OBJECTIVE: To assess the relationships of prenatal and childhood smoke exposure with specific neurodevelopmental and behavioral problems during early childhood. STUDY DESIGN: A subsample (n = 386) of mother-child dyads from the Newborn Epigenetic Study (NEST) prebirth cohort participated in the study. Cotinine concentrations were used to objectively measure prenatal and childhood smoke exposure when youth were aged 3-13 years. Multivariable regression models were used to estimate associations of prenatal and childhood cotinine concentrations with performance on the National Institutes of Health (NIH) Toolbox and attention-deficit/hyperactivity disorder and behavioral symptoms, measured using the Behavior Assessment System for Children, 2nd edition (BASC-2). RESULTS: After adjusting for confounders, childhood cotinine concentrations were associated with poorer cognitive performance on tasks measuring cognitive flexibility (B = -1.29; P = .03), episodic memory (B = -0.97; P = .02), receptive language development (B = -0.58; P = .01), and inhibitory control and attention (B = -1.59; P = .006). Although childhood cotinine concentration was associated with higher levels of attention problems (B = 0.83; P = .004) on the BASC-2, after adjustment for confounders, the association is nonsignificant. Although associations for maternal cotinine concentrations were null, an interaction was detected between prenatal and childhood cotinine concentrations on the NIH Toolbox Picture Vocabulary Task (P = .02). CONCLUSIONS: Our findings suggest that childhood tobacco smoke exposure may lead to poorer attention regulation and language acquisition, complex visual processing ability, and attention problems.

Department of Biological Sciences North Carolina State University Raleigh NC

Department of Biological Sciences North Carolina State University Raleigh NC; Department of Obstetrics and Gynecology University of North Carolina at Chapel Hill NC

Department of Health Behavior and Policy Virginia Commonwealth University School of Medicine Richmond VA

Department of Obstetrics and Gynecology Duke University School of Medicine Durham NC

Department of Psychiatry and Behavioral Sciences Duke University School of Medicine Durham NC

Holmusk Durham NC

Nicholas School of the Environment Duke University Durham NC

RAND Corporation Arlington VA

Research Center for Toxic Compounds in the Environment Faculty of Science Masaryk University Brno Czech Republic

School of Public Health Guangxi Medical University Nanning China

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Thapar A, Cooper M, Rutter M. Neurodevelopmental disorders. Lancet Psychiatry 2017;4:339–46. 10.1016/S2215-0366(16)30376-5 PubMed DOI

Wehmeier PM, Schacht A, Barkley RA. Social and emotional impair ment in children and adolescents with ADHD and the impact on quality of life. J Adolesc Health 2010;46:209–17. 10.1016/j.jadohealth.2009.09.009 PubMed DOI

Barbaresi WJ, Colligan RC, Weaver AL, Voigt RG, Killian JM, Katusic SK. Mortality, ADHD, and psychosocial adversity in adults with childhood ADHD: a prospective study. Pediatrics 2013;131:637–44. 10.1542/peds.2012-2354 PubMed DOI PMC

Clegg J, Hollis C, Mawhood L, Rutter M. Developmental language dis orders–a follow-up in later adult life. Cognitive, language and psychosocial outcomes. J Child Psychol Psychiatry 2005;46:128–49. 10.1111/j.1469-7610.2004.00342.x PubMed DOI

Ahmed SF, Kuhfeld M,Watts TW, Davis-Kean PE, Vandell DL. Preschool executive function and adult outcomes: a developmental cascade model. Dev Psychol 2021;57:2234–49. 10.1037/dev0001270 PubMed DOI

DiFranza JR, Aligne CA, Weitzman M. Prenatal and postnatal environ mental tobacco smoke exposure and children’s health. Pediatrics 2004;113:1007–15. PubMed

Fried PA, Watkinson B. 36- and 48-month neurobehavioral follow-up of children prenatally exposed to marijuana, cigarettes, and alcohol. J Dev Behav Pediatr 1990;11:49–58. PubMed

Ghassabian A, Sundaram R, Chahal N, McLain AC, Bell E, Lawrence DA, et al. Determinants of neonatal brain-derived neurotrophic factor and association with child development. Dev Psychopathol 2017;29:1499–511. 10.1017/S0954579417000414 PubMed DOI PMC

Keyes KM, Davey Smith G, Susser E. Associations of prenatal maternal smoking with offspring hyperactivity: causal or confounded? Psychol Med 2014;44:857–67. 10.1017/S0033291713000986 PubMed DOI PMC

Kiechl-Kohlendorfer U, Merkle U, Deufert D, Neubauer V, Peglow UP, Griesmaier E. Effect of developmental care for very premature infants on neurodevelopmental outcome at 2 years of age. Infant Behav Dev 2015;39:166–72. 10.1016/j.infbeh.2015.02.006 PubMed DOI

