Abstract
The objective of the present study was to evaluate hair essential and trace element levels and metabolic risk markers in overweight and obese subjects in relation to body mercury burden. According to 2 × 2 factorial design a total of 440 adults were distributed to four groups: (i) low-Hg normal-weight subjects (n = 114); (ii) high-Hg normal weight subjects (n = 113); (iii) low-Hg overweight (BMI > 25) subjects (n = 110); (iv) high-Hg overweight (BMI > 25) subjects (n = 110). Hg-exposed groups consisted of subjects characterized by frequent seafood consumption (> 4 times/week) subsequently evaluated by hair analysis (> 0.58 μg/g). Dietary-exposed subjects were characterized by a more than 3-fold higher hair Hg content irrespectively of body weight values. Both low-Hg and high-Hg overweight subjects were characterized by significantly higher ALT activity, as well as elevated serum glucose, LDL, and triglyceride levels as compared to the respective groups of normal weight subjects. High Hg body burden had a more significant effect on metabolic parameters in overweight and obese adults. Particularly, high-Hg overweight subjects were characterized by significantly higher serum creatinine and uric acid levels, as well as increased GGT and CK activity as compared to low-Hg overweight counterparts. In addition, hair Mg, Mn, and Sr content in high-Hg overweight subjects was significantly lower than that in low-Hg normal weight and overweight examinees. In turn, high Hg levels in overweight subjects were associated with significantly higher hair Se and Zn levels when compared to unexposed overweight adults. Generally, the obtained data demonstrate that increased hair Hg levels in overweight and obese subjects is associated with adverse metabolic profile. It is proposed that observed metabolic alterations may be at least partially mediated by Hg-associated disturbances in essential trace element and mineral metabolism.
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References
Organisation for Economic Co-operation and Development. Obesity update 2017. OECD https://www.oecd.org/els/health-systems/Obesity-Update-2017.pdf (2017)
Blüher M (2019) Obesity: global epidemiology and pathogenesis. Nat Rev Endocrinol 15(5):288–298. https://doi.org/10.1038/s41574-019-0176-8
Baillie-Hamilton PF (2002) Chemical toxins: a hypothesis to explain the global obesity epidemic. J Altern Complement Med 8(2):185–192. https://doi.org/10.1089/107555302317371479
Nappi F, Barrea L, Di Somma C, Savanelli MC, Muscogiuri G, Orio F, Savastano S (2016) Endocrine aspects of environmental “Obesogen” pollutants. Int J Environ Res Public Health 13(8):765. https://doi.org/10.3390/ijerph13080765
Wang X, Mukherjee B, Park SK (2018) Associations of cumulative exposure to heavy metal mixtures with obesity and its comorbidities among U.S. adults in NHANES 2003-2014. Environ Int 121(Pt 1):683–694. https://doi.org/10.1016/j.envint.2018.09.035
Heindel JJ (2019) History of the Obesogen field: looking back to look forward. Front Endocrinol (Lausanne) 10:14. https://doi.org/10.3389/fendo.2019.00014
Skalnaya MG, Tinkov AA, Demidov VA, Serebryansky EP, Nikonorov AA, Skalny AV (2014) Hair toxic element content in adult men and women in relation to body mass index. Biol Trace Elem Res 161(1):13–19. https://doi.org/10.1007/s12011-014-0082-9
Shin YY, Ryu IK, Park MJ, Kim SH (2018) The association of total blood mercury levels and overweight among Korean adolescents: analysis of the Korean National Health and Nutrition Examination Survey (KNHANES) 2010-2013. Korean J Pediatr 61(4):121–128. https://doi.org/10.3345/kjp.2018.61.4.121
Park JS, Ha KH, He K, Kim DJ (2017) Association between blood mercury level and visceral adiposity in adults. Diabetes Metab J 41(2):113–120. https://doi.org/10.4093/dmj.2017.41.2.113
Eom SY, Choi SH, Ahn SJ, Kim DK, Kim DW, Lim JA, Choi BS, Shin HJ, Yun SW, Yoon HJ, Kim YM, Park K, Seo E (2016) Association between toenail mercury and metabolic syndrome is modified by selenium. Nutrients 8(7):424. https://doi.org/10.3390/nu8070424
