Characterization of trace elements exposure in pregnant women in the United States, NHANES 1999–2016.

https://doi.org/10.1016/j.envres.2020.109208Get rights and content

Highlights

  • Pregnant women in the U.S. are exposed to several trace elements simultaneously.

  • A majority of metal concentrations were higher in pregnant women compared to non-pregnant women.

  • Blood lead, cadmium, mercury, as well as urine antimony, cadmium and lead in women of childbearing age decreased over time.

  • Urine cobalt in women of childbearing age increased over time.

Abstract

Objective

The objective of the current study is to report on urine, blood and serum metal concentrations to characterize exposures to trace elements and micronutrient levels in both pregnant women and women of child-bearing age in the U.S. National Health and Nutrition Examination Survey (NHANES) years 1999–2016.

Methods

Urine and blood samples taken from NHANES participants were analyzed for thirteen urine metals, three blood metals, three serum metals, speciated mercury in blood and speciated arsenic in urine. Adjusted and unadjusted least squares geometric means and 95% confidence intervals were calculated for all participants among women aged 15–44 years. Changes in exposure levels over time were also examined. Serum cotinine levels were used to adjust for smoke exposure, as smoking is a source of metal exposure.

Results

Detection rates for four urine metals from the ATSDR Substance Priority List: arsenic, lead, mercury and cadmium were ~83–99% for both pregnant and non-pregnant women of child bearing age. A majority of metal concentrations were higher in pregnant women compared to non-pregnant women. Pregnant women had higher mean urine total arsenic, urine mercury, and urine lead; however, blood lead and mercury were higher in non-pregnant women. Blood lead, cadmium, mercury, as well as urine antimony, cadmium and lead in women of childbearing age decreased over time, while urine cobalt increased over time.

Conclusions

Pregnant women in the US have been exposed to several trace metals, with observed concentrations for some trace elements decreasing since 1999.

Introduction

The Agency for Toxic Substance and Disease Registry (ATSDR) includes trace metals on the Substance Priority List based on frequency of occurrence at National Priorities List (NPL) sites, toxicity, and potential for human exposure (ATSDR, 2019). Metals such as lead, mercury, cadmium and arsenic are on the list. Trace elements from anthropogenic sources, such as manufacturing and mining, have been shown to accumulate in the environment (Wu et al., 2016). People can be exposed to these and other metals through soil, water, diet, air, commercial products and occupational sources. Exposure sources for individual metals may differ by geographical location and lifestyle characteristics (King et al., 2015; Callan et al., 2013). For example, the primary routes of arsenic exposure in the United States are drinking water and breathing airborne particles (ATSDR, 2007; Bloom et al., 2014), while exposure to methylmercury is the result of dietary intake (Hong et al., 2012).

Pregnant women are particularly vulnerable to metal accumulation due to changing body chemistry. For example, blood iron concentration can decrease during pregnancy, resulting in an accumulation of blood cadmium (Lee and Kim, 2012). Additionally, metals, such as arsenic and lead, can cross the placenta during pregnancy (Zhou et al., 2017). Maternal exposure to heavy metals has been linked to adverse birth outcomes including low birth weight, small head circumference, and developmental delays (Kumar et al., 2017; Shirai et al., 2010). Even low dose exposure to cadmium, lead, mercury and arsenic has been linked to low birth weight (King et al., 2015). Cadmium, in particular, has been linked to both low birth weight and decreased head circumference (Cheng et al., 2017). Smoking remains a non-occupational source of cadmium exposure (Ikeh-Tawari et al., 2013), and an estimated 13.8% of expectant mothers in the U.S. smoked while pregnant in 2005 (Centers for Disease Control and Prevention, 2017). Some metals, e.g. mercury and arsenic, exist in both organic and inorganic species and have different exposure routes and health effects depending on the chemical characteristics of the specific species (Park and Zheng, 2012). For example, there is little evidence linking elemental mercury exposure to adverse maternal health outcomes, while mercury metabolites like methylmercury are highly teratogenic and have been linked to developmental delays (Hinwood et al., 2013).

Other elements, such as iodine, copper, selenium, zinc, cobalt, and molybdenum are essential micronutrients and are particularly important during pregnancy, provided exposure does not exceed recommended levels. Micronutrient deficiencies have a range of negative health implications and can lead to low birth weight, preterm birth, fetal malformations, developmental delays, and miscarriage (Cetin et al., 2010; Gernand et al., 2016). Iodine is necessary for thyroid hormone synthesis; maternal iodine deficiency can lead to neurological complications and mental retardation in the developing fetus (Bailey et al., 2015). Zinc is a component of over 300 enzymes and is involved in DNA/RNA transcription (Zimmermann and Andersson, 2012; Andersson et al., 2010; Hu et al., 2014). Zinc deficiency in the maternal diet has been linked to intrauterine growth retardation and teratogenesis (Uriu-Adams and Keen, 2010). Copper helps ensure normal fetal hematopoiesis, and low copper levels have been linked to low birth weight (Bermudez et al., 2015). However, high levels of maternal copper have been linked to congenital heart defects (Hu et al., 2014). Selenium helps prevent free radical accumulation, and cobalt is used in the formation of vitamin B12 and red cell production (Fort et al., 2015; Mistry et al., 2014).

