Abstract
Background:
The relationship between early trauma, hyperarousal and aberrant salience has been investigated exclusively in specific clinical samples, such as post-traumatic stress disorder (PTSD) and psychotic patients, and the results suggest that both dimensions are trauma-induced events, which may lead to the later onset, or increase the vulnerability to psychiatric disorders. The aim of the present research was to evaluate the possible relationships among early childhood trauma subtypes and the dimensions of hyperarousal and aberrant salience in an adult sample of psychiatric patients.
Materials and Methods:
One-hundred psychiatric adult outpatients were assessed by Early Trauma Inventory Self Report-Short Form (ETISR-SF), Aberrant Salience Inventory (ASI) and Hyperarousal Scale (H-Scale). A linear regression analysis was performed in order to investigate which early traumatic events were a predictor of the aberrant salience and the hyperarousal.
Results:
Regression analysis indicated that only ETISR-SF ‘Emotional abuse’ was the unique predictor of ASI ‘Total score’ (p < .0001) and H-Scale ‘Total score’ (p = .031), whereas other ETISR-SF variables did not give a significant additional contribution to the prediction of aberrant salience and the hyperarousal dimension.
Conclusions:
These findings support the role of emotional abuse as predictor of hyperarousal, a basic dimension associated with general vulnerability to mental illness. The awareness of the psychiatric consequences of early childhood trauma leads us to consider the need for better identification of children at risk, to develop effective interventions for the protection of minors from violent and/or inappropriate behaviors and to promote the development of protective resilience factors against re-victimization.
Introduction
Stress occurring during early life, also known as early trauma, refers to childhood and adolescence traumatic experiences and has been categorized into five main subtypes (Bremner, Bolus, & Mayer, 2007): emotional abuse (verbal aggression or conduct that affects the welfare of the child), physical abuse (physical aggression with injury or risk for injury), sexual abuse (sexual conduct that involves a child and someone older), physical neglect (any failure in providing for basic physical needs) and emotional neglect (any failure in providing for basic emotional and psychological needs). Childhood trauma has been found strictly associated with long-term consequences for mental health in adulthood (Badr et al., 2018; Capaldo & Perrella, 2018; Kendall-Tackett, 2009; McLaughlin et al., 2010; Shonkoff et al., 2012) and represents a serious risk factor for adult psychiatric morbidity (Carr, Martins, Stingel, Lemgruber, & Juruena, 2013; Edwards, Holden, Felitti, & Anda, 2003; Van der Kolk, 2017). A large amount of literature has explored the potential pathways of early life adversity in later adult life; in particular, the most relevant associations were found with borderline personality disorder (Cattane, Rossi, Lanfredi, & Cattaneo, 2017), major depression (Infurna et al., 2016), bipolar disorder (Aas et al., 2016), anxiety disorders (Hovens, Giltay, Spinhoven, van Hemert, & Penninx, 2015), post-traumatic stress disorder (Messman-Moore & Bhuptani, 2017), schizophrenia (Isvoranu et al., 2017), substance abuse disorders (Edalati & Krank, 2016), eating disorders (Trottier & MacDonald, 2017), disruptive behavior disorders (Sege, Amaya-Jackson, & American Academy of Pediatrics Committee on Child Abuse Neglect, 2017) and dissociative disorders (Kong, Kang, Oh, & Kim, 2018). Beyond psychiatric disorders, early adverse life events have also been associated with an increased risk for the development of chronic medical conditions, such as pain disorders and irritable bowel syndrome (Gupta et al., 2014; Muscatello, Bruno, Mento, Pandolfo, & Zoccali, 2016; Muscatello, Bruno, Scimeca, Pandolfo, & Zoccali, 2014). The mechanisms by which early traumatic experiences can exert, in a significant percentage of cases, a long-lasting influence on brain functioning and behavior are probably subtended by the dysregulation of neural circuitry and connectivity triggered by chronic and frequent physiological and neurobiological stress responses that can awaken individual’s latent vulnerabilities. Maybe this could be a putative explanation of the association among early trauma with eclectic categories of psychiatric disorders, as previously reported. When considering outcomes of early trauma, it seems more reliable to examine, rather than psychiatric symptoms and/or syndromes, several basic dimensions of brain functioning that should be closely related with those key structures primarily affected by early aversive experiences and prolonged stress responses, such as the insula, amygdala, the prefrontal cortex and hippocampus, all regions also involved in large-scale major intrinsic connectivity networks (ICNs; Carrion & Wong, 2012). ICNs, as identified by connectivity methods, are related with distinctive functions, are stable over time, demonstrate direct behavioral correlates and contribute to distinct psychopathological dimensions (Xia et al., 2018). Among ICNs, Salience Network (SN) is particularly relevant for trauma responses. SN involves amygdala and insula as brain centers, and it is the ICN responsible for attributing significance or salience to stimuli, orienting attentional resources toward them and maintaining balance between internal and externally oriented attentional focus. In neuroscience and psychology, the term salience describes a process by which a stimulus or a feature of a stimulus is perceived as most important and deserving attention. Salience, that is influenced by previous memories and experiences, drives and current psychological and/or emotional state, habitually occurs without conscious awareness; moreover, the integration of autonomic, sensory and visceral systems with homeostatic functions of the brain can condition what is perceived as ‘salient’ (Uddin, 2015). In defining aberrant salience, a condition in which attention is captured by irrelevant stimuli or information with behavioral repercussions, the role of early-life stress has been emphasized in psychotic disorders, due to the function that dopamine plays in both conditions. However, aberrant salience may be also involved in neurodevelopmental and neurodegenerative disorders, such as autism spectrum disorders (ASD), fronto-temporal dementia (FTD), in functional neurological symptoms (FNS) and in affective disorders, such as depression and anxiety (Fiess, Rockstroh, Schmidt, Wienbruch, & Steffen, 2016; Uddin, 2015).