Rothenberg SE, Korrick SA, Fayad R (2015) The influence of obesity on blood mercury levels for U.S. non-pregnant adults and children: NHANES 2007-2010. Environ Res 138:173–180. https://doi.org/10.1016/j.envres.2015.01.018
Tinkov AA, Ajsuvakova OP, Skalnaya MG, Popova EV, Sinitskii AI, Nemereshina ON, Gatiatulina ER, Nikonorov AA, Skalny AV (2015) Mercury and metabolic syndrome: a review of experimental and clinical observations. Biometals 28(2):231–254. https://doi.org/10.1007/s10534-015-9823-2
Roy C, Tremblay PY, Ayotte P (2017) Is mercury exposure causing diabetes, metabolic syndrome and insulin resistance? A systematic review of the literature. Environ Res 156:747–760. https://doi.org/10.1016/j.envres.2017.04.038
Lee K (2018) Blood mercury concentration in relation to metabolic and weight phenotypes using the KNHANES 2011-2013 data. Int Arch Occup Environ Health 91(2):185–193. https://doi.org/10.1007/s00420-017-1269-0
Wiernsperger N, Rapin J (2010) Trace elements in glucometabolic disorders: an update. Diabetol Metab Syndr 2:70. https://doi.org/10.1186/1758-5996-2-70
Olechnowicz J, Tinkov A, Skalny A, Suliburska J (2018) Zinc status is associated with inflammation, oxidative stress, lipid, and glucose metabolism. J Physiol Sci 68(1):19–31. https://doi.org/10.1007/s12576-017-0571-7
Vincent JB (2019) Effects of chromium supplementation on body composition, human and animal health, and insulin and glucose metabolism. Curr Opin Clin Nutr Metab Care 22(6):483–489. https://doi.org/10.1097/MCO.0000000000000604
Treviño S, Diaz A (2020) Vanadium and insulin: partners in metabolic regulation. J Inorg Biochem 208:111094. https://doi.org/10.1016/j.jinorgbio.2020.111094
Tinkov AA, Ajsuvakova OP, Filippini T, Zhou JC, Lei XG, Gatiatulina ER, Michalke B, Skalnaya MG, Vinceti M, Aschner M, Skalny AV (2020) Selenium and selenoproteins in adipose tissue physiology and obesity. Biomolecules 10(4):658. https://doi.org/10.3390/biom10040658
Nielsen FH (2018) Magnesium deficiency and increased inflammation: current perspectives. J Inflamm Res 11:25–34. https://doi.org/10.2147/JIR.S136742
Astrup A, Bügel S (2010) Micronutrient deficiency in the aetiology of obesity. Int J Obes 34(6):947–948. https://doi.org/10.1038/ijo.2010.81
Via M (2012) The malnutrition of obesity: micronutrient deficiencies that promote diabetes. ISRN Endocrinol 2012:103472–103478. https://doi.org/10.5402/2012/103472
Gu K, Xiang W, Zhang Y, Sun K, Jiang X (2019) The association between serum zinc level and overweight/obesity: a meta-analysis. Eur J Nutr 58(8):2971–2982. https://doi.org/10.1007/s00394-018-1876-x
Ynalvez R, Gutierrez J, Gonzalez-Cantu H (2016) Mini-review: toxicity of mercury as a consequence of enzyme alteration. Biometals. 29(5):781–788. https://doi.org/10.1007/s10534-016-9967-8
Bjørklund G, Aaseth J, Ajsuvakova OP, Nikonorov AA, Skalny AV, Skalnaya MG, Tinkov AA (2017) Molecular interaction between mercury and selenium in neurotoxicity. Coord Chem Rev 332:30–37. https://doi.org/10.1016/j.ccr.2016.10.009
Bogden JD, Kemp FW, Troiano RA, Jortner BS, Timpone C, Giuliani D (1980) Effect of mercuric chloride and methylmercury chloride exposure on tissue concentrations of six essential minerals. Environ Res 21(2):350–359. https://doi.org/10.1016/0013-9351(80)90037-7
Feng W, Wang M, Li B, Liu J, Chai Z, Zhao J, Deng G (2004) Mercury and trace element distribution in organic tissues and regional brain of fetal rat after in utero and weaning exposure to low dose of inorganic mercury. Toxicol Lett 152(3):223–234. https://doi.org/10.1016/j.toxlet.2004.05.001
Trasande L, DiGangi J, Evers DC, Petrlik J, Buck DG, Šamánek J, Beeler B, Turnquist MA, Regan K (2016) Economic implications of mercury exposure in the context of the global mercury treaty: hair mercury levels and estimated lost economic productivity in selected developing countries. J Environ Manag 183:229–235. https://doi.org/10.1016/j.jenvman.2016.08.058
