Developmental trajectories of externalizing behavior from ages 4 to 12: Prenatal cocaine exposure and adolescent correlates
Introduction
Externalizing behavior refers to overt behavior problems that are characterized by impulsivity and lack of self-regulation (Tucker et al., 2015). It typically involves conflicts with other people (Achenbach and Rescorla, 2001), such as aggression, rule-breaking, and disruptive behavior. Externalizing behavior in childhood is associated with school failure, peer problems, and juvenile delinquency; it is also a well-established precursor to substance use (King et al., 2004; Iacono et al., 2008) and sexual risk behaviors (Min et al., 2015, 2016). These problems have life-long implications in terms of interfering with vocational and educational opportunities and attainment, and developing stable, supportive relationships, all pivotal for successful adjustment in adulthood.
Prenatal cocaine exposure (PCE) may increase the risk of externalizing behavioral problems (Bada et al., 2007; Minnes et al., 2010; Ackerman et al., 2010; Min et al., 2017a). PCE directly impedes fetal brain development by altering the monoamine neurotransmitter system involving dopamine, serotonin, and norepinephrine in the prefrontal cortex, a brain region known to impact emotional and behavioral arousal and regulation (Kosofsky et al., 1994; McCarthy et al., 2014). PCE may also alter brain function indirectly via its vasoconstrictive properties that limit oxygen and nutrition to the developing fetal brain (Volpe, 1992). These structural and functional alterations in the brain may underlie cognitive deficits including problems with executive function, attention, inhibitory control, and stress response in PCE children (Minnes et al., 2016; Singer et al., 2008; Thompson et al., 2009), contributing to the development of externalizing behavior problems.
Studies from longitudinal prospective birth cohorts reported conflicting evidence of PCE effects on externalizing behavior problems during the preschool years (Dixon et al., 2008; Frank et al., 2001), yet consistent findings have been observed at early school age and during preadolescence, despite methodological variability (Ackerman et al., 2010; Bada et al., 2007; Minnes et al., 2010). For example, PCE was related to child-reported symptoms of oppositional defiant disorder and attention-deficit/hyperactivity disorder at 6 years of age (Linares et al., 2005), caregiver-reported aggressive and delinquent behavior at 9 years (McLaughlin et al., 2011), teacher- and caregiver-rated externalizing behavior problems at 7, 9 and 11 years (Bada et al., 2011), and child-reported externalizing behavior at age 12 (Min et al., 2014). However, the effect sizes were generally small at 0.20 SD on average (Ackerman et al., 2010).
Although these studies demonstrated that PCE accounts for individual variation in externalizing behavior problems, many of them used cross-sectional analyses, precluding any determination of how PCE effects may vary by developmental stages. When studies did employ longitudinal analyses (e.g., Bada et al., 2011; Minnes et al., 2010), they were based on the assumption that all children with PCE would follow a common developmental trajectory of either increase or decline, estimating a single trajectory that averages the individual trajectories of all participants in a given sample. However, given that the majority of children in these studies do not have externalizing behavior problems (Bongers et al., 2004; Vaughn et al., 2014), there may not be a common developmental course for externalizing behavior. Differing developmental patterns may partially explain the previously reported small effect size of PCE on externalizing behavior, calling for an alternative strategy to investigate potential heterogeneity of subgroups with distinctive trajectories. Little is known about whether and how PCE may contribute to different childhood developmental trajectories of externalizing behavioral problems, which may persist, desist, or escalate over time.
A widely used developmental taxonomy of externalizing behavior is Moffitt’s (1993) model of antisocial behavior proposing two mutually exclusive subgroups of antisocial individuals: the early-onset life-course-persistent antisocial individuals, representing approximately 5% of the population, whose antisocial/externalizing behavior problems start early in childhood and continue to be high throughout development including adulthood, and the late-onset adolescence-limited antisocial individuals, who engage in antisocial behaviors only during the teen years. Moffitt posits that the early and persistent antisocial behavior is likely related to a biological or genetic vulnerability that is exacerbated by poor parenting and early school failure, while adolescence-limited antisocial behavior tends to stem from later socialization experiences such as deviant peer affiliations in early adolescence.
