Abstract
Most investigations conducted in the last four decades have shown a rising incidence of thyroid diseases worldwide. Although our knowledge of the molecular pathways of thyroid disease has advanced, the initial steps in thyroid cancerogenesis have not yet been sufficiently elucidated. However, recent human biomonitoring studies have shown that specific trace metals, as major endocrine disrupters, could be considered as risk factors for impaired thyroid health and the evolution of thyroid cancer (TC). In this review, the impact of essential and toxic trace metals from the environment on thyroid health and TC was evaluated. Furthermore, this review clarifies which trace metals most likely contribute to the etiology of TC. Biomarkers based on trace metal ratios are proposed. Overall, the information described in this review is expected to be useful in planning future fundamental and applied studies on the endocrine toxicity of essential and toxic trace metals.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdullah MI, Junit SM, Ng KL, Jayapalan JJ, Karikalan B, Hashim OH (2019) Papillary thyroid cancer: genetic alterations and molecular biomarker investigations. Int J Med Sci 16:450–460
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
AJCC (American Joint Committee on Cancer) (2017) Cancer Staging Manual 8th ed. Corr. 3rd Edn
Albi E, Cataldi S, Lazzarini A, Codini M, Beccari T, Ambesi-Impiombato FS, Curcio F (2017) Radiation and thyroid cancer. Int J Mol Sci 18:911. https://doi.org/10.3390/ijms18050911
Alimonti A, Mattei D (2008) Biomarkers for human biomonitoring. In: Conti ME (ed) Biological monitoring: theory and applications bioindicators and biomarkers for environmental quality and human exposure assessment. The sustainable world, vol 17. WIT Press, Southampton, pp 163–211
Alkharashi NAO, Periasamy VS, Athinarayanan J, Alshatwi AA (2017) Cadmium triggers mitochondrial oxidative stress in human peripheral blood lymphocytes and monocytes: analysis using in vitro and system toxicology approaches. J Trace Elem Med Biol 42:117–128
Al-Sayer H, Mathew TC, Asfar S, Khourshed M, Al-Bader A, Behbehani A, Dashti H (2004) Serum changes in trace elements during thyroid cancers. Mol Cell Biochem 260:1–5. https://doi.org/10.1023/b:mcbi.0000026027.20680.c7
Baeyens W, Vrijens J, Gao Y, Croes K, Schoeters G, Den Hond E, Sioen I, Bruckers L, Nawrot T, Nelen V, Van Den Mieroop E, Morrens B, Loots I, Van Larebeke N, Leermakers M (2014) Trace metals in blood and urine of newborn/mother pairs, adolescents and adults of the Flemish population (2007–2011). Int J Hyg Environ Health 217:878–890. https://doi.org/10.1016/j.ijheh.2014.06.007
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
Baverstock K, Williams D (2006) The Chernobyl accident 20 years on: an assessment of the health consequences and the international response. Environ Health Perspect 114:1312–1317
Bishop ML, Fody EP, Schoeff LE (2010) Clinical chemistry: techniques, principles, correlations, 6th ed. Lippincott Williams & Wilkins, ISBN: 978-0-7817-9045-1.
Błazewicz A, Dolliver W, Sivsammye S, Deol A, Randhawa R, Orlicz-Szczesna G, Błazewicz R (2010) Determination of cadmium, cobalt, copper, iron, manganese, and zinc in thyroid glands of patients with diagnosed nodular goitre using ion chromatography. J Chromatogr B 878:34–38. https://doi.org/10.1016/j.jchromb.2009.11.014
Bocca B, Bena A, Pino A, D’Aversa J, Orengia M, Farina E, Salamina G, Procopio E, Chiusolo M, Gandini M, Cadum E, Musmeci L, Alimonti A (2016) Human biomonitoring of metals in adults living near a waste-to-energy incinerator in ante-operam phase: focus on reference values and health-based assessments. Environ Res 148:338–350. https://doi.org/10.1016/j.envres.2016.04.013
Bocca B, Ruggieri F, Pino A, Rovira J, Calamandrei G, Martínez MÁ, Domingo JL, Alimonti A, Schuhmacher M (2019) Human biomonitoring to evaluate exposure to toxic and essential trace elements during pregnancy. Part A: concentrations in maternal blood, urine and cord blood. Environ Res 177:108599. https://doi.org/10.1016/j.envres.2019.108599
Bocca B, Ruggieri F, Pino A, Rovira J, Calamandrei G, Mirabella F, Martínez MÁ, Domingo JL, Alimonti A, Schuhmacher M (2020) Human biomonitoring to evaluate exposure to toxic and essential trace elements during pregnancy. Part B: predictors of exposure. Environ Res 182:109108. https://doi.org/10.1016/j.envres.2019.109108
Boulyga S, Becker J, Malenchenko A et al (2000) Application of ICP-MS for multielement analysis in small sample amounts of pathological thyroid tissue. Microchim Acta 134:215–222. https://doi.org/10.1007/s006040050069
Briffa J, Sinagra E, Blundell R (2020) Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 6:e04691. https://doi.org/10.1016/j.heliyon.2020.e04691
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
Bursalıoğlu EO, Alkan FA, Barutçu UB, Demir M, Karabul Y, Balkan B, Öz E, İçelli O (2017) Prediction of electron density and trace element concentrations in human blood serum following radioiodine therapy in differentiated thyroid cancer patients. Measurement 100:19–25. https://doi.org/10.1016/j.measurement.2016.12.035
Burtis CA, Ashwood ER, Bruns DE, Tietz NW (2012) Textbook of clinical chemistry and molecular diagnostics, 5th edn. Elsevier, ISBN: 978-1-4160-6164-9.