Kim HR, Han MA (2018) Association between serum liver enzymes and metabolic syndrome in Korean adults. Int J Environ Res Public Health 15(8):1658. https://doi.org/10.3390/ijerph15081658
Lee DS, Evans JC, Robins SJ, Wilson PW, Albano I, Fox CS, Wang TJ, Benjamin EJ, D'Agostino RB, Vasan RS (2007) Gamma glutamyl transferase and metabolic syndrome, cardiovascular disease, and mortality risk: the Framingham Heart Study. Arterioscler Thromb Vasc Biol 27(1):127–133. https://doi.org/10.1161/01.ATV.0000251993.20372.40
Wang J, Li X, Han X, Yang K, Liu B, Li Y, Wu P, Liu X, Yu K, Dai X, Yuan J, Yao P, Zhang X, Guo H, Wang Y, Chen W, Wei S, Miao X, Min X, Liang Y, Yang H, Hu FB, Wu T, He M (2015) Serum creatinine levels and risk of metabolic syndrome in a middle-aged and older Chinese population. Clin Chim Acta 440:177–182. https://doi.org/10.1016/j.cca.2014.11.025
Yang T, Chu CH, Bai CH, You SL, Chou YC, Chou WY, Chien KL, Hwang LC, Su TC, Tseng CH, Sun CA (2012 Feb) Uric acid level as a risk marker for metabolic syndrome: a Chinese cohort study. Atherosclerosis. 220(2):525–531. https://doi.org/10.1016/j.atherosclerosis.2011.11.014
Chen ZW, Chen LY, Dai HL, Chen JH, Fang LZ (2008) Relationship between alanine aminotransferase levels and metabolic syndrome in nonalcoholic fatty liver disease. J Zhejiang Univ Sci B 9(8):616–622. https://doi.org/10.1631/jzus.B0720016
Liu X, Zhang H, Liang J (2013) Blood urea nitrogen is elevated in patients with non-alcoholic fatty liver disease. Hepatogastroenterology 60(122):343–345
Seo MS, Lee HR, Shim JY, Kang HT, Lee YJ (2014) Relationship between blood mercury concentrations and serum γ-glutamyltranspeptidase level in Korean adults using data from the 2010 Korean National Health and Nutrition Examination Survey. Clin Chim Acta 430:160–163. https://doi.org/10.1016/j.cca.2014.01.042
Tinkov AA, Skalnaya MG, Demidov VA, Serebryansky EP, Nikonorov AA, Skalny AV (2014) Hair mercury association with selenium, serum lipid spectrum, and gamma-glutamyl transferase activity in adults. Biol Trace Elem Res 161(3):255–262. https://doi.org/10.1007/s12011-014-0124-3
Gowda S, Desai PB, Kulkarni SS, Hull VV, Math AA, Vernekar SN (2010) Markers of renal function tests. N Am J Med Sci 2(4):170–173
Bridges CC, Zalups RK (2017) The aging kidney and the nephrotoxic effects of mercury. J Toxicol Environ Health B Crit Rev 20(2):55–80. https://doi.org/10.1080/10937404.2016.1243501
Chen J, Gu D, Chen CS, Wu X, Hamm LL, Muntner P, Batuman V, Lee CH, Whelton PK, He J (2007) Association between the metabolic syndrome and chronic kidney disease in Chinese adults. Nephrol Dial Transplant 22(4):1100–1106. https://doi.org/10.1093/ndt/gfl759
Schrager S (2005) Dietary calcium intake and obesity. J Am Board Fam Pract 18(3):205–210. https://doi.org/10.3122/jabfm.18.3.205
Skowrońska-Jóźwiak E, Jaworski M, Lorenc R, Karbownik-Lewińska M, Lewiński A (2017) Low dairy calcium intake is associated with overweight and elevated blood pressure in Polish adults, notably in premenopausal women. Public Health Nutr 20(4):630–637. https://doi.org/10.1017/S1368980016002706
He YH, Li ST, Wang YY, Wang G, He Y, Liao XL, Sun CH, Li Y (2012) Postweaning low-calcium diet promotes later-life obesity induced by a high-fat diet. J Nutr Biochem 23(10):1238–1244. https://doi.org/10.1016/j.jnutbio.2011.07.004
Marotte C, Bryk G, Gonzales Chaves MM, Lifshitz F, de Portela ML, Zeni SN (2014) Low dietary calcium and obesity: a comparative study in genetically obese and normal rats during early growth. Eur J Nutr 53(3):769–778. https://doi.org/10.1007/s00394-013-0581-z
Zhang F, Ye J, Zhu X, Wang L, Gao P, Shu G, Jiang Q, Wang S (2019) Anti-obesity effects of dietary calcium: the evidence and possible mechanisms. Int J Mol Sci 20(12):3072. https://doi.org/10.3390/ijms20123072
