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Maternal tobacco smoking in pregnancy and children’s socio-emotional development at age 5: The EDEN mother-child birth cohort study

Published online by Cambridge University Press:  15 April 2020

M. Melchior*
Affiliation:
INSERM, UMR-S 1136, Department of Social Epidemiology, Pierre-Louis Institute of Epidemiology and Public Health, 75013Paris, France UMR-S 1136, Department of Social Epidemiology, Pierre Louis Institute of Epidemiology and Public Health, Sorbonne Universités, UPMC – Université Paris 06, 75013Paris, France
R. Hersi
Affiliation:
INSERM, UMR-S 1136, Department of Social Epidemiology, Pierre-Louis Institute of Epidemiology and Public Health, 75013Paris, France UMR-S 1136, Department of Social Epidemiology, Pierre Louis Institute of Epidemiology and Public Health, Sorbonne Universités, UPMC – Université Paris 06, 75013Paris, France
J. van der Waerden
Affiliation:
INSERM, UMR-S 1136, Department of Social Epidemiology, Pierre-Louis Institute of Epidemiology and Public Health, 75013Paris, France UMR-S 1136, Department of Social Epidemiology, Pierre Louis Institute of Epidemiology and Public Health, Sorbonne Universités, UPMC – Université Paris 06, 75013Paris, France
B. Larroque
Affiliation:
INSERM, Obstetrical, Perinatal and Pediatric Epidemiology Research Team, Center for Epidemiology and Biostatistics (U1153), Paris-Descartes University, 75020Paris, France UMR-S 953, UPMC – Université Paris 06, 75020Paris, France
M.-J. Saurel-Cubizolles
Affiliation:
INSERM, Obstetrical, Perinatal and Pediatric Epidemiology Research Team, Center for Epidemiology and Biostatistics (U1153), Paris-Descartes University, 75020Paris, France UMR-S 953, UPMC – Université Paris 06, 75020Paris, France
A. Chollet
Affiliation:
INSERM, UMR-S 1136, Department of Social Epidemiology, Pierre-Louis Institute of Epidemiology and Public Health, 75013Paris, France UMR-S 1136, Department of Social Epidemiology, Pierre Louis Institute of Epidemiology and Public Health, Sorbonne Universités, UPMC – Université Paris 06, 75013Paris, France
C. Galéra
Affiliation:
Department of Child and Adolescent Psychiatry, Charles-Perrens Hospital, University of Bordeaux, 33076Bordeaux, France INSERM U897, Center for Research in Epidemiology and Biostatistics, prévention et prise en charge des traumatismes, Bordeaux, France
*
Corresponding author. INSERM, UMR-S 1136, hôpital Paul-Brousse, 16, avenue Paul-Vaillant-Couturier, 94800 Villejuif, France. Tel.: +33 1 77 74 74 27. E-mail address: maria.melchior@inserm.fr (M. Melchior).
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Abstract

Background

There is debate as to whether maternal tobacco use in pregnancy is related to offspring behaviour later on. We tested this association examining multiple aspects of children's behaviour at age 5 and accounting for parental smoking outside of pregnancy, as well as child and family characteristics.

Methods

Data come from a prospective community based birth cohort study (EDEN; n = 1113 families in France followed since pregnancy in 2003–2005 until the child's 5th birthday). Maternal tobacco use in pregnancy was self-reported. Children's socio-emotional development (emotional symptoms, conduct problems, symptoms of hyperactivity/inattention, peer relationship problems, prosocial behaviour) was assessed by mothers using the Strengths and Difficulties Questionnaire (SDQ) at age 5 years. Logistic regression analyses controlled for Inverse Probability Weights (IPW) of maternal tobacco use calculated based on study center, children's characteristics (sex, premature birth, low birth weight, breastfeeding), maternal characteristics (age at the child's birth, psychological difficulties and alcohol use in pregnancy, post-pregnancy depression, and smoking), paternal smoking in and post-pregnancy, parental educational attainment, family income, parental separation, and maternal negative life events.

