A prospective examination of the role of childhood sexual abuse and physiological asymmetry in the development of psychopathology

Abstract

Objective

Recent literature has emphasized the simultaneous assessment of multiple physiological stress response systems in an effort to identify biobehavioral risk factors of psychopathology in maltreated populations. The current study assessed whether an asymmetrical stress response, marked by activation in one system and a blunted response in another system, predicted higher levels of psychopathology over time.

Methods

Data were collected from an ongoing, prospective study of females with a substantiated history of childhood sexual abuse (n = 52) and a non-abused comparison group (n = 77). Childhood sexual abuse was determined at the initial study visit. Vagal tone and cortisol were measured 7 years later to assess physiological response to a laboratory stressor across these systems. Depressive symptoms and antisocial behaviors were assessed 6 years after the completion of the laboratory stressor.

Results

Structural equation modeling indicated that a prior history of childhood sexual abuse predicted an asymmetrical physiological response to stress in late adolescence. In turn, this asymmetrical response predicted both higher levels of depression and antisocial behaviors in young adulthood.

Conclusions

Childhood sexual abuse may sensitize females to respond to moderate daily stressors in a manner that places them at higher risk for experiencing depressive symptoms and antisocial behaviors over time.

Practice implications

The management of mild to moderate stress in the everyday lives of maltreated females may be a particularly useful point of intervention in order to protect against later psychopathology.

Introduction

Childhood maltreatment, including physical abuse, sexual abuse, and neglect, has been linked to a number of adverse developmental outcomes in childhood, adolescence and young adulthood. Developmental correlates of childhood maltreatment include increased aggression, emotion dysregulation, anxiety, depression, and post-traumatic stress disorder (Cicchetti and Rogosch, 2001a, Kaufman et al., 1997, Paolucci et al., 2001, Shields and Cicchetti, 1998, Shipman and Zeman, 2001, Trickett and Schellenbach, 1998). Despite this substantial research connecting childhood maltreatment to negative outcomes, not all maltreated children develop subsequent psychopathology (Binder et al., 1996, Kendall-Tackett et al., 1993). This variability in outcome represents a considerable opportunity to gain understanding of specific risk and protective factors that may shape the development of psychopathology in maltreated populations.

Toward this end, researchers have given considerable attention to identifying biobehavioral markers of risk in maltreated populations to help explain individual differences in the development of psychopathology. The autonomic nervous system (ANS) and hypothalamic–pituitary–adrenal (HPA) axis have been targeted predominantly because they are the two main physiological systems activated during environmental stress including childhood adversity and maltreatment. In healthy individuals, the sympathetic branch of the ANS is activated through the locus coeruleus which elevates production of norepinephrine and stimulates the adrenal medulla to release epinephrine. Catecholamines such as norepinephrine and epinephrine are ultimately responsible for increasing blood glucose, heart rate, and blood pressure that aid the body in resolving a stressor (Cacioppo, 1994). Vagal influence over cardiac activity, which is responsible for modulating increased sympathetic activity through the hypothalamus and amygdala, often withdraws during stressor situations (Porges, 2003). Hence, the process of a reduction in vagal influence observed in stressor situations has been referred to as vagal suppression or withdrawal. Activation of the HPA axis begins when a stressor stimulates the corticotrophin-releasing hormone (CRH) in the hypothalamus, leading to secretion of the adrenocorticotropic hormone (ACTH) in the anterior pituitary, and resulting in increased concentrations of cortisol produced by the adrenal cortex (Chrousos & Gold, 1992).

When the stressor is resolved, the hypothalamus and anterior pituitary regulate cortisol concentrations by suppressing production of CRH and ACTH in a process known as the negative-feedback loop (Munck, Guyre, & Holbrook, 1984). Despite being separate arms of the body's stress response, the ANS and HPA are designed to assist the individual under stressful conditions, are influenced by similar brain structures, possess similar physiologic functions such as “fight or flight,” and contain regulatory capacities that modulate heightened physiological activity.

One potential risk associated with exposure to severe and chronic stress such as childhood maltreatment is that the inordinate stress may impair ANS or HPA functioning as well as the interplay that occurs between these two systems. Exposure to childhood maltreatment has been related to persistently high levels of catecholamine activity (DeBellis et al., 1999, DeBellis et al., 1994, Perry and Murburg, 1994), heightened sympathetic activity under novel stress situations (Heim et al., 2000b, Luecken, 1998, Orr et al., 1998), and vagal withdrawal in those people experiencing symptoms of post-traumatic stress disorder (Sack, Hopper, & Lamprecht, 2004). Similarly, severe childhood stress has been associated with high concentrations of cortisol (Carrion et al., 2002, Cicchetti and Rogosch, 2001b, Delahanty et al., 2005, Pfeffer et al., 2007), disrupted diurnal rhythms in cortisol production (Gunnar and Vazquez, 2001, King et al., 2001), and blunted cortisol response in stress reactivity paradigms (Carpenter et al., 2007, Hart et al., 1995). Thus, exposure to severe or chronic forms of stress, such as childhood maltreatment, may result in the dysregulation of both ANS and HPA functioning, each of which has been associated with various forms of psychopathology (Dietrich et al., 2007, Goodyer et al., 1991, Mezzacappa et al., 1997, Pajer et al., 2001, Raine et al., 1990).

