Applying a traumatic stress approach to understanding PCS following pediatric mild TBI.

Child Neuropsychology A Journal on Normal and Abnormal Development in Childhood and Adolescence

ISSN: 0929-7049 (Print) 1744-4136 (Online) Journal homepage: http://www.tandfonline.com/loi/ncny20

Applying a traumatic stress approach to understanding PCS following pediatric mild TBI Katharine Donlon & Russell T. Jones To cite this article: Katharine Donlon & Russell T. Jones (2015) Applying a traumatic stress approach to understanding PCS following pediatric mild TBI, Child Neuropsychology, 21:6, 803-822, DOI: 10.1080/09297049.2014.944491 To link to this article: http://dx.doi.org/10.1080/09297049.2014.944491

Published online: 07 Aug 2014.

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Date: 11 November 2015, At: 14:23

Child Neuropsychology, 2015 Vol. 21, No. 6, 803–822, http://dx.doi.org/10.1080/09297049.2014.944491

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Applying a traumatic stress approach to understanding PCS following pediatric mild TBI Katharine Donlon and Russell T. Jones Department of Psychology, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA Pediatric traumatic brain injury is a significant public health concern affecting hundreds of thousands of children each year. The majority of children who sustain traumatic brain injuries are classified as having a mild traumatic brain injury, and a subset of these children go on to experience persistent physical, cognitive, and emotional symptoms. These symptoms, known as postconcussive symptoms, can endure for months and even years after injury. The outcomes of mild traumatic brain injury are variable and not well understood for a small percentage of children who experience persistent symptoms. The current article explores the potential influence of children’s posttraumatic stress symptoms on persistent postconcussive symptoms. Despite the high incidence of posttraumatic stress symptoms after pediatric accidental injury, they have not yet been identified as an important factor for consideration in the understanding of pediatric postconcussive outcomes. The article will review the literature on posttraumatic stress and postconcussive symptoms after pediatric injury and consider neurobiological and cognitive factors to propose a model explaining a pathway through which posttraumatic stress reactions may serve as the mechanism for the expression and maintenance of postconcussive symptoms after mild traumatic brain injury. The clinical implications for the proposed relationship between posttraumatic stress symptoms and postconcussive symptoms are considered prior to the conclusion of the article, which acknowledges limitations in the current literature and provides suggestions for future research. Keywords: Brain injury; Posttraumatic stress; Postconcussive; Children; Appraisals.

Traumatic brain injuries (TBI) are the leading cause of death and disability among children (Keenan & Bratton, 2006) and are responsible for 475,000 emergency department visits each year among children 0–14 years of age (Faul, Xu, Wald, & Coronado, 2010; Langlois, Rutland-Brown, & Wald, 2006). Pediatric TBI is a significant source of burden on society, as many of these children require specialized educational or community-based services after their injuries (Rivara et al., 2011). The total annual costs related to pediatric TBI amount to more than one billion dollars, illustrating the significance of this public health concern (Schneier, Shields, Hostetler, Xiang, & Smith, 2006). We would like to thank Kirby Deater-Deckard, Thomas H. Ollendick, and Susan W. White for their thoughtful input and helpful feedback with this paper. Address correspondence to Katharine Donlon, Department of Psychology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA. E-mail: [email protected]

