Disruptive behaviors and HPA-axis activity in young adolescent boys and girls from the general population

https://doi.org/10.1016/j.jpsychires.2006.04.002Get rights and content

Abstract

It is important to investigate associations between biological factors and disruptive behaviors in children and adolescents. Antisocial, aggressive, and criminal behaviors in adults often begin early in life. Disruptive behaviors are often thought to be associated with low activity of the hypothalamic–pituitary–adrenal (HPA) axis. Cortisol, the end-product of this axis, can be measured to investigate HPA-axis activity. Previous studies on this topic concerned clinical or high risk samples. The aim of the present study was to investigate to which extent HPA-axis functioning plays a role in disruptive behaviors in pre-adolescents from the general population. One thousand seven hundred and sixty eight 10- to 12-year-olds from the Dutch general population were investigated. Disruptive behaviors were assessed with the Child Behavior Checklist, the Youth Self-Report, and the Antisocial Behavior Questionnaire. Baseline morning and evening salivary cortisol levels were assessed. Unexpectedly, small associations were found between disruptive behaviors, including attention problems, and higher cortisol levels. However, all effect sizes of significant effects were very small. Our study indicated that HPA-axis functioning may be more relevant in clinical or high risk samples than at the general population level. The association between HPA-axis functioning and attention problems, that has gotten less attention than that with aggressive or delinquent behaviors, requires further research. Furthermore, because effect sizes were relatively small, it can be concluded that, in pre-adolescence, the measures of baseline HPA-axis functioning that were used for the present study can not be used as biological markers for disruptive behaviors.

Introduction

It is important to investigate associations between biological factors and disruptive behaviors in children and adolescents, because antisocial, aggressive, and criminal behaviors often have their onset early in life (Moffitt, 1993). Disruptive behaviors in children and adolescents are often thought to be associated with low activity of the hypothalamic–pituitary–adrenal (HPA) axis (Van Goozen et al., 2000, McBurnett et al., 2000, Raine, 1993, Raine, 1996). Cortisol, the end-product of this axis, is often measured to investigate HPA-axis activity. It is obvious why HPA-axis functioning and antisocial behaviors are often mentioned in the same breath. Two influential theories have postulated an association between disruptive behaviors and low arousal (Raine, 1996). According to the first, the fearlessness theory, a low tendency to become aroused in reaction to fearful stimuli would result in a higher likelihood to become disruptive (Raine, 1993). The immediate fear reaction (increased heart rate, blood pressure, sweat production, etc., within seconds) is mediated by sympathetic nervous system activity. The somewhat postponed fear reaction, meant to enable an individual to resist long-term environmental stresses, is mediated by the HPA-axis. Hence, based on the fearlessness theory, an association between high disruptive behavior levels and low HPA-axis activity could be expected (Van Goozen et al., 2000).

A second important theory is the sensation-seeking theory (Eysenck, 1964, Quay, 1965, Raine, 1993, Zuckerman and Neeb, 1979). This theory hypothesizes that low arousal is an unpleasant physiological state. To get rid of this state, individuals with low arousal levels would seek stimulation, for instance by initiating antisocial behaviors that increase physical tension. It could be argued that sensation seeking activities would mainly help to temporarily obtain a higher sympathetic arousal level, and would not induce higher HPA-axis activity. However, mutual functional connections exist between the sympathetic nervous system and the HPA-axis (Chrousos and Gold, 1998). For instance, sympathetic activation results in higher production of corticotropin-releasing factor (CRF) in the hypothalamus (Calogero et al., 1988), which ultimately induces cortisol production. Vice versa, CRF may stimulate noradrenergic neurons as well (Sapolsky et al., 1986). Hence, individuals with low sympathetic arousal levels, who may tend to seek sensation, may display low HPA-axis activity as well.

