This study was conducted to evaluate the levels of trace metals Fe, Cr, Co, Cd, Cu, Ni, Hg, Zn, and Pb in healthy individuals and patients with thyroid disease (hyperthyroidism, hypothyroidism, and cancerous). The serum levels of 110 participants living in Birjand City, east of Iran, were collected and analyzed using ICP-MS (Agilent 7900). Results showed that the concentration levels of Cr, Co, Zn, Cd, and Pb were significantly higher at case-patients (p < 0.05), but the levels of Fe, Ni, and Hg were similar between healthy and patient subjects (p > 0.05). In patients with high or low thyroid activity, strong mutual correlations between Cr, Ni, and Fe were noticeable (p < 0.05). In hypothyroid patients, no significant correlation between Zn and Hg, Co, and Cd was found, but Zn was moderately and positively correlated with other trace metals. The moderate negative correlations between Cd-Cr (p = − 0.46) and Cd-Fe (p = − 0.43) were also observed. Logistic regression analysis showed that the effect of Cr, Co, Pb, Cu, Zn, and Cd was significant in developing hyperthyroidism and hypothyroidism; whereas, in patients with thyroid cancer, the effect of Cr, Cd, and Pb was found to be significant. In conclusion, our findings suggest that toxic metals such as Pb, Cd, and Cr can increase the risk of developing hypothyroidism and thyroid cancer, but more research is needed to evaluate the potential toxicity mechanisms of Pb, Cd, and Cr.
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Afrifa J, Ogbordjor WD, Duku-Takyi R (2018) Variation in thyroid hormone levels is associated with elevated blood mercury levels among artisanal small-scale miners in Ghana. Plos One 13:e0203335. https://doi.org/10.1371/journal.pone.0203335
Aziz MA, Habil NY, AKS D (2016) Effectiveness of zinc supplementation in regulating serum hormonal and inflammatory status in hypothyroidism patients. Med J Babylon 13:347–353
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 175:57–64. https://doi.org/10.1007/s12011-016-0768-2
Barysheva ES (2018) Experimental simulation of the effects of essential and toxic trace elements on thyroid function. Bull Exp Biol Med 164:439–441. https://doi.org/10.1007/s10517-018-4007-z
Brandão-Neto J, Silva CAB, Shuhama T, SilvaJA, Oba L (2001) Renal handling of zinc in insulin-dependent diabetes mellitus patients. BioMetals 14:75–80
Bocca B, Madeddu R, Asara Y, Tolu P, Marchal JA, Forte G (2011) Assessment of reference ranges for blood Cu, Mn, Se and Zn in a selected Italian population. J Trace Elem Med Biol 25:19–26. https://doi.org/10.1016/j.jtemb.2010.12.004
Buha A, Matovic V, Antonijevic B, Bulat Z, Curcic M, Renieri EA, Tsatsakis AM, Schweitzer A, Wallace D (2018) Overview of cadmium thyroid disrupting effects and mechanisms. Int J Mol Sci 19:1501
Bulat Z, Duki´c-Cosic D, Antonijevic B, Buha A, Bulat P, Pavlovic Z, Matovic V (2017) Can zinc supplementation ameliorate cadmium-induced alterations in the bioelement content in rabbits? Arh Hig Rada Toksikol 68:38–45
Chen A, Kim SS, Chung E, Dietrich KN (2012) Thyroid hormones in relation to lead, mercury, and cadmium exposure in the National Health and Nutrition Examination Survey, 2007–2008. Environ Health Perspect 121:181–186. https://doi.org/10.1289/ehp.1205239
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. https://doi.org/10.1007/s12011-015-0502-5
Cooper DS (2003) Hyperthyroidism. Lancet:459–468
Dhawan D, Singh B, Chand B, Singh N, Mangal PC (1995) X-ray fluorescence in the assessment of inter-elemental interaction in rat liver following lead treatment. Bio Metals 8:105–110
Dundar B, Öktem F, Arslan MK, Delibas N, Baykal B, Arslan Ç, Gultepe M, Ilhan IE (2006) The effect of long-term low-dose lead exposure on thyroid function in adolescents. Environ Res 101:140–145. https://doi.org/10.1016/j.envres.2005.10.002
Ebrahim AM, Eltayeb M, Benker B, Grill P, Attahir M, Osman A, Elsadig M, Michalke B (2011) Study on some trace element contents in serum and nail samples obtained from Sudanese subjects. Biol Trace Elem Res 144:225–233. https://doi.org/10.1007/s12011-011-9076-z
Erdal M, Sahin M, Hasimi A, Uckaya G, Kutlu M, Saglam K (2008) Trace element levels in hashimoto thyroiditis patients with subclinical hypothyroidism. Biol Trace Elem Res 123:1–7. https://doi.org/10.1007/s12011-008-8117-8