Abdel Hamed NA, Hammad EEM, Salama RH, Yassa HA, Awaga MM. Secondhand smoke as a risk factor for attention deficit hyperactivity dis order in children. Inhal Toxicol 2019;31:420–7. 10.1080/08958378.2019.1705440 PubMed DOI

Kovess V, Keyes KM, Hamilton A, Pez O, Bitfoi A, Koc C, et al. Maternal smoking and offspring inattention and hyperactivity: results from a cross-national European survey. Eur Child Adolesc Psychiatry 2015;24: 919–29. 10.1007/s00787-014-0641-9 PubMed DOI PMC

Joo H, Lim MH, Ha M, Kwon HJ, Yoo SJ, Choi KH, et al. Secondhand smoke exposure and low blood lead levels in association with attention deficit hyperactivity disorder and its symptom domain in children: a community-based case-control study. Nicotine Tob Res 2017;19:94–101. 10.1093/ntr/ntw152 PubMed DOI PMC

Margolis AE, Pagliaccio D, Ramphal B, Banker S, Thomas L, Robinson M, et al. Prenatal environmental tobacco smoke exposure al ters children’s cognitive control circuitry: a preliminary study. Environ Int 2021;155:106516. 10.1016/j.envint.2021.106516 PubMed DOI PMC

Ellis-Suriani Z, Norsa’adah B, Othman A, Siti-Azrin AH. Association be tween secondhand smoke exposure at home and cognitive performance among rural primary school children in Malaysia. Tob Induc Dis 2021;19:27. 10.18332/tid/133638 PubMed DOI PMC

Max W, Sung HY, Shi Y. Childhood secondhand smoke exposure and ADHD-attributable costs to the health and education system. J Sch Health 2014;84:683–6. 10.1111/josh.12191 PubMed DOI

Eskenazi B, Trupin LS. Passive and active maternal smoking during preg nancy, as measured by serum cotinine, and postnatal smoke exposure. II: effects on neurodevelopment at age 5 years. Am J Epidemiol 1995;142: S19–29. 10.1093/aje/142.Supplement_9.S19 PubMed DOI

Knopik VS. Maternal smoking during pregnancy and child outcomes: real or spurious effect? Dev Neuropsychol 2009;34:1–36. 10.1080/87565640802564366 PubMed DOI PMC

Trasti N, Vik T, Jacobsen G, Bakketeig LS. Smoking in pregnancy and children’s mental and motor development at age 1 and 5 years. Early Hum Dev 1999;55:37–147. 10.1016/S0378-3782(99)00017-1 PubMed DOI

Yolton K, Dietrich K, Auinger P, Lanphear BP, Hornung R. Exposure to environmental tobacco smoke and cognitive abilities among US children and adolescents. Environ Health Perspect 2005;113:98–103. 10.1289/ehp.7210 PubMed DOI PMC

Yang S, Decker A, Kramer MS. Exposure to parental smoking and child growth and development: a cohort study. BMC Pediatr 2013;13:104. 10.1186/1471-2431-13-104 PubMed DOI PMC

Oh K, Xu Y, Terrizzi BF, Lanphear B, Chen A, Kalkbrenner AE, et al. As sociations between early low-level tobacco smoke exposure and execu tive function at age 8 years. J Pediatr 2020;221:174–80.e1. 10.1016/j.jpeds.2019.11.032 PubMed DOI PMC

Hoyo C, Murtha AP, Schildkraut JM, Forman MR, Calingaert B, Demark-Wahnefried W, et al. Folic acid supplementation before and during pregnancy in the Newborn Epigenetics STudy (NEST). BMC Public Health 2011;11:46. 10.1186/1471-2458-11-46 PubMed DOI PMC

Liu Y, Murphy SK, Murtha AP, Fuemmeler BF, Schildkraut J, Huang Z, et al. Depression in pregnancy, infant birth weight and DNA methylation of imprint regulatory elements. Epigenetics 2012;7:735–46. 10.4161/epi.20734 PubMed DOI PMC

Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. The unity and diversity of executive functions and their con tributions to complex “frontal lobe” tasks: a latent variable analysis. Cog nit Psychol 2000;41:49–100. 10.1006/cogp.1999.0734 PubMed DOI

Wechsler D. Wechsler abbreviated Scale of intelligence. 2nd ed. London: Pearson; 2011.

