Skip to main content
Log in

Urinary concentrations of environmental metals and associating factors in pregnant women

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Pregnant women, a vulnerable population, can be exposed to a variety of environmental metals that may adversely affect their health at elevated concentrations. Moreover, environmental exposure and risk disparities are associated with several factors such as sociodemographic characteristics, pregnancy complications, and nutritional supplementation indicators. Our aim was to investigate whether and how the urinary metal concentrations vary according to these factors in a large pregnancy and birth cohort. Urinary levels of seven metals including manganese, zinc, selenium, arsenic, cadmium, thallium, and lead were assessed in 7359 participants across Wuhan City in China. In all, 7359 urine samples from the third trimester were analyzed and 15 sociodemographic characteristics, pregnancy complications, and nutritional supplementation indicators were assessed: maternal age, household income, multivitamin supplements during pregnancy, etc. Concentrations of Zn, As, and Cd were detected in all urine samples; Mn, Se, Tl, and Pb were detected in 95.3%, 99.8%, 99.8%, and 99.9% urine samples, respectively. The geometric mean (GM) of creatinine-adjusted urinary Mn, Zn, Se, As, Cd, Tl, and Pb concentrations were 1.42, 505.44, 18.24, 30.49, 0.64, 0.55, and 3.69 μg/g. Factors that associated with environmental metals concentration were as follows: (1) Urinary Zn and Cd concentrations increased with maternal age. (2) Pregnant women with higher education had lower Cd concentrations. (3) Pregnant women with folic acid supplementation had lower Mn and with multivitamin supplementation had higher Se and lower Tl. Our results demonstrated that the maternal age, education level, folic acid supplementation, and multivitamin supplementation were significantly associated with environmental metal concentrations. Furthermore, studies are recommended to explore the influence of diet on biological metals concentrations in more detail.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Amaya E, Gil F, Freire C et al (2013) Placental concentrations of heavy metals in a mother–child cohort. Environ Res 120(complete):63–70

    CAS  Google Scholar 

  • Askari G, Iraj B, Salehi-Abargouei A, Fallah AA, Jafari T (2015) The association between serum selenium and gestational diabetes mellitus: a systematic review and meta-analysis. J Trace Elem Med Biol 29:195–201

    CAS  Google Scholar 

  • Behboudi-Gandevani S, Safary K, Moghaddam-Banaem L, Lamyian M, Goshtasbi A, Alian-Moghaddam N (2013) The relationship between maternal serum iron and zinc levels and their nutritional intakes in early pregnancy with gestational diabetes. Biol Trace Elem Res 154(1):7–13.14

    CAS  Google Scholar 

  • Bellinger DC (2005) Teratogen update: lead and pregnancy. Birth Defects Res A Clin Mol Teratol 73(6):409–420

    CAS  Google Scholar 

  • Black RE (2001) Micronutrients in pregnancy. Br J Nutr 85:193–197

    Google Scholar 

  • Bo S, Lezo A, Menato G, Gallo ML, Bardelli C, Signorile A, Berutti C, Massobrio M, Pagano GF (2005) Gestational hyperglycemia, zinc, selenium, and antioxidant vitamins. Nutrition 21(2):186–191

    CAS  Google Scholar 

  • Borella P, Szilagyi A, Than G, Csaba I, Giardino A, Facchinetti F (1990) Maternal plasma concentrations of magnesium, calcium, zinc and copper in normal and pathological pregnancies. Sci Total Environ 99(1–2):67–76

    CAS  Google Scholar 

  • Cakmak I (2008) Zinc crops 2007: improving crop production and human health. Plant Soil 306(1–2):1–2

    CAS  Google Scholar 

  • Callan AC, Hinwood AL, Ramalingam M, Boyce M, Heyworth J, McCafferty P, Odland JØ (2013) Maternal exposure to metals—concentrations and predictors of exposure. Environ Res 126(4):111–117

    CAS  Google Scholar 

  • Chang CM, Edwards S, Arab A et al (2017) Biomarkers of tobacco exposure: summary of an FDA-sponsored public workshop. Cancer Epidemiol Biomark Prev 26(3):291–302

