Examining the concurrent and longitudinal relationship between diurnal cortisol rhythms and conduct problems during childhood
Introduction
Externalizing behaviors, such as attention problems, rule breaking, and aggressive behavior, during early childhood are associated with a host of negative outcomes. Conduct disorder, specifically, is one of the more severe externalizing disorders, associated with such problems as substance abuse, theft, lower educational attainment, and poor physical health that significantly impair the functioning of affected individuals and their families, and have high costs for society at large (McMahon, 1994; Moffitt, 1993; Kim-Cohen et al., 2014, Rolon-Arroyo et al., 2014). The majority of studies have reported that hypoactivity of the hypothalamus-pituitary-adrenal (HPA) axis, characterized by blunted diurnal rhythms of cortisol, is associated with conduct problems and externalizing behaviors in school-aged children and adolescents (e.g., Alink et al., 2008, Bernard et al., 2015a, Bernard et al., 2015b, Bernard et al., 2015c; Martin et al., 2014). However, some studies have reported contradictory results, suggesting that externalizing behavior may have no relationship to HPA axis activity, or that problem behavior may be positively associated with levels of cortisol in young children (Alink et al., 2008, Fairchild et al., 2008; Klimes-Dougan et al., 2001; Van Bokhoven et al., 2005). Using a longitudinal design, the current study seeks to examine both the concurrent and longitudinal association between childhood externalizing behaviors, particularly those related to conduct problems, and HPA axis functioning.
The HPA axis regulates a host of biological processes including the body’s response to stress and maintenance of the circadian rhythm. As an end product of the HPA axis, cortisol provides an informative measure of HPA axis functioning. Not only is cortisol released in direct response to acute stressors, but secretion follows a regular diurnal rhythm (i.e., highest soon after awakening, and lowest at the end of the day; Van Cauter, 1990). The diurnal rhythm is evident by three months of life (Price et al., 1983), but continues to become more pronounced and more similar to an adult-like rhythm between the ages of 5 and 8 months (de Weerth et al., 1999). Healthy HPA axis functioning promotes protective and adaptive outcomes such as the replenishment and management of energy or metabolism, retention of memories, and maintenance of the immune system (McEwen and Seeman, 1999). In contrast with the typical steep decline in cortisol from morning to evening, some individuals show a flattened or blunted pattern of cortisol across the day, characterized by morning levels that are atypically low and evening levels that are atypically high (Gunnar and Vazquez, 2001).
Much of the research on school-aged children and adolescents suggests that low levels of cortisol at various times during the day are significantly associated with conduct disorder (Kariyawasam et al., 2002; Oosterlaan et al., 2005, Pajer et al., 2001, Pajer et al., 2006, Vanyukov et al., 1993). Further, both blunted (or smaller) cortisol awakening responses (CAR, the difference between cortisol at waking to 30 min post-waking) and blunted change across the day are associated with delinquency and/or a diagnosis of conduct disorder (Popma et al., 2007). Hawes et al. (2009) found that children with higher levels of callous-unemotional traits, an important feature and potential subtype of conduct disorder (Frick et al., 2014), were more likely to have blunted cortisol and severe antisocial behavior than children with lower levels of callous-unemotional traits.
Although there is a wealth of evidence suggesting that hypocortisolism is related to problem behavior in school-aged children, a number of studies have found no association, or that this relationship may be reversed in younger children (Alink et al., 2008, Fairchild et al., 2008, Klimes-Dougan et al., 2001; Van Bokhoven et al., 2005). This literature suggests that HPA axis activity and its relation to externalizing behavior may change over time in young children age. In fact, a meta-analysis by Alink et al. (2008) found that the relationship between basal cortisol and general externalizing behavior in children was moderated by age; externalizing behavior was associated with higher cortisol levels in preschool-aged children, and with lower cortisol levels in elementary school-aged children.
Previous work on the assessment of cortisol and externalizing behavior in children has typically used cross-sectional rather than longitudinal data. Given the mixed findings in younger children, it is unclear whether externalizing problems are associated with lower levels of cortisol across development, or whether externalizing behavior is associated with hypercortisolism in early childhood, but hypocortisolism in older childhood and adolescence. Further, it is unknown whether cortisol levels predict changes in behavior problems, behavior problems predict changes in cortisol levels, or both influence each other over time. As discussed in Saridjan et al. (2014), the longitudinal examination of diurnal cortisol rhythm and problem behavior is necessary in order to disentangle the direction of these effects.
