{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,30]],"date-time":"2026-04-30T00:00:13Z","timestamp":1777507213303,"version":"3.51.4"},"reference-count":62,"publisher":"Ovid Technologies (Wolters Kluwer Health)","issue":"2","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>Toxic metals have been associated with lower birth weight while essential metals have been associated with higher birth weight. Evidence for other metals is either inconsistent or limited in terms of number of studies. This study analyzed 17 urinary metals, individually and as a mixture, and their association with measures of fetal growth in the LIFECODES birth cohort. Ultrasound was used to measure the abdominal circumference, head circumference, and femur length and measures were used to calculate estimated fetal weight at ~26 and ~35 weeks. We calculated the <jats:italic toggle=\"yes\">z<\/jats:italic> score based on gestational age at scan, and estimated fetal weight (EFW) was combined with birth weight for longitudinal analyses. Metals were measured in samples collected at ~26 weeks. We used linear mixed-effects models to examine associations between metals and repeated measures of each outcome, controlling for covariates. Principal components analysis reduced the biomarkers to predictors that may share some commonality. We found that an interquartile range increase in selenium was inversely associated with femur length <jats:italic toggle=\"yes\">z<\/jats:italic> score as well as other growth outcomes. Other essential metals, however, were associated with an increase in growth. Finally, the PCA component comprised of arsenic, mercury, and tin was associated with decreased head circumference <jats:italic toggle=\"yes\">z<\/jats:italic> score (\u22120.14 [95% CI, \u22120.23, \u22120.05]).<\/jats:p>","DOI":"10.1097\/ee9.0000000000000075","type":"journal-article","created":{"date-parts":[[2020,2,14]],"date-time":"2020-02-14T12:59:17Z","timestamp":1581685157000},"page":"e075","source":"Crossref","is-referenced-by-count":19,"title":["Urinary trace metals in association with fetal ultrasound measures during pregnancy"],"prefix":"10.1097","volume":"4","author":[{"given":"Stephani S.","family":"Kim","sequence":"first","affiliation":[{"name":"Epidemiology Branch, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"John D.","family":"Meeker","sequence":"additional","affiliation":[{"name":"Department of Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, Michigan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Max T.","family":"Aung","sequence":"additional","affiliation":[{"name":"Department of Environmental Health Sciences, University of Michigan School of Public Health, Ann Arbor, Michigan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Youfei","family":"Yu","sequence":"additional","affiliation":[{"name":"Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, Michigan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bhramar","family":"Mukherjee","sequence":"additional","affiliation":[{"name":"Department of Biostatistics, University of Michigan School of Public Health, Ann Arbor, Michigan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"David E.","family":"Cantonwine","sequence":"additional","affiliation":[{"name":"Division of Maternal-Fetal Medicine, Brigham and Women\u2019s Hospital, Harvard Medical School, Boston, Massachusetts"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Thomas F.","family":"McElrath","sequence":"additional","affiliation":[{"name":"Division of Maternal-Fetal Medicine, Brigham and Women\u2019s Hospital, Harvard Medical School, Boston, Massachusetts"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kelly K.","family":"Ferguson","sequence":"additional","affiliation":[{"name":"Epidemiology Branch, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"276","published-online":{"date-parts":[[2020,4]]},"reference":[{"key":"R1-20231116","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1093\/ije\/31.6.1235","article-title":"Fetal origins of adult disease: strength of effects and biological basis.","volume":"31","author":"Barker","year":"2002","journal-title":"Int J Epidemiol"},{"key":"R2-20231116","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1056\/NEJM198501103120204","article-title":"The contribution of low birth weight to infant mortality and childhood morbidity.","volume":"312","author":"McCormick","year":"1985","journal-title":"N Engl J Med"},{"key":"R3-20231116","doi-asserted-by":"crossref","first-page":"1234","DOI":"10.1056\/NEJM199904223401603","article-title":"Birth