    CAS  Google Scholar 

  • Choi RH, Sun JY, Yoo HJ, Kim S, Cho Y, Kim H, Kim S, Chung J, Oh SY, Lee SY (2016) A prospective study of serum trace elements in healthy Korean pregnant women. Nutrients 8(11):749

    Google Scholar 

  • Dejmek J, Solansk YI, Podrazilová K, Srám RJ (2002) The exposure of nonsmoking and smoking mothers to environmental tobacco smoke during different gestational phases and fetal growth. Environ Health Perspect 110(6):601–606

    Google Scholar 

  • Edwards SE, Maxson P, Miranda ML et al (2014) Cadmium levels in a North Carolina cohort: identifying risk factors for elevated levels during pregnancy. J Expo Sci Environ Epidemiol 25(4):427–432

    Google Scholar 

  • Esteban M, Castano A (2009) Non-invasive matrices in human biomonitoring: a review. Environ Int 35(2):438–449

    CAS  Google Scholar 

  • Ettinger AS, Arbuckle TE, Fisher M, Liang CL, Davis K, Cirtiu CM, Bélanger P, LeBlanc A, Fraser WD, MIREC Study Group (2017) Arsenic levels among pregnant women and newborns in Canada: results from the Maternal-Infant Research on Environmental Chemicals (MIREC) cohort. Environ Res 153:8–16

    CAS  Google Scholar 

  • Fort M, Cosíntomás M, Grimalt JO et al (2014) Assessment of exposure to trace metals in a cohort of pregnant women from an urban center by urine analysis in the first and third trimesters of pregnancy. Environ Sci Pollut Res Int 21(15):9234–9241

    CAS  Google Scholar 

  • Freire C, Koifman RJ, Fujimoto D, de Oliveira Souza VC, Barbosa F Jr, Koifman S (2015) Reference values of cadmium, arsenic and manganese in blood and factors associated with exposure levels among adult population of Rio Branco, Acre, Brazil. Chemosphere 128:70–78

    CAS  Google Scholar 

  • Grazuleviciene R, Nadisauskiene R, Buinauskiene J et al (2009) Effects of elevated levels of manganese and iron in drinking water on birth outcomes. Pol J Environ Stud 18(5):819–825

    CAS  Google Scholar 

  • Gunier RB, Mora AM, Smith D, Arora M, Austin C, Eskenazi B, Bradman A (2014) Biomarkers of manganese exposure in pregnant women and children living in an agricultural community in California. Environ Sci Technol 48(24):14695–14702

    CAS  Google Scholar 

  • Haines DA, Saravanabhavan G, Werry K et al (2017) An overview of human biomonitoring of environmental chemicals in the Canadian Health Measures Survey: 2007–2019. Int J Hyg Environ Health 220(2 Pt A):13–28

    CAS  Google Scholar 

  • Hinwood AL, Callan AC, Ramalingam M, Boyce M, Heyworth J, McCafferty P, Odland JØ (2013) Cadmium, lead and mercury exposure in non-smoking pregnant women. Environ Res 126(4):118–124

    CAS  Google Scholar 

  • Jablan J, Inic S, Stosnach H et al (2017) Level of minerals and trace elements in the urine of the participants of mountain ultra-marathon race. J Trace Elem Med Biol 41:54–59

    CAS  Google Scholar 

  • Jain RB (2013) Effect of pregnancy on the levels of blood cadmium, lead, and mercury for females aged 17–39 years old: data from National Health and Nutrition Examination Survey 2003–2010. J Toxicol Environ Health A 76(7):409–421

    CAS  Google Scholar 

  • Janakiraman V, Ettinger A, Mercadogarcia A et al (2003) Calcium supplements and bone resorption in pregnancy: a randomized crossover trial. Am J Prev Med 24(3):260–264

    Google Scholar 

  • Jiang Y, Xia W, Zhang B et al (2017) Predictors of thallium exposure and its relation with preterm birth. Environ Pollut

  • Juste C, Robert M (2000) Origin and deposition of trace contaminants. AIP Conference Proceedings, pp 83–92

  • Karbowska B (2016) Presence of thallium in the environment: sources of contaminations, distribution and monitoring methods. Environ Monit Assess 188(11):640

