Environmental Science and Pollution Research

, Volume 24, Issue 12, pp 11573–11581 | Cite as

Association between level of urinary trace heavy metals and obesity among children aged 6–19 years: NHANES 1999–2011

  • Wentao Shao
  • Qian Liu
  • Xiaowei He
  • Hui Liu
  • Aihua GuEmail author
  • Zhaoyan JiangEmail author
Research Article


Global prevalence of obesity has been increasing dramatically in all ages. Although traditional causes for obesity development have been studied widely, it is unclear whether environmental exposure of substances such as trace heavy metals affects obesity development among children and adolescents so far. Data from the National Health and Nutrition Examination Survey (1999–2011) were retrieved, and 6602 US children were analyzed in this study. Urinary level of nine trace heavy metals, including barium, cadmium, cobalt, cesium, molybdenum, lead, antimony, thallium, and tungsten, was analyzed for their association with the prevalence of obesity among children aged 6–19 years. Multiple logistic regression was performed to assess the associations adjusted for age, race/ethnicity, gender, urinary creatinine, PIR, serum cotinine, and television, video game, and computer usage. A remarkable association was found between barium exposure (OR 1.43; 95% CI 1.09–1.88; P < 0.001) and obesity in children aged 6–19 years. Negative association was observed between cadmium (OR 0.46; 95% CI 0.33–0.64; P < 0.001), cobalt (OR 0.56; 95% CI: 0.41–0.76; P < 0.001), and lead (OR 0.57; 95% CI 0.41–0.78; P = 0.018), and obesity. All the negative associations were stronger in the 6–12 years group than in the 13–19 years group. The present study demonstrated that barium might increase the occurrence of obesity, but cadmium, cobalt, and lead caused weight loss among children. The results imply that trace heavy metals may represent critical risk factors for the development of obesity, especially in the area that the state of metal contamination is serious.


Trace heavy metal Obesity Children Urine National Health and Nutrition Examination Survey 



This work was supported by the National Natural Science Foundation of China (Grant Nos. 81270537, 81570574, and 81573174), the Outstanding Youth Fund of Jiangsu Province (SBK2014010296), the Research Project of Chinese Ministry of Education (213015A), the Priority Academic Program Development of Jiangsu Higher Education Institutions, the Flagship Major Development of Jiangsu Higher Education Institutions, and the Open Project Program of the State Key Laboratory of Environmental Chemistry and Ecotoxicology (KF2015-01).

Compliance with ethical standards

Conflict of interests

None to be declared.

Supplementary material

11356_2017_8803_MOESM1_ESM.docx (14 kb)
Table S1 (DOCX 13 kb)
11356_2017_8803_MOESM2_ESM.docx (15 kb)
Table S2 (DOCX 14 kb)
11356_2017_8803_MOESM3_ESM.docx (17 kb)
Table S3 (DOCX 17 kb)


