Effect of antenatal exposure to maternal smoking on behavioural problems and academic achievement in childhood: prospective evidence from a Dutch birth cohort

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Abstract

Aim: To examine effects of maternal smoking during pregnancy on academic achievement and emotional and behavioural problems during childhood. Methods: Least squares regression was used to examine associations between maternal smoking prior to delivery and subsequent academic performance and behaviour of 1186 children aged 5.5–11 years. Crude associations were adjusted for risk factors that were significantly related to the respective outcomes. Main outcome measures: Parents and teachers were asked to indicate, on a 10-item questionnaire, whether they regarded the child as more, the same, or less shy/withdrawn (internalising), troublesome (externalising), and attention deficient than the average child. Reading, spelling, and arithmetic performance levels were assessed with short standardised Dutch tests. Results: After adjustment for confounders like socio-economic status and pre- and perinatal complications, children of mothers who smoked during pregnancy showed more signs of attention deficit and displayed higher levels of troublesome (externalising) behaviour than non-cigarette-exposed children. Also, children of smoking mothers performed worse on arithmetic and spelling tasks. Spelling problems were more pronounced when the mother continued to smoke after the child's birth. Excessively withdrawn (internalising) behaviour was not related to maternal smoking but to factors like the mother's use of psychotropic drugs and bottle—instead of breastfeeding. Conclusion: Perinatal antecedents of internalising behaviour on the one hand and externalising behaviour, attention deficit, and learning problems on the other seem to be distinct. Only the latter are independently associated with maternal smoking during pregnancy and thus potentially amenable to early preventive effort, for instance, through continued health education emphasising the health hazards of nicotine use by pregnant women.

Introduction

Smoking during pregnancy has decreased significantly in recent decades, but an estimated 13–34% of pregnant women still smoke daily [1], [2], [3]. Most of these women are young, unmarried, and from low socio-economic strata [1]. Smoking during pregnancy affects the foetus possibly because of direct toxic effects. Nicotine passes rapidly and completely across the placental barrier, with foetal concentrations generally being 15% above maternal levels [4]. Besides nicotine, tobacco contains many other toxic substances.

The adverse effects of maternal smoking on pregnancy outcome were first described by Simpson and Linda [5]. Harmful effects reported since include not only perinatal complications like preterm delivery and low birth weight [6], [7], [8], [9] but also more specific physical abnormalities in the newborn like hypertension [6], [10], oral clefts [11], and abnormal lung function [12], [13], [14]. Nicotine has also been found to affect brain development. Animal studies have demonstrated decreased cerebral blood flow and decreased total brain weight in foetuses exposed to nicotine [4]. These findings may be related to the smaller head circumferences in children of smoking mothers [15].

Prenatal exposure to nicotine may cause neurodevelopmental and neurobehavioural problems [4], [16]. Delayed intellectual development [4], [17], [18], [19] and impulsive behaviour [20], [21], [22], [23], [24], [25], [26] have been reported in toddlers and older children who were prenatally exposed to nicotine. As regards nicotine's effects on children's behaviour, the literature suggests that maternal smoking during pregnancy is linked with conduct and behavioural (externalising) more than with emotional (internalising) disorders, whilst harmful effects on boys may be more pronounced than on girls [26], [27], [28].

Whilst the link of maternal smoking with adverse pregnancy and developmental outcomes may be attributable entirely to foetal exposure to nicotine or other toxic substances in tobacco in utero, various other possibilities have not been satisfactorily excluded. Thus, it remains unclear to what extent effects of maternal smoking are distinct from those of low social class or suboptimal prenatal and perinatal conditions on development [29]. Moreover, little is known of whether, and if so, how, paternal smoking affects risk of cognitive and behavioural problems in children [18].

The purpose of this study is, first, to test the hypothesis that the link between maternal smoking and impaired cognitive and behavioural development in offspring cannot be accounted for entirely by effects of important confounders like social class, associated perinatal adversities, and paternal smoking. Secondly, we examine if links between maternal smoking and learning and behaviour problems are stronger in boys than girls. Finally, we test the hypothesis that effects are stronger in older than in younger children. This because it is well known that during preadolescence the prevalence of minor neurological dysfunction, and behavioural and cognitive disorders rises with increasing age [30].

Section snippets

Sample

In the Groningen Perinatal Project (GPP), detailed social, prenatal, perinatal, and neonatal data were collected for all consecutive live singleton births (n=3162) from 1975 to 1978 inclusive at the University Hospital Groningen. Subsamples of this birth cohort were re-examined when aged between 5.5 and 11 years (mean 7.45, S.D. 1.69, median 8). Children with cerebral palsy were excluded from the present analysis. The subsamples consisted of:

  • all children with a definitely abnormal neonatal

Construction of behavioural endpoints: internalisation, externalisation and attention deficit

Three principal components accounted for the bulk of the variance of scores on the behavioural items (Table 1). The first represented signs of attention deficit. Since parents' and teachers' assessments loaded on the same factor, overall attention deficit scores were obtained by summing the items.

The second and third principal component represented externalisation and internalisation, respectively, and could be identified in teachers' as well as parents' ratings.

Externalising and internalising

Strengths and limitations of the study

The existence of a link between maternal smoking during pregnancy and cognitive and behavioural difficulties in children is well documented [16], [17], [18], [20], [21], [22], [23], [24], [25], [26], [27], [28], [38]. The strength of our study lies in its prospective character and its ability to control for many psychosocial factors linked to maternal smoking and child behaviour. Some methodological issues warrant discussion however.

First, despite the adjustment for many confounders, it is

Conclusion

This study's findings add to the growing evidence suggesting causal links between maternal smoking and increased rates of externalising behaviour and school problems in offspring. In contrast, internalising problems were not related to smoking behaviour of the mother. Internalising and externalising behavioural styles can be recognised as early as in the third year of life and are known to predict depression and antisocial behaviour, respectively, later on [48]. Our study suggests that these

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