Cabanillas ME, McFadden DG, Durante C (2016) Thyroid cancer. Lancet 388:2783–2795. https://doi.org/10.1016/S0140-6736(16)30172-6
Cabral-Pinto MMS, Inácio M, Neves O, Almeida AA, Pinto E, Oliveiros B, Ferreira da Silva EA (2020) Human health risk assessment due to agricultural activities and crop consumption in the surroundings of an industrial area. Expo Health 12:629–640. https://doi.org/10.1007/s12403-019-00323-x
Carling T, Udelsman R (2014) Thyroid cancer. Annu Rev Med 65:125–137. https://doi.org/10.1146/annurev-med-061512-105739
Ceballos E, Dubny S, Othax N, Zabala ME, Peluso F (2021) Assessment of human health risk of chromium and nitrate pollution in groundwater and soil of the Matanza-Riachuelo river basin, Argentina. Expo Health, https://doi.org/10.1007/s12403-021-00386-9.
Ceolin L, Duval MADS, Benini AF, Ferreira CV, Maia AL (2019) Medullary thyroid carcinoma beyond surgery: advances, challenges, and perspectives. Endocr Relat Cancer 26:499–518. https://doi.org/10.1530/ERC-18-0574
Cerná M, Krsková A, Cejchanová M, Spěváčková V (2012) Human biomonitoring in the Czech Republic: an overview. Int J Hyg Environ Health 215:109–119. https://doi.org/10.1016/j.ijheh.2011.09.007
Chen A, Kim SS, Chung E, Dietrich KN (2013) 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
Chen CJ, Lai JS, Wu CC, Lin TS (2006) Serum selenium in adult Taiwanese. Sci Total Environ 367:448–450. https://doi.org/10.1016/j.scitotenv.2006.03.004
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 11:54–62. https://doi.org/10.1007/s12011-015-0502-5
Correia MM, Chammas MC, Zavariz JD, Arata A, Martins LC, Marui S, Pereira LAA (2020) Evaluation of the effects of chronic occupational exposure to metallic mercury on the thyroid parenchyma and hormonal function. Int Arch Occup Environ Health 93:491–502. https://doi.org/10.1007/s00420-019-01499-0
Danforth E Jr, Burger AG (1989) The impact of nutrition on thyroid hormone physiology and action. Annu Rev Nutr 9:201–227. https://doi.org/10.1146/annurev.nu.09.070189.001221
Davies L, Ouellette M, Hunter M, Welch HG (2010) The increasing incidence of small thyroid cancers: where are the cases coming from? Laryngoscope 120:2446–2451
Davies L, Welch HG (2006) Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA 295:2164–2167
D’Cruz AK, Vaish R, Vaidya A, Nixon IJ, Williams MD, Vander Poorten V, López F, Angelos P, Shaha AR, Khafif A, Skalova A, Rinaldo A, Hunt JL, Ferlito A (2018) Molecular markers in well-differentiated thyroid cancer. Eur Arch Otorhinolaryngol 275:1375–1384. https://doi.org/10.1007/s00405-018-4944-1
de Oliveira MM, Batista BAM, Sousa MP, de Souza LM, Maia CSC (2020) Selenium and thyroid cancer: a systematic review. Nutr Cancer 72:1255–1263. https://doi.org/10.1080/01635581.2019.1679194
Derelanko MJ, Hollinger MA (2002) Handbook of toxicology, 2nd edn. Taylor & Francis, ISBN: 0-8493-0370-2.