Fallahzadeh RA, Khosravi R, Dehdashti B, Ghahramani E, Omidi F, Adli A, Miri M (2018) Spatial distribution variation and probabilistic risk assessment of exposure to chromium in ground water supplies; a case study in the east of Iran. FCT. 115:260–266. https://doi.org/10.1016/j.fct.2018.03.019
Ferrari SM, Fallahi P, AntonelliA., Benvenga S (2017) Environmental issues in thyroid diseases. Front Endocrinol 8:50. https://doi.org/10.3389/fendo.2017.00050
Gil F, Hernández AF, Márquez C, Femia P, Olmedo P, López-Guarnido O, Pla A (2011) Biomonitorization of cadmium, chromium, manganese, nickel and lead in whole blood, urine, axillary hair and saliva in an occupationally exposed population. Sci Total Environ 409:1172–1180. https://doi.org/10.1016/j.scitotenv.2010.11.033
Giray B, Arnaud J, Sayek İ, Favier A, Hıncal F (2010) Trace elements status in multinodular goiter. J Trace Elem Med Biol 24:106–110. https://doi.org/10.1016/j.jtemb.2009.11.003
Hammouda F, Messaoudi I, El Hani J, Baati T, Saïd K, Kerkeni A (2008) Reversal of cadmium-induced thyroid dysfunction by selenium, zinc, or their combination in rat. Biol Trace Elem Res 126:194–203
Hanif S, Ilyas A, Shah MH (2018) Statistical evaluation of trace metals, TSH and T4 in blood serum of thyroid disease patients in comparison with controls. Biol Trace Elem Res 183:58–70. https://doi.org/10.1007/s12011-017-1137-5
Hassanin KMA, Abd El-Kawi SH, Hashem KS (2013) The prospective protective effect of selenium nanoparticles against chromium-induced oxidative and cellular damage in rat thyroid. Int J Nanomed 8:1713–1720. https://doi.org/10.2147/IJN.S42736
Hybsier S, Höfig C, Mittag J, Brabant G, Schomburg L (2015) Control of serum copper (Cu) and selenium (Se) status by thyroid hormones. Exp Clin Endocrinol Diabetes 122:12–18. https://doi.org/10.1055/s-0035-1547752
Kasperczyk A, Prokopowicz A, Dobrakowski M, Pawlas N, Kasperczyk S (2012) The effect of occupational lead exposure on blood levels of zinc, iron, copper, selenium and related proteins. Biol Trace Elem Res 150:49–55
Kazi TG, Kandhro GA, Afridi HI, Kazi N, Baig JA, Arain MB, Shah AQ, Syed N, Kumar S, Kolachi NF, Khan S (2010) Interaction of copper with iron, iodine, and thyroid hormone status in goitrous patients. Biol Trace Elem Res 134:265–279. https://doi.org/10.1007/s12011-009-8478-7
Kolpak E, Kabrits S, Bubalo V (2015) The follicle function and thyroid gland cancer. Biol Med 7:1–6
Krężel A, Maret W (2016) The biological inorganic chemistry of zinc ions. Arch Biochem Biophys 611:3–19. https://doi.org/10.1016/j.abb.2016.04.010
Kuriyama C, Mori K, Nakagawa Y, Hoshikawa S, Ozaki H, Ito S, Inoue M, Ohta M, Yoshida K (2011) Erythrocyte zinc concentration as an indicator to distinguish painless thyroiditis-associated transient hypothyroidism from permanent hypothyroidism. Endocr J 58:59–63. https://doi.org/10.1507/endocrj.K10E-152
Laurberg P, Andersen S, Karmisholt J (2005) Cold adaptation and thyroid hormone metabolism. Horm Metab Res 37:545–549
Li J, Liu Y, Kong D, Ren S, Li N (2016) T-screen and yeast assay for the detection of the thyroid-disrupting activities of cadmium, mercury, and zinc. Environ Sci Pollut Res. 23:9843–9851. https://doi.org/10.1007/s11356-016-6095-5
Liao LM, Friesen M C, Xiang YB, Cai H, Koh DH, Ji BT, Yang G, Li HL, Locke S J, Rothman N, Zheng W, Gao YT, Shu XO, Purdue M P (2016) Occupational lead exposure and associations with selected cancers: the Shanghai Men’s and Women’s Health Study cohorts. Environ Health Perspect 124:97–103. https://doi.org/10.1289/ehp.1408171
Liu Y, Liu S, Mao J, Piao S, Qin J, Peng S, Xie X, Guan H, Li Y, Shan Z, Teng W (2018) Serum trace elements profile in graves’ disease patients with or without orbitopathy in Northeast China. Biomed Res Int 2018:3029379. https://doi.org/10.1155/2018/3029379
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 53:471–479. https://doi.org/10.1007/s12020-015-0761-0
Manisha A, Roshan K M, Sudeep K, Imran M, Sumesh P S (2018) Study of trace elements in patients of hypothyroidism with special reference to zinc and copper. Biomed J Sci Tech Res 6:5190–5194
