Cardiovascular reactivity as a mechanism linking child trauma to adolescent psychopathology
Introduction
Patterns of physiological reactivity to stress have frequently been shown to be disrupted following exposure to adverse childhood environments (Ellis, Essex, & Boyce, 2005; Gunnar, Morison, Chisholm, & Schuder, 2001; Gunnar, Sebanc, Tout, Donzella, & van Dulmen, 2003). These disruptions in stress response system functioning have been proposed as a predominant mechanism linking experiences of childhood adversity to risk for psychopathology (Ellis and Boyce, 2008, Tarullo and Gunnar, 2006). This work has led to the development of several influential theories regarding the role of adverse early environments in shaping the development of stress response systems and, ultimately, risk for psychopathology (Boyce & Ellis, 2005; Del Giudice, Ellis, & Shirtcliff, 2011; Ellis and Boyce, 2008, Tarullo and Gunnar, 2006). However, a central limitation in prior work on early adversity and stress reactivity has been a failure to distinguish between distinct forms of childhood adversity. Although support for existing theoretical models has been found in studies of children exposed to chronic stressors (e.g., family conflict, low socio-economic status) (Ellis et al., 2005, Evans and Kim, 2007; Gunnar, Frenn, Wewerka, & Van Ryzin, 2009), the predictions of these models are not consistent with patterns of stress reactivity observed in children exposed to traumatic events (e.g. child abuse, domestic violence), which we define as the unexpected experience of actual or threatened death, injury, sexual violation, or other harm to one’s physical integrity, consistent with the Diagnostic and Statistical Manual of Mental Disorders (American Psychiatric Association, 2013). In the current paper we examine an alternative model – the biopsychosocial model of challenge and threat – for explaining patterns of physiological reactivity to stress among adolescents exposed to a diverse range of traumatic events.
The prevailing model of the development of individual differences in stress reactivity – the biological sensitivity to context theory (Boyce and Ellis, 2005, Ellis et al., 2005) – posits that many children exposed to either high levels of stress or to very protected environments develop sensitivity to these environments characterized by heightened sympathetic nervous system (SNS) reactivity. This heightened SNS response is argued to be developmentally adaptive in that heightened reactivity may prepare children to be hyper-vigilant in dangerous environments, as well as to be most receptive to the benefits of adaptive environments (Ellis et al., 2005). Evidence from samples of children exposed to chronic family stressors (e.g., marital conflict, poverty, and parental mental illness) have generally supported this theory (Blair, Granger, & Razza, 2005; Ellis et al., 2005, Evans and Kim, 2007, Feldman et al., 2009; Obradović, Bush, Stamperdahl, Adler, & Boyce, 2010). However the predictions of biological sensitivity to context theory are inconsistent with a growing body of evidence that children exposed to traumatic stressors display a physiological stress response pattern characterized by blunted, not heightened, sympathetic nervous system reactivity (Cooley-Quille, Boyd, Frantz, & Walsh, 2001; Gump, Reihman, Stewart, Lonky, & Darvill, 2005; McLaughlin, Sheridan, Alves, & Mendes, 2014; Oosterman, De Schipper, Fisher, Dozier, & Schuengel, 2010).
The biological sensitivity to context theory has recently been extended to account for a more diverse range of physiological responses to stress in children exposed to adversity. The adaptive calibration model predicts that distinct stress-response profiles will emerge depending on the quality of early life experiences (Del Giudice, Benjamin, Ellis, & El-Sheikh, 2012; Del Giudice et al., 2011). Of these, the profile most relevant to this study posits that children reared in dangerous and unpredictable environments will develop stress reactivity patterns and their behavioral correlates that vary by gender, due to differences in stress response profiles that have evolved to enhance reproductive selection in severe environments. In particular, the adaptive calibration model argues that males will exhibit a pattern of blunted physiological reactivity and females will display heightened physiological reactivity following childhood exposure to traumatic stress. This theory is supported by several studies that have found that stress reactivity interacts with gender to predict psychopathology among children exposed to non-traumatic stressors such as marital conflict and harsh parenting (El-Sheikh, Keller, & Erath, 2007; Erath, El-Sheikh, & Mark Cummings, 2009). However, previous studies of children exposed to traumatic stress have not observed sex differences in patterns of physiological reactivity (Cooley-Quille et al., 2001, Gump et al., 2005, McLaughlin et al., 2014, Oosterman et al., 2010 Oosterman et al., 2010).