In studies of children without PCE that empirically classified trajectory groups, heterogeneity in externalizing trajectories was demonstrated, consistently identifying two groups: a high persistent and chronic group, resembling Moffitt’s life-course-persistent trajectory for some children, and a larger, low stable, normative group. Other additional trajectories were also empirically identified, although with less consensus, such as a moderate to decreasing group or an increasing/escalating group, especially in a sample of maltreated children. For example, the National Institute of Child Health and Human Development (NICHD) Study of Early Child Care reported five distinctive groups of externalizing trajectories from ages 2 to 12, with high chronic (8.4% of the sample), low (27%), moderate (19.4%), and two (high and moderate) decreasing groups (45%), but not an increasing/escalating group (Fanti and Henrich, 2010). Similarly, the Shaw et al. (2003) study on boys’ conduct problems from ages 2–8, recruited from low-income families using the Women, Infants, and Children (WIC) Program, also identified multiple trajectories: high chronic (6%); low (14%); and two (high and moderate) decreasing (80%) groups. However, studies of maltreated children from ages 4–10 years utilizing data from the Longitudinal Study of Child Abuse and Neglect (LONGSCAN) or the National Survey of Child and Adolescent Well-Being (NSCAW), a nationally representative longitudinal study of children and families involved with the Child Protective Services (CPS), identified an increasing/escalating subgroup (8% in LONGSCAN; 7.8% in NSCAW) in addition to the high chronic (10.8%; 4.4%), low stable (56.9%; 32.6%), and decreasing (24.3%; 12.5%) groups (Woodruff and Lee, 2011; Tabone et al., 2011). Although differences in the nature of the samples, operationalization of problem behaviors, and the length of the follow-up period may yield variability in the number and shape of different trajectories and in the proportions of children following different trajectories, these studies collectively demonstrate that there are empirically identifiable subgroups of youth with distinct developmental trajectories of externalizing behavior.
The current study aimed, first, to identify developmental trajectories of externalizing behavioral problems from early childhood (ages 4–12) in children with PCE by utilizing a person-oriented analytic approach, which uncovers empirically distinct subgroups of individuals following a similar pattern of change over time on externalizing behavior (Nagin, 2015). Different trajectories may reflect distinctive etiologies (Nagin, 2005). The person-centered approach allows the detection of small, yet meaningful subgroups of the larger sample that do not fit the shape of the average trajectory generated by variable-centered approaches that have been traditionally used; what might be considered error variance at the group level in typical variable-oriented analyses are critically examined for understanding diversity in process and outcome (Cicchetti, 2013). Thus, person-oriented analyses are especially useful for identifying a subgroup representing highly skewed outcomes such as externalizing behaviors (NICHD Early Child Care Research Network, 2004).
Second, we examined whether PCE predicts developmental trajectories that are problematic, controlling for multiple biological and environmental confounders that may obscure the long-term effects of PCE. Prenatal exposure to other substances such as alcohol (Larkby et al., 2011), tobacco (Maughan et al., 2004), and marijuana (Goldschmidt et al., 2000), maternal/caregiver’s continuous, postpartum substance use (Bada et al., 2007), poor quality of the home environment (Min et al., 2014), and adoptive/foster care placement (Linares et al., 2005) have been reported to be related to childhood externalizing behavior problems in children with PCE. In particular, maternal cocaine use has been consistently associated with higher levels of maternal psychological distress symptoms (e.g., Min et al., 2013; Minnes et al., 2010; Singer et al., 1997). Given the well-established causal role of caregiving quality shaping children’s adjustment, especially in the early formative years of life, both independently (Jaffee, 2007; Olson et al., 2017; Shaw et al., 2003; Fanti and Henrich, 2010; Tabone et al., 2011) and interactively with biological risk factors (Brennan et al., 2003: Moffitt, 1993; Min et al., 2017b; Molnar et al., 2014), we explored the interaction between PCE and maternal psychological distress. The diathesis-stress model (Zahn-Waxler et al., 2008) suggests that those with a biological vulnerability are disproportionately likely to be adversely affected by an environmental stressor. The effects of PCE may be greater when a mother could not provide optimal care due to her high psychological distress. Thus, the joint influences of PCE and high maternal psychological distress would be associated with the most problematic developmental trajectory.