  1. Adams JB et al (2013) Toxicological status of children with autism vs. neurotypical children and the association with autism severity. Biol Trace Elem Res 151:171–180. doi: 10.1007/s12011-012-9551-1 CrossRefGoogle Scholar
  2. Amzal B, Julin B, Vahter M, Wolk A, Johanson G, Akesson A (2009) Population toxicokinetic modeling of cadmium for health risk assessment. Environ Health Perspect 117:1293–1301. doi: 10.1289/ehp.0800317 CrossRefGoogle Scholar
  3. Blaurock-Busch E, Amin OR, Rabah T (2011) Heavy metals and trace elements in hair and urine of a sample of Arab children with autistic spectrum disorder. Maedica 6:247–257Google Scholar
  4. Cefalu WT, Hu FB (2004) Role of chromium in human health and in diabetes. Diabetes Care 27:2741–2751CrossRefGoogle Scholar
  5. Collaboration NCDRF (2016) Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet 387:1377–1396. doi: 10.1016/S0140-6736(16)30054-X CrossRefGoogle Scholar
  6. Cuypers A et al (2010) Cadmium stress: an oxidative challenge. Biometals : an international journal on the role of metal ions in biology, biochemistry, and medicine 23:927–940. doi: 10.1007/s10534-010-9329-x CrossRefGoogle Scholar
  7. Delvaux I et al (2014) Prenatal exposure to environmental contaminants and body composition at age 7-9 years. Environ Res 132:24–32. doi: 10.1016/j.envres.2014.03.019 CrossRefGoogle Scholar
  8. Devi P, Bajala V, Garg VK, Mor S, Ravindra K (2016) Heavy metal content in various types of candies and their daily dietary intake by children. Environ Monit Assess 188:86. doi: 10.1007/s10661-015-5078-1 CrossRefGoogle Scholar
  9. Dietz WH (1998) Health consequences of obesity in youth: childhood predictors of adult disease. Pediatrics 101:518–525Google Scholar
  10. Feng W et al (2015) Association of urinary metal profiles with altered glucose levels and diabetes risk: a population-based study in China. PLoS One 10:e0123742. doi: 10.1371/journal.pone.0123742 CrossRefGoogle Scholar
  11. Fortin MC et al (2012) Increased lead biomarker levels are associated with changes in hormonal response to stress in occupationally exposed male participants. Environ Health Perspect 120:278–283. doi: 10.1289/ehp.1103873 CrossRefGoogle Scholar
  12. Gardner RM et al (2013) Environmental exposure to metals and children’s growth to age 5 years: a prospective cohort study. Am J Epidemiol 177:1356–1367. doi: 10.1093/aje/kws437 CrossRefGoogle Scholar
  13. Hackney AC, Muoio D, Meyer WR (2000) The effect of sex steroid hormones on substrate oxidation during prolonged submaximal exercise in women. The Japanese journal of physiology 50:489–494CrossRefGoogle Scholar
  14. Iavicoli I, Fontana L, Bergamaschi A (2009) The effects of metals as endocrine disruptors. Journal of toxicology and environmental health Part B, Critical reviews 12:206–223. doi: 10.1080/10937400902902062 CrossRefGoogle Scholar
  15. Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283:65–87. doi: 10.1016/j.tox.2011.03.001 CrossRefGoogle Scholar
  16. Kamel NM, Ramadan AM, Kamel MI, Mostafa YA, Abo el-Naga RM, Ali AM (2003) Impact of lead exposure on health status and scholastic achievement of school pupils in Alexandria. The Journal of the Egyptian Public Health Association 78:1–28Google Scholar
  17. 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 258:32–42. doi: 10.1016/j.taap.2011.10.004 CrossRefGoogle Scholar
  18. Kravchenko J, Darrah TH, Miller RK, Lyerly HK, Vengosh A (2014) A review of the health impacts of barium from natural and anthropogenic exposure. Environ Geochem Health 36:797–814. doi: 10.1007/s10653-014-9622-7 CrossRefGoogle Scholar
  19. Kuiper N, Rowell C, Nriagu J, Shomar B (2014) What do the trace metal contents of urine and toenail samples from Qatar’s farm workers bioindicate? Environ Res 131:86–94. doi: 10.1016/j.envres.2014.02.011 CrossRefGoogle Scholar
  20. Liang Y et al (2015) Childhood obesity affects adult metabolic syndrome and diabetes. Endocrine 50:87–92. doi: 10.1007/s12020-015-0560-7 CrossRefGoogle Scholar
  21. Mailloux R, Lemire J, Appanna V (2007) Aluminum-induced mitochondrial dysfunction leads to lipid accumulation in human hepatocytes: a link to obesity. Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 20:627–638. doi: 10.1159/000107546 CrossRefGoogle Scholar
  22. Martin MB et al (2002) Role of cadmium in the regulation of AR gene expression and activity. Endocrinology 143:263–275. doi: 10.1210/endo.143.1.8581 CrossRefGoogle Scholar
  23. Moon SS (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 46:263–271. doi: 10.1007/s12020-013-0061-5 CrossRefGoogle Scholar
