Log in

The Effect of Mixture of Heavy Metals on Obesity in Individuals ≥50 Years of Age

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Little is known about the association between a mixture of heavy metals and obesity among individuals ≥50 years of age with comorbidities. Thus, we identified the associations of serum cadmium (Cd), lead (Pb), and mercury (Hg) with obesity using linear regression models; weighted quantile sum (WQS) regression, quantile g-computation (qgcomp), and Bayesian kernel machine regression (BKMR) were conducted as secondary analyses. Of the 6434 subjects included in the analysis, 13.8% had obesity and 44.6% had abdominal obesity. In the logistic regression model, serum Hg was associated with obesity and abdominal obesity, and significant trends were observed for these heavy metal tertiles (p < 0.001). Serum Hg levels were also associated with body mass index (BMI) and waist circumference (WC). The WQS index was significantly associated with both obesity (OR = 1.43, 95% CI: 1.40–1.46) and abdominal obesity (β = 1.51, 95% CI: 1.48–1.54). The qgcomp index also found a significant association between heavy metals and both obesity (OR = 1.35, 95% CI: 1.12–1.63) and abdominal obesity (OR = 1.34, 95% CI: 1.12–1.60). Serum Hg was the most heavily weighed heavy metal in these models. In BKMR analysis, the overall effect of the mixture was significantly associated with obesity, BMI, and WC. Serum Hg showed positive trends and was observed as the most important factor associated with obesity, BMI, and WC. Our findings were largely robust to secondary analyses that used three novel mixture modeling approaches: WQS, qpcomp, and BKMR. Given increasing exposure to heavy metals, well-characterized cohorts of individuals aged ≥50 years are required to determine the mixed effects of heavy metals on obesity and related diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

The data used to support the findings of this study are available from the corresponding author upon request.

References

  1. Baik I (2018) Forecasting obesity prevalence in Korean adults for the years 2020 and 2030 by the analysis of contributing factors. Nutrition Res Pract 12(3):251

    Article  Google Scholar 

  2. Okosun IS, Chandra KD, Choi S, Christman J, Dever GA, Prewitt TE (2001) Hypertension and type 2 diabetes comorbidity in adults in the United States: risk of overall and regional adiposity. Obesity Res 9(1):1–9

    Article  CAS  Google Scholar 

  3. Krauss RM, Winston M, Fletcher BJ, Grundy SM (1998) Obesity: impact on cardiovascular disease. Circulation 98(14):1472–1476

    Article  PubMed  Google Scholar 

  4. Beccuti G, Pannain S (2011) Sleep and obesity. Current Opinion Clin Nutrition Metab Care 14(4):402

    Article  Google Scholar 

  5. Guh DP, Zhang W, Bansback N, Amarsi Z, Birmingham CL, Anis AH (2009) The incidence of co-morbidities related to obesity and overweight: a systematic review and meta-analysis. BMC Public Health 9(1):1–20

    Article  Google Scholar 

  6. Wallström P, Bjartell A, Gullberg B, Olsson H, Wirfält E (2009) A prospective Swedish study on body size, body composition, diabetes, and prostate cancer risk. British J Cancer 100(11):1799–1805

    Article  Google Scholar 

  7. Sowers MR, Karvonen-Gutierrez CA (2010) The evolving role of obesity in knee osteoarthritis. Current Opinion Rheumatol 22(5):533

    Article  Google Scholar 

  8. Stenholm S, Rantanen T, Alanen E, Reunanen A, Sainio P, Koskinen S (2007) Obesity history as a predictor of walking limitation at old age. Obesity 15(4):929–938

    Article  PubMed  Google Scholar 

  9. Zaninotto P, Pierce M, Breeze E, De Oliveira C, Kumari M (2010) BMI and waist circumference as predictors of well-being in older adults: findings from the English Longitudinal Study of Ageing. Obesity 18(10):1981–1987

    Article  PubMed  Google Scholar 

  10. Park SS, Skaar DA, Jirtle RL, Hoyo C (2017) Epigenetics, obesity and early-life cadmium or lead exposure. Epigenomics 9(1):57–75