Pannu PK, Calton EK, Soares MJ (2016) Calcium and vitamin D in obesity and related chronic disease. Adv Food Nutr Res 77:57–100. https://doi.org/10.1016/bs.afnr.2015.11.001
Takaya J, Yamato F, Kuroyanagi Y, Higashino H, Kaneko K (2010) Intracellular magnesium of obese and type 2 diabetes mellitus children. Diabetes Ther 1(1):25–31. https://doi.org/10.1007/s13300-010-0003-7
Sarrafzadegan N, Khosravi-Boroujeni H, Lotfizadeh M, Pourmogaddas A, Salehi-Abargouei A (2016) Magnesium status and the metabolic syndrome: a systematic review and meta-analysis. Nutrition 32(4):409–417. https://doi.org/10.1016/j.nut.2015.09.014
Guerrero-Romero F, Rodriguez-Moran M (2013) Serum magnesium in the metabolically-obese normal-weight and healthy-obese subjects. Eur J Intern Med 24(7):639–643. https://doi.org/10.1016/j.ejim.2013.02.014
Volpe SL (2013) Magnesium in disease prevention and overall health. Adv Nutr 4(3):378S–383S. https://doi.org/10.3945/an.112.003483
Freitas EP, Cunha AT, Aquino SL, Pedrosa LF, Lima SC, Lima JG, Almeida MG, Sena-Evangelista KC (2017) Zinc status biomarkers and cardiometabolic risk factors in metabolic syndrome: a case control study. Nutrients 9(2):175. https://doi.org/10.3390/nu9020175
Kim J, Ahn J (2014) Effect of zinc supplementation on inflammatory markers and adipokines in young obese women. Biol Trace Elem Res 157(2):101–106. https://doi.org/10.1007/s12011-013-9885-3
Franciscato C, Moraes-Silva L, Duarte FA, Oliveira CS, Ineu RP, Flores EM, Dressler VL, Peixoto NC, Pereira ME (2011) Delayed biochemical changes induced by mercury intoxication are prevented by zinc pre-exposure. Ecotoxicol Environ Saf 74(3):480–486. https://doi.org/10.1016/j.ecoenv.2010.11.011
Peixoto NC, Serafim MA, Flores EM, Bebianno MJ, Pereira ME (2007) Metallothionein, zinc, and mercury levels in tissues of young rats exposed to zinc and subsequently to mercury. Life Sci 81(16):1264–1271. https://doi.org/10.1016/j.lfs.2007.08.038
Tinkov AA, Skalnaya MG, Ajsuvakova OP, Serebryansky EP, Chao JC, Aschner M, Skalny AV (2020) Selenium, zinc, chromium, and vanadium levels in serum, hair, and urine samples of obese adults assessed by inductively coupled plasma mass spectrometry. Biol Trace Elem Res 1-8. https://doi.org/10.1007/s12011-020-02177-w.
Kanda H, Sumi D, Endo A, Toyama T, Chen CL, Kikushima M, Kumagai Y (2008) Reduction of arginase I activity and manganese levels in the liver during exposure of rats to methylmercury: a possible mechanism. Arch Toxicol 82(11):803–808. https://doi.org/10.1007/s00204-008-0307-9
Li L, Yang X (2018) The essential element manganese, oxidative stress, and metabolic diseases: links and interactions. Oxidative Med Cell Longev 2018:7580707–7580711. https://doi.org/10.1155/2018/7580707
Yamashita Y, Yamashita M, Iida H (2013) Selenium content in seafood in Japan. Nutrients 5(2):388–395. https://doi.org/10.3390/nu5020388
Park K, Seo E (2016) Association between toenail mercury and metabolic syndrome is modified by selenium. Nutrients 8(7):424
Qian Z, Luo F, Wu C, Zhao R, Cheng X, Qin W (2017) Indicator polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs) in seafood from Xiamen (China): levels, distributions, and risk assessment. Environ Sci Pollut Res 24:10443–10453
Heindel JJ, Blumberg B (2019) Environmental obesogens: mechanisms and controversies. Annu Rev Pharmacol Toxicol 59:89–106
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The study was supported by grants No. 20-515-S52003 from the Russian Foundation for Basic Research (Russia) and MOST 109-2923-B-038-001-MY3 from the Ministry of Science and Technology (Taiwan).
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Skalny, A.V., Chang, JS., Bobrovnitsky, I.P. et al. Relationship Between Elevated Hair Mercury Levels, Essential Element Status, and Metabolic Profile in Overweight and Obese Adults. Biol Trace Elem Res 199, 2874–2881 (2021). https://doi.org/10.1007/s12011-020-02430-2
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DOI: https://doi.org/10.1007/s12011-020-02430-2