Lastly, to evaluate the clinical significance and validity of these trajectory groups, each trajectory was compared on adolescent substance use and early sexual risk behavior, controlling for potential covariates of the outcomes such as parental attachment and monitoring, family conflict, violence exposure, childhood maltreatment, and sexual victimization (Wills et al., 2003; Dittus et al., 2015; Voisin et al., 2011; Min et al., 2007, 2016). Interaction between trajectory group and gender was explored due to well-known gender differences in patterns of drug use (Becker et al., 2016) and sexual behavior (Dir et al., 2014; Zimmer-Gembeck and Helfand, 2008; Min et al., 2015). It was hypothesized that: (1) heterogeneous externalizing trajectories exist in children with PCE and can be identified as distinct subgroups; (2) PCE and maternal psychological distress would predict, independently and interactively, membership in groups with children exhibiting more problematic externalizing behavior trajectories; and (3) more problematic externalizing behavior trajectories (e.g., high chronic) in childhood would be related to subsequent adolescent substance use and early sexual behavior.
Section snippets
Sample and procedure
This study included 386 (197 PCE, 189 NCE) children and their mothers or caregivers recruited at infant birth (September 1994 to June 1996) from an urban county hospital for a longitudinal investigation of the effects of PCE. All recruited mothers were identified from a high-risk population screened for drug use. Urine drug toxicology screens were performed by the hospital on women who received no prenatal care, appeared intoxicated or taking drugs, had a history of involvement with the
Sample characteristics
Compared to NCE children, children with PCE had a shorter gestational age and lower birth weight, length, and head circumference (Table 1). They were prenatally exposed to more tobacco, alcohol and marijuana on average, more likely to be placed in non-kinship foster or adoptive care by age 4, and tended to have lower IQ at age 4. Birth mothers of children with PCE were older, less educated, primarily unmarried, had lower vocabulary scores and reported more psychological distress than birth
Discussion
The current study identified four distinctive developmental trajectories of externalizing behavior from ages 4 to 12 in a sample of children at risk for externalizing problems due to exposure to cocaine and other substances. About 36% of the children exhibited problematic (accelerated risk and elevated-chronic) trajectories. PCE and maternal psychological distress conjointly differentiated developmental trajectories of externalizing behavior. The accelerated risk group (G3) was composed of
Role of the funding sources
This research was supported by the National Institute on Drug Abuse (NIDA)R01-07957 and R01-042747. This publication was also made possible by the Clinical and Translational Science Collaborative of Cleveland, UL1TR000439 from the National Center for Advancing Translational Sciences (NCATS) component of the National Institutes of Health (NIH) and NIH roadmap for Medical Research. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the
Contributors
Dr. Meeyoung O. Min conceptualized the paper, performed the statistical analyses, and wrote the initial and final draft. Dr. Sonia Minnes designed the study and interpreted the data. Dr. Hyungyong Park analyzed the data and summarized the findings. Dr. Ty Ridenour participated in the interpretation of the findings. Ms. June-Yung Kim assisted in the literature review, and drafting the manuscript. Ms. Miyoung Yoon assisted in the literature review and drafting the manuscript. Dr. Lynn T. Singer
Conflict of interest
No conflict of interest declared.
Acknowledgements
The authors would like to thank all of our families who participated in our research for 15 years. We would also like to thank Adelaide Lang, PhD for reviewing early drafts, and Laurie Ellison, LISW, and Paul Weishampel, MA for research assistance. Portions of this work were previously presented at the 41 st Annual Meeting of the Developmental Neurotoxicology Society (DNTS), Denver, Colorado, June 2017.
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2021, Neurotoxicology and TeratologyCitation Excerpt :EF dysfunction may impact school readiness and achievements, language development, and behaviors leading to increases in violence and initiation of alcohol use and binge drinking (Cruz et al., 2020; McClelland et al., 2013; Morgan et al., 2019; Nayfeld et al., 2013; Peeters et al., 2015; White et al., 2017). EF deficits are also associated with externalizing problems (Schoemaker et al., 2013), an outcome that youth with prenatal cocaine exposure (PCE) may be at increased risk of exhibiting (Bennett et al., 2013; Min et al., 2018). According to data from the 2018 National Survey of Drug Use and Health (Center for Behavioral Health Statistics and Quality, 2019), past month use of illicit drugs by pregnant women was 5.4%, while cocaine use in lifetime among females aged 12 or older was 11.5%, suggesting that the potential for PCE remains high today.