Díaz MJ, Del Pino J, Frejo MT (2016) Metals and Thyroid Toxicity. Thyroid Tox 1:97. https://doi.org/10.2174/9781681082219116010010
Djordjevic VR, Wallace DR, Schweitzer A, Boricic N, Knezevic D, Matic S, Grubor N, Kerkez M, Radenkovic D, Bulat Z, Antonijevic B, Matovic V, Buha A (2019) Environmental cadmium exposure and pancreatic cancer: evidence from case control, animal and in vitro studies. Environ Int 128:353–361. https://doi.org/10.1016/j.envint.2019.04.048
Doumouchtsis KK, Doumouchtsis SK, Doumouchtsis EK, Perrea DN (2009) The effect of lead intoxication on endocrine functions. J Endocrinol Invest 32:175–183
Dragutinović VV, Tatić SB, Nikolić-Mandić SD, Tripković TM, Dunđerović DM, Paunović IR (2014) Copper as ancillary diagnostic tool in preoperative evaluation of possible papillary thyroid carcinoma in patients with benign thyroid disease. Biol Trace Elem Res 160:311–315. https://doi.org/10.1007/s12011-014-0071-z
Duntas LH (2011) Environmental factors and thyroid autoimmunity. Ann Endocrinol (paris) 72:108–113. https://doi.org/10.1016/j.ando.2011.03.019
Duntas LH (2015) Chemical contamination and the thyroid. Endocrine 48:53–64. https://doi.org/10.1007/s12020-014-0442-4
Duntas LH (2016) Volcanic environments: biomonitoring their links to thyroid cancer. Endocrine 53:343–346. https://doi.org/10.1007/s12020-016-0977-7
Duntas LH, Smyth PPA (2011) Selenoproteins and thyroid cancer. In: selenoproteins and mimics. Advanced topics in science and technology in China. Springer, Heidelberg
Ermakov V, Jovanović L (2010) Selenium deficiency as a consequence of human activity and its correction. J Geochem Expl 107:193–199. https://doi.org/10.1016/j.gexplo.2010.07.004
Ertek S, Cicero AF, Caglar O, Erdogan G (2010) Relationship between serum zinc levels, thyroid hormones and thyroid volume following successful iodine supplementation. Hormones (athens) 9:263–268
Esteban M, Castaño A (2009) Non-invasive matrices in human biomonitoring: a review. Environ Int 35:438–449. https://doi.org/10.1016/j.envint.2008.09.003
Fairweather-Tait SJ, Bao Y, Broadley MR, Collings R, Ford D, Hesketh JE, Hurst R (2011) Selenium in human health and disease. Antioxid Redox Signal 14:1337–1383. https://doi.org/10.1089/ars.2010.3275
Falnoga I, Tusek-Znidaric M, Horvat M, Stegnar P (2000) Mercury, selenium, and cadmium in human autopsy samples from Idrija residents and mercury mine workers. Environ Res 84:211–218. https://doi.org/10.1006/enrs.2000.4116
Ferrari SM, Fallahi P, Antonelli A, Benvenga S (2017) Environmental issues in thyroid diseases. Front Endocrinol (lausanne) 8:50. https://doi.org/10.3389/fendo.2017.00050
Filippini T, Tancredi S, Malagoli C, Malavolti M, Bargellini A, Vescovi L, Nicolini F, Vinceti M (2020) Dietary estimated intake of trace elements: risk assessment in an Italian population. Expo Health 12:641–655. https://doi.org/10.1007/s12403-019-00324-w
Fiore M, Oliveri Conti G, Caltabiano R, Buffone A, Zuccarello P, Cormaci L, Cannizzaro MA, Ferrante M (2019) Role of emerging environmental risk factors in thyroid cancer: a brief review. Int J Environ Res Public Health 16:1185. https://doi.org/10.3390/ijerph16071185
Forte G, Madeddu R, Tolu P, Asara Y, Marchal JA, Bocca B (2011) Reference intervals for blood Cd and Pb in the general population of Sardinia (Italy). Int J Hyg Environ Health 214:102–109. https://doi.org/10.1016/j.ijheh.2010.09.006
Frazzoli C, Bocca B, Mantovani A (2015) The one health perspective in trace elements biomonitoring. J Toxicol Environ Health B Crit Rev 18:344–370. https://doi.org/10.1080/10937404.2015.1085473
Garrido MCA, Navarro PJ, Asensio JP, Suárez MJV, Sanz MDT (2020) Tap water lead levels in Madrid (Spain): degree of compliance and health risk assessment. Expo Health. https://doi.org/10.1007/s12403-020-00374-5
Gaw MJ, Murphy R, Srivastava RA, Cowan DSt, O’Reilly J (2013) Clinical biochemistry, 5th edn. Elsevier, ISBN: 978-0-7020–5179-1.