Although the number of studies is limited, extant longitudinal work on this topic has been informative. In a population-based sample, Saridjan et al. (2014) found that high diurnal HPA axis activity in infancy was predictive of later internalizing problems in preschool. However, these researchers did not find any relationship between HPA axis activity in infancy and externalizing behavior in preschool-aged children. In another longitudinal study, Shoal et al. (2003) found that low resting cortisol in 10- to 12-year-olds predicted elevated physical and verbal aggression at 15–17 years of age, with this pathway mediated by low self-control. Similarly, McBurnett et al. (2000) found that lower cortisol at age 10 and age 12 were associated with aggressive behavior at age 12. However, neither McBurnett et al. (2000) nor Shoal et al. (2003) measured the diurnal rhythm of cortisol; rather, each used only one or two samples in all analyses. More importantly, neither study controlled for pre-existing aggressive behavior at the first assessment period. Without measuring pre-existing aggression, it is impossible to determine whether cortisol predicts change in behavior problems, and only correlational inferences are warranted.
Finally, Ruttle et al. (2011) examined whether there was a change in the relationship between externalizing behavior and HPA axis functioning over time in a sample of 96 children. Children were assessed first at 6.3–10.8 (M = 7.7) years of age, and then again at 9.3–13.5 (M = 10.87) years. Both concurrent and longitudinal analyses suggested that externalizing behavior was related to a blunted diurnal cortisol. However, their results suggested that the longitudinal relationship between early externalizing disorders and later blunted cortisol was slightly stronger than the concurrent relationship during childhood. This work, combined with the inconsistent literature on problem behavior and HPA axis functioning in younger children, suggests that the HPA axis may develop and change over time. Using a longitudinal design, the current study seeks to examine both the concurrent and longitudinal association between HPA axis functioning and childhood externalizing behaviors, particularly those related to conduct problems.
The current study aimed to investigate both the concurrent and longitudinal association between childhood externalizing behaviors, particularly those related to conduct problems and aggression, and HPA axis functioning. In order to understand this relationship in normally developing children, the current sample is community-based and consists of both boys and girls at two time points (age 6 and age 9). Externalizing behaviors were measured at both ages using the Child Behavior Checklist (CBCL; Achenbach and Rescorla, 2001), and saliva samples were collected in the morning and evening at both time points to assess the diurnal rhythm of cortisol. Based on previous literature, we predicted that we would find a different relationship when externalizing disorders and HPA axis functioning are analyzed concurrently, than when analyzed longitudinally; concurrent analyses at age 6 may reveal a weaker, or even positive, relationship between externalizing behaviors and cortisol slope. However, when analyzed longitudinally, we hypothesized that a more blunted rhythm of cortisol from the morning to the evening, or a less pronounced decline, would predict increases in externalizing behavior over time. Further, given the longitudinal nature of our data, we were also able to investigate directionality of this relationship (i.e., does HPA axis functioning predict externalizing behavior, or does externalizing behavior predict HPA axis functioning?) Given that most of the previous evidence on externalizing disorders and HPA axis functioning has focused on conduct problems and aggression, we predicted that the CBCL scales related to conduct problems and aggressive behaviors, rather than those related to attention problems, would drive the association between cortisol and externalizing behavior.
Section snippets
Study population
The original sample consisted of 815 families with a child between the ages of 3 and 4 and an English-speaking biological parent (see Olino et al., 2010 for details). Participants were identified through a commercial mailing list and screened by telephone. Exclusion criteria included the existence of a significant medical condition or a developmental disability in the child. Of the families deemed eligible, 66.4% (N = 541) entered into the study. Analyses indicated that there were no differences
Results
Table 1 shows descriptive statistics for cortisol at both time points and Table 2 shows bivariate correlations among key study variables. Bivariate correlations suggest that more blunted cortisol rhythms at age 6 are correlated with increased conduct behavior (r = 0.17, p = 0.009) and increased rule-breaking behavior (r = 0.16, p = 0.014) from age 6–9.
For the full model testing the longitudinal associations between cortisol and the composite measure of externalizing behavior, fit indices demonstrated
Discussion
Our concurrent findings demonstrated no significant associations between HPA axis functioning and externalizing behavior at age 6 or at age 9. However, our longitudinal findings demonstrated that, after controlling for age 6 externalizing behavior, blunted cortisol rhythms at age 6 (i.e., less change across the day from morning to evening, measured as a latent change score) predicted externalizing behavior problems at age 9. These results suggest that blunted cortisol predicts an increase in
Conflict of interest
None.
Contributors
All authors have made substantial contributions to all of the following (1) the conception and design of the study, or acquisition of data, or analysis and interpretation of data, (2) drafting the article or revising it critically for important intellectual content, and (3) final approval of the version to be submitted.
Katie Lee Salis—proposing the idea for the article, interpretation of data, drafting the article, revising, final approval of the version to be submitted.
Kristin
Funding
National Institute of Mental Health grant R01 MH069942.
Acknowledgement
We would like to acknowledge the National Institute of Mental Health grant R01 MH069942 as our funding source. This is also listed in the funding source section.
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