5. Kim HS, Kim YJ, Seo YR (2015) An overview of carcinogenic heavy metal: molecular toxicity mechanism and prevention. J Cancer Prev 20(4):232–240

    Article  PubMed  PubMed Central  Google Scholar 

  6. Pasha Q, Malik SA, Shaheen N, Shah MH (2010) Investigation of trace metals in the blood plasma and scalp hair of gastrointestinal cancer patients in comparison with controls. Clin Chim Acta 411(7–8):531–539

    Article  CAS  PubMed  Google Scholar 

  7. Hanif S, Ilyas A, Shah MH (2017) Statistical evaluation of trace metals, TSH and T4 in blood serum of thyroid disease patients in comparison with controls. Biol Trace Elem Res 183(1):58–70

    Article  PubMed  CAS  Google Scholar 

  8. Vigneri R, Malandrino P, Giani F, Russo M, Vigneri P (2017) Heavy metals in the volcanic environment and thyroid cancer. Mol Cell Endocrinol 457:73–80

    Article  CAS  PubMed  Google Scholar 

  9. Fei X, Lou Z, Christakos G, Liu Q, Ren Y, Wu J (2018) Contribution of industrial density and socioeconomic status to the spatial distribution of thyroid cancer risk in Hangzhou, China. Sci Total Environ 613:679–686

    Article  PubMed  CAS  Google Scholar 

  10. Malandrino P, Russo M, Ronchi A, Minoia C, Cataldo D, Regalbuto C, Giordano C, Attard M, Squatrito S, Trimarchi F, Vigneri R (2016) Increased thyroid cancer incidence in a basaltic volcanic area is associated with non-anthropogenic pollution and biocontamination. Endocrine 53(2):471–479

    Article  CAS  PubMed  Google Scholar 

  11. Vigneri R, Malandrino P, Vigneri P (2015) The changing epidemiology of thyroid cancer: why is incidence increasing? Curr Opin Oncol 27(1):1–7

    Article  PubMed  Google Scholar 

  12. Qayyum MA, Shah MH (2017) Study of trace metal imbalances in the blood, scalp hair and nails of oral cancer patients from Pakistan. Sci Total Environ 593–594:191–201

    Article  PubMed  CAS  Google Scholar 

  13. Baltaci AK, Dundar TK, Aksoy F, Mogulkoc R (2017) Changes in the serum levels of trace elements before and after the operation in thyroid cancer patients. Biol Trace Elem Res 175(1):57–64

    Article  CAS  PubMed  Google Scholar 

  14. Rosati MV, Montuori L, Caciari T, Sacco C, Marrocco M, Tomei G, Scala B, Sancini A, Anzelmo V, Bonomi S, Tomei F (2016) Correlation between urinary cadmium and thyroid hormones in outdoor workers exposed to urban stressors. Toxicol Ind Health 32:1978–1986

    Article  CAS  PubMed  Google Scholar 

  15. Jain RB (2014) Thyroid function and serum copper, selenium, and zinc in general US population. Biol Trace Elem Res 159(1–3):87–98

    Article  CAS  PubMed  Google Scholar 

  16. Kudabayeva KI, Koshmaganbetova GK, Mickuviene N, Skalnaya MG, Tinkov AA, Skalny AV (2016) Hair trace elements are associated with increased thyroid volume in schoolchildren with goiter. Biol Trace Elem Res 174(2):261–266

    Article  CAS  PubMed  Google Scholar 

  17. El-Fadeli S, Bouhouch S, Skalny AV, Barkouch Y, Pineau A, Cherkaoui M, Sedki A (2016) Effects of imbalance in trace element on thyroid gland from Moroccan children. Biol Trace Elem Res 170(2):288–293

    Article  CAS  PubMed  Google Scholar 

  18. Jain RB, Choi YS (2016) Interacting effects of selected trace and toxic metals on thyroid function. Int J Environ Health Res 26(1):75–91

    Article  CAS  PubMed  Google Scholar 

  19. Mendy A, Gasana J, Vieira ER (2013) Low blood lead concentrations and thyroid function of American adults. Int J Environ Health Res 23(6):461–473

    Article  CAS  PubMed  Google Scholar 

  20. Park S, Lee BK (2013) Strong positive association of traditional Asian-style diets with blood cadmium and lead levels in the Korean adult population. Int J Environ Health Res 23:531–543