weight in relation to morbidity and mortality among newborn infants.","volume":"340","author":"McIntire","year":"1999","journal-title":"N Engl J Med"},{"key":"R4-20231116","first-page":"165","article-title":"Predictive factors for intrauterine growth restriction.","volume":"7","author":"Albu","year":"2014","journal-title":"J Med Life"},{"key":"R5-20231116","doi-asserted-by":"crossref","first-page":"708126","DOI":"10.1155\/2013\/708126","article-title":"Intrauterine growth restriction: effects of physiological fetal growth determinants on diagnosis.","volume":"2013","author":"Haram","year":"2013","journal-title":"Obstet Gynecol Int"},{"key":"R6-20231116","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1002\/uog.11204","article-title":"Fetal growth: a review of terms, concepts and issues relevant to obstetrics.","volume":"41","author":"Mayer","year":"2013","journal-title":"Ultrasound Obstet Gynecol"},{"key":"R7-20231116","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.aogh.2016.01.008","article-title":"Effects of environmental exposures on fetal and childhood growth trajectories.","volume":"82","author":"Zheng","year":"2016","journal-title":"Ann Glob Health"},{"key":"R8-20231116","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/j.envint.2017.12.011","article-title":"Environmental phenol associations with ultrasound and delivery measures of fetal growth.","volume":"112","author":"Ferguson","year":"2018","journal-title":"Environ Int"},{"key":"R9-20231116","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1016\/j.envint.2016.06.013","article-title":"Urinary phthalate metabolite and bisphenol A associations with ultrasound and delivery indices of fetal growth.","volume":"94","author":"Ferguson","year":"2016","journal-title":"Environ Int"},{"key":"R10-20231116","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/j.envint.2016.11.023","article-title":"Prenatal lead exposure and fetal growth: smaller infants have heightened susceptibility.","volume":"99","author":"Rodosthenous","year":"2017","journal-title":"Environ Int"},{"key":"R11-20231116","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.envres.2018.09.006","article-title":"Placental concentrations of essential, toxic, and understudied metals and relationships with birth outcomes in Chattanooga, TN.","volume":"168","author":"Mikelson","year":"2019","journal-title":"Environ Res"},{"key":"R12-20231116","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1017\/S204017441800106X","article-title":"First trimester maternal exposures to endocrine disrupting chemicals and metals and fetal size in the Michigan Mother-Infant Pairs study.","volume":"10","author":"Goodrich","year":"2019","journal-title":"J Dev Orig Health Dis"},{"key":"R13-20231116","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1080\/10937400801921320","article-title":"Epidemiologic evidence of relationships between reproductive and child health outcomes and environmental chemical contaminants.","volume":"11","author":"Wigle","year":"2008","journal-title":"J Toxicol Environ Health B Crit Rev"},{"key":"R19-20231116","doi-asserted-by":"crossref","first-page":"e109661","DOI":"10.1371\/journal.pone.0109661","article-title":"Maternal cadmium levels during pregnancy associated with lower birth weight in infants in a North Carolina cohort.","volume":"9","author":"Johnston","year":"2014","journal-title":"PLoS One"},{"key":"R20-20231116","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/j.ijheh.2013.04.009","article-title":"Birth outcome measures and maternal exposure to heavy metals (lead, cadmium and mercury) in Saudi Arabian population.","volume":"217","author":"Al-Saleh","year":"2014","journal-title":"Int J Hyg Environ Health"},{"key":"R21-20231116","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1093\/ajcn\/51.4.678","article-title":"A positive association between maternal serum zinc concentration and birth weight.","volume":"51","author":"Neggers","year":"1990","journal-title":"Am J Clin Nutr"},{"key":"R22-20231116","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1001\/jama.1995.03530060037030","article-title":"The effect of zinc supplementation on pregnancy outcome.","volume":"274","author":"Goldenberg","year":"1995","journal-title":"JAMA"},{"key":"R23-20231116","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1016\/j.nutres.2006.08.008","article-title":"Low-normal serum selenium early in human pregnancy predicts lower birth weight.","volume":"26","author":"Bogden","year":"2006","journal-title":"Nutrition