    Article  CAS  PubMed  Google Scholar 

  11. Lopomo A, Burgio E, Migliore L (2016) Epigenetics of obesity. Progress Mol Biol Translational Sci 140:151–184

    Article  CAS  Google Scholar 

  12. Nguyen HD, Kim M-S (2021) Effects of heavy metal, vitamin, and curry consumption on metabolic syndrome during menopause: a Korean community-based cross-sectional study. J Menopause 28(8):1. https://doi.org/10.1097/GME.0000000000001825

    Article  Google Scholar 

  13. Nguyen HD, Oh H, Hoang NHM, Kim M-S (2021) Association between heavy metals, high-sensitivity C-reaction protein and 10-year risk of cardiovascular diseases among adult Korean population. Scientific Reports 11(1):14664. https://doi.org/10.1038/s41598-021-94158-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Arbi S, Oberholzer HM, Van Rooy MJ, Venter C, Bester MJ (2017) Effects of chronic exposure to mercury and cadmium alone and in combination on the coagulation system of Sprague-Dawley rats. Ultrastructural Pathol 41(4):275–283

    Article  Google Scholar 

  15. Angeli JK, Pereira CAC, de Oliveira FT, Stefanon I, Padilha AS, Vassallo DV (2013) Cadmium exposure induces vascular injury due to endothelial oxidative stress: the role of local angiotensin II and COX-2. Free Radical Biol Med 65:838–848

    Article  CAS  Google Scholar 

  16. Valera B, Muckle G, Poirier P, Jacobson SW, Jacobson JL, Dewailly E (2012) Cardiac autonomic activity and blood pressure among Inuit children exposed to mercury. Neurotoxicology 33(5):1067–1074

    Article  CAS  PubMed  Google Scholar 

  17. Poursafa P, Ataee E, Motlagh ME, Ardalan G, Tajadini MH, Yazdi M, Kelishadi R (2014) Association of serum lead and mercury level with cardiometabolic risk factors and liver enzymes in a nationally representative sample of adolescents: the CASPIAN-III study. Environ Sci Pollution Res 21(23):13496–13502

    Article  CAS  Google Scholar 

  18. Ali H, Khan E, Ilahi I (2019) Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem 2019

  19. Nguyen HD, Oh H, Hoang NHM, Jo WH, Kim MS (2021) Environmental science and pollution research role of heavy metal concentrations and vitamin intake from food in depression: a national cross-sectional study (2009-2017). Environ Sci Poll Res Int:1-13. https://doi.org/10.1007/s11356-021-15986-w

  20. Satarug S, Vesey DA, Gobe GC (2017) Current health risk assessment practice for dietary cadmium: Data from different countries. Food Chem Toxicol 106:430–445

    Article  CAS  PubMed  Google Scholar 

  21. Tinkov AA, Filippini T, Ajsuvakova OP, Aaseth J, Gluhcheva YG, Ivanova JM, Bjørklund G, Skalnaya MG, Gatiatulina ER, Popova EV (2017) The role of cadmium in obesity and diabetes. Sci Total Environ 601:741–755

    Article  PubMed  CAS  Google Scholar 

  22. Çamur D, Güler Ç, Vaizoğlu SA, Özdilek B (2016) Determining mercury levels in anchovy and in individuals with different fish consumption habits, together with their neurological effects. Toxicol Industrial Health 32(7):1215–1223

    Article  CAS  Google Scholar 

  23. Wolkin A, Hunt D, Martin C, Caldwell KL, McGeehin MA (2012) Blood mercury levels among fish consumers residing in areas with high environmental burden. Chemosphere 86(9):967–971

    Article  CAS  PubMed  Google Scholar 

  24. Garí M, Grimalt JO, Torrent M, Sunyer J (2013) Influence of socio-demographic and diet determinants on the levels of mercury in preschool children from a Mediterranean island. Environ Pollution 182:291–298

    Article  CAS  Google Scholar 

  25. Aelion CM, Davis HT, Lawson AB, Cai B, McDermott S (2012) Associations of estimated residential soil arsenic and lead concentrations and community-level environmental measures with mother–child health conditions in South Carolina. Health & Place 18(4):774–781

    Article  Google Scholar 

  26. Hrubá F, Strömberg U, Černá M, Chen C, Harari F, Harari R, Horvat M, Koppová K, Kos A, Krsková A (2012) Blood cadmium, mercury, and lead in children: an international comparison of cities in six European countries, and China, Ecuador, and Morocco. Environ Int 41:29–34