    Article  CAS  PubMed  Google Scholar 

  21. Ilyas A, Shah MH (2015) Abnormalities of selected trace elements in patients with coronary artery disease. Acta Cardiol Sin 31(6):518–527

    PubMed  PubMed Central  Google Scholar 

  22. Petrosino V, Motta G, Tenore G, Coletta M, Guariglia A, Testa D (2018) The role of heavy metals and polychlorinated biphenyls (PCBs) in the oncogenesis of head and neck tumors and thyroid diseases: a pilot study. Biometals 31(2):285–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Arrebola JP, Fernández MF, Martín-Olmedo P, Molina-Molina JM, Sánchez-Pérez MJ, Sánchez-Cantalejo E, Molina-Portillo E, Expósito J, Bonde JP, Olea N (2014) Adipose tissue concentrations of persistent organic pollutants and total cancer risk in an adult cohort from southern Spain: preliminary data from year 9 of the follow-up. Sci Total Environ 500:243–249

    Article  PubMed  CAS  Google Scholar 

  24. Marcello MA, Malandrino P, Almeida JF, Martins MB, Cunha LL, Bufalo NE, Pellegriti G, Ward LS (2014) The influence of the environment on the development of thyroid tumors: a new appraisal. Endocr Relat Cancer 21(5):T235–T254

    Article  CAS  PubMed  Google Scholar 

  25. Hashimoto A, Kambe T (2015) Mg, Zn and Cu transport proteins: a brief overview from physiological and molecular perspectives. J Nutr Sci Vitaminol 61(Supplement):S116–S118

    Article  PubMed  Google Scholar 

  26. Zhang WH, Wu XJ, Niu JX, Yan H, Wang XZ, Yin XD, Pang Y (2012) Serum zinc status and Helicobacter pylori infection in gastric disease patients. Asian Pac J Cancer Prev 13:5043–5046

    Article  PubMed  Google Scholar 

  27. Li P, Xu J, Shi Y, Ye Y, Chen K, Yang J, Wu Y (2014) Association between zinc intake and risk of digestive tract cancers: a systematic review and meta-analysis. Clin Nutr 33:415–420

    Article  CAS  PubMed  Google Scholar 

  28. Gumulec J, Masarik M, Adam V, Eckschlager T, Provaznik I (2014) Serum and tissue zinc in epithelial malignancies, a meta-analysis. PLoS One 9(6):e99790

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Pakseresht M, Forman D, Malekzadeh R, Yazdanbod A, West RM, Greenwood DC (2011) Dietary habits and gastric cancer risk in north-west Iran. Cancer Causes Control 22(5):725–736

    Article  PubMed  Google Scholar 

  30. Hordyjewska A, Popiołek Ł, Kocot J (2014) The many “faces” of copper in medicine and treatment. Biometals 27(4):611–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Chung HK, Nam JS, Ahn CW, Lee YS, Kim KR (2016) Some elements in thyroid tissue are associated with more advanced stage of thyroid cancer in Korean women. Biol Trace Elem Res 171:54–62

    Article  CAS  PubMed  Google Scholar 

  32. Buha A, Matovic V, Antonijevic B, Bulat Z, Curcic M, Renieri E, Tsatsakis A, Schweitzer A, Wallace D (2018) Overview of cadmium thyroid disrupting effects and mechanisms. Int J Mol Sci 19(5):1501

    Article  PubMed Central  CAS  Google Scholar 

  33. Kim JH, Lee JY, Seo JE, Jeong JY, Jung KK, Yoon HJ, Park KS (2012) Lead, cadmium and mercury levels in the 2010 Korean diet. Food Addit Contam Part B Surveill 5(4):260–264

    Article  CAS  PubMed  Google Scholar 

  34. Bishak YK, Payahoo L, Osatdrahimi A, Nourazarian A (2015) Mechanisms of cadmium carcinogenicity in the gastrointestinal tract. Asian Pac J Cancer Prev 16(1):9–21

    Article  PubMed  Google Scholar 

  35. Ostadrahimi A, Payahoo L, Somi MH, Hashemzade SH, Esfahani A, Asgharijafarabadi M, Mobasseri M, Samadi N, Faraji S, KhajeBishak Y (2017) The association between blood cadmium levels and the risk of gastrointestinal cancer in Tabriz, northwest of Iran. Pol Ann Med 24(2):133–137