Bender AH, Auciello D, Morrison CE, MacAllister WS, Zaroff CM. Comparing the convergent validity and clinical utility of the behavior assessment system for children-parent rating Scales and child behavior checklist in children with epilepsy. Epilepsy Behav 2008;13:237–42. 10.1016/j.yebeh.2008.03.007 PubMed DOI

Harrison JR, Vannest KJ, Reynolds CR. Behaviors that discriminate ADHD in children and adolescents: primary symptoms, symptoms of comorbid conditions, or indicators of functional impairment? J Atten Disord 2011;15:147–60. 10.1177/1087054709356170 PubMed DOI

Conners CK, Erhardt D, Epstein JN, Parker JDA, Sitarenios G, Sparrow E. Self-ratings of ADHD symptoms in adults I: factor structure and normative data. J Atten Disord 1999;3:141–51. 10.1177/108705479900300303 DOI

Textor J, Hardt J, Knuppel S. DAGitty: A graphical tool for analyzing € causal diagrams. Epidemiology 2011;22:745. 10.1097/EDE.0b013e318225c2be PubMed DOI

Benowitz NL, Dains KM, Dempsey D, Wilson M, Jacob P. Racial differ ences in the relationship between number of cigarettes smoked and nico tine and carcinogen exposure. Nicotine Tob Res 2011;13:772–83. 10.1093/ntr/ntr072 PubMed DOI PMC

Moore BF, Shapiro AL, Wilkening G, Magzamen S, Starling AP, Allshouse WB, et al. Prenatal exposure to tobacco and offspring neuro cognitive development in the Healthy Start study. J Pediatr 2020;218:28–34.e2. 10.1016/j.jpeds.2019.10.056 PubMed DOI PMC

National Center for Chronic Disease Prevention and Health Promotion (US) Office on Smoking and Health. The health consequences of smok ing—50 years of progress: a report of the Surgeon General. Atlanta (GA): Centers for Disease Control and Prevention; 2014. 10.1037/e510072014-001 PubMed DOI

Andersen SL. Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 2003;27:3–18. 10.1016/S0149-7634(03)00005-8 PubMed DOI

Deoni SCL. Neuroimaging of the developing brain and impact of nutri tion. Nestle Nutr Inst Workshop Ser 2018;89:155–74. 10.1159/000486500 PubMed DOI

Tregellas JR, Legget KT. Rapid early brain development highlights a crit ical period and possible intervention window. Biol Psychiatry Cogn Neurosci Neuroimaging 2020;5:937–8. 10.1016/j.bpsc.2020.08.007 PubMed DOI

Benowitz NL, Hukkanen J, Jacob P 3rd. Nicotine chemistry, metabolism, kinetics and biomarkers. Handb Exp Pharmacol 2009;192:29–60. 10.1007/978-3-540-69248-5_2 PubMed DOI PMC

Dempsey D, Jacob P 3rd, Benowitz NL. Accelerated metabolism of nico tine and cotinine in pregnant smokers. J Pharmacol Exp Ther 2002;301: 594–8. 10.1124/jpet.301.2.594 PubMed DOI

Jedrychowski W, Perera F,Mroz E, Edwards S, Flak E, Bernert JT, et al. Fetal exposure to secondhand tobacco smoke assessed by maternal self-reports and cord blood cotinine: prospective cohort study in Krakow. Matern Child Health J 2009;13:415–23. 10.1007/s10995-008-0350-4 PubMed DOI

Pichini S, Basagana XB, Pacifici R, Garcia O, Puig C, Vall O, et al. Cord ~ serum cotinine as a biomarker of fetal exposure to cigarette smoke at the end of pregnancy. Environ Health Perspect 2000;108:1079–83. 10.1289/ehp.001081079 PubMed DOI PMC

Zevin S, Jacob P, Geppetti P, Benowitz NL. Clinical pharmacology of oral cotinine. Drug Alcohol Depend 2000;60:13–8. 10.1016/S0376-8716(00)80003-4 PubMed DOI

Hajizadeh M, Nandi A. The socioeconomic gradient of secondhand smoke exposure in children: evidence from 26 low-income and middle-income countries. Tob Control 2016;25:e146–55. 10.1136/tobaccocontrol-2015-052828 PubMed DOI

Galvez MP, McGovern K, Teitelbaum SL, Windham G, Wolff MS. Neighborhood factors and urinary metabolites of nicotine, phthalates, and dichlorobenzene. Pediatrics 2018;141:S87–95. 10.1542/peds.2017-1026L PubMed DOI PMC

Fingerhut LA, Kleinman JC, Kendrick JS. Smoking before, during, and after pregnancy. Am J Public Health 1990;80:541–4. 10.2105/AJPH.80.5.541 PubMed DOI PMC

Kahn RS, Certain L, Whitaker RC. A reexamination of smoking before, during, and after pregnancy. Am J Public Health 2002;92:1801–8. 10.2105/AJPH.92.11.1801 PubMed DOI PMC

Andra SS, Austin C, Wright RO, Arora M. Reconstructing pre-natal and early childhood exposure to multi-class organic chemicals using teeth: towards a retrospective temporal exposome. Environ Int 2015;83:137–45. 10.1016/j.envint.2015.05.010 PubMed DOI PMC