Maternal smoking during pregnancy has been consistently associated with aggressive behaviors among offspring across the life course. We posit that anger, as a precedent of aggression, may have mediated the association. The current study examines the relation between maternal smoking during pregnancy and anger proneness among the adult offspring. Participants were 611 adult offspring (ages 38–48 years) of mothers enrolled in the Collaborative Perinatal Project between 1959 and 1966 in Boston and Providence. Information on maternal smoking during pregnancy was collected during prenatal visits. Spielberger’s trait anger scale was used to measure anger proneness which has two components: anger temperament and angry reaction. Results from the full sample analyses showed that offspring whose mother smoked one pack or more per day on average scored 1.7 higher in anger temperament T scores in comparison to offspring whose mother never smoked during pregnancy (β = 1.7, 95% Confidence Interval (CI): 0.1, 3.2). The fixed effects analyses among siblings that accounted for more confounding found a greater effect of around one standard deviation increase in anger temperament T scores corresponding to maternal smoking of one pack or more (β = 7.4, 95% CI: 0.5, 14.4). We did not observe an association of maternal smoking during pregnancy with offspring angry reaction or other negative emotions including anxiety and depression. We concluded that prenatal exposure to heavy cigarette smoke was associated with an increased level of anger temperament, a stable personality trait that may carry the influence of prenatal smoking through the life course.
Maternal smoking during pregnancy has been consistently linked to a range of mild to severe aggressive behaviors among offspring across the life course (Brennan et al., 1999, Ernst et al., 2001, Fergusson et al., 1998, Rasanen et al., 1999, Tremblay et al., 2004, Wakschlag et al., 1997 and Wakschlag et al., 2002). It has been proposed that exposure to cigarette smoke toxins during the prenatal period may cause deficits in the developmental fetal brain that subsequently lead to disruptive behaviors (Ernst et al., 2001 and Slotkin, 2004) although the precise pathway remains unclear.
Cigarette smoke contains many known toxicants, some of which, such as nicotine and carbon monoxide, have been suggested as the key neurobehavioral teratogens (Richardson and Tizabi, 1994 and Singh, 1986). They could pass the placenta to influence the normal development of the fetal brain through (1) teratologic effects on the developing fetal nervous system, and (2) hypoxic effects on the fetal–placental unit that reduce the fetal blood circulation (DiFranza et al., 2004 and Wakschlag et al., 2002). Reduced thickness of the orbital prefrontal cortex had been found among adolescents exposed to maternal smoking during the prenatal period (Toro et al., 2008). Patients with lesions in the orbital prefrontal cortex and adjacent regions showed explosive bursts of anger, impulsive aggression and violent behaviors (Anderson et al., 1999 and Blair and Cipolotti, 2000). In addition, evidence for the impact of exposure to cigarette smoke during the prenatal period on neural substrates of disruptive behaviors had also been provided in functional MRI neuroimaging (Bennett et al., 2009), genotype (Wakschlag et al., 2010) and phenotype (Wakschlag et al., 2011) studies.
Temperament as a stable personality trait has long been suggested as having a neurobiological basis (Whittle et al., 2006) For instance, the orbital prefrontal cortex region had been proposed as a key region associated with a fundamental dimension of temperament – restraint (Whittle et al., 2006). In normal individuals, activation of certain brain regions including the orbital prefrontal cortex that occur during anger arousal constrains the impulsive expression of emotion and the presence of aggressive behaviors (Davidson et al., 2000).
Previous studies had shown that infants and school aged children who were exposed to maternal smoking during the prenatal period were more likely to have difficult temperament, for example low positive/high negative mood, in comparison to their unexposed counterparts (Martin et al., 2006 and Pickett et al., 2008). Temperament reflects prepositions to behavior patterns as it underlies and drives behavioral manifestations (Dadds and Salmon, 2003). Among a diverse set of temperamental traits, we consider that anger temperament might be particularly relevant to impulsive aggressive behaviors. Anger as a negative effect has been identified as a fundamental cause or pre-condition for impulsive aggression. It reduces inhibitions against and sometimes justifies and energizes aggressive behaviors towards others (Anderson and Bushman, 2002).
Spielberger’s trait anger scale (Spielberger, 1999) that had been widely used to measure anger proneness consists of two components. (1) Anger temperament that refers to a person’s propensity to outbursts of anger with minimum provocation; and (2) angry reaction that denotes the tendency to become angry when treated unfairly by others. In the current study, we examine the relation between maternal smoking during pregnancy and anger temperament, angry reaction as well as trait anger among the adult offspring. We posit that the frequently noted link between maternal smoking during pregnancy and subsequent aggressive behaviors may be mediated through offspring anger temperament. In addition, because a high level of anger temperament may co-occur with other negative effect such as anxiety and depression, we further assess their relation with maternal smoking during pregnancy to test the specificity of the study finding.
