Is prenatal tobacco exposure a risk factor for early adolescent smoking? A follow-up study
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.
Section snippets
Procedures
The data for this report come from two samples recruited during the years 1982–1984. The women were randomly selected from an urban hospital-based prenatal clinic. All prenatal and delivery interviews were conducted in a private office setting at the Magee Womens Hospital, Pittsburgh. Informed consent was obtained from the mothers and the study protocol received approval from the Institutional Review Board of the University of Pittsburgh and Human Experimentation Committee of the Magee Womens
Adolescent smoking
Forty-seven percent (n = 268) of the 14-year-olds reported ever smoking; 21% reported any use in the past 30 days. Average daily use among current smokers was 2.5 cigarettes per day (range: 0.005–45). The average age of onset of cigarette use was 12 years (range: 5–15.7), and the two most popular brands of cigarettes were Newport (67%) and Marlboro (12%) cigarettes. Of the total group, 74% reported having friends who used tobacco, while 84% of those who were current smokers reported having
Discussion
Our analyses show that although PTE is a significant predictor of adolescent smoking at age 14, when intervening variables, such as current maternal tobacco use and peer use, are entered into the model, PTE is no longer a significant predictor. This finding is different from what we found when the children were 10 years old. In an earlier analysis, we found that PTE significantly predicted tobacco use after controlling for maternal use at 10 years, other prenatal substance use, maternal and
Acknowledgements
This research was supported by grants from the National Institute of Drug Abuse (PI: N. Day) and the National Institute on Alcoholism and Alcohol Abuse (PI: N. Day) and the National Institute on Child Health and Development (PI: N. Day; Co-PI: M. Cornelius). Dr. Cornelius presented some of these findings at the Society for Nicotine and Tobacco Research, February, 2003, New Orleans.
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