Intrauterine exposure to tobacco and executive functioning in high school

Highlights

• High School teachers masked to study objectives rated executive functioning (EF).

• Intrauterine tobacco exposure associated with less optimal behavioral regulation.

• <0.5 pack tobacco exposure resulted in 2–3 times greater odds executive dysfunction.

• Neither other intrauterine nor environmental exposures predicted less optimal EF.

• Prenatal counseling should emphasize all legal and illegal substance abstinence.

Abstract

Background

Executive functioning (EF), an umbrella construct encompassing gradual maturation of cognitive organization/management processes, is important to success in multiple settings including high school. Intrauterine tobacco exposure (IUTE) correlates with negative cognitive/behavioral outcomes, but little is known about its association with adolescent EF and information from real-life contexts is sparse. We evaluated the impact of IUTE on teacher-reported observations of EF in urban high school students controlling for covariates including other intrauterine and adolescent substance exposures.

Methods

A prospective low-income birth cohort (51% male; 89% African American/Caribbean) was followed through late adolescence (16–18 years old). At birth, intrauterine exposures to cocaine and other substances (52% cocaine, 52% tobacco, 26% marijuana, 26% alcohol) were identified by meconium and/or urine assays, and/or maternal self-report. High school teachers knowledgeable about the student and unaware of study aims were asked to complete the Behavior Rating Inventory of Executive Functioning-Teacher Form (BRIEF-TF) annually.

Results

Teachers completed at least one BRIEF-TF for 131 adolescents. Multivariable analyses included controls for: demographics; intrauterine cocaine, marijuana, and alcohol exposures; early childhood exposures to lead; and violence exposure from school-age to adolescence. IUTE was associated with less optimal BRIEF-TF Behavioral Regulation scores (p <0.05). Other intrauterine substance exposures did not predict less optimal BRIEF-TF scores, nor did exposures to violence, lead, nor adolescents’ own substance use.

Conclusions

IUTE is associated with offspring’s less optimal EF. Prenatal counseling should emphasize abstinence from tobacco, as well as alcohol and illegal substances.

Introduction

Approximately 12% of pregnant U.S. women in 2008 reported smoking tobacco during the third trimester, despite increased long-term health risks for themselves and offspring (Tong et al., 2013). Executive functioning (EF) encompasses a set of higher-level neurocognitive functions (e.g., working memory, inhibitory control, organization, and planning) necessary for independent, purposeful, goal-directed day-to-day activity. Intrauterine tobacco exposure (IUTE) has been associated with less optimal performance on measures of children’s neurocognitive abilities (Fried et al., 2003) including working memory (Fried and Watkinson, 2001), attention, emotion and behavioral regulation (Cornelius et al., 2012, Wiebe et al., 2014) and aggression/other anti-social behaviors in older children and adolescents (Huizink and Mulder, 2006, Wakschlag et al., 2011). Few studies specifically examine IUTE effects on executive functioning (EF) during adolescence (Clifford et al., 2012). EF encompasses a set of higher-level neurocognitive functions (e.g., working memory, inhibitory control, organization, and planning) necessary for independent, purposeful, goal-directed day-to-day activity including helping to manage competing performance demands (Alvarez and Emory, 2006, Lezak et al., 2012).

Prior studies evaluating IUTE effects on neurobehavioral outcomes usually focus on individualized, laboratory-based assessments rather than measures of functioning in real-life contexts where environmental stimuli may influence individuals’ behavior (Chaytor et al., 2006, Clifford et al., 2012). Context is known to be an important factor influencing EF (Williams et al., 2009). For example, success in high school requires constant adaptation to variable, unpredictable conditions, but it is not known whether adolescents with versus without IUTE show observable EF differences in this “real world”, rather than a controlled laboratory environment (Diamantopoulou et al., 2007).

Regardless of setting, studies of specific effects of any single intrauterine substance exposure also must evaluate potential environmental, demographic and biologic covariates, particularly other intrauterine substance exposures and adolescents’ own substance use (Fried et al., 2003, Richardson et al., 2013, Rose-Jacobs et al., 2011). As evident in substance-exposure literature, outcomes may be influenced by specific samples, ages tested, assessments used, and covariates included (Clifford et al., 2012, Piper and Corbett, 2012). Potential covariates based on published literature should be evaluated to avoid misinterpretation of results. For example, in low-income, urban populations, environmental exposure to second-hand tobacco smoke (Cornelius and Day, 2009), lead (Min et al., 2009), and violence (Frank et al., 2011, Perkins and Graham-Bermann, 2012) may influence EF.

The present study goal is to evaluate possible associations between IUTE and EF reported by participants’ high school teachers. We hypothesize that after controlling for contextual variables including demographics, childhood blood lead levels, childhood and adolescent exposure to violence, other intrauterine substance exposures, and the adolescent’s own substance use, IUTE will be negatively associated with high school teachers’ ratings of students’ classroom EF.