Beyond increased threat sensitivity, also impaired attentional control and hyperarousal have been attributed to abnormalities in the SN (Sripada et al., 2012). Hyperarousal, a fundamental basic dimension associated with stress responses, is defined as a state of hypervigilance, startle response, increased responsiveness to stimuli and increased levels of alertness and anxiety (Lanius et al., 2010). Hyperarousal would represent the expression of an activation/deregulation of the biological stress response, associated with heightened threat sensitivity and chronic, involuntary and exaggerated reaction to stimuli, even in conditions of non-imminent danger.
Based on the evidence from the literature, which suggest a role of early trauma in affecting neural circuitry and connectivity, and the basic, trans-nosographic dimensions of salience and hyperarousal, the aim of the present research was to evaluate possible relationships among early-childhood trauma subtypes, salience and hyperarousal in an adult sample of psychiatric patients.
Materials and methods
Participants
One-hundred outpatients (18–65 years old) consecutively admitted to the Psychiatry Unit of the University Hospital of Messina, Italy, between January and June 2018, were included in the study.
Patients with diseases that could interfere with the outcome of the study protocol (mental retardation, organic brain disorders, history of alcohol/substance dependence, personality disorders, post-traumatic stress disorder and significant concomitant medical conditions) were excluded.
All the patients provided written informed consent after a full explanation of the protocol design, which had been approved by the local ethics committee and was conducted according to the Declaration of Helsinki.
Instruments
The following psychometric measures were used:
The Early Trauma Inventory Self-Report-Short Form (ETISR-SF; Bremner et al., 2007): a 27-item dichotomic (yes = 1/no = 0) questionnaire used for the assessment of the domains of physical (5 items), emotional (5 items), sexual (6 items) and general (11 items) traumatic experiences that occurred before the age of 18 years. Physical abuse includes physical contacts and/or constraint aimed to hurt; emotional abuse refers to verbal abuse and criticism with the intention of humiliating the victim. Sexual abuse is unwanted sexual contacts with perpetrators using force or taking advantage of victims not able to give consent. General traumatic events encompass distressing events that can be secondary to chance events; sample items on this scale include death of a parent, death or sickness of a sibling or friend and discordant relationships or divorce between parents. The sum of scores of each domain and the total scores were calculated. The ETISR-SF is a valid and reliable instrument, as indicated by Cronbach’s alphas for these four domains ranging from .70 to .87 (Bremner et al., 2007).
The Aberrant Salience Inventory (ASI; Cicero, Kerns, & McCarthy, 2010): a 29-item dichotomic (yes = 1/no = 0) self-report grouped into five subscales: ‘Feelings of increased significance’, ‘Sense sharpening’, ‘Impending understanding’, ‘Heightened emotionality’ and ‘Heightened cognition’. Scores are assigned by summing the ‘yes’ replies. The Italian Version of the ASI shows good psychometric properties, high internal consistency and test–retest reliability, as demonstrated by Cronbach’s alpha = .89 (Lelli et al., 2015).
