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Predictors of toxic metal exposures among US women of reproductive age

Journal of Exposure Science & Environmental Epidemiology volume 29, pages 597–612 (2019)Cite this article

Abstract

Background

Arsenic, cadmium, lead, and mercury are ubiquitous toxicants that may be especially harmful to unborn children. We therefore sought to identify temporal trends and predictors of toxic metal biomarkers among US women of reproductive age, including those who were pregnant and/or breastfeeding.

Methods

Interviews and examinations were performed among a representative sample of women, aged 20–44 years, as part of the 2003–2014 National Health and Nutrition Examination Surveys. A range of sociodemographic, lifestyle, and dietary factors were evaluated as predictors of urinary inorganic arsenic, urinary cadmium, blood mercury, and blood lead concentrations.

Results

Levels of all four toxic metal biomarkers declined during the study period. Older age, racial/ethnic minorities, and a birthplace outside of the US were independently associated with higher toxic metal concentrations. Associations were similar for women who were pregnant or breastfeeding and those who were not.

Conclusion

US women of reproductive age were exposed to lower levels of toxic metals in 2013–2014 compared to 2003–2004. However, because the long-term health effects of early life exposures are unclear, public health efforts to address toxic metals should pay particular attention to older, nonwhite, and foreign-born women if they are pregnant or planning to become pregnant.

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References

  1. Agency of Toxic Substances and Disease Registry. ATSDR’s Substance Priority List. Atlanta, GA. 2017. https://www.atsdr.cdc.gov/spl/.

  2. Milton AH, Hussain S, Akter S, Rahman M, Mouly TA, Mitchell K. A review of the effects of chronic arsenic exposure on adverse pregnancy outcomes. Int J Environ Res Public Health. 2017;14:556.

    Article  Google Scholar 

  3. Lamadrid-Figueroa H, Tellez-Rojo MM, Hernandez-Avila M, Trejo-Valdivia B, Solano-Gonzalez M, Mercado-Garcia A, et al. Association between the plasma/whole blood lead ratio and history of spontaneous abortion: a nested cross-sectional study. BMC Pregnancy Childbirth. 2007;7:22.

    Article  Google Scholar 

  4. Sun H, Chen W, Wang D, Jin Y, Chen X, Xu Y. The effects of prenatal exposure to low-level cadmium, lead and selenium on birth outcomes. Chemosphere. 2014;108:33–9.

    Article  CAS  Google Scholar 

  5. Murcia M, Ballester F, Enning AM, Iniguez C, Valvi D, Basterrechea M, et al. Prenatal mercury exposure and birth outcomes. Environ Res. 2016;151:11–20.

    Article  CAS  Google Scholar 

  6. Rudge CV, Rollin HB, Nogueira CM, Thomassen Y, Rudge MC, Odland JO. 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. 2009;11:1322–30.

    Article  CAS  Google Scholar 

  7. Garcia-Esquinas E, Perez-Gomez B, Fernandez MA, Perez-Meixeira AM, Gil E, de Paz C, et al. Mercury, lead and cadmium in human milk in relation to diet, lifestyle habits and sociodemographic variables in Madrid (Spain). Chemosphere. 2011;85:268–76.

    Article  CAS  Google Scholar 

  8. Axelrad DA, Bellinger DC, Ryan LM, Woodruff TJ. Dose-response relationship of prenatal mercury exposure and IQ: an integrative analysis of epidemiologic data. Environ Health Perspect. 2007;115:609–15.

    Article  Google Scholar 

  9. Freire C, Amaya E, Gil F, Fernandez MF, Murcia M, Llop S, et al. Prenatal co-exposure to neurotoxic metals and neurodevelopment in preschool children: The Environment and Childhood (INMA) Project. Sci Total Environ. 2018;621:340–51.

    Article  CAS  Google Scholar 

  10. Jacobson JL, Muckle G, Ayotte P, Dewailly E, Jacobson SW. Relation of Prenatal Methylmercury Exposure from Environmental Sources to Childhood IQ. Environ Health Perspect. 2015;123:827–33.

    Article  CAS  Google Scholar 

  11. Valeri L, Mazumdar MM, Bobb JF, Claus Henn B, Rodrigues E, Sharif OIA, et al. The joint effect of prenatal exposure to metal mixtures on neurodevelopmental outcomes at 20–40 months of age: evidence from rural Bangladesh. Environ Health Perspect. 2017;125:067015.

    Article  Google Scholar 

  12. McDermott S, Wu J, Cai B, Lawson A, Marjorie Aelion C. Probability of intellectual disability is associated with soil concentrations of arsenic and lead. Chemosphere. 2011;84:31–8.

    Article  CAS  Google Scholar 

  13. Shim YK, Lewin MD, Ruiz P, Eichner JE, Mumtaz MM. Prevalence and associated demographic characteristics of exposure to multiple metals and their species in human populations: the United States NHANES, 2007-2012. J Toxicol Environ Health A. 2017;80:502–12.