    Google Scholar 

  • Kennedy DA, Woodland C, Koren G (2012) Lead exposure, gestational hypertension and pre-eclampsia: a systematic review of cause and effect. J Obstet Gynaecol 32(6):512–517

    CAS  Google Scholar 

  • Kim Y, Ha EH, Park H, Ha M, Kim Y, Hong YC, Kim EJ, Kim BN (2013) Prenatal lead and cadmium co-exposure and infant neurodevelopment at 6 months of age: the Mothers and Children’s Environmental Health (MOCEH) study. Neurotoxicology 35(4):15–22

    CAS  Google Scholar 

  • Kippler M, Tofail F, Gardner R, Rahman A, Hamadani JD, Bottai M, Vahter M (2012) Maternal cadmium exposure during pregnancy and size at birth: a prospective cohort study. Environ Health Perspect 120(2):284–289

    CAS  Google Scholar 

  • Kurokawa S, Berry MJ (2013) Selenium. Role of the essential metalloid in health. Met Ions Life Sci 13:499–534

    Google Scholar 

  • Lee JW, Lee CK, Chan SM et al (2012) Korea National Survey for Environmental Pollutants in the Human Body 2008: heavy metals in the blood or urine of the Korean population. Int J Hyg Environ Health 215(4):449–457

    CAS  Google Scholar 

  • Lewin A, Arbuckle TE, Fisher M et al (2017) Univariate predictors of maternal concentrations of environmental chemicals: the MIREC study. Int J Hyg Environ Health 220(2 Pt A):77–85

    CAS  Google Scholar 

  • Liu H, Xia W, Xu S et al (2017a) Cadmium body burden and pregnancy-induced hypertension. Int J Hyg Environ Health 221:246–251

    Google Scholar 

  • Liu X, Zhang Y, Piao J, Mao D, Li Y, Li W, Yang L, Yang X (2017b) Reference values of 14 serum trace elements for pregnant Chinese women: a cross-sectional study in the China Nutrition and Health Survey 2010–2012. Nutrients 9(3):309

    Google Scholar 

  • Liu W, Zhang B, Huang Z, Pan X, Chen X, Hu C, Liu H, Jiang Y, Sun X, Peng Y, Xia W, Xu S, Li Y (2018) Cadmium body burden and gestational diabetes mellitus: a prospective study. Environ Health Perspect 126(2):027006

    Google Scholar 

  • Morris JS, Crane SB (2013) Selenium toxicity from a misformulated dietary supplement, adverse health effects, and the temporal response in the nail biologic monitor. Nutrients 5(4):1024–1057

    CAS  Google Scholar 

  • Moyene JPE, Scheers H, Tanduumba B et al (2016) Preeclampsia and toxic metals: a case-control study in Kinshasa, DR Congo. Environ Health 15(1):1–12

    Google Scholar 

  • Osorio-Yañez C, Gelaye B, Miller RS et al (2016) Associations of maternal urinary cadmium with trimester-specific blood pressure in pregnancy: role of dietary intake of micronutrients. Biol Trace Elem Res 174(1):71–81

    Google Scholar 

  • Pieczynska J, Grajeta H (2015) The role of selenium in human conception and pregnancy. J Trace Elem Med Biol 29:31–38

    CAS  Google Scholar 

  • Ramakrishnan U, Manjrekar R, Rivera J, Gonzáles-Cossío T, Martorell R (1999) Micronutrients and pregnancy outcome: a review of the literature. Nutr Res 19(1):103–159

    CAS  Google Scholar 

  • Roels HA, Bowler RM, Kim Y, Claus Henn B, Mergler D, Hoet P, Gocheva VV, Bellinger DC, Wright RO, Harris MG, Chang Y, Bouchard MF, Riojas-Rodriguez H, Menezes-Filho JA, Téllez-Rojo MM (2012) Manganese exposure and cognitive deficits: a growing concern for manganese neurotoxicity. Neurotoxicology 33(4):872–880

    CAS  Google Scholar 

  • Romano ME (2013) Maternal body burden of cadmium: impacts on gestational diabetes and fetal growth

  • Romano ME, Enquobahrie DA, Simpson CD, Checkoway H, Williams MA (2015) A case-cohort study of cadmium body burden and gestational diabetes mellitus in American women. Environ Health Perspect 123(10):993–998