Results

Maternal smoking in pregnancy only predicted children's high symptoms of hyperactivity/inattention (sex and study center-adjusted ORs: maternal smoking in the 1st trimester: 1.95, 95%CI: 1.13–3.38; maternal smoking throughout pregnancy: OR = 2.11, 95%CI: 1.36–3.27). In IPW-controlled regression models, only children of mothers who smoked throughout pregnancy had significantly elevated levels of hyperactivity/inattention (OR = 2.20, 95%CI: 1.21–4.00).

Conclusions

Maternal tobacco smoking in pregnancy may contribute directly or through epigenetic mechanisms to children's symptoms of hyperactivity/inattention.

Type
Original article
Copyright
Copyright © Elsevier Masson SAS 2015

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Footnotes

1

Deceased.

2

The EDEN Mother-Child Cohort Study Group: I. Annesi-Maesano, J. Botton, M.A. Charles, P. Dargent-Molina, B. de Lauzon-Guillain, P. Ducimetière, M. de Agostini, B. Foliguet, A. Forhan, X. Fritel, A. Germa, V. Goua, R. Hankard, B. Heude, M. Kaminski, B. Larroque, N. Lelong, J. Lepeule, G. Magnin, L. Marchand, C. Nabet, R. Slama, M.J. Saurel-Cubizolles, M. Schweitzer, O. Thiebaugeorge.