Both the biological sensitivity to context and adaptive calibration models predict cardiovascular reactivity profiles among children exposed to adversity (e.g. heightened reactivity, or reactivity that differs by gender) that have not been supported by research on youth exposed specifically to trauma. In the current study we apply an alternative theoretical model to better characterize physiological reactivity patterns in adolescents exposed to traumatic stress: the biopsychosocial model of challenge and threat. This model differentiates between adaptive and maladaptive patterns of response to acute stressors based on specific patterns of cardiovascular reactivity (Mendes, Blascovich, Major, & Seery, 2001; Mendes, Major, McCoy, & Blascovich, 2008). According to the theory (Blascovich, Mendes, Hunter, Lickel, & Kowai-Bell, 2001; Blascovich & Tomaka, 1996), appraisals that one’s resources exceed situational demands are accompanied by an adaptive “challenge” response, in which increases in SNS activation are accompanied by increases in cardiac output (CO) and arterial vasodilation that facilitates the delivery of oxygen, glucose, and other nutrients to the brain and peripheral tissues. In contrast, appraisals that the demands of the situation exceed one’s own resources to cope are paired with a maladaptive “threat” response consisting of SNS activation – although typically less SNS response than in challenge states (Mendes et al., 2008) – accompanied by static or blunted increases in CO and increased vascular resistance. This latter style of physiological responding has been associated with poor cognitive, affective, and behavioral responses to laboratory stressors, in both males and females (Drach-Zahavy & Erez, 2002; Jamieson, Nock, & Mendes, 2012; Tomaka, Blascovich, Kelsey, & Leitten, 1993).
We recently examined the utility of the biopsychosocial theory in characterizing patterns of cardiovascular reactivity in a sample of adolescents exposed to trauma related to physical and sexual abuse. Exposure to child maltreatment was associated with a pattern of cardiovascular reactivity consistent with threat; specifically, both male and female maltreated adolescents experienced similar, although slightly reduced, increases in SNS activation as those with no maltreatment history to a social-evaluative stressor but exhibited significantly blunted increases in CO and greater increases in peripheral vascular resistance (McLaughlin et al., 2014). This study provides preliminary evidence for the utility of the biopsychosocial model as a tool for differentiating adaptive and maladaptive patterns of physiological reactivity following traumatic stress; however, it represents the only existing test of the theory in youths exposed to trauma and was focused on a sample of youths exposed to physical and sexual abuse, a severe traumatic stressor. Given the high prevalence of exposure to trauma in adolescents (McLaughlin et al., 2013), we examined whether the biopsychosocial model explained patterns of cardiovascular reactivity in adolescents exposed to a wider range of more commonly occurring traumatic events. Specifically, we examined whether trauma exposure was associated with an indicator of the pattern of cardiovascular reactivity consistent with threat using data from a large population-based sample of adolescents with exposure to a wide range of traumatic events including natural disasters, accidents, inter-parental violence, and other forms of victimization.
In addition, we examined whether an indicator of the threat pattern of cardiovascular reactivity was associated with adolescent internalizing and externalizing psychopathology. Consistent evidence suggests that patterns of cardiovascular responding are associated with internalizing and externalizing psychopathology in youth (Beauchaine, Gatzke-Kopp, & Mead, 2007; Boyce, 2001, Crowell et al., 2006, El-Sheikh, 2005; Fowles, Kochanska, & Murray, 2000; Graziano & Derefinko, 2013; Shannon, Beauchaine, Brenner, Neuhaus, & Gatzke-Kopp, 2007; Weems, Zakem, Costa, Cannon, & Watts, 2005). Children and adolescents who report higher levels of internalizing problems, including symptoms of anxiety and depression, exhibit a distinctive pattern of heightened SNS and blunted parasympathetic nervous system (PNS) response to stress (Boyce, 2001, El-Sheikh, 2005, Fowles et al., 2000, Graziano and Derefinko, 2013; Obradović, Bush, & Boyce, 2011; Shannon et al., 2007, Weems et al., 2005). In contrast, a growing body of literature has identified blunted SNS reactivity − indicated by smaller reduction in the pre-ejection period (PEP) interval during a challenge task as compared to baseline − as a neurobiological marker of child and adolescent externalizing psychopathology including disruptive behavior disorders, conduct disorder, and attention deficit hyperactivity disorder (Beauchaine et al., 2007, Boyce, 2001, Crowell et al., 2006, Shannon et al., 2007). Interestingly, the same physiological pattern of blunted SNS responding has been identified in children and adolescents exposed to trauma (Cooley-Quille et al., 2001, Gump et al., 2005, Oosterman et al., 2010), suggesting that blunted SNS might be a mechanism linking trauma exposure with externalizing psychopathology. Indeed, in the one previous study examining trauma and CO reactivity in adolescents, blunted CO reactivity to a social stressor was associated with elevated symptoms of externalizing psychopathology (McLaughlin et al., 2014).