    CAS  Google Scholar 

  • Rudge CV, Rollin HB, Nogueira CM et al (2009) The placenta as a barrier for toxic and essential elements in paired maternal and cord blood samples of South African delivering women. J Environ Monit 11(7):1322–1330

    CAS  Google Scholar 

  • Schulz C, Wilhelm M, Heudorf U, Kolossa-Gehring M, Human Biomonitoring Commission of the German Federal Environment Agency (2011) Update of the reference and HBM values derived by the German Human Biomonitoring Commission. Int J Hyg Environ Health 215(1):26–35

    CAS  Google Scholar 

  • Shirai S, Suzuki Y, Yoshinaga J, Mizumoto Y (2010) Maternal exposure to low-level heavy metals during pregnancy and birth size. J Environ Sci Health A Tox Hazard Subst Environ Eng 45(11):1468–1474

    CAS  Google Scholar 

  • Staff JF, Cotton RJ, Warren ND et al (2014) Comparison of urinary thallium levels in non-occupationally exposed people and workers. Int Arch Occup Environ Health 87(3):275–284

    CAS  Google Scholar 

  • Sun H, Chen W, Wang D, Jin Y, Chen X, Xu Y (2014) The effects of prenatal exposure to low-level cadmium, lead and selenium on birth outcomes. Chemosphere 108:33–39

    CAS  Google Scholar 

  • Taylor CM, Tilling K, Golding J et al (2016) Low level lead exposure and pregnancy outcomes in an observational birth cohort study: dose–response relationships. BMC Res Notes 9(1):1–5

    Google Scholar 

  • Vahter M (2009) Effects of arsenic on maternal and fetal health. Annu Rev Nutr 29(1):381–399

    CAS  Google Scholar 

  • Wang H, Hu YF, Hao JH, Chen YH, Wang Y, Zhu P, Zhang C, Xu YY, Tao FB, Xu DX (2016) Maternal serum zinc concentration during pregnancy is inversely associated with risk of preterm birth in a Chinese population. J Nutr 146(3):509–515

    CAS  Google Scholar 

  • Wigle DT, Arbuckle TE, Turner MC, Berube A, Yang Q, Liu S, Krewski D (2008) Epidemiologic evidence of relationships between reproductive and child health outcomes and environmental chemical contaminants. J Toxicol Environ Health B Crit Rev 11(5–6):373–517

    CAS  Google Scholar 

  • Woodruff TJ, Zota AR, Schwartz JM (2011) Environmental chemicals in pregnant women in the United States: NHANES 2003-2004. Environ Health Perspect 119(6):878–885

    Google Scholar 

  • Xia W, Du X, Zheng T et al (2016a) A case–control study of prenatal thallium exposure and low birth weight in China. Environ Health Perspect 124(1):164–169

    Google Scholar 

  • Xia W, Zhou Y, Zheng T, Zhang B, Bassig BA, Li Y, Wise JP, Zhou A, Wan Y, Wang Y, Xiong C, Zhao J, Li Z, Yao Y, Hu J, Pan X, Xu S (2016b) Maternal urinary manganese and risk of low birth weight: a case–control study. BMC Public Health 16(1):142

    Google Scholar 

  • Xing Y, Xia W, Zhang B, et al (2018). Relation between cadmium exposure and gestational diabetes mellitus. Environ Int 113

  • Yu XD, Yan CH, Shen XM, Tian Y, Cao LL, Yu XG, Zhao L, Liu JX (2011) Prenatal exposure to multiple toxic heavy metals and neonatal neurobehavioral development in Shanghai, China. Neurotoxicol Teratol 33(4):437–443

    Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (91743101, 91643207 and 21437002), the National Key Research and Development Plan of China (2016YFC0206700 and 2016YFC0206203), and the Fundamental Research Funds for the Central Universities, Huazhong University of Science and Technology (2016YXZD043 and 2018KFYXMPT00).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yuanyuan Li or Hongling Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Qi, L., Peng, Y. et al. Urinary concentrations of environmental metals and associating factors in pregnant women. Environ Sci Pollut Res 26, 13464–13475 (2019). https://doi.org/10.1007/s11356-019-04731-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-04731-z

Keywords

Navigation