    Article  PubMed  CAS  Google Scholar 

  27. Zhang A, Hu H, Sánchez BN, Ettinger AS, Park SK, Cantonwine D, Schnaas L, Wright RO, Lamadrid-Figueroa H, Tellez-Rojo MM (2012) Association between prenatal lead exposure and blood pressure in children. Environ Health Perspect 120(3):445–450

    Article  CAS  PubMed  Google Scholar 

  28. Rothenberg SE, Korrick SA, Fayad R (2015) The influence of obesity on blood mercury levels for US non-pregnant adults and children: NHANES 2007–2010. Environ Res 138:173–180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zhang Y, Dong T, Hu W, Wang X, Xu B, Lin Z, Hofer T, Stefanoff P, Chen Y, Wang X, **a Y (2019) Association between exposure to a mixture of phenols, pesticides, and phthalates and obesity: comparison of three statistical models. Environ Int 123:325–336. https://doi.org/10.1016/j.envint.2018.11.076

    Article  CAS  PubMed  Google Scholar 

  30. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Lee S, Yoon J-H, Won J-U, Lee W, Lee J-H, Seok H, Kim Y-K, Kim C-N, Roh J (2016) The association between blood mercury levels and risk for overweight in a general adult population: results from the Korean National Health and Nutrition Examination Survey. Biol Trace Element Res 171(2):251–261

    Article  CAS  Google Scholar 

  32. 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

    Article  PubMed  Google Scholar 

  33. Moon S-S (2014) Additive effect of heavy metals on metabolic syndrome in the Korean population: the Korea National Health and Nutrition Examination Survey (KNHANES) 2009–2010. Endocrine 46(2):263–271

    Article  CAS  PubMed  Google Scholar 

  34. You C-H, Kim B-G, Kim J-M, Yu S-D, Kim Y-M, Kim R-B, Hong Y-S (2011) Relationship between blood mercury concentration and waist-to-hip ratio in elderly Korean individuals living in coastal areas. J Prevent Med Public Health 44(5):218

    Article  Google Scholar 

  35. Welfare KMoHa (2021) Korea National Health & Nutrition Examination Survey. https://knhanes.cdc.go.kr/knhanes/eng/index.do. Jan 20, 2021

  36. Duc HN, Oh H, Kim MS (2021) Effects of antioxidant vitamins, curry consumption, and heavy metal levels on metabolic syndrome with comorbidities: a Korean community-based cross-sectional study. Antioxidants (Basel, Switzerland) 10 (5). https://doi.org/10.3390/antiox10050808

  37. Duc HN, Oh H, Yoon IM, Kim M-S (2021) Association between levels of thiamine intake, diabetes, cardiovascular diseases and depression in Korea: a national cross-sectional study. J Nutritional Sci 10:e31. https://doi.org/10.1017/jns.2021.23

    Article  CAS  Google Scholar 

  38. Yun S, Nguyen HD, Park JS, Oh C, Kim MS (2021) The association between the metabolic syndrome and iron status in pre- and postmenopausal women: Korean National Health and Nutrition Examination Survey (KNHANES) in 2012. British J Nutrition:1–11. https://doi.org/10.1017/s0007114521001331

  39. Nguyen HD, Oh H, Kim M-S (2021) Effects of heavy metals on hypertension during menopause: a Korean community-based cross-sectional study. Menopause 28 (12). https://doi.org/10.1097/GME.0000000000001865

  40. Organization WH (2000) Western Pacific Region, International Association for the Study of Obesity. The Asia-Pacific Perspective. Redefining obesity and its treatment

  41. Carrico C, Gennings C, Wheeler DC, Factor-Litvak P (2015) Characterization of weighted quantile sum regression for highly correlated data in a risk analysis setting. J Agric Biol Environ Statistics 20(1):100–120. https://doi.org/10.1007/s13253-014-0180-3

    Article  Google Scholar 

  42. Shih Y-H, Howe CG, Scannell Bryan M, Shahriar M, Kibriya MG, Jasmine F, Sarwar G, Graziano JH, Persky VW, Jackson B, Ahsan H, Farzan SF, Argos M (2021) Exposure to metal mixtures in relation to blood pressure among children 5–7 years old: An observational study in Bangladesh. 5 (2):e135. https://doi.org/10.1097/ee9.0000000000000135