The present study examined whether exposure to traumatic stress in childhood is associated with blunted SNS and CO reactivity to stress using data from a large, population-representative cohort of adolescents from the Dutch TRacking Adolescents’ Individual Lives Survey (TRAILS). We did not examine increased vascular resistance as a second indicator of the “threat” profile because it was not recorded during the task of interest in our study. Although the threat and challenge profiles are defined using measures of both cardiac output and vascular resistance, either measure can be conceptualized as an indicator of cardiovascular efficiency and used to distinguish the threat from the challenge profile (Blascovich, Seery, Mugridge, Norris, & Weisbuch, 2004; Mendes et al., 2008). Given growing evidence that slower cardiovascular recovery to baseline is associated with social stressors perceived as uncontrollable and may be an additional cardiac marker of a threat response (e.g., Dickerson & Kemeny, 2004), we also conducted an exploratory analysis examining the associations of CO recovery following stress with trauma exposure and with symptoms of psychopathology. We examined three hypotheses: (a) greater exposure to traumatic experiences would be associated with blunted SNS reactivity – measured using PEP reactivity – to a social evaluative stressor; (b) greater exposure to trauma would be associated with blunted CO reactivity and slower recovery characteristic of the “threat” response predicted by biopsychosocial theory; (c) that blunted CO reactivity and recovery would be associated with elevated symptoms of externalizing psychopathology among adolescents. Given sex differences in physiological reactivity during adolescence (Gunnar et al., 2009, Stroud et al., 2009) and the hypothesized sex differences in physiological reactivity among youths with traumatic stress exposure predicted by the adaptive calibration model, we tested whether these associations varied by gender. Finally, we examined whether blunted CO reactivity mediated the association between trauma and externalizing symptoms in a supplementary analysis.
Section snippets
Participants
Data were collected in a focus sample of TRAILS, a large prospective population study of Dutch adolescents with bi-or triennial measurements from age 11 years into adulthood. For a detailed description of this sample and how it was recruited please see Huisman et al. (2008). The first four assessment waves ran from March 2001 to July 2002 (T1), September 2003 to December 2004 (T2), September 2005 to December 2007 (T3), and October 2008 to September 2010 (T4). During T1, 2230 children were
Descriptive statistics
Table 1 provides the means and standard deviations of all measures separately for males and females. Table 2 provides the zero-order correlations among all measures of trauma exposure, pre-ejection period, cardiac output, and internalizing and externalizing symptoms. For raw CO difference scores for the whole sample and for trauma-exposed and non-trauma exposed adolescents separately, please see Appendix Table A1 in Supplementary data.
Trauma and psychopathology
Trauma history was associated strongly with both
Discussion
Exposure to a wide range of adverse early environments, including traumatic events and chronic stressors that are not traumatic, has been consistently linked to atypical patterns of stress reactivity (Cooley-Quille et al., 2001; De Bellis, MD et al., 1994; Elzinga et al., 2008, McLaughlin et al., 2014, Ornitz and Pynoos, 1989). Existing conceptual models are supported by evidence from samples of children exposed to a range of chronic stressors, including poverty, family psychopathology, and
Acknowledgments
This research is part of the TRacking Adolescents' Individual Lives Survey (TRAILS). Participating centers of TRAILS include various departments of the University Medical Center and University of Groningen, the Erasmus University Medical Center Rotterdam, the University of Utrecht, the Radboud Medical Center Nijmegen, and the Parnassia Bavo group, all in the Netherlands. TRAILS has been financially supported by various grants from the Netherlands Organization for Scientific Research NWO
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