Maret W (2017) Zinc in cellular regulation: The nature and significance of “zinc signals”. Int J Mol Sci 18:2285. https://doi.org/10.3390/ijms18112285
Meeker JD, Rossano MG, Protas B, Diamond MP, Puscheck E, Daly D, Paneth N, Wirth JJ (2009) Multiple metals predict prolactin and thyrotropin (TSH) levels in men. Environ Res 109:869–873. https://doi.org/10.1016/j.envres.2009.06.004
Memon NS, Kazi TG, Afridi HI, Baig JA, Arain SS, Sahito OM, Baloch S, Waris M (2016) Evaluation of calcium and lead interaction, in addition to their impact on thyroid functions in hyper and hypothyroid patients. Environ Sci Pollut Res 23:878–886. https://doi.org/10.1007/s11356-015-5325-6
Mendy A, Gasana J, Vieira ER (2013) Low blood lead concentrations and thyroid function of American adults. Int J Environ Health Res 23:461–473. https://doi.org/10.1080/09603123.2012.755155
Petering HG, Choudhury H, Stemmer KL (1979) Some effects of oral ingestion of cadmium on zinc, copper, and iron metabolism. Environ Health Perspect 28:97–106. https://doi.org/10.1289/ehp.792897
Porcheron G, Garenaux A, Proulx J, Sabri M, Dozois C (2013) Iron, copper, zinc, and manganese transport and regulation in pathogenic enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence. Front Cell Infect Microbiol 3:90. https://doi.org/10.3389/fcimb.2013.00090
Rana SVS (2014) Perspectives in endocrine toxicity of heavy metals—a review. Biol Trace Elem Res 160:1–14. https://doi.org/10.1007/s12011-014-0023-7
Severo JS, Morais JBS, de Freitas TEC, Andrade ALP, Feitosa MM, Fontenelle LC, do Nascimento Marreiro D (2019) The role of zinc in thyroid hormones metabolism. Int J Vitamin Nut Res 89: 80-88.
Sherif MM, Mohammed YS, Zedan HAEM, Kheder MAE, Mohammed AHAES (2017) Toxic effect of some heavy metals (cadmium and lead) on thyroid function. Egypt J Hosp Med 69:2512–2516. https://doi.org/10.12816/0041703
Sirchia R, Longo A, Luparello C (2008) Cadmium regulation of apoptotic and stress response genes in tumoral and immortalized epithelial cells of the human breast. Biochimie 90:1578–1590
Stojsavljević A, Trifković J, Rasić-Milutinović Z, Jovanović D, Bogdanović G, Mutić J, Manojlović D (2018) Determination of toxic and essential trace elements in serum of healthy and hypothyroid respondents by ICP-MS: a chemometric approach for discrimination of hypothyroidism. J Trace Elem Med Biol 48:134–140. https://doi.org/10.1016/j.jtemb.2018.03.020
Stojsavljević A, Rovčanin B, Krstić Đ, Borković-Mitić S, Paunović I, Kodranov I, Manojlović D (2019) Evaluation of trace metals in thyroid tissues: comparative analysis with benign and malignant thyroid diseases. Ecotoxicol Environ Safe 183:109479
Unnikrishnan AG, Menon UV (2011) Thyroid disorders in India: an epidemiological perspective. Indian. J Endocrinol Metab 15:S78–S81. https://doi.org/10.4103/2F2230-8210.83329
Vigneri R, Malandrino P, Gianì F, Russo M, Vigneri P (2017) Heavy metals in the volcanic environment and thyroid cancer. Mol Cell Endocrinol 457:73–80. https://doi.org/10.1016/j.mce.2016.10.027
Wagner MS, Wajner SM, Maia AL (2008) The role of thyroid hormone in testicular development and function. J Endocrinol 199:351–365. https://doi.org/10.1677/JOE-08-0218
Yu J (2014) Endocrine disorders and the neurologic manifestations. Ann Pediatr Endocrinol Metab 19:184–190. https://doi.org/10.6065/2Fapem.19.4.184
Zaichick VY, Tsyb AF, Vtyurin BM (1995) Trace elements and thyroid cancer. Analyst. 120:817–821
Zhang C, Wu HB, Cheng MX, Wang L, Gao CB, Huang F (2019) Association of exposure to multiple metals with papillary thyroid cancer risk in China. Environ Sci Pollut Res:1–13
The authors would like to appreciate M Amirabadizadeh and H Ataei, who provided logistic for chemicals and samples. Moreover, the authors thank Dr. J Afrifa for their nice comments in improving the manuscript.
This study has been carried out with financial support from Birjand University of Medical Sciences (Grant number: 1397/4809).
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Rezaei, M., Javadmoosavi, S.Y., Mansouri, B. et al. Thyroid dysfunction: how concentration of toxic and essential elements contribute to risk of hypothyroidism, hyperthyroidism, and thyroid cancer . Environ Sci Pollut Res 26, 35787–35796 (2019). https://doi.org/10.1007/s11356-019-06632-7
- Thyroid diseases