Several studies found low basal HPA-axis activity in disruptive individuals (Vanyukov et al., 1993, Moss et al., 1995, Van Goozen et al., 1998, McBurnett et al., 2000, Pajer et al., 2001, Kariyawasam et al., 2002, Shoal et al., 2003, Van de Wiel et al., 2004). McBurnett et al. (2000) found evidence for an association between low salivary cortisol levels and high symptom levels in 38 referred 7- to 12-year-old boys with conduct disorder. A single saliva cortisol sample – time of sampling was not standardized – was obtained during two visits to the clinic. Vanyukov et al. (1993) studied a high-risk sample of 78 10- to 12-year-old sons of fathers with addiction problems. Low saliva cortisol concentrations – assessed at 9 a.m. – were associated with high levels of conduct problems. Pajer et al. (2001) found lower morning basal plasma cortisol levels in 47 15- to 17- year-old girls with conduct disorder than in 37 control girls from the community. However, there are also studies reporting a lack of associations (Dabbs et al., 1991, Stoff et al., 1992, Scerbo and Kolko, 1994, Schulz et al., 1997, Jansen et al., 1999, Van Goozen et al., 2000, Snoek et al., 2002, Oosterlaan et al., 2005). All in all, evidence for low basal cortisol in children with disruptive behavior problems is inconsistent.

Previous studies mainly concerned relatively small samples, and some suffered from methodological problems with cortisol measurements, such as the fact that cortisol levels were not assessed at a standardized time point during the day (McBurnett et al., 2000), despite the abundant knowledge we have about diurnal fluctuations (Pruessner et al., 1997, Weitzman et al., 1971, Wüst et al., 2000). However, an even more important methodological obstacle is the fact that previous studies mainly investigated clinical or high risk samples, and did not address the importance of HPA-axis functioning as a possible correlate of disruptive behaviors in the general population. Hence, important evidence that may help us to understand etiological mechanisms that determine the occurrence of disruptive behaviors at the level of the general population is lacking. Of course, it would be valuable to gather empirical data regarding the HPA-axis–disruptive behavior association in the general population. If the association that was found in clinical and high risk samples would be confirmed in the general population, this would help us to formulate further hypotheses regarding the mechanisms that might explain this association. Further, the usefulness of early assessment of HPA-axis functioning, for the purpose of early detection of those who are at risk for future adverse development, should be tested as a next step. However, if an association between disruptive behaviors and low HPA-axis activity would not be confirmed in the general population, this would indicate that efforts to reveal putative etiological mechanisms should be made in other directions.

Another area that received too little attention thus far is HPA-axis functioning in girls with disruptive behaviors. Although lower than in boys, the prevalence of disruptive behavior problems in girls is not negligible (Côté et al., 2001, Tremblay et al., 1992). Cortisol levels are associated with pubertal stage (Keiss et al., 1995), and gonadal steroids interact with HPA-axis functioning (Burgess and Handa, 1992, Handa et al., 1994, Roy et al., 1999, Vamvakopoulos and Chrousos, 1993). Hence, associations between disruptive behaviors and HPA-axis functioning might be different in girls than in boys. Studies aimed at revealing etiological mechanisms, in our opinion, are equally important for both sexes. Given the paucity of empirical data on this topic in girls, studies filling this gap are needed.

The aim of the present study was to investigate if high levels of disruptive behaviors are indeed associated with low baseline HPA-axis activity. More specifically, the present study tested if the association between disruptive behaviors and HPA-axis functioning, as previously found in small high risk or clinical samples that mainly consisted of boys, could be confirmed in a large representative general population sample of 10- to 12-year-olds, that did not only contain males, but females as well.

Section snippets

Sample and procedure

This study was part of the TRacking Adolescents’ Individual Lives Survey (TRAILS) study. The target sample of TRAILS consisted of 10- to 12-year-olds from five municipalities in the North of the Netherlands, that includes urban and rural areas, who were assessed between March 2001 and July 2002. Of all eligible individuals (N = 2935), 76.0% participated in the study (N = 2230, mean age 11.09 years, SD .55, 50.8% (1132) girls, 15.3% (341) single parent families, 9.0% (201) participants without

Results

Descriptive information, including raw data separately for boys and girls, regarding the CBCL/YSR ADH, OD, and CD Problems scales, the ASBQ total score, and Cort 1, Cort 2, Cort 3, and AUC is presented in Table 1.

Discussion

The present study indicated that, in a large representative general population sample of pre-adolescent boys and girls, the association between disruptive behaviors and indices of basal HPA-axis functioning were weak, and not always in the direction we expected a priori (McBurnett et al., 2000, Pajer et al., 2001, Vanyukov et al., 1993). Hence, the findings from previous studies, that were conducted with clinical or high risk samples, could not be generalized to this general population sample.