  43. Renzetti S, Curtin P, Just A, Gennings CJRpv (2016) Gwqs: generalized weighted quantile sum regression. 1 (0)

  44. Keil AP, Buckley JP, O’Brien KM, Ferguson KK, Zhao S, White AJJEhp (2020) A quantile-based g-computation approach to addressing the effects of exposure mixtures. 128 (4):047004

  45. Rager JE, Clark J, Eaves LA, Avula V, Niehoff NM, Kim YH, Jaspers I, Gilmour MI (2021) Mixtures modeling identifies chemical inducers versus repressors of toxicity associated with wildfire smoke. Sci Total Environ 775:145759. https://doi.org/10.1016/j.scitotenv.2021.145759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Bobb JF, Valeri L, Claus Henn B, Christiani DC, Wright RO, Mazumdar M, Godleski JJ, Coull BA (2015) Bayesian kernel machine regression for estimating the health effects of multi-pollutant mixtures. Biostatistics (Oxford, England) 16(3):493–508. https://doi.org/10.1093/biostatistics/kxu058

    Article  Google Scholar 

  47. Coker E, Chevrier J, Rauch S, Bradman A, Obida M, Crause M, Bornman R, Eskenazi B (2018) Association between prenatal exposure to multiple insecticides and child body weight and body composition in the VHEMBE South African birth cohort. Environ Int 11(3):122–132. https://doi.org/10.1016/j.envint.2018.01.016

    Article  CAS  Google Scholar 

  48. WHO J (2017) Preventing noncommunicable diseases (NCDs) by reducing environmental risk factors. World Health Organization.(WHO/FWC/EPE/17.1), Geneva

    Google Scholar 

  49. Wang M, Liu R, Chen W, Peng C, Markert B (2018) Effects of urbanization on heavy metal accumulation in surface soils, Bei**g. J Environ Sci 64:328–334

    Article  CAS  Google Scholar 

  50. Chang J-W, Chen H-L, Su H-J, Liao P-C, Guo H-R, Lee C-C (2011) Simultaneous exposure of non-diabetics to high levels of dioxins and mercury increases their risk of insulin resistance. J Hazardous Mater 185(2-3):749–755

    Article  CAS  Google Scholar 

  51. Regnier SM, Sargis RM (2014) Adipocytes under assault: environmental disruption of adipose physiology. Biochimica et Biophysica Acta (BBA)-Mol Basis Disease 1842(3):520–533

    Article  CAS  Google Scholar 

  52. Iavicoli I, Fontana L, Bergamaschi A (2009) The effects of metals as endocrine disruptors. J Toxicol Environ Health Part B 12(3):206–223

    Article  CAS  Google Scholar 

  53. Kawakami T, Hanao N, Nishiyama K, Kadota Y, Inoue M, Sato M, Suzuki S (2012) Differential effects of cobalt and mercury on lipid metabolism in the white adipose tissue of high-fat diet-induced obesity mice. Toxicol Appl Pharmacol 258(1):32–42. https://doi.org/10.1016/j.taap.2011.10.004

    Article  CAS  PubMed  Google Scholar 

  54. Chen X (2007) Accumulation of heavy metals and organochlorine pesticides in human milk and adipose tissues, and its health concerns.

  55. Qin YY, Leung CKM, Leung AOW, Wu SC, Zheng JS, Wong MH (2010) Persistent organic pollutants and heavy metals in adipose tissues of patients with uterine leiomyomas and the association of these pollutants with seafood diet, BMI, and age. Environ Sci Pollut Res 17(1):229–240

    Article  CAS  Google Scholar 

  56. Yamamoto M, Yanagisawa R, Motomura E, Nakamura M, Sakamoto M, Takeya M, Eto K (2014) Increased methylmercury toxicity related to obesity in diabetic KK-Ay mice. J Appl Toxicol 34(8):914–923

    Article  CAS  PubMed  Google Scholar 

  57. Brzóska M, Moniuszko-Jakoniuk J (2001) Interactions between cadmium and zinc in the organism. Food Chem Toxicol 39(10):967–980

    Article  PubMed  Google Scholar 

  58. Michalek JE (1996) Pharmacokinetics of TCDD in veterans of Operation Ranch Hand: 10-year follow-up. J Toxicol Environ Health Part A 47(3):209–220