The Hyperarousal Scale (H-Scale; Regestein, Dambrosia, Hallett, Murawski, & Paine, 1993): a 26-item self-report inventory that assesses hyperarousal behavioral traits on a 4-point Likert-type scale (0 = Not At All; 1 = A little; 2 = Quite a bit; 3 = Extremely). The scale produces a Total Summation Score (HSUM), a score of ‘Introspectiveness’ (6 items), ‘Reactivity’ (3 items) and ‘Extreme responses’, referring to the total number of items checked as ‘extremely’. Higher scores (max. 78) are representative of higher levels of hyperarousal. Psychometric data have been reported (Edéll-Gustafsson, Carstensen, Regestein, Swahn, & Svanborg, 2006): internal consistency and test–retest reliability are good (Cronbach’s alpha = .84, and r = .80, respectively).
Statistical analysis
Descriptive statistics were used to summarize the data obtained from the study. Continuous data are expressed as the mean ± SD (standard deviation); non-continuous data are expressed as percentages. A linear regression analysis, where ASI and H-Scale total scores were taken as dependent variables and all the ETISR-SF factors were entered into the equation, was performed in order to investigate which early traumatic events were a predictor of the aberrant salience and the hyperarousal dimension. A significance value of p < .05 was chosen. The statistical analysis was performed with Statistical Package for the Social Sciences–SPSS 16.0 software (SPSS Inc, Chicago, IL, USA).
Results
The sample, 42 (42%) males and 58 (58%) females, was characterized by a mean age of 43.22 years (±SD = 13.9 years). Regarding mental disorders, the diagnostic category most represented was ‘Major Depressive Disorder’ (28%, n = 28), followed by ‘Schizophrenia and other psychotic disorders’ (24%, n = 24), ‘Bipolar disorder’ (22%; n = 22), ‘Anxiety disorders’ (20%; n = 20) and ‘Obsessive–compulsive disorder’ (6%, n = 6).
Table 1 shows the descriptive statistics of the psychometric measures applied in study participants: in relation to the score ranges, the subjects included in the study reported low mean scores in all scales, except for the ETISR-SF domain ‘Emotional abuse’ (2.22 ± 1.8), and the H-Scale Total score (38.50 ± 10.9), both moderately high.
Descriptive statistics (mean ± SD) of the total sample (n = 100).
ASI and H-Scale Total scores, as dependent variables, and all ETISR-SF factors (‘Physical abuse’, ‘Emotional abuse’, ‘Sexual abuse’ and ‘General traumatic experiences’), as independent variables, were analyzed in two linear regression models, as reported in Table 2. Results from the regression analysis indicate that the predictor models accounted for 29.2% and 10.7% of the total variance, respectively, in ASI (F = 4.643; df = 4; p = .003), and H-Scale (F = 1.348; df = 4; p = .031) total scores. Moreover, regression analysis indicated that only ETISR-SF ‘Emotional abuse’ was the unique predictor of ASI ‘Total score’ (p < .0001) and H-Scale ‘Total score’ (p = .031), whereas other ETISR-SF variables did not give a significant additional contribution to the prediction of aberrant salience and the hyperarousal dimension.
Linear regression analysis.
R = .541; F = 4.643; p = .003.
R = .327; F = 1.348; p = .031.
Discussion
The association between early trauma and adult psychiatric disorders is a relatively recent research area, which began in the last 20 years (Edwards et al., 2003; Kessler, Davis, & Kendler, 1997). The growing awareness that environment fundamentally contributes to build the synaptic structure of the adult brain has led researchers to focus attention on the possible consequences of the educational aspects and to highlight that traumatic events experienced during development can cause neurobiological and neuroendocrine damages, which remain throughout life and may be responsible for greater vulnerability in the onset of psychopathological alterations (Baes, Tofoli, Martins, & Juruena, 2012). Given the impact of early trauma on child development in behavioral, emotional, social, physical and cognitive contexts (Bremne & Vermetten, 2001; Middlebrooks & Audage, 2008), less is known about the exact mechanisms by which these pathogenic effects are exerted; it has been suggested that the primary neural systems affected by exposure to early adversities are the neural stress pathway and the emotion processing and regulation pathway, with following repercussions on cognitive control and selective attention (Lim et al., 2015).
Therefore, based on the hypothesis that aberrant salience and hyperarousal seem to be reasonable candidates for mediators/moderators of the effect of early trauma as a general vulnerability factor for psychopathology, the present research aimed to assess the presence of early childhood trauma in the clinical history of adult patients affected by psychiatric disorders and to highlight possible relationships among different trauma subtypes, aberrant salience and hyperarousal dimension.