Genchi G, Sinicropi MS, Lauria G, Carocci A, Catalano A (2020) The effects of cadmium toxicity. Int J Environ Res Public Health 17:3782. https://doi.org/10.3390/ijerph17113782
Gil F, Hernández AF (2015) Toxicological importance of human biomonitoring of metallic and metalloid elements in different biological samples. Food Chem Toxicol 80:287–297. https://doi.org/10.1016/j.fct.2015.03.025
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
Greene FL, Page DL, Fleming ID, Fritz AG, Balch CM, Haller DG, Morrow M (eds) (2002) AJCC cancer staging manual, 6th edn. Springer, New York
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 KM, 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 Nanomedicine 8:1713–1720
He H, Jazdzewski K, Li W, Liyanarachchi S, Nagy R, Volinia S, Calin GA, Liu C, Franssila K, Suster S et al (2005) The role of microRNA genes in papillary thyroid carcinoma. Proc Natl Acad Sci USA 102:19075–19080
Hegerova L, Griebeler ML, Reynolds JP, Henry MR, Gharib H (2015) Metastasis to the thyroid gland: report of a large series from the Mayo Clinic. Am J Clin Oncol 38:338–342
Howie AF, Arthur JR, Nicol F, Walker SW, Beech SG, Beckett GJ (1998) Identification of a 57- kilodalton selenoprotein in human thyrocytes as thioredoxin reductase and evidence that its expression is regulated through the calcium-phosphoinositol signalling pathway. Clin Endocrinol Metab 83:2052–2058
Howie AF, Walker SW, Akesson B, Arthur JR, Beckett GJ (1995) Thyroidal extracellular glutathione peroxidase: a potential regulator of thyroid-hormone synthesis. Biochem 308:713–717
Huff J, Lunn RM, Waalkes MP, Tomatis L, Infante PF (2007) Cadmium-induced cancers in animals and in humans. Int J Occup Environ Health 13:202–212
Hunt JL (2005) Unusual thyroid tumors: a review of pathologic and molecular diagnosis. Expert Rev Mol Diagn 5:725–734. https://doi.org/10.1586/14737159.5.5.725
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
IAEA (International Atomic Energy Agency) (2006). https://www.iaea.org/sites/default/files/publications/reports/2006/anrep2006_full.pdf
IARC (International Agency for Research on Cancer) (2012). file:///C:/Users/win10/Downloads/mono100F.pdf
Iavicoli I, Fontana L, Bergamaschi A (2009) The effects of metals as endocrine disruptors. J Toxicol Environ Health Part B 12:206–223
Iijima K, Otake T, Yoshinaga J, Ikegami M, Suzuki E, Naruse H, Yamanaka T, Shibuya N, Yasumizu T, Kato N (2007) Cadmium, lead, and selenium in cord blood and thyroid hormone status of newborns. Biol Trace Elem Res 119:10–18. https://doi.org/10.1007/s12011-007-0057-1
Jagodić J, Rovčanin B, Paunović I, Jovanović M, Gavrović-Jankulović M, Manojlović D, Stojsavljević A (2021) The first insight into the trace element status of human adrenal gland accompanied by elemental alterations in adrenal adenomas. J Trace Elem Med Biol 63:126658. https://doi.org/10.1016/j.jtemb.2020
Jain RB, Choi YS (2016) Interacting effects of selected trace and toxic metals on thyroid function. Int J Environ Health Res 26:75–91. https://doi.org/10.1080/09603123.2015.1020416
Jancic SA, Stosic BZ (2014) Cadmium effects on the thyroid gland. Vitam Horm 94:391–425
Katoh Y, Sato T, Yamamoto Y (2002) Determination of multielement concentrations in normal human organs from the Japanese. Biol Trace Elem Res 90:57–70. https://doi.org/10.1385/BTER:90:1-3:57
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
Khlifi R, Olmedo P, Gil F, Feki-Tounsi M, Hammami B, Rebai A, Hamza-Chaffai A (2014) Biomonitoring of cadmium, chromium, nickel and arsenic in general population living near mining and active industrial areas in Southern Tunisia. Environ Monit Assess 186:761–779. https://doi.org/10.1007/s10661-013-3415-9
Kim HS, Kim YJ, Seo YR (2015) An overview of carcinogenic heavy metal: molecular toxicity mechanism and prevention. J Cancer Prev 20:232–240. https://doi.org/10.15430/JCP.2015.20.4.232
Kobayashi J, Ikeda K, Sugiyama H (2017) Cytotoxicity of heavy metals to a thyroid carcinoma cell line. J Environ Anal Toxicol 7:3. https://doi.org/10.4172/2161-0525.1000461
Köhrle J (2013) Selenium and the thyroid. Curr Opin Endocrinol Diabetes Obes 20:441–448. https://doi.org/10.1097/01.med.0000433066.24541.88
Köhrle J (2015) Selenium and the thyroid. Curr Opin Endocrinol Diabetes Obes 22:392–401. https://doi.org/10.1097/MED.0000000000000190
Köhrle J, Gärtner R (2009) Selenium and thyroid. Best Pract Res Clin Endocrinol Metab 23:815–827. https://doi.org/10.1016/j.beem.2009.08.002
Kolpak E, Kabrits S, Bubalo V (2015) The follicle function and thyroid gland cancer. Biol Med 7:1–6