The objective of the current study is to report on trace element concentrations in urine, blood and serum in pregnant women of childbearing age (here defined as age 15–44 years) in the U.S compared to non-pregnant women of childbearing age. The National Health and Nutrition Examination Survey (NHANES) screens for chemicals and trace elements in the U.S. general population and the data is publicly available (National Center for Health Statistics, 2008). While the aim of NHANES is to collect data from 5000 participants annually and report the data biannually (also referred to as a “cycle”), the urine metal analyses are conducted on subsamples of this population, while the blood metals analysis captures the entire population. To increase sample sizes, multiple NHANES cycles from 1999 to 2016 were used in this analysis. This paper reports on trace metal exposure in pregnant women, compares the concentrations to non-pregnant women, and includes an analysis of geometric means by NHANES cycle for maternal exposure to metals since 1999.

Section snippets

Study populations

NHANES is administered by the National Center for Health Statistics, Centers for Disease Control and Prevention (CDC) and combines questionnaires, medical examinations, and laboratory biomonitoring methods to determine the prevalence of diseases and environmental exposures in the civilian, non-institutionalized general U.S. population. Participants receive a health examination at mobile examination centers (MECs). At the time of the exam, pregnancy status is ascertained by urine pregnancy tests

Results

Covariate sample sizes, means (continuous variables) and percent estimates (classification variables) are reported in Table 2. Estimates of least squares regression covariates in Table 2 from combined years represent the average over the time period covered by a particular multicycle, and thus these estimates vary somewhat across multicycles. Nevertheless, Table 2 shows a general pattern in which pregnant women tended to be younger, to be non-White, and to have lower cotinine levels across the

Discussion

Characterization of trace elements in urine, blood and serum in pregnant women living in the U.S. (NHANES, 1999–2016) is presented here. Pregnant women and non-pregnant women of childbearing age had 14 metals (antimony, barium, cadmium, cesium, cobalt, dimethylarsinic acid, iodine, lead, inorganic mercury, molybdenum, thallium, arsenic, tungsten and uranium) measured in urine with a detection rate greater than 75% in NHANES 1999–2016. Meanwhile, six metals (copper, lead, mercury, methyl

Disclaimer

The findings and conclusions in this manuscript have not been formally disseminated by the Centers for Disease Control and Prevention/the Agency for Toxic Substances and Disease Registry and should not be construed to represent any agency determination or policy.

Declaration of competing interest

The authors have no competing financial interests in relation to the work described.

References (64)

  • D.R. Jones

    Analysis of whole human blood for Pb, Cd, Hg, Se, and Mn by ICP-DRC-MS for biomonitoring and acute exposures

    Talanta

    (2017)
  • B.K. Lee et al.

    Iron deficiency is associated with increased levels of blood cadmium in the Korean general population: analysis of 2008-2009 Korean National Health and Nutrition Examination Survey data

    Environ. Res.

    (2012)
  • E. Oken

    Decline in fish consumption among pregnant women after a national mercury advisory

    Obstet. Gynecol.

    (2003)
  • F.A. Rabito

    Changes in low levels of lead over the course of pregnancy and the association with birth outcomes

    Reprod. Toxicol.

    (2014)
  • S. Thomas

    Metals exposure and risk of small-for-gestational age birth in a Canadian birth cohort: the MIREC study

    Environ. Res.

    (2015)
  • M.S. Tsai

    The critical fetal stage for maternal manganese exposure

    Environ. Res.

    (2015)
  • M. Abbassi-Ghanavati et al.

    Pregnancy and laboratory studies: a reference table for clinicians

    Obstet. Gynecol.

    (2009)
  • Toxicological Profile for Arsenic

    (2007)
  • Agency for Toxic Substances and Disease Registry Public Health Statement for Antimony

    (2015)
  • R.L. Bailey et al.

    The epidemiology of global micronutrient deficiencies

    Ann. Nutr. Metab.

    (2015)
  • L. Bermudez

    Assessment of ten trace elements in umbilical cord blood and maternal blood: association with birth weight

    J. Transl. Med.

    (2015)
  • J.T. Bernert

    Interlaboratory comparability of serum cotinine measurements at smoker and nonsmoker concentration levels: a round-robin study

    Nicotine Tob. Res.

    (2009)
  • K.L. Caldwell

    Use of inductively coupled plasma mass spectrometry to measure urinary iodine in NHANES 2000: comparison with previous method

    Clin. Chem.

    (2003)
  • K.L. Caldwell

    Inductively coupled plasma mass spectrometry to measure multiple toxic elements in urine in NHANES 1999-2000

    Atom. Spectros

    (2005)
  • K.L. Caldwell

    Iodine status in pregnant women in the National Children's Study and in U.S. women (15-44 years)

    Nat. Health Nut. Exam. Survey 2005-2010

    (2013)
  • Tobacco Use and Pregnancy

    (2017)
  • I. Cetin et al.

    Role of micronutrients in the periconceptional period

    Hum. Reprod. Update

    (2010)
  • L. Cheng

    Critical windows of prenatal exposure to cadmium and size at birth

    Int. J. Environ. Res. Publ. Health

    (2017)
  • Fourth national report on human exposure to environmental chemicals

  • A.D. Gernand

    Micronutrient deficiencies in pregnancy worldwide: health effects and prevention

    Nat. Rev. Endocrinol.

    (2016)
  • Y.S. Hong et al.

    Methylmercury exposure and health effects

    J. Prev. Med. Pub. Health

    (2012)
  • H. Hu

    Correlation between congenital heart defects and maternal copper and zinc concentrations

    Birth Defects Res. A Clin. Mol. Teratol.

    (2014)
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