Is prenatal tobacco exposure a risk factor for early adolescent smoking? A follow-up study

Abstract

Recent reports indicate a relation between prenatal tobacco exposure (PTE) and offspring smoking. Many of these reports have been retrospective or have not included important variables such as other prenatal substance exposures, maternal and child psycho-social characteristics, mother's current smoking, and friends' smoking. No prior study has examined the timing of PTE.

In this prospective study of a birth cohort of 567 14-year-olds, we examined the relation between trimester-specific PTE, offspring smoking, and other correlates of adolescent smoking. Average age of the adolescents was 14.8 years (range: 13.9–16.6 years), 51% were female, 54% were African-American. Data on maternal tobacco and other substance use were collected both prenatally and postnatally, 51% of the mothers were prenatal smokers and 53% smoked when their children were 14 years.

PTE in the third trimester significantly predicted offspring smoking (ever/never, smoking level, age of onset) when demographic and other prenatal substances were included in the analyses. PTE remained a significant predictor of the level of adolescent smoking when maternal and child psychological characteristics were added to the model. When more proximal measures of the child's smoking were included in the model, including mother's current smoking and friends' smoking, PTE was no longer significant. Significant predictors of adolescent smoking at age 14 were female gender, Caucasian race, child externalizing behavior, maternal anxiety, and child depressive symptoms.

Although direct effects of PTE on offspring smoking behavior have previously been reported from this study and by others, by early-adolescence, this association is not significant after controlling for the more proximal covariates of adolescent smoking such as mother's current smoking and peer smoking.

Introduction

Prenatal tobacco exposure (PTE) has long been identified as a cause of problems in the neonate. In the last few decades, studies have reported adverse effects of PTE on older offspring, as well. The affected outcomes include externalizing behaviors [7], [13], [27], [31], [56], [79], attention problems, impulsivity, and hyperactivity [25], [32], [45], [47], [50], [51], [71], [72], conduct disorder [48], [76], [78], depression [24], [16], [36], [46], and delinquency [11], [61]. Many of these outcomes are also predictors and correlates of adolescent smoking and other substance use [9], [10], [12], [33], [52], [70], [74]. In addition, environmental factors including parental smoking [8], [67] predict smoking in the offspring. One of the most robust environmental predictors of adolescent smoking is peer smoking. Peer smoking, or perceived peer smoking, has a greater association with adolescent smoking than family influences [4], [5], [16], [28], [30], [35], [43], [57], [80]. The effects of peer use, however, may be most influential in the earlier stages of tobacco use [21].

Only a limited number of studies have considered the etiological role of PTE on predicting tobacco use among exposed offspring. In a retrospective study, Kandel et al. [40] reported a four-fold increased risk of tobacco use among adolescent girls prenatally exposed to tobacco. They hypothesized that tobacco had a biological effect on the dopaminergic neurons in the developing brain. In a later report from this same group, Griesler et al. [34] showed that maternal smoking during pregnancy was significantly associated with higher levels of child behavior problems and that these behavior problems mediated the effects of PTE on smoking among the daughters. Buka et al. [14] also found that young adults with PTE had significantly higher rates of lifetime tobacco dependence using DSM-IV criteria, although they did not control for prenatal alcohol exposure or environmental tobacco exposure. Lieb et al. [47] reported that offspring of nicotine-dependent women had a higher rate of nicotine dependence, and this relation was greater if the mother also smoked during the offspring's gestation. These data were retrospective and information was not available on other prenatal substance exposures. Oncken et al. [55] reported that in utero tobacco exposure accelerated the progression from experimentation to daily use among girls and led to earlier experimentation among boys. Data for PTE were collected retrospectively from the offspring who were in treatment for smoking cessation. Information was not collected on other prenatal substance exposures or postnatal passive smoking exposure. In the Maternal Health Practices and Child Development (MHPCD) cohort, we earlier reported that 10-year-old offspring who were exposed to 1 / 2 pack or more per day during gestation had a 5.5-fold increased risk of early tobacco experimentation. These analyses controlled for other prenatal substance exposures, mother's current smoking, and maternal and child psychological covariates [23].

Animal studies have shown links between PTE and offspring substance use. Several studies have identified changes that result from prenatal nicotine exposure that might affect the susceptibility to later tobacco use among the exposed offspring [66], [67]. In one study, an upregulation of nicotinic acetylcholine receptors was found among adult rats that had been exposed to nicotine in the immediate neonatal period [49], a time comparable to the third trimester in the human. These authors speculated that their findings have implications for humans. If offspring are exposed to nicotine early in their development, they may be at greater risk for nicotine addiction later in life. An earlier study demonstrated permanent changes in brain nicotinic receptors in mice exposed in the neonatal period [54]. The authors hypothesized that nicotine exposure during early brain growth and development could create a vulnerability for dependence on nicotine by changing the distribution of the nicotinic receptor subtypes in the brain.

The theoretical framework for the current study is the teratologic model. This model hypothesizes that if a toxin is a teratogen, it will have a direct biological effect on the fetus [75]. Additional factors influence the expression of biological effects on child development and behavior; dominant among these are the effects of the environment. This framework has been extended to consider environmental influences in the current study.

This report uses data from the Maternal Health Practices and Child Development Project (MHPCD), a consortium of projects that evaluate the long-term effects of prenatal substance exposure. The children in the study used for this analysis have been followed from the fourth month of gestation through the age of 14 years. The current report has two goals: 1) to explore the relations between PTE and offspring smoking, and if significant, 2) to consider whether this association is significant after controlling for other prenatal substance exposure and other risk factors that are associated with adolescent tobacco use. This study will extend current knowledge by prospectively examining trimester-specific PTE effects. In addition, we consider the effects of other prenatal substance exposures, maternal and child psychological factors related to smoking, and more proximal measures of the adolescent smoking behavior including mother's current tobacco use and peer tobacco use. Our hypothesis is that PTE will predict higher rates of smoking in early adolescence (ever/never), a higher level of smoking, and an earlier age of onset of smoking among the exposed 14-year-olds.