© 2014 Taylor & Francis


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K. DONLON & R. T. JONES

The primary causes of pediatric TBI include falls, motor-vehicle-related traumas (MVRT; i.e., passenger in a motor vehicle or being hit while walking as a pedestrian or riding a bicycle), and sports-related injuries (e.g., bicycling, football, basketball, and soccer). While moderate and severe injuries account for the majority of TBI-related deaths, 80–90% of all pediatric TBI are mild in severity (Kraus & McArthur, 1996). Although multiple classification criteria have been proposed for mild TBI, the American Congress of Rehabilitation Medicine (ACRM) definition is the most widely accepted. Accordingly, mild TBI results from a traumatically induced physiological disruption of brain function involving one or more of the following: a loss of consciousness (LOC), loss of memory for events immediately before or after the accident, alteration in mental state at the time of the accident (e.g., feeling dazed, disoriented, or confused), or focal neurological deficit(s) that may or may not be transient. Approximately 20% of children who sustain mild TBI experience acute, impairing physical, cognitive, and psychological symptoms within 3 months of the injury. Conceptualized as Postconcussional Disorder in the Diagnostic and Statistical Manual of Mental Disorders, text revision (DSM-IV-TR; American Psychiatric Association, 2000), the DSM-V (American Psychiatric Association, 2013) omitted criteria for this disorder. While PCS typically resolve within 3 months, an estimated 10% of these children will have persistent symptoms enduring for more than 3 months after mild TBI (Barlow et al., 2010; Taylor et al., 2010). There is a continued need to better understand the problem of persistent symptoms following mild TBI; as such, the present discussion will center on the research that has been conducted to date on PCS. The symptoms of PCS fall into three symptom clusters: somatic (e.g., low-energy level, headaches, nausea), cognitive (difficulty concentrating, forgetfulness), and emotional (e.g., fearfulness, withdrawal) problems. As stated in a paper issued by the World Health Organization’s Task Force on mild TBI, a primary concern in the study of PCS is the nonspecificity of symptoms, as children without TBI can also report experiencing these symptoms (Carroll et al., 2004). Although much attention has been placed on learning more about the factors contributing to chronic PCS in 10% of children (i.e., premorbid PCS, parental distress, cognitive ability, coping, pain, bias, symptom exaggeration, and postinjury management), there is still some confusion regarding these specific factors (see Table 1 for an overview of factors). This article proposes a theoretical model presenting a novel mechanism through which PCS may persist following mild TBI in children. The proposed model explores the potential role of posttraumatic stress symptoms (PTSS) in the development and maintenance of pediatric PCS. However, it should be noted that inherent in the measurement of PCS and PTSS is the potential for an artificially inflated correlation between the constructs given the significant number of shared symptoms (i.e., difficulty concentrating, restricted range of affect, negative emotional state, lack of interest in interacting with others, and associated symptoms of PTSS, such as memory problems and fatigue related to sleep difficulties). Despite the symptom overlap and differential diagnosis problem, the model contends that an interdependent relationship between PTSS and PCS exists; that is, the presence of PTSS may result in chronic PCS in a subset of children. Although additional empirical evidence is needed to provide firm support for the model, the proposed theoretical framework seeks to demonstrate how traumatic stress reactions may be expressed as PCS via an information processing bias towards threat to physical and emotional well-being. Further, the model highlights the role of premorbid

TRAUMATIC STRESS AND PEDIATRIC PCS

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Table 1. Factors contributing to persistent PCS. Factor Empirically supported factors

Premorbid PCS Parental distress Cognitive ability Age


Coping strategies Pain Bias Exaggeration for external benefit Postinjury management Preinjury anxiety

Empirical support McNally et al. (2013) Olsson et al. (2013) Fay et al. (2010) Anderson et al. (2008); Verger et al. (2000) Woodrome et al. (2011) Smith-Seemiller et al. (2003) Brooks et al. (2013); Gunstad and Suhr (2001) Kirkwood et al. (2010); Kirkwood and Kirk (2010) Kirkwood et al. (2008) Mittenberg et al. (1997); anecdotal evidence

Proposed factor without PTSS (manifesting as an informationstrong empirical processing bias towards threat to wellsupport being) Relevant factors that Trait anxiety Kimble et al. (2012); Hensley and Varela may contribute to the (2008); Kılıç et al. (2008); Meiserdevelopment of PTSS Stedman et al. (2009); Smith et al. (2010); Levi et al. 1999 Peritraumatic perceptions of life threat Olff, Langeland, and Gersons (2005a, 2005b); Ehlers and Clark (2000) Maladaptive appraisals resulting in a Ehlers and Clark (2000); Meiser-Stedman sense of current threat (i.e., fear of et al. (2007, 2009); Bryant et al. permanent change, heightened sense (2007); Stallard and Smith (2007) of future danger) Maladaptive cognitive coping strategies Ehlers and Clark (2000); Ehlers et al. (i.e., avoidance, rumination, selective (2003); Stallard and Smith (2007) attention to threat)

anxiety in the development of traumatic stress reactions, which are subsequently reported as symptoms of PCS. Prior to discussion of the proposed model, this article will review the existing literature on PCS, PTSS, the relationship between PCS and PTSS, and the mechanisms through which PTSS results in hypervigilance to threat, and the subsequent report of PCS. More specifically, the levels of analysis framework will be used to explore the role of relevant brain mechanisms, neuropsychological factors, and preinjury anxiety in the development of hypervigilance to threat. Children may attribute symptoms they perceive as threatening to their physical and emotional well-being to PCS. As such, symptoms of traumatic stress may be misidentified as PCS in a subset of children with chronic PCS following mild TBI.

Pediatric PCS The expression of PCS following pediatric mild TBI is variable