Research"},{"key":"R24-20231116","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1111\/j.1740-8709.2012.00430.x","article-title":"Maternal selenium, copper and zinc concentrations in pregnancy associated with small-for-gestational-age infants.","volume":"10","author":"Mistry","year":"2014","journal-title":"Matern Child Nutr"},{"key":"R25-20231116","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1097\/EDE.0b013e3181df8e52","article-title":"Early postnatal blood manganese levels and children\u2019s neurodevelopment.","volume":"21","author":"Claus Henn","year":"2010","journal-title":"Epidemiology"},{"key":"R26-20231116","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1007\/s40572-016-0108-x","article-title":"Manganese exposure and cognition across the lifespan: contemporary review and argument for biphasic dose-response health effects.","volume":"3","author":"Vollet","year":"2016","journal-title":"Curr Environ Health Rep"},{"key":"R27-20231116","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.envres.2017.09.018","article-title":"Prenatal exposure to mercury and longitudinally assessed fetal growth: Relation and effect modifiers.","volume":"160","author":"Ballester","year":"2018","journal-title":"Environ Res"},{"key":"R28-20231116","doi-asserted-by":"crossref","first-page":"1096","DOI":"10.1017\/S0007114510001947","article-title":"Prenatal mercury contamination: relationship with maternal seafood consumption during pregnancy and fetal growth in the \u2018EDEN mother-child\u2019 cohort.","volume":"104","author":"Drouillet-Pinard","year":"2010","journal-title":"Br J Nutr"},{"key":"R29-20231116","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1001\/jamapediatrics.2013.3699","article-title":"Environmental phthalate exposure and preterm birth.","volume":"168","author":"Ferguson","year":"2014","journal-title":"JAMA Pediatr"},{"issue":"pt 1","key":"R30-20231116","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1016\/j.envint.2018.09.052","article-title":"Urinary trace metals individually and in mixtures in association with preterm birth.","volume":"121","author":"Kim","year":"2018","journal-title":"Environ Int"},{"key":"R31-20231116","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/0002-9378(85)90298-4","article-title":"Estimation of fetal weight with the use of head, body, and femur measurements\u2013a prospective study.","volume":"151","author":"Hadlock","year":"1985","journal-title":"Am J Obstet Gynecol"},{"key":"R32-20231116","doi-asserted-by":"crossref","first-page":"e0146532","DOI":"10.1371\/journal.pone.0146532","article-title":"Utilizing longitudinal measures of fetal growth to create a standard method to assess the impacts of maternal disease and environmental exposure.","volume":"11","author":"Cantonwine","year":"2016","journal-title":"PLoS One"},{"key":"R33-20231116","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1080\/1047322X.1990.10389587","article-title":"Estimation of Average Concentration in the Presence of Nondetectable Values.","volume":"5","author":"Hornung","year":"1990","journal-title":"Applied Occupational and Environmental Hygiene"},{"key":"R34-20231116","first-page":"611","article-title":"A comparison of several methods for analyzing censored data.","volume":"51","author":"Hewett","year":"2007","journal-title":"Ann Occup Hyg"},{"key":"R35-20231116","doi-asserted-by":"crossref","first-page":"1323","DOI":"10.1002\/sim.2283","article-title":"Secondary analysis of case-control data.","volume":"25","author":"Jiang","year":"2006","journal-title":"Stat Med"},{"key":"R37-20231116","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1111\/ppe.12486","article-title":"Foetal ultrasound measurement imputations based on growth curves versus multiple imputation chained equation (MICE).","volume":"32","author":"Ferguson","year":"2018","journal-title":"Paediatr Perinat Epidemiol"},{"key":"R38-20231116","first-page":"1","article-title":"mice: multivariate imputation by chained equations in R.","volume":"45","author":"van Buuren","year":"2011","journal-title":"J Stat Softw"},{"key":"R42-20231116","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1080\/10590501.2015.1055163","article-title":"Selenium and human health: witnessing a copernican revolution?","volume":"33","author":"Jablonska","year":"2015","journal-title":"J Environ Sci Health C Environ Carcinog Ecotoxicol Rev"},{"key":"R43-20231116","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.jtemb.2006.01.006","article-title":"Zinc requirements and the risks and