Recent efforts to further explicate potential biobehavioral pathways to the development of psychopathology have called for the simultaneous assessment of both ANS and HPA activity as opposed to a single system approach. For example, Bauer and colleagues (Bauer, Quas, & Boyce, 2002) outline two models that may improve the manner by which physiological biomarkers and risk for psychopathology are pursued. The first such model is an additive or symmetrical model where the extreme ends of the continuum in both ANS and HPA activity places children and adolescents at greater risk for psychopathology. According to this additive model, individuals who experience negligible stimulation in both ANS and HPA systems, as well as those who experience extreme stimulation in both these systems, are at increased risk for the development of psychopathology. Prior evidence has supported this view claiming that understimulation in these systems may be an aversive physiological state prompting aggressive and antisocial behavior (Raine et al., 1990), and where overstimulation in these systems may prompt internalizing behaviors (Cicchetti and Rogosch, 2001a, Mezzacappa et al., 1997), all with the aim of regulating or coping with these physiological states. Research to date has supported such symmetrical models of psychopathology where understimulation in both sympathetic and cortisol response (Gordis, Granger, Susman, & Trickett, 2006) and overstimulation in both sympathetic and cortisol response (El-Sheikh, Erath, Buckhalt, Granger, & Mize, 2008) were associated with higher rates of behavior problems.

The second model proposed by Bauer and colleagues is described as an interactive model where a response to stress is observed in one system and an understimulated or blunted response is observed in another. The interactive model is particularly important as activation in one system combined with a blunted response in another may represent global impairment in the body's physiological response to stress, thereby limiting an individual's physiological resources to effectively cope with the demands of a stressor. While the exact physiological mechanisms responsible for an asymmetric response remain unknown, there are several findings that shed light on why an asymmetrical response pattern may occur in maltreated individuals. First, the attenuation hypothesis (Susman, 2006) suggests that after a period of hypersecretion of cortisol in the HPA axis, this system down-regulates cortisol via decreased biosynthesis of hormones in the HPA axis, down-regulation of pituitary receptors, and increased negative feedback sensitivity (Fries et al., 2005, Heim et al., 2000a). While severe or chronic stress may induce potential changes in shared brain structures, such as the hypothalamus and amygdala, across the HPA axis and ANS, this same attenuation process may not occur in the ANS. For instance, ANS functioning had continued sensitivity to repeated exposure to a laboratory stressor whereas HPA axis functioning declined over time (Schommer, Hellhammer, & Kirschbaum, 2003). Thus, ANS and HPA axis functioning may exhibit differential patterns of habituation to stress in that ANS response remains sensitive to stressors whereas cortisol response attenuates over time. Although previous research has linked ANS and HPA axis functioning to various forms of psychopathology (Pajer et al., 2001, Sack et al., 2004), the extent to which this asymmetrical pattern is related to levels of psychopathology, above and beyond single system indicators, is unknown.

As such, this study is an empirical test of Bauer et al.’s (2002) interactive model and its utility in making predictions about subsequent psychopathology. In the current study, an asymmetrical response profile was defined as consisting of a withdrawal of vagal influence over cardiac activity and a blunted cortisol response to a laboratory stressor. This type of asymmetrical response is similar to previous research in that it assesses cortisol reactivity as an indication of HPA axis activity while differing by using vagal withdrawal, instead of salivary alpha-amylase or skin conductance, as an indication of ANS activity. Vagal withdrawal may be a particularly beneficial index as it is purported to measure the physiological regulation of stress and emotions (Porges, 2003). To date, much of the literature explicating the relationship between childhood maltreatment and psychopathology has used retrospective methods in cross-sectional designs. However, prospective assessment of childhood maltreatment in a repeated measures design with an appropriate non-abused comparison condition adds needed experimental rigor and control that can strengthen conclusions about the long-term effects of maltreatment on relevant psychological and physiological outcomes. The current study is one such attempt to assess the effects of an asymmetrical physiological response to stress as a potential biobehavioral pathway to the development of subsequent psychopathology in sexually abused and comparison females followed prospectively for 13 years. By homogenizing the maltreatment experience of our sample, generalization to the experience of sexual abuse can be more readily made, whereas previous studies have included a conglomeration of maltreatment types without parsing the effects of one form of maltreatment over the others. However, because multiple forms of maltreatment tend to co-occur and since there is not ample sampling of alternative forms of abuse in the current analysis, inferences are made about the potential for asymmetry in a group of females with truncated variability with regard to maltreatment type. The two main aims were as follows: (1) determine whether sexual abuse in childhood predicted adolescent ANS/HPA asymmetry, specifically parasympathetic withdrawal combined with blunted cortisol reactivity, during a laboratory stressor paradigm, and (2) assess whether this asymmetrical response predicted higher levels of depressive symptoms and antisocial behaviors in young adulthood.