Kotyzova D, Eybl V, Mihaljevic M, Glattre E (2005) Effect of long-term administration of arsenic (III) and bromine with and without selenium and iodine supplementation on the element level in the thyroid of rat. Biomed Pap Med Fac Univ Palacky Olomouc Czech 149:329–333
Kravchenko VI, Andrusyshyna IM, Luzanchuk IA, Polumbryk MO, Tarashchenko YM (2020) Association between thyroid hormone status and trace elements in serum of patients with nodular goiter. Biol Trace Elem Res 196:393–399. https://doi.org/10.1007/s12011-019-01943-9
Kucharzewski M, Braziewicz J, Majewska U, Góźdź S (2002) Concentration of selenium in the whole blood and the thyroid tissue of patients with various thyroid diseases. Biol Trace Elem Res 88:25–30. https://doi.org/10.1385/BTER:88:1:25
Kucharzewski M, Braziewicz J, Majewska U, Gózdz S (2003) Copper, zinc, and selenium in whole blood and thyroid tissue of people with various thyroid diseases. Biol Trace Elem Res 93:9–18. https://doi.org/10.1385/BTER:93:1-3:9
Kuno R, Roquetti MH, Becker K, Seiwert M, Gouveia N (2013) Reference values for lead, cadmium and mercury in the blood of adults from the metropolitan area of Sao Paulo, Brazil. Int J Hyg Environ Health 216:243–249. https://doi.org/10.1016/j.ijheh.2012.05.010
Ladeira C, Viegas S (2016) Human biomonitoring—an overview on biomarkers and their application in occupational and environmental health. Biomonitoring 3:15–24
Ledda C, Rapisarda V (2020) Biomarkers and human biomonitoring in occupational medicine. Appl Sci 10:6181. https://doi.org/10.3390/app10186181
Limaiem F, Rehman A, Mazzoni T (2020) Papillary thyroid carcinoma. [Updated 2020 Oct 16]. In: StatPearls. Treasure island (FL): StatPearls publishing. Available from: https://www.ncbi.nlm.nih.gov/books/NBK536943/
Liu J, Gao M, Jin D, Wang T, Yang J (2020) Assessment of groundwater quality and human health risk in the aeolian-sand area of Yulin city, Northwest China. Expo Health 12:671–680. https://doi.org/10.1007/s12403-019-00326-8
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
Luo J, Hendryx M (2014) Relationship between blood cadmium, lead, and serum thyroid measures in US adults—the national health and nutrition examination survey (NHANES) 2007–2010. Int J Environ Health Res 24:125–136. https://doi.org/10.1080/09603123.2013.800962
Maksimović ZJ, Djujić I, Jović V, Rsumović M (1992) Selenium deficiency in Yugoslavia. Biol Trace Elem Res 33:187–196
Malandrino P, Russo M, Gianì F, Pellegriti G, Vigneri P, Belfiore A, Rizzarelli E, Vigneri R (2020a) Increased thyroid cancer incidence in volcanic areas: a role of increased heavy metals in the environment. Int J Mol Sci 21:3425. https://doi.org/10.3390/ijms21103425
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
Malandrino P, Russo M, Ronchi A, Moretti F, Gianì F, Vigneri P, Masucci R, Pellegriti G, Belfiore A, Vigneri R (2020b) Concentration of metals and trace elements in the normal human and rat thyroid: comparison with muscle and adipose tissue and volcanic versus control areas. Thyroid 30:290–299. https://doi.org/10.1089/thy.2019.0244
Maret W (2017) Zinc in cellular regulation: the nature and significance of Bzinc signals. Int J Mol Sci 18:2285. https://doi.org/10.3390/ijms18112285
Marotta V, Malandrino P, Russo M, Panariello I, Ionna F, Chiofalo MG, Pezzullo L (2020) Fathoming the link between anthropogenic chemical contamination and thyroid cancer. Crit Rev Oncol Hematol 150:102950. https://doi.org/10.1016/j.critrevonc.2020.102950
Maruf MAh, Punom NJ, Saha B, Moniruzzaman M, Suchi PD, Eshik ME, Rahman MS (2021) Assessment of human health risks associated with heavy metals accumulation in the freshwater fish pangasianodon hypophthalmus in Bangladesh. Expo Health. https://doi.org/10.1007/s12403-021-00387-8
Maxwell C, Volpe SL (2007) Effect of zinc supplementation on thyroid hormone function. Ann Nutr Metab 51:188–194
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
Metere A, Frezzotti F, Graves CE, Vergine M, De Luca A, Pietraforte D, Giacomelli L (2018) A possible role for selenoprotein glutathione peroxidase (GPx1) and thioredoxin reductases (TrxR1) in thyroid cancer: our experience in thyroid surgery. Cancer Cell Int 18:2–9
Miao L, St Clair DK (2009) Regulation of superoxide dismutase genes: implications in disease. Free Radic Biol Med 47:344–356. https://doi.org/10.1016/j.freeradbiomed.2009.05.018
Mirallié E, Rigaud J, Mathonnet M, Gibelin H, Regenet N, Hamy A, Bretagnol F, de Calan L, Le Néel JC, Kraimps JL (2005) Management and prognosis of metastases to the thyroid gland. J Am Coll Surg 200:203–207
Moghaddam PA, Cornejo KM, Khan A (2013) Metastatic carcinoma to the thyroid gland: a single institution 20-year experience and review of the literature. Endocr Pathol 24:116–124