    Article  Google Scholar 

  36. Valko M, Jomova K, Rhodes CJ, Kuca K, Musielk K (2016) Redox- and non-redox-metal-induced formation of free radicals and their role in human disease. Arch Toxicol 90(1):1–37

    Article  CAS  PubMed  Google Scholar 

  37. Bertin G, Averbeck D (2006) Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 88(11):1549–1559

    Article  CAS  PubMed  Google Scholar 

  38. Lee JC, Son YO, Kumar P, Shi X (2012) Oxidative stress and metal carcinogenesis. Free Radic Biol Med 53:742–757

    Article  CAS  PubMed  Google Scholar 

  39. Zhao Q, Wang Y, Cao Y, Chen A, Ren M, Ge Y, Yu Z, Wan S (2014) Potential health risks of heavy metals in cultivated topsoil and grain, including correlations with human primary liver, lung and gastric cancer, in Anhui province, eastern China. Sci Total Environ 470-471:340–347

    Article  CAS  PubMed  Google Scholar 

  40. Lam TV, Agovino P, Niu X, Roche L (2007) Linkage study of cancer risk among lead-exposed workers in New Jersey. Sci Total Environ 372:455–462

    Article  CAS  PubMed  Google Scholar 

  41. Rousseau MC, Parent ME, Nadon L, Latreille B, Siemiatycki J (2007) Occupational exposure to lead compounds and risk of cancer among men: a population-based case-control study. Am J Epidemiol 166(9):1005–1014

    Article  PubMed  Google Scholar 

  42. Lopes ACBA, Peixe TS, Mesas AE, Paoliello MMB (2015) Lead exposure and oxidative stress: a systematic review. Rev Environ Contam Toxicol 236:193–238

    Google Scholar 

  43. Straif K, Benbrahim-Tallaa L, Baan R, Grosse Y, Secretan B, El Ghissassi F (2009) A review of human carcinogens-part C: metals, arsenic, dusts, and fibres. Lancet Oncol 10:453–454

    Article  PubMed  Google Scholar 

  44. Nickens KP, Patierno SR, Ceryak S (2010) Chromium genotoxicity: a double-edged sword. Chem Biol Interact 188(2):276–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Gatto NM, Kelsh AM, Mai DH, Suh M, Proctor DM (2010) Occupational exposure to hexavalent chromium and cancers of the gastrointestinal tract, a meta-analysis. Cancer Epidemiol 34:388–399

    Article  CAS  PubMed  Google Scholar 

  46. Beaumont JJ, Sedman RM, Reynolds SD, Sherman CD, Li LH, Howd RA (2008) Cancer mortality in a Chinese population exposed to hexavalent chromium in drinking water. Epidemiology 19(1):12–23

    Article  PubMed  Google Scholar 

  47. Bhattacharyya A, Chattopadhyay R, Mitra S, Crowe SE (2014) Oxidative stress: an essential factor in the pathogensis of gastrointestinal mucosal diseases. Physiol Rev 94(2):329–354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Li Q, Chuang SC, Eluf-Neto J, Menezes A, Matos E, Koifman S, Wünsch-Filho V, Fernandez L, Daudt AW, Curado MP, Winn DM (2012) Vitamin or mineral supplement intake and the risk of head and neck cancer: pooled analysis in the INHANCE consortium. Int J Cancer 131:1686–1699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are grateful to the administrations of the Nuclear Oncology and Radiotherapy Institute (NORI), Islamabad, Pakistan, for their invaluable help during the sample collection. Technical and financial help by the Quaid-i-Azam University, Islamabad, Pakistan, to execute this project is also acknowledged.

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  1. Department of Chemistry, Quaid-i-Azam University, Islamabad, 45320, Pakistan

    Kalsoom Bibi & Munir H. Shah

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  1. Kalsoom Bibi
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Correspondence to Munir H. Shah.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (Ethical Review Committee, NORI, Islamabad REF. NO. QAUC-2017-A77) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Bibi, K., Shah, M.H. Appraisal of Metal Imbalances in the Blood of Thyroid Cancer Patients in Comparison with Healthy Subjects. Biol Trace Elem Res 198, 410–422 (2020). https://doi.org/10.1007/s12011-020-02088-w

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