benefits of zinc supplementation.","volume":"20","author":"Maret","year":"2006","journal-title":"J Trace Elem Med Biol"},{"key":"R44-20231116","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1007\/s40572-018-0213-0","article-title":"Environmental selenium and human health: an update.","volume":"5","author":"Vinceti","year":"2018","journal-title":"Curr Environ Health Rep"},{"key":"R45-20231116","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1016\/S0140-6736(11)61452-9","article-title":"Selenium and human health.","volume":"379","author":"Rayman","year":"2012","journal-title":"Lancet"},{"key":"R48-20231116","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.envres.2017.06.016","article-title":"Maternal exposure to selenium and cadmium, fetal growth, and placental expression of steroidogenic and apoptotic genes.","volume":"158","author":"Everson","year":"2017","journal-title":"Environ Res"},{"key":"R49-20231116","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.chemosphere.2014.02.080","article-title":"The effects of prenatal exposure to low-level cadmium, lead and selenium on birth outcomes.","volume":"108","author":"Sun","year":"2014","journal-title":"Chemosphere"},{"issue":"2 suppl","key":"R50-20231116","doi-asserted-by":"crossref","first-page":"499S","DOI":"10.1093\/ajcn\/68.2.499S","article-title":"Potential contribution of maternal zinc supplementation during pregnancy to maternal and child survival.","volume":"68","author":"Caulfield","year":"1998","journal-title":"Am J Clin Nutr"},{"key":"R51-20231116","doi-asserted-by":"crossref","first-page":"641","DOI":"10.3390\/nu8100641","article-title":"Association between maternal zinc status, dietary zinc intake and pregnancy complications: a systematic review.","volume":"8","author":"Wilson","year":"2016","journal-title":"Nutrients"},{"key":"R52-20231116","doi-asserted-by":"crossref","first-page":"1473","DOI":"10.1289\/ehp.11490","article-title":"Cadmium, lead, and other metals in relation to semen quality: human evidence for molybdenum as a male reproductive toxicant.","volume":"116","author":"Meeker","year":"2008","journal-title":"Environ Health Perspect"},{"key":"R53-20231116","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.fertnstert.2008.09.044","article-title":"Environmental exposure to metals and male reproductive hormones: circulating testosterone is inversely associated with blood molybdenum.","volume":"93","author":"Meeker","year":"2010","journal-title":"Fertil Steril"},{"key":"R54-20231116","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1016\/j.chemosphere.2016.08.142","article-title":"Exploratory analysis of the potential relationship between urinary molybdenum and bone mineral density among adult men and women from NHANES 2007-2010.","volume":"164","author":"Lewis","year":"2016","journal-title":"Chemosphere"},{"key":"R55-20231116","doi-asserted-by":"crossref","first-page":"1468","DOI":"10.1080\/10934529.2010.500942","article-title":"Maternal exposure to low-level heavy metals during pregnancy and birth size.","volume":"45","author":"Shirai","year":"2010","journal-title":"J Environ Sci Health A Tox Hazard Subst Environ Eng"},{"key":"R57-20231116","doi-asserted-by":"crossref","first-page":"e0185645","DOI":"10.1371\/journal.pone.0185645","article-title":"Heavy metals exposure levels and their correlation with different clinical forms of fetal growth restriction.","volume":"12","author":"Sabra","year":"2017","journal-title":"PLoS One"},{"key":"R58-20231116","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1038\/sj.jp.7211453","article-title":"Effect of magnitude and timing of maternal pregnancy blood lead (Pb) levels on birth outcomes.","volume":"26","author":"Jelliffe-Pawlowski","year":"2006","journal-title":"J Perinatol"},{"key":"R59-20231116","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1111\/1471-0528.12756","article-title":"Adverse effects of maternal lead levels on birth outcomes in the ALSPAC study: a prospective birth cohort study.","volume":"122","author":"Taylor","year":"2015","journal-title":"BJOG"},{"key":"R60-20231116","doi-asserted-by":"crossref","first-page":"5744","DOI":"10.1016\/j.scitotenv.2010.07.079","article-title":"Perinatal lead and mercury exposure in Austria.","volume":"408","author":"Gundacker","year":"2010","journal-title":"Sci Total Environ"},{"key":"R61-20231116","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1016\/j.envpol.2013.07.023","article-title":"Levels of prenatal mercury exposure and their relationships to neonatal anthropometry in Wujiang City, China.","volume":"182","author":"Guo","year":"2013","journal-title":"Environ Pollut"},{"key":"R63-20231116","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1093\/aje\/kwn332","article-title":"Arsenic exposure during pregnancy and size at birth: a prospective cohort study in Bangladesh.","volume":"169","author":"Rahman","year":"2009","journal-title":"Am J Epidemiol."