Moley JF (2010) Medullary thyroid carcinoma: management of lymph node metastases. J Natl Compr Canc Netw 8:549–556
Navas-Carrillo D, Rodriguez JM, Montoro-García S, Orenes-Piñero E (2017) High-resolution proteomics and metabolomics in thyroid cancer: deciphering novel biomarkers. Crit Rev Clin Lab Sci 54:446–457. https://doi.org/10.1080/10408363.2017.1394266
Nettore IC, Colao A, Macchia PE (2018) Nutritional and environmental factors in thyroid carcinogenesis. Int J Environ Res Public Health 15:1735. https://doi.org/10.3390/ijerph15081735
Nikiforov YE, Nikiforova MN (2011) Molecular genetics and diagnosis of thyroid cancer. Nat Rev Endocrinol 7:569–580. https://doi.org/10.1038/nrendo.2011.142
Nisse C, Tagne-Fotso R, Howsam M (2017) Members of health examination centres of the Nord—Pas-de-Calais region network, Richeval C, Labat L, Leroyer A. Blood and urinary levels of metals and metalloids in the general adult population of Northern France: the IMEPOGE study, 2008–2010. Int J Hyg Environ Health 220:341–363. https://doi.org/10.1016/j.ijheh.2016.09.020
Nixon AM, Provatopoulou X, Kalogera E, Zografos GN, Gounaris A (2017) Circulating thyroid cancer biomarkers: current limitations and future prospects. Clin Endocrinol 87:117–126. https://doi.org/10.1111/cen.13369
Nunes JA, Batista BL, Rodrigues JL, Caldas NM, Neto JA, Barbosa FJr, (2010) A simple method based on ICP-MS for estimation of background levels of arsenic, cadmium, copper, manganese, nickel, lead, and selenium in blood of the Brazilian population. J Toxicol Environ Health A 73:878–887. https://doi.org/10.1080/15287391003744807
Pal D, Maiti SK (2019) Evaluation of potential human health risks from toxic metals via consumption of cultured fish species labeo rohita: a case study from an urban aquaculture pond. Expo Health 11:33–46. https://doi.org/10.1007/s12403-017-0264-8
Palazzolo DL, Jansen KP (2008) The minimal arsenic concentration required to inhibit the activity of thyroid peroxidase activity in vitro. Biol Trace Elem Res 126:49–55
Patisaul HB, Fenton SE, Aylor D (2018) Animal models of endocrine disruption. Best Pract Res Clin Endocrinol Metab 32:283–297. https://doi.org/10.1016/j.beem.2018.03.011
Pavlović Z, Miletić I, Jokić Z, Stevanović J, Šobajić S, Bulat Z (2013) The influence of selenium supplementation of animal feed on human selenium intake in Serbia. Biotechnol Anim Husb 29:345–352
Pavlovic Z, Miletic I, Zekovic M, Nikolic M, Glibetic M (2018) Impact of selenium addition to animal feeds on human selenium status in Serbia. Nutrients 10:1–7
Plonczak AM, DiMarco AN, Dina R et al (2017) Breast cancer metastases to the thyroid gland—an uncommon sentinel for diffuse metastatic disease: a case report and review of the literature. J Med Case Reports 11:2694. https://doi.org/10.1186/s13256-017-1441-x
Prozialeck WC, Lamar PC, Lynch SM (2003) Cadmium alters the localization of N-cadherin, E-cadherin, and β-catenin in the proximal tubule epithelium. Toxicol Appl Pharmacol 189:180–195
Przybylik-Mazurek E, Zagrodzki P, Kuźniarz-Rymarz S, Hubalewska-Dydejczyk A (2011) Thyroid disorders-assessments of trace elements, clinical, and laboratory parameters. Biol Trace Elem Res 141:65–75. https://doi.org/10.1007/s12011-010-8719-9
Rana SV (2014) Perspectives in endocrine toxicity of heavy metals–a review. Biol Trace Elem Res 160:1–14
Raue F, Frank-Raue K (2015) Epidemiology and clinical presentation of medullary thyroid carcinoma recent results. Cancer Res 204:61–90. https://doi.org/10.1007/978-3-319-22542-5_3
Rehman K, Fatima F, Waheed I, Akash MSH (2018) Prevalence of exposure of heavy metals and their impact on health consequences. J Cell Biochem 119:157–184. https://doi.org/10.1002/jcb.26234
Rezaei M, Javadmoosavi SY, Mansouri B, Azadi NA, Mehrpour O, Nakhaee S (2019) Thyroid dysfunction: how concentration of toxic and essential elements contribute to risk of hypothyroidism, hyperthyroidism, and thyroid cancer. Environ Sci Pollut Res Int 26:35787–35796. https://doi.org/10.1007/s11356-019-06632-7
Roohani N, Hurrell R, Kelishadi R, Schulin R (2013) Zinc and its importance for human health: an integrative review. J Res Med Sci 18:144–157
Rovcanin B, Damjanovic S, Zivaljevic V, Diklic A, Jovanovic M, Paunovic I (2016a) The results of molecular genetic testing for RET proto-oncogene mutations in patients with medullary thyroid carcinoma in a referral center after the two decade period. Hippokratia 20:187–191
Rovcanin B, Gopcevic K, Kekic D, Zivaljevic V, Diklic A, Tatic S, Jovanovic M, Odalovic B, Paunovic I (2019) Redox metabolism correlates with cellular turnover and clinical phenotype of papillary thyroid carcinoma and colloid goiter. Arch Med Sci. https://doi.org/10.5114/aoms.2019.88374