    Article  CAS  Google Scholar 

  14. Schober SE, Sinks TH, Jones RL, Bolger PM, McDowell M, Osterloh J, et al. Blood mercury levels in US children and women of childbearing age, 1999–2000. J Am Med Assoc. 2003;289:1667–74.

    Article  CAS  Google Scholar 

  15. Toxicological profile for mercury. Atlanta, GA: Agency for Toxic Substances and Disease Registries; 1999.

  16. Toxicological profile for lead. Atlanta, GA: Agency for Toxic Substances and Disease Registries; 2007.

  17. Toxicological profile for cadmium. Atlanta, GA: Agency for Toxic Substances and Disease Registries; 2012.

  18. Jones MR, Tellez-Plaza M, Vaidya D, Grau M, Francesconi KA, Goessler W, et al. Estimation of inorganic arsenic exposure in populations with frequent seafood intake: evidence from MESA and NHANES. Am J Epidemiol. 2016;184:590–602.

    Article  Google Scholar 

  19. Pirkle JL, Flegal KM, Bernert JT, Brody DJ, Etzel RA, Maurer KR. Exposure of the US population to environmental tobacco smoke: the Third National Health and Nutrition Examination Survey, 1988 to 1991. J Am Med Assoc. 1996;275:1233–40.

    Article  CAS  Google Scholar 

  20. Bailey RL, Fakhouri TH, Park Y, Dwyer JT, Thomas PR, Gahche JJ, et al. Multivitamin-mineral use is associated with reduced risk of cardiovascular disease mortality among women in the United States. J Nutr. 2015;145:572–8.

    Article  CAS  Google Scholar 

  21. United States Department of Agriculture. Food patterns equivalents database (FPED). Beltsville, Maryland: Agriculture Research Service; 2018.

    Google Scholar 

  22. Nigra AE, Sanchez TR, Nachman KE, Harvey D, Chillrud SN, Graziano JH. et al. The effect of the environmental protection agency maximum contaminant level on arsenic exposure in the USA from 2003 to 2014: an analysis of the National Health and Nutrition Examination Survey (NHANES). Lancet Public Health.2017;2:e513–21.

    Article  Google Scholar 

  23. Barr DB, Wilder LC, Caudill SP, Gonzalez AJ, Needham LL, Pirkle JL. Urinary creatinine concentrations in the U.S. population: implications for urinary biologic monitoring measurements. Environ Health Perspect. 2005;113:192–200.

    Article  CAS  Google Scholar 

  24. Benjamini Y. YH controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Stat Methodol Ser B. 1995;57:289–300.

    Google Scholar 

  25. Bradley MA, Barst BD, Basu N. A review of mercury bioavailability in humans and fish. Int J Environ Res Public Health. 2017;14:169.

    Article  Google Scholar 

  26. Davis MA, Gilbert-Diamond D, Karagas MR, Li Z, Moore JH, Williams SM, et al. A dietary-wide association study (DWAS) of environmental metal exposure in US children and adults. PLoS ONE. 2014;9:e104768.

    Article  Google Scholar 

  27. Mania M, Rebeniak M, Szynal T, Wojciechowska-Mazurek M, Starska K, Ledzion E, et al. Total and inorganic arsenic in fish, seafood and seaweeds–exposure assessment. Rocz Panstw Zakl Hig. 2015;66:203–10.

    CAS  PubMed  Google Scholar 

  28. Xue J, Zartarian V, Wang SW, Liu SV, Georgopoulos P. Probabilistic modeling of dietary arsenic exposure and dose and evaluation with 2003–2004 NHANES data. Environ Health Perspect. 2010;118:345–50.

    Article  CAS  Google Scholar 

  29. Forbes LE, Graham JE, Berglund C, Bell RC. Dietary change during pregnancy and women’s reasons for change. Nutrients. 2018;10:1032.

    Article  Google Scholar 

  30. Wang X, Ding N, Tucker KL, Weisskopf MG, Sparrow D, Hu H, et al. A western diet pattern is associated with higher concentrations of blood and bone lead among middle-aged and elderly men. J Nutr. 2017;147:1374–83.

    Article  CAS  Google Scholar 

  31. Arbuckle TE, Liang CL, Morisset AS, Fisher M, Weiler H, Cirtiu CM, et al. Maternal and fetal exposure to cadmium, lead, manganese and mercury: the MIREC study. Chemosphere. 2016;163:270–82.

    Article  CAS  Google Scholar 

  32. Luo Y, McCullough LE, Tzeng JY, Darrah T, Vengosh A, Maguire RL, et al. Maternal blood cadmium, lead and arsenic levels, nutrient combinations, and offspring birthweight. BMC Public Health. 2017;17:354.