References

Amone-P’olak, K., Burger, H., Ormel, J., Huisman, M., Verhulst, F.C., Oldehinkel, A.J.. Socioeconomic position and mental health problems in pre- and early-adolescents: the TRAILS study. Soc Psychiatry Psychiatr Epidemiol 2009;44:231238.CrossRefGoogle ScholarPubMed
Andres, R.L., Day, M.C.. Perinatal complications associated with maternal tobacco use. Semin Neonatol 2000;5:231241.CrossRefGoogle ScholarPubMed
Austin, P.C.. An introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivar Behav Res 2011;46:399424.CrossRefGoogle ScholarPubMed
Betoko, A., Charles, M.A., Hankard, R., Forhan, A., Bonet, M., Saurel-Cubizolles, M.J., et al.Infant feeding patterns over the first year of life: influence of family characteristics. Eur J Clin Nutr 2013;67:631637.CrossRefGoogle ScholarPubMed
Blondel, B., Lelong, N., Kermarrec, M., Goffinet, F.. Trends in perinatal health in France between 1995 and 2010: results from the National Perinatal Surveys. J Gynecol Obstet Biol Reprod (Paris) 2012;41:151166.CrossRefGoogle ScholarPubMed
Brion, M.J., Victora, C., Matijasevich, A., Horta, B., Anselmi, L., Steer, C., et al.Maternal smoking and child psychological problems: disentangling causal and noncausal effects. Pediatrics 2010;126:e57e65.CrossRefGoogle ScholarPubMed
Bublitz, M.H., Stroud, L.R.. Maternal smoking during pregnancy and offspring brain structure and function: review and agenda for future research. Nicotine Tob Res 2012;14:388397.CrossRefGoogle ScholarPubMed
Chittleborough, C.R., Lawlor, D.A., Lynch, J.W.. Prenatal prediction of poor maternal and offspring outcomes: implications for selection into intensive parent support programs. Matern Child Health J 2012;16:909920.CrossRefGoogle ScholarPubMed
Cornelius, M.D., Day, N.L.. Developmental consequences of prenatal tobacco exposure. Curr Opin Neurol 2009;22:121125.CrossRefGoogle ScholarPubMed
Cox, J.L., Chapman, G., Murray, D., Jones, P.. Validation of the Edinburgh Postnatal Depression Scale (EPDS) in non-postnatal women. J Affect Disord 1996;39:185189.CrossRefGoogle Scholar
Dwyer, J.B., McQuown, S.C., Leslie, F.M.. The dynamic effects of nicotine on the developing brain. Pharmacol Ther 2009;122:125139.CrossRefGoogle ScholarPubMed
Ernst, M., Moolchan, E.T., Robinson, M.L.. Behavioral and neural consequences of prenatal exposure to nicotine. J Am Acad Child Adolesc Psychiatry 2001;40:630641.CrossRefGoogle ScholarPubMed
Frisell, T., Oberg, S., Kuja-Halkola, R., Sjolander, A.. Sibling comparison designs: bias from non-shared confounders and measurement error. Epidemiology 2012;23:713720.CrossRefGoogle ScholarPubMed
Gaysina, D., Fergusson, D.M., Leve, L.D., Horwood, J., Reiss, D., Shaw, D.S., et al.Maternal smoking during pregnancy and offspring conduct PROBLEMS: evidence from 3 independent genetically sensitive research designs. JAMA Psychiatry 2013;70:956963.CrossRefGoogle ScholarPubMed
Goodman, R.. The Strengths and Difficulties Questionnaire: a research note. J Child Psychol Psychiatry 1997;38:581586.CrossRefGoogle ScholarPubMed
Hanley, J.. A heuristic approach to the formulas for population attributable fraction. J Epidemiol Community Health 2001;55:508514.CrossRefGoogle ScholarPubMed
Heath, C.J., King, S.L., Gotti, C., Marks, M.J., Picciotto, M.R.. Cortico-thalamic connectivity is vulnerable to nicotine exposure during early postnatal development through alpha4/beta2/alpha5 nicotinic acetylcholine receptors. Neuropsychopharmacology 2010;35:23242338.CrossRefGoogle ScholarPubMed
Hellstrom-Lindahl, E., Nordberg, A.. Smoking during pregnancy: a way to transfer the addiction to the next generation?. Respiration 2002;69:289293.CrossRefGoogle ScholarPubMed
Hernan, M., Robbins, J.IP weighting and marginal structural models. Causal inference 2013;1121.Google Scholar
Herrmann, M., King, K., Weitzman, M.. Prenatal tobacco smoke and postnatal secondhand smoke exposure and child neurodevelopment. Curr Opin Pediatr 2008;20:184190.CrossRefGoogle ScholarPubMed
Iniguez, C., Ballester, F., Costa, O., Murcia, M., Souto, A., Santa-Marina, L., et al.Maternal smoking during pregnancy and fetal biometry: the INMA Mother and Child Cohort Study. Am J Epidemiol 2013;178:10671075.CrossRefGoogle ScholarPubMed
Jauniaux, E., Burton, G.J.. Morphological and biological effects of maternal exposure to tobacco smoke on the feto-placental unit. Early Hum Dev 2007;83:699706.CrossRefGoogle ScholarPubMed
Keyes, K.M., Davey, S.G., Susser, E.. Associations of prenatal maternal smoking with offspring hyperactivity: causal or confounded?. Psychol Med 2014;44:857867.CrossRefGoogle ScholarPubMed
Keyes, K.M., Smith, G.D., Susser, E.. Commentary: smoking in pregnancy and offspring health: early insights into family-based and ‘negative control’ studies?. Int J Epidemiol 2014;43:13811388.CrossRefGoogle ScholarPubMed
Langley, K., Heron, J., Smith, G.D., Thapar, A.. Maternal and paternal smoking during pregnancy and risk of ADHD symptoms in offspring: testing for intrauterine effects. Am J Epidemiol 2012;176:261268.CrossRefGoogle ScholarPubMed
Linnet, K.M., Wisborg, K., Obel, C., Secher, N.J., Thomsen, P.H., Agerbo, E., et al.Smoking during pregnancy and the risk for hyperkinetic disorder in offspring. Pediatrics 2005;116:462467.CrossRefGoogle ScholarPubMed
Maccani, M.A., Avissar-Whiting, M., Banister, C.E., McGonnigal, B., Padbury, J.F., Marsit, C.J.. Maternal cigarette smoking during pregnancy is associated with downregulation of miR-16, miR-21, and miR-146a in the placenta. Epigenetics 2010;5:583589.CrossRefGoogle ScholarPubMed
Magee, S.R., Bublitz, M.H., Orazine, C., Brush, B., Salisbury, A., Niaura, R., et al.The relationship between maternal-fetal attachment and cigarette smoking over pregnancy. Matern Child Health J 2014;18:10171022.CrossRefGoogle ScholarPubMed
Marzocchi, G.M., Capron, C., Di, P.M., Duran, T.E., Duyme, M., Frigerio, A., et al.The use of the Strengths and Difficulties Questionnaire (SDQ) in Southern European countries. Eur Child Adolesc Psychiatry 2004;13(Suppl. 2):II40II46.CrossRefGoogle Scholar
Massey, S.H., Compton, M.T.. Psychological differences between smokers who spontaneously quit during pregnancy and those who do not: a review of observational studies and directions for future research. Nicotine Tob Res 2013;15:307319.CrossRefGoogle Scholar
McClernon, F.J., Kollins, S.H.. ADHD and smoking: from genes to brain to behavior. Ann N Y Acad Sci 2008;1141:131147.CrossRefGoogle Scholar
Melchior, M., Chastang, J.-F., de Lauzon, B., Galéra, C., Saurel-Cubizolles, M.-J., Larroque, B.. Maternal depression, socioeconomic position, and temperament in early childhood: the EDEN mother-child cohort. J Affect Disord 2012;137:165169.CrossRefGoogle ScholarPubMed
Obel, C., Olsen, J., Henriksen, T.B., Rodriguez, A., Jarvelin, M.R., Moilanen, I., et al.Is maternal smoking during pregnancy a risk factor for hyperkinetic disorder? – Findings from a sibling design. Int J Epidemiol 2011;40:338345.CrossRefGoogle ScholarPubMed
Radloff, L.. The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Measur 1977;1(37):385401.CrossRefGoogle Scholar
Roza, S.J., Verhulst, F.C., Jaddoe, V.W., Steegers, E.A., Mackenbach, J.P., Hofman, A., et al.Maternal smoking during pregnancy and child behaviour problems: the Generation R Study. Int J Epidemiol 2009;38:680689.CrossRefGoogle ScholarPubMed
Skoglund, C., Chen, Q., D’Onofrio, B.M., Lichtenstein, P., Larsson, H.. Familial confounding of the association between maternal smoking during pregnancy and ADHD in offspring. J Child Psychol Psychiatry 2014;55:6168.CrossRefGoogle ScholarPubMed
Spielberger, C.State-Trait Anxiety Inventory (Form Y). Palo Alto, CA: Mind Garden; 1983.Google Scholar
Storebo, O.J., Darling, R.P., Simonsen, E.Association between insecure attachment and ADHD: environmental mediating factors. J Atten Disord 2013.CrossRefGoogle Scholar
Suter, M., Abramovici, A., Aagaard-Tillery, K.Genetic and epigenetic influences associated with intrauterine growth restriction due to in utero tobacco exposure Pediatr Endocrinol Rev 2010;8:94102Google ScholarPubMed
Suter, M., Ma, J., Harris, A., Patterson, L., Brown, K.A., Shope, C., et al.Maternal tobacco use modestly alters correlated epigenome-wide placental DNA methylation and gene expression. Epigenetics 2011;6:12841294.CrossRefGoogle ScholarPubMed
Thapar, A., Rutter, M.Do prenatal risk factors cause psychiatric disorder? Be wary of causal claims. Br J Psychiatry 2009;195:100101.CrossRefGoogle ScholarPubMed
Thapar, A., Rice, F., Hay, D., Boivin, J., Langley, K., van den Bree, M., et al.Prenatal smoking might not cause attention-deficit/hyperactivity disorder: evidence from a novel design. Biol Psychiatry 2009;66:722727.CrossRefGoogle Scholar
Weiler, M.D., Bellinger, D., Marmor, J., Rancier, S., Waber, D.Mother and teacher reports of ADHD symptoms: DSM-IV questionnaire data. J Am Acad Child Adolesc Psychiatry 1999;38:11391147.CrossRefGoogle ScholarPubMed
Weissman, M.M., Wickramaratne, P., Warner, V., John, K., Prusoff, B.A., Merikangas, K.R., et al.Assessing psychiatric disorders in children. Discrepancies between mothers’ and children's reports. Arch Gen Psychiatry 1987;44:747753.CrossRefGoogle ScholarPubMed
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