Rovcanin BR, Gopcevic KR, Kekic DLJ, Zivaljevic VR, Diklic ADJ, Paunovic IR (2016b) Papillary thyroid carcinoma: a malignant tumor with increased antioxidant defense capacity. Tohoku J Exp Med 240:101–111. https://doi.org/10.1620/tjem.240.101
Rovcanin B, Stojsavljevic A, Kekic D, Gopcevic K, Manojlovic D, Jovanovic M, Knezevic S, Zivaljevic V, Diklic A, Paunovic I (2020) Redox status and antioxidative cofactor metals influence clinical and pathological characteristics of papillary thyroid carcinoma and colloid goiter. Biol Trace Elem Res 197:349–359. https://doi.org/10.1007/s12011-019-01995-x
Santos LR, Neves C, Melo M, Soares P (2018) Selenium and selenoproteins in immune mediated thyroid disorders. Diagnostics (basel). https://doi.org/10.3390/diagnostics8040070
Savinov SS, Sharypova RM, Drobyshev AI (2020) Determination of the trace element composition of human nails. J Anal Chem 75:409–415. https://doi.org/10.1134/S1061934820030168
Schmutzler C, Mentrup B, Schomburg L, Hoang-Vu C, Herzog V, Kohrle J (2007) Selenoproteins of the thyroid gland: expression, localization and possible function of glutathione peroxidase 3. Bio Chem 388:1053–1059
Shen F, Cai WS, Li JL, Feng Z, Cao J, Xu B (2015) The association between serum levels of selenium, copper, and magnesium with thyroid cancer: a meta-analysis. Biol Trace Elem Res 167:225–235. https://doi.org/10.1007/s12011-015-0304-9
Sherman SI (2003) Thyroid carcinoma. Lancet 361:501–511. https://doi.org/10.1016/s0140-6736(03)12488-9
Smith-Bindman R, Lebda P, Feldstein VA et al (2013) Risk of thyroid cancer based on thyroid ultrasound imaging characteristics: results of a population-based study. JAMA Intern Med 173:1788–1796
Snoj Tratnik J, Falnoga I, Mazej D, Kocman D, Fajon V, Jagodic M, Stajnko A, Trdin A, Šlejkovec Z, Jeran Z, Osredkar J, Sešek-Briški A, Krsnik M, Kobal AB, Kononenko L, Horvat M (2019) Results of the first national human biomonitoring in Slovenia: trace elements in men and lactating women, predictors of exposure and reference values. Int J Hyg Environ Health 222:563–582. https://doi.org/10.1016/j.ijheh.2019.02.008
Stojsavljević A, Borković-Mitić S, Vujotić L, Grujičić D, Gavrović-Jankulović M, Manojlović D (2019a) The human biomonitoring study in Serbia: background levels for arsenic, cadmium, lead, thorium and uranium in the whole blood of adult Serbian population. Ecotoxicol Environ Saf 169:402–409. https://doi.org/10.1016/j.ecoenv.2018.11.043
Stojsavljević A, Jagodić J, Vujotić L, Borković-Mitić S, Rašić-Milutinović Z, Jovanović D, Gavrović-Jankulović M, Manojlović D (2020a) Reference values for trace essential elements in the whole blood and serum samples of the adult Serbian population: significance of selenium deficiency. Environ Sci Pollut Res Int 27:1397–1405. https://doi.org/10.1007/s11356-019-06936-8
Stojsavljević A, Rovčanin B, Jagodić J, Krstić Đ, Paunović I, Gavrović-Jankulović M, Manojlović D (2021) Alteration of trace elements in multinodular goiter, thyroid adenoma, and thyroid cancer. Biol Trace Elem Res. https://doi.org/10.1007/s12011-020-02542-9
Stojsavljević A, Rovčanin B, Jagodić J, Radojković DD, Paunović I, Gavrović-Jankulović M, Manojlović D (2020b) Significance of arsenic and lead in Hashimoto’s thyroiditis demonstrated on thyroid tissue, blood, and urine samples. Environ Res 186:109538. https://doi.org/10.1016/j.envres.2020.109538
Stojsavljević A, Rovčanin B, Krstić Đ, Borković-Mitić S, Paunović I, Kodranov I, Gavrović-Jankulović M, Manojlović D (2019b) Evaluation of trace metals in thyroid tissues: comparative analysis with benign and malignant thyroid diseases. Ecotoxicol Environ Saf 183:109479. https://doi.org/10.1016/j.ecoenv.2019.109479
Stojsavljević A, Rovčanin B, Krstić Đ, Jagodić J, Borković-Mitić S, Paunović I, Živaljević V, Mitić B, Gavrović-Jankulović M, Manojlović D (2019c) Cadmium as main endocrine disruptor in papillary thyroid carcinoma and the significance of Cd/Se ratio for thyroid tissue pathophysiology. J Trace Elem Med Biol 55:190–195. https://doi.org/10.1016/j.jtemb.2019.06.009
Stojsavljević A, Rovčanin B, Krstić Đ et al (2020c) Risk assessment of toxic and essential trace metals on the thyroid health at the tissue level: the significance of lead and selenium for colloid goiter disease. Expo Health 12:255–264. https://doi.org/10.1007/s12403-019-00309-9
Stojsavljević A, Škrivanj S, Trifković J, Djoković N, Trifunović SR, Borković-Mitić S, Manojlović D (2019d) The content of toxic and essential elements in trabecular and cortical femoral neck: a correlation with whole blood samples. Environ Sci Pollut Res Int 26:16577–16587. https://doi.org/10.1007/s11356-019-04796-w