    Article  CAS  Google Scholar 

  59. 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 Element Res 161(1):13–19

    Article  CAS  Google Scholar 

  60. Eom S-Y, Choi S-H, Ahn S-J, Kim D-K, Kim D-W, Lim J-A, Choi B-S, Shin H-J, Yun S-W, Yoon H-J (2014) Reference levels of blood mercury and association with metabolic syndrome in Korean adults. Int Archives Occupational Environ Health 87(5):501–513

    Article  CAS  Google Scholar 

  61. Kim Y-N, Kim YA, Yang A-R, Lee B-H (2014) Relationship between blood mercury level and risk of cardiovascular diseases: results from the Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV) 2008–2009. Preventive Nutrition Food Sci 19(4):333

    Article  Google Scholar 

  62. Cho S, Jacobs DR, Park K (2014) Population correlates of circulating mercury levels in Korean adults: the Korea National Health and Nutrition Examination Survey IV. BMC Public Health 14(1):1–10

    Article  CAS  Google Scholar 

  63. Son J-Y, Lee J, Paek D, Lee J-T (2009) Blood levels of lead, cadmium, and mercury in the Korean population: results from the Second Korean National Human Exposure and Bio-monitoring Examination. Environ Res 109(6):738–744

    Article  CAS  PubMed  Google Scholar 

  64. Zamboni M, Mazzali G (2012) Obesity in the elderly: an emerging health issue. Int J Obesity 36(9):1151–1152

    Article  CAS  Google Scholar 

  65. Yamamoto C, Kaji T, Sakamoto M, Kozuka H (1993) Cadmium stimulation of plasminogen activator inhibitor-1 release from human vascular endothelial cells in culture. Toxicology 83(1-3):215–223

    Article  CAS  PubMed  Google Scholar 

  66. Houston MC (2011) Role of mercury toxicity in hypertension, cardiovascular disease, and stroke. J Clin Hypertension 13(8):621–627

    Article  CAS  Google Scholar 

  67. Salonen JT, Seppänen K, Lakka TA, Salonen R, Kaplan GA (2000) Mercury accumulation and accelerated progression of carotid atherosclerosis: a population-based prospective 4-year follow-up study in men in eastern Finland. Atherosclerosis 148(2):265–273

    Article  CAS  PubMed  Google Scholar 

  68. Chen YW, Yang CY, Huang CF, Hung DZ, Leung YM, Liu SH (2009) Heavy metals, islet function and diabetes development. Islets 1(3):169–176

    Article  PubMed  Google Scholar 

  69. Gupta VK, Singh S, Agrawal A, Siddiqi NJ, Sharma B (2015) Phytochemicals mediated remediation of neurotoxicity induced by heavy metals. Biochem Res Int

  70. Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283(2-3):65–87

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to all research staff for their excellent contributions in data collection in the survey.

Funding

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MEST) (grant nos. NRF2013R1A1A3008851 and 2018R1D1A1B07049610).

Author information

Authors and Affiliations

Authors

Contributions

Study concept and design (H.N.D); acquisition of data (H.N.D, H.O, M.S.K); analysis and interpretation of data (H.N.D.); statistical analysis (H.N.D); and drafting of the manuscript (H.N.D).

Corresponding author

Correspondence to Min-Sun Kim.

Ethics declarations

Consent to Participate

Before investigations, all participants in KNHANES provided written informed consent, which was carried out by the Health and Nutrition Examination Department of the Korea Centers for Disease Control and Prevention. This study was approved by the KNHANES inquiry commission (IRB Approval numbers: 2009-01CON-03-2C, 2010-02CON-21-C, 2011-02CON-06-C, 2012-01EXP-01-2C, 2013-07CON-03-4C, 2013-12EXP-03-5C). From 2016 to 2017, KNHANES was exempt from review regarding research ethics under the Bioethics and Safety Act.

Consent for Publication

Not applicable.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 209 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Duc, H.N., Oh, H. & Kim, MS. The Effect of Mixture of Heavy Metals on Obesity in Individuals ≥50 Years of Age. Biol Trace Elem Res 200, 3554–3571 (2022). https://doi.org/10.1007/s12011-021-02972-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-021-02972-z

Keywords

Navigation