},{"key":"R64-20231116","first-page":"190","article-title":"Arsenic in drinking-water and reproductive health outcomes: a study of participants in the Bangladesh Integrated Nutrition Programme.","volume":"24","author":"Kwok","year":"2006","journal-title":"J Health Popul Nutr"},{"key":"R65-20231116","doi-asserted-by":"crossref","first-page":"1051","DOI":"10.1016\/j.scitotenv.2014.05.076","article-title":"Associations between land cover categories, soil concentrations of arsenic, lead and barium, and population race\/ethnicity and socioeconomic status.","volume":"490","author":"Davis","year":"2014","journal-title":"Sci Total Environ"},{"key":"R66-20231116","doi-asserted-by":"crossref","first-page":"2040","DOI":"10.1093\/clinchem\/39.10.2040","article-title":"Urinary selenium concentrations.","volume":"39","author":"Sanz Alaejos","year":"1993","journal-title":"Clin Chem"},{"key":"R67-20231116","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/j.yrtph.2014.07.017","article-title":"Biomonitoring equivalents for selenium.","volume":"70","author":"Hays","year":"2014","journal-title":"Regul Toxicol Pharmacol"},{"key":"R68-20231116","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1097\/00001648-199607000-00008","article-title":"Use of selenium concentration in whole blood, serum, toenails, or urine as a surrogate measure of selenium intake.","volume":"7","author":"Longnecker","year":"1996","journal-title":"Epidemiology"},{"key":"R70-20231116","doi-asserted-by":"crossref","first-page":"2040S","DOI":"10.3945\/ajcn.2009.27230G","article-title":"Methods of assessment of zinc status in humans: a systematic review.","volume":"89","author":"Lowe","year":"2009","journal-title":"Am J Clin Nutr"},{"key":"R71-20231116","doi-asserted-by":"crossref","first-page":"3252","DOI":"10.3390\/nu7053252","article-title":"Determination of zinc status in humans: which indicator should we use?","volume":"7","author":"Wieringa","year":"2015","journal-title":"Nutrients"},{"key":"R72-20231116","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1093\/ajcn\/62.4.790","article-title":"Molybdenum absorption, excretion, and retention studied with stable isotopes in young men at five intakes of dietary molybdenum.","volume":"62","author":"Turnlund","year":"1995","journal-title":"Am J Clin Nutr"},{"key":"R73-20231116","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.1093\/ajcn\/61.5.1102","article-title":"Molybdenum absorption, excretion, and retention studied with stable isotopes in young men during depletion and repletion.","volume":"61","author":"Turnlund","year":"1995","journal-title":"Am J Clin Nutr"},{"key":"R75-20231116","doi-asserted-by":"crossref","first-page":"1669","DOI":"10.1289\/ehp.7917","article-title":"A critical review of biomarkers used for monitoring human exposure to lead: advantages, limitations, and future needs.","volume":"113","author":"Barbosa","year":"2005","journal-title":"Environ Health Perspect"},{"key":"R76-20231116","doi-asserted-by":"crossref","first-page":"9234","DOI":"10.1007\/s11356-014-2827-6","article-title":"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.","volume":"21","author":"Fort","year":"2014","journal-title":"Environ Sci Pollut Res Int"},{"key":"R77-20231116","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1002\/uog.1751","article-title":"A systematic review of the ultrasound estimation of fetal weight.","volume":"25","author":"Dudley","year":"2005","journal-title":"Ultrasound Obstet Gynecol"}],"container-title":["Environmental Epidemiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.lww.com\/10.1097\/EE9.0000000000000075","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,16]],"date-time":"2023-11-16T16:00:55Z","timestamp":1700150455000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.lww.com\/10.1097\/EE9.0000000000000075"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,11]]},"references-count":62,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2020]]}},"URL":"https:\/\/doi.org\/10.1097\/ee9.0000000000000075","relation":{},"ISSN":["2474-7882"],"issn-type":[{"value":"2474-7882","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,2,11]]}}}