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, Vujotić L, Rovčanin B, Borković-Mitić S, Gavrović-Jankulović M, Manojlović D (2020d) Assessment of trace metal alterations in the blood, cerebrospinal fluid and tissue samples of patients with malignant brain tumors. Sci Rep 10:3816. https://doi.org/10.1038/s41598-020-60774-0
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. https://doi.org/10.3322/caac.21660
Tiedje V, Stuschke M, Weber F, Dralle H, Moss L, Führer D (2018) Anaplastic thyroid carcinoma: review of treatment protocols. Endocr Relat Cancer 25:153–161. https://doi.org/10.1530/ERC-17-0435
Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160:1–40. https://doi.org/10.1016/j.cbi.2005.12.009
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
Vorkamp K, Castaño A, Antignac JP, Boada LD, Cequier E, Covaci A, Esteban López M, Haug LS, Kasper-Sonnenberg M, Koch HM, Pérez Luzardo O, Osīte A, Rambaud L, Pinorini MT, Sabbioni G, Thomsen C (2021) Biomarkers, matrices and analytical methods targeting human exposure to chemicals selected for a European human biomonitoring initiative. Environ Int 146:106082. https://doi.org/10.1016/j.envint.2020.106082
Wang XF, Deng CB, Sunahara G, Yin J, Xu GP, Zhu KX (2020) Risk assessments of heavy metals to children following non-dietary exposures and sugarcane consumption in a rural area in Southern China. Expo Health 12:1–8. https://doi.org/10.1007/s12403-018-0275-0
Wells SA Jr, Asa SL, Dralle H, Elisei R, Evans DB, Gagel RF, Lee N, Machens A, Moley JF, Pacini F, Raue F, Frank-Raue K, Robinson B, Rosenthal MS, Santoro M, Schlumberger M, Shah M, Waguespack SG (2015) American thyroid association guidelines task force on medullary thyroid carcinoma. Revised American thyroid association guidelines for the management of medullary thyroid carcinoma. Thyroid 25:567–610. https://doi.org/10.1089/thy.2014.0335
World Health Organization (WHO) (2006) Health effects of the chernobyl accident and special health care programmes, Report of the UN Chernobyl Forum, Expert Group “Health”
Wu C, Fang C, Wu X, Zhu G (2020) Health-risk assessment of arsenic and groundwater quality classification using random forest in the Yanchi region of Northwest China. Expo Health 12:761–774. https://doi.org/10.1007/s12403-019-00335-7
Xing M (2013) Molecular pathogenesis and mechanisms of thyroid cancer. Nat Rev Cancer 13:184–199. https://doi.org/10.1038/nrc3431
Yamamoto S, Konishi Y, Matsuda T, Murai T, Shibata MA, Matsui-Yuasa I, Otani S, Kuroda K, Endo G, Fukushima S (1995) Cancer induction by an organic arsenic compound, dimethylarsinic acid (cacodylic acid), in F344/DuCrj rats after pretreatment with five carcinogens. Cancer Res 55:1271–1276
Zaichick V, Zaichick S (2018) Associations between age and 50 trace element contents and relationships in intact thyroid of males. Aging Clin Exp Res 30:1059–1070. https://doi.org/10.1007/s40520-018-0906-0
Zakir HM, Quadir QF, Mollah MZI (2020) Human health risk assessment of heavy metals through the consumption of common foodstuffs collected from two divisional cities of Bangladesh. Expo Health. https://doi.org/10.1007/s12403-020-00380-7
Zeng HL, Zhang B, Wang X, Yang Q, Cheng L (2021) Urinary trace elements in association with disease severity and outcome in patients with COVID-19. Environ Res 194:110670. https://doi.org/10.1016/j.envres.2020.110670
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 Int 20:20560–20572. https://doi.org/10.1007/s11356-019-04733-x
Zhu H, Wang N, Zhang Y, Wu Q, Chen R, Gao J, Chang P, Liu Q, Fan T, Li J, Wang J, Wang J (2010) Element contents in organs and tissues of Chinese adult men. Health Phys 98:61–73. https://doi.org/10.1097/HP.0b013e3181bad921
Acknowledgements
This study was supported by Ministry of Education, Science and Technological Development of the Republic of Serbia Contract Number: 451-03-9/2021-14/200288.
Author information
Authors and Affiliations
Contributions
A.S. and B.R. designed the investigation, analyzed the data, and wrote the first and last version of the paper; both authors participated in writing through reviewing and editing. Both authors contributed critically to the draft and gave final approval for publication.
Corresponding author
Ethics declarations
conflict of Interest
Both authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Stojsavljević, A., Rovčanin, B. Impact of Essential and Toxic Trace Metals on Thyroid Health and Cancer: A Review. Expo Health 13, 613–627 (2021). https://doi.org/10.1007/s12403-021-00406-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12403-021-00406-8