Data analysis showed that the subjects included in the study reported low scores in all the trauma categories identified by the ETISR-SF scale, except for the subtype ‘Emotional abuse’, which resulted of a moderate level; these findings support a small association among the presence of early trauma and psychiatric disorders in our sample. This result is partially congruent with previous researches, which have revealed a common and robust association between adulthood psychiatric disorders and childhood trauma. Early traumatic experiences as a whole resulted strong predictors of mental illness, closely related to the severity of psychiatric symptoms, poorer response to treatment, increased chronicity, the worsening of patients’ conditions and suicide risk (Green et al., 2010; Hovens et al., 2015; McLaughlin et al., 2010). However, when dissecting early-trauma subtypes, emotional abuse, a pattern of behavior or attitude by caregivers that may cause severe adverse effects on child’s psychological growth and emotional development has been shown to have the highest impact in community samples, though being consistently associated with depressive risk in clinical samples as well (Mandelli, Petrelli, & Serretti, 2015). It has been suggested that also the damaging effect of child sexual abuse, considered as the most severe form of early trauma, get worse when other negative experiences occur (parental indifference and/or criticism, poor parental care, verbal humiliation, severe rejection, terrorizing), and that almost all types of trauma will have their greatest impact when they involve an emotionally abusive component. This explanation supports the argument that emotional abuse unifies and underlies all forms of childhood abuse (Edwards et al., 2003).
A further regression analysis carried out to evaluate possible associations among early trauma categories, aberrant salience and hyperarousal, showed that ETISR-SF ‘Emotional abuse’ subtype represents a valid predictor of the examined dimensions, whereas other ETISR-SF variables do not seem to add a significant contribution. These data, however, are barely comparable with previous research, since no studies have examined the possible role of early trauma linking together two dimensions derived from SN circuitry that have been separately studied in specific clinical conditions, within the context of sleep disorders and post-traumatic disorders (hyperarousal), and psychosis (aberrant salience), with results suggesting that both dimensions may be trauma-induced events, which may lead to the later onset, or increase the vulnerability to psychiatric disorders. Regarding aberrant salience, and according to the model proposed by Kapur, Mizrahi and Li (2005), the tendency to assign salience to neutral stimuli is due to excessive dopamine release that underlies psychotic symptoms. Indeed, aberrant salience has been correlated to the development of psychotic symptoms (Cicero, Becker, Martin, Docherty, & Kerns, 2013; Roiser, Howes, Chaddock, Joyce, & McGuire, 2012) and appears to mediate the relationship between childhood trauma and psychotic-like experiences (PLEs) in the general population (Gawęda, Göritz, & Moritz, 2018).
The obtained results should be interpreted with extreme caution due to several limitations: first of all, the small sample size and the lack of a control group do not allow extending our data to the general psychiatric population neither to compare patients with different psychiatric disorders. Another limitation is represented by the reliance on retrospective assessment of early trauma based on self-report psychometric tools dependent on the subjects’ memory; this can raise concern on the possible influence of traumatic experiences on memory storing and recall processes (dissociation), as well as on the meaning attributed to the events. Also hyperarousal was tested in this study as a self-report: it should be considered that there might be a discrepancy between self-report measure and observed behavior or physiological responses than can be tested in behavioral paradigms. Furthermore, it should be noted that the age in which the early trauma occurred was not specifically considered, and this could be a confounding factor both for increasing the risk of developing psychopathology and for severity and course of the disorder. Finally, the cross-sectional nature of the study limits the causal interpretation of the findings.
Beyond limitations, this study has been an attempt to understand the effect of early childhood trauma on two basic constructs of psychopathology that could encompass and overcome psychiatric categories and that are often used to explain mechanisms of the development of a disorder or symptoms. Maintaining the focus on early trauma in psychiatric research could have significant repercussions on clinical practice; first, the identification of children at risk for traumatic experiences would permit to develop effective interventions for the protection of minors from violent and/or inappropriate behaviors. Strategies should be settled at different levels. Regarding prevention, education for healthy parenting would be suitable, as well as early diagnosis and treatment of children and adolescents with traumatic experiences. Concerning the diagnosis, in adult users of mental health services, any stories of early maltreatment, often unrevealed due to the shame and stigma associated with them, should be systematically assessed by specific tools. Finally, once abuse has occurred, psychoeducational therapeutic interventions, parental counseling and group therapy become necessary to overcome the associated stigma and to promote the development of protective resilience factors against re-victimization.
Footnotes
Acknowledgements
The authors thank all the participants and the whole staff of the Section of Psychiatry, Department of Biomedical, Dental Sciences and Morpho-functional Imaging, University of Messina, Italy, for assistance with recruitment and data collection.
Conflict of interest
The author(s) declared no potential conflicts of interest with respect to the research, authorship and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship and/or publication of this article.