Acknowledgements

This research is part of the TRacking Adolescents’ Individual Lives Survey (TRAILS). Participating centers of TRAILS include various Departments of the University of Groningen, the Erasmus Medical Center of Rotterdam, the University of Nijmegen, University of Leiden, and the Trimbos Institute The Netherlands. TRAILS is financially supported by grants from the Netherlands Organization for Scientific Research (GB-MW 940-38-011, GB-MAGW 480-01-006, GB-MAGW 457-03-018, GB-MAGW 175.010.2003.005,

References (64)

  • J.C. Pruessner et al.

    Free cortisol levels after awakening: a reliable biological marker for the assessment of adrenocortical activity

    Life Science

    (1997)
  • J.C. Pruessner et al.

    Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change

    Psychoneuroendocrinology

    (2003)
  • J.G.M. Rosmalen et al.

    Determinants of salivary cortisol levels in 10-12 year old children; a population-based study of individual differences

    Psychoneuroendocrinology

    (2005)
  • K. Sayal

    The role of parental burden in child mental health service use: longitudinal study

    Journal of the American Academy of Child and Adolescent Psychiatry

    (2004)
  • A.S. Scerbo et al.

    Salivary testosterone and cortisol in disruptive children: relationship to aggressive, hyperactive, and internalizing behaviors

    Journal of the American Academy of Child and Adolescent Psychiatry

    (1994)
  • K.P. Schulz et al.

    Plasma cortisol and aggression in boys with ADHD

    Journal of the American Academy of Child and Adolescent Psychiatry

    (1997)
  • G.D. Shoal et al.

    Salivary cortisol, personality, and aggressive behavior in adolescent boys: a 5-year longitudinal study

    Journal of the American Academy of Child and Adolescent Psychiatry

    (2003)
  • H. Snoek et al.

    Serotonergic functioning in children with oppositional defiant disorder: a sumatriptan challenge study

    Biological Psychiatry

    (2002)
  • D.M. Stoff et al.

    Neuroendocrine responses to challenge with DL-fenfluramine and aggression in disruptive behavior disorders of children and adolescents

    Psychiatry Research

    (1992)
  • N.M. Van de Wiel et al.

    Cortisol and treatment effect in children with disruptive behavior disorders: a preliminary study

    Journal of the American Academy of Child and Adolescent Psychiatry

    (2004)
  • S.H. Van Goozen et al.

    Salivary cortisol and cardiovascular activity during stress in oppositional-defiant disorder boys and normal controls

    Biological Psychiatry

    (1998)
  • S.H. Van Goozen et al.

    Hypothalamic–pituitary–adrenal axis and autonomic nervous system activity in disruptive children and matched controls

    Journal of the American Academy of Child and Adolescent Psychiatry

    (2000)
  • M.M. Vanyukov et al.

    Antisocial symptoms in preadolescent boys and in their parents: associations with cortisol

    Psychiatry Research

    (1993)
  • S. Wüst et al.

    Genetic factors, perceived chronic stress, and the free cortisol response to awakening

    Psychoneuroendocrinology

    (2000)
  • M. Zuckerman et al.

    Sensation seeking and psychopathology

    Psychiatry Research

    (1979)
  • E. Aardal et al.

    Cortisol in saliva – Reference ranges and relation to cortisol in serum

    European Journal of Clinical Chemistry and Clinical Biochemistry

    (1995)
  • T.M. Achenbach

    Manual for the child behavior checklist/4-18 and 1991 child profiles

    (1991)
  • T.M. Achenbach

    Manual for the youth self-report and 1991 profiles

    (1991)
  • T.M. Achenbach et al.

    Advances in empirically based assessment: revised cross-informant syndromes and new DSM-oriented scales for the CBCL, YSR, and TRF: comment on Lengua, Sadowski, Friedrich, and Fisher (2001)

    Journal of Consulting and Clinical Psychology

    (2001)
  • T.M. Achenbach et al.

    DSM-oriented and empirically based approaches to constructing scales from the same item pools

    Journal of Clinical Child and Adolescent Psychology

    (2003)
  • American Psychiatric Association

    Diagnostic and statistical manual of mental disorders

    (1994)
  • A. Angold et al.

    Comorbidity

    Journal of Child Psychology and Psychiatry

    (1999)
  • Cited by (0)

    View full text