  24. Nie X et al (2016) Blood cadmium in Chinese adults and its relationships with diabetes and obesity. Environ Sci Pollut Res Int. doi: 10.1007/s11356-016-7078-2 Google Scholar
  25. Nomura Y, Okamoto S, Sakamoto M, Feng Z, Nakamura T (2005) Effect of cobalt on the liver glycogen content in the streptozotocin-induced diabetic rats. Mol Cell Biochem 277:127–130. doi: 10.1007/s11010-005-5777-y CrossRefGoogle Scholar
  26. Ogden CL, Carroll MD, Curtin LR, Lamb MM, Flegal KM (2010) Prevalence of high body mass index in US children and adolescents, 2007-2008. JAMA 303:242–249. doi: 10.1001/jama.2009.2012 CrossRefGoogle Scholar
  27. Ogden CL, Carroll MD, Kit BK, Flegal KM (2014) Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 311:806–814. doi: 10.1001/jama.2014.732 CrossRefGoogle Scholar
  28. Padilla MA, Elobeid M, Ruden DM, Allison DB (2010) An examination of the association of selected toxic metals with total and central obesity indices: NHANES 99-02. Int J Environ Res Public Health 7:3332–3347. doi: 10.3390/ijerph7093332 CrossRefGoogle Scholar
  29. Pollack AZ et al (2013) Trace elements and endometriosis: the ENDO study. Reprod Toxicol 42:41–48. doi: 10.1016/j.reprotox.2013.05.009 CrossRefGoogle Scholar
  30. Rank M et al (2013) The cardio-metabolic risk of moderate and severe obesity in children and adolescents. J Pediatr 163:137–142. doi: 10.1016/j.jpeds.2013.01.020 CrossRefGoogle Scholar
  31. Rosin A (2009) The long-term consequences of exposure to lead. The Israel Medical Association journal : IMAJ 11:689–694Google Scholar
  32. Scinicariello F, Buser MC, Mevissen M, Portier CJ (2013) Blood lead level association with lower body weight in NHANES 1999-2006. Toxicol Appl Pharmacol 273:516–523. doi: 10.1016/j.taap.2013.09.022 CrossRefGoogle Scholar
  33. 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 161:13–19. doi: 10.1007/s12011-014-0082-9 CrossRefGoogle Scholar
  34. Skelton JA, Cook SR, Auinger P, Klein JD, Barlow SE (2009) Prevalence and trends of severe obesity among US children and adolescents. Acad Pediatr 9:322–329. doi: 10.1016/j.acap.2009.04.005 CrossRefGoogle Scholar
  35. Stoica A, Katzenellenbogen BS, Martin MB (2000) Activation of estrogen receptor-alpha by the heavy metal cadmium. Mol Endocrinol 14:545–553. doi: 10.1210/mend.14.4.0441 Google Scholar
  36. Sughis M, Nawrot TS, Riaz A, Ikram-Dar U, Mahmood A, Haufroid V, Nemery B (2014) Metal exposure in schoolchildren and working children. A urinary biomonitoring study from Lahore, Pakistan. Int J Hyg Environ Health 217:669–677. doi: 10.1016/j.ijheh.2014.02.002 CrossRefGoogle Scholar
  37. Tang-Peronard JL, Andersen HR, Jensen TK, Heitmann BL (2011) Endocrine-disrupting chemicals and obesity development in humans: a review. Obesity reviews : an official journal of the International Association for the Study of Obesity 12:622–636. doi: 10.1111/j.1467-789X.2011.00871.x CrossRefGoogle Scholar
  38. Tascilar ME, Ozgen IT, Abaci A, Serdar M, Aykut O (2011) Trace elements in obese Turkish children. Biol Trace Elem Res 143:188–195. doi: 10.1007/s12011-010-8878-8 CrossRefGoogle Scholar
  39. Vacchi-Suzzi C et al (2015) Dietary intake estimates and urinary cadmium levels in Danish postmenopausal women. PLoS One 10:e0138784. doi: 10.1371/journal.pone.0138784 CrossRefGoogle Scholar
  40. Vasudevan H, McNeill JH (2007) Chronic cobalt treatment decreases hyperglycemia in streptozotocin-diabetic rats. Biometals : an international journal on the role of metal ions in biology, biochemistry, and medicine 20:129–134. doi: 10.1007/s10534-006-9020-4 CrossRefGoogle Scholar
  41. Vidal AC et al (2015) Maternal cadmium, iron and zinc levels, DNA methylation and birth weight. BMC pharmacology & toxicology 16:20. doi: 10.1186/s40360-015-0020-2 CrossRefGoogle Scholar
  42. Waisberg M, Joseph P, Hale B, Beyersmann D (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192:95–117. doi: 10.1016/s0300-483x(03)00305-6 CrossRefGoogle Scholar
  43. White LD et al (2007) New and evolving concepts in the neurotoxicology of lead. Toxicol Appl Pharmacol 225:1–27. doi: 10.1016/j.taap.2007.08.001 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Center of Gallbladder Disease, Shanghai East HospitalTongji University School of MedicineShanghaiChina
  2. 2.State Key Laboratory of Reproductive Medicine, Institute of ToxicologyNanjing Medical UniversityNanjingChina
  3. 3.Key Laboratory of Modern Toxicology of Ministry of Education, School of Public HealthNanjing Medical UniversityNanjingChina
  4. 4.NanjingChina

Personalised recommendations