    Article  Google Scholar 

  33. Li H, Hansen AR, McGalliard Z, Gover L, Yan F, Zhang J. Trends in smoking and smoking cessation during pregnancy from 1985 to 2014, racial and ethnic disparity observed from multiple national surveys. Matern Child Health J. 2018;22:685–93.

    Article  Google Scholar 

  34. Cusack LK, Smit E, Kile ML, Harding AK. Regional and temporal trends in blood mercury concentrations and fish consumption in women of child bearing age in the united states using NHANES data from 1999 to 2010. Environ Health. 2017;16:10.

    Article  Google Scholar 

  35. Pirkle JL, Kaufmann RB, Brody DJ, Hickman T, Gunter EW, Paschal DC. Exposure of the U.S. population to lead, 1991–1994. Environ Health Perspect. 1998;106:745–50.

    Article  CAS  Google Scholar 

  36. Carrington CD, Montwill B, Bolger PM. An intervention analysis for the reduction of exposure to methylmercury from the consumption of seafood by women of child-bearing age. Regul Toxicol Pharmacol. 2004;40:272–80.

    Article  CAS  Google Scholar 

  37. Yang L, Tong EK, Mao Z, Hu TW, Lee AH. A clustered randomized controlled trial to reduce secondhand smoke exposure among nonsmoking pregnant women in sichuan province, China. Nicotine Tob Res. 2016;18:1163–70.

    Article  Google Scholar 

  38. Zhai Q, Narbad A, Chen W. Dietary strategies for the treatment of cadmium and lead toxicity. Nutrients. 2015;7:552–71.

    Article  Google Scholar 

  39. Prasanthi RP, Devi CB, Basha DC, Reddy NS, Reddy GR. Calcium and zinc supplementation protects lead (Pb)-induced perturbations in antioxidant enzymes and lipid peroxidation in developing mouse brain. Int J Dev Neurosci. 2010;28:161–7.

    Article  CAS  Google Scholar 

  40. Enli Y, Turgut S, Oztekin O, Demir S, Enli H, Turgut G. Cadmium intoxication of pregnant rats and fetuses: interactions of copper supplementation. Arch Med Res. 2010;41:7–13.

    Article  CAS  Google Scholar 

  41. Freudenheim JL, Johnson NE, Wardrop RL. Misclassification of nutrient intake of individuals and groups using one-, two-, three-, and seven-day food records. Am J Epidemiol. 1987;126:703–13.

    Article  CAS  Google Scholar 

  42. Caldwell KL, Cheng PY, Jarrett JM, Makhmudov A, Vance K, Ward CD, et al. Measurement challenges at low blood lead levels. Pediatrics. 2017;140:e20170272.

    Article  Google Scholar 

  43. Donald JM, Bradley M, O’Grady JE, Cutler MG, Moore MR. Effects of low-level lead exposure on 24 h activity patterns in the mouse. Toxicol Lett. 1988;42:137–47.

    Article  CAS  Google Scholar 

  44. Buchet JP, Lauwerys R, Roels H. Urinary excretion of inorganic arsenic and its metabolites after repeated ingestion of sodium metaarsenite by volunteers. Int Arch Occup Environ Health. 1981;48:111–8.

    Article  CAS  Google Scholar 

  45. Suwazono Y, Kido T, Nakagawa H, Nishijo M, Honda R, Kobayashi E, et al. Biological half-life of cadmium in the urine of inhabitants after cessation of cadmium exposure. Biomarkers. 2009;14:77–81.

    Article  CAS  Google Scholar 

  46. Jo S, Woo HD, Kwon HJ, Oh SY, Park JD, Hong YS, et al. Estimation of the biological half-life of methylmercury using a population toxicokinetic model. Int J Environ Res Public Health. 2015;12:9054–67.

    Article  CAS  Google Scholar 

  47. Tsoi MF, Cheung CL, Cheung TT, Cheung BM. Continual decrease in blood lead level in Americans: United States National Health Nutrition and Examination Survey 1999–2014. Am J Med. 2016;129:1213–8.

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank the staff and participants of the National Health and Nutritional Examination Survey. PAB was supported by the National Institute of Environmental Health Sciences (NIEHS) T32ES007018.

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Authors and Affiliations

  1. Department of Environmental Sciences and Engineering, Gilling School of Global Public Health, University of North Carolina, Chapel Hill, NC, USA

    Catherine M. Bulka, Paige A. Bommarito & Rebecca C. Fry

  2. Institute for Environmental Health Solutions, Gilling School of Global Public Health, University of North Carolina, Chapel Hill, NC, USA

    Rebecca C. Fry

  3. Curriculum in Toxicology, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

    Rebecca C. Fry

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  1. Catherine M. Bulka
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Correspondence to Rebecca C. Fry.

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Bulka, C.M., Bommarito, P.A. & Fry, R.C. Predictors of toxic metal exposures among US women of reproductive age. J Expo Sci Environ Epidemiol 29, 597–612 (2019). https://doi.org/10.1038/s41370-019-0152-3

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