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