Objective. Previous studies have linked maternal smoking during pregnancy with behavioral disturbance in children. However, additional evidence is needed to address the causality of the relationship. The present study analyses result from an Australian cohort of 5342 5-year-old children whose mothers were recruited early in pregnancy.

Methods. Smoking history was gathered for prepregnancy, first clinic visit (FCV), late pregnancy, and when the child was 6 months and 5 years of age. Behavior problems at the age of 5 were assessed using a modified Child Behavior Check List (CBCL) shown to have high agreement with the complete CBCL. This resulted in the formation of three scales: internalizing; social, attentional and thought; and externalizing behavior problems, which were then dichotimized at the 90th percentile in each case. Logistic regression was used to model these outcomes as a function of maternal smoking at five time points during which it was assessed. A series of models explored the effect of additional adjustment for confounding. The predictors of attrition (29.5%) throughout the cohort were also identified by multivariate modeling.

Results. The final analysis was carried out on a cohort of mother-child pairs for whom data and child behavior outcomes were complete. The mean age of children was 5 years, 6 months with a range from 4 to 6 years. The mean age of mothers at the time of birth of the child was 25 years, with a range from 13 to 47 years. Mothers lost to follow-up were more likely to be younger, single, and less well-educated than those who continued participation, although maternal smoking was not an independent determinant.

Unadjusted analyses showed strong associations between externalizing child behavior and maternal smoking during pregnancy and at the 5-year follow-up, with relative risks (RRs) up to 2.6 for children of women smoking at least 20 cigarettes per day at the first antenatal clinic visit. A clear dose-response relationship existed in most relationships with higher levels of smoking being associated with higher rates of externalizing behavior problems. Weaker relationships occurred for internalizing behavior and social, attentional and thought behavior problems.

Multivariate analysis of the timing in more detail that the association between maternal smoking and child behavior problems persisted, although the evidence for dose-response diminished. Moreover, it was primarily associated with smoking as determined by questions asked at the FCV (RR = 1.52, 2.03, 2.16) for 1 to 9, 10 to 19, and ≥20 cigarettes per day, respectively, compared with nonsmoking and secondarily by smoking determined at the 5-year follow-up (RR = 1.52, 1.87, 1.29) for 1 to 9, 10 to 19, and ≥20 cigarettes per day respectively, compared with nonsmoking. This association appeared to be independent of a wide range of possible confounders such as maternal age, education, social class, marital status and mental health, gestation at FCV, complications during pregnancy, the child's sex, gestational age at birth, and age at last follow-up. Adjustments were also made for the mother's employment since birth, family structure, and maternal mental health at the time of the CBCL assessment. Associations between externalizing behavior problems and maternal smoking at other times, and those between other behavioral problems examined and maternal smoking were not significant.

Conclusion. Although previous studies have found evidence for an association between maternal smoking and child behavior problems, the strength of this study lies in its size, its detailed and consistent measurement of maternal smoking, and its ability to control for many social and biological factors linked to maternal smoking and child behavior.

The statistical evidence for a causal relationship between maternal smoking as measured at the first antenatal clinic visit and the development of externalizing behavior in children is strongly suggestive, because of the specificity of effect and timing, and the adjustment for a comprehensive range of other risk factors. An alternative explanation that mothers who smoke might be inclined to report behavior problems differently was considered unlikely because the effect was specific to externalizing behavior and the major exposure occurred 5 years before the reported behavior. Additionally, the existence of a factor (beyond those already included in the analysis) that might be related to both behavior problems and any propensity to misreport smoking seems sufficiently implausible to rule out misclassification of smoking status as another alternative explanation for the findings.

The timing of the relationship between smoking in pregnancy and externalizing behavior problems, and its independence of small for gestational age status at birth, suggests that placental insufficiency and oxygen deprivation are not important in the pathogenesis. It is possible that nicotine in the fetal brain derived from maternal smoking may alter gene expression and the nature and function of the nicotine receptors developing in early pregnancy. The presence of a separate, although slightly weaker, association between concurrent maternal smoking and externalizing child behavior suggests both biological and social explanations, including a direct psychopharmocologic effect of nicotine through passive smoking.

Assuming the relationship to be causal, it is estimated that maternal smoking in early pregnancy may account for 25% of externalizing (aggressive) behavior while maternal smoking when the child is 5 years old may account for an additional 16%. These findings provide further support for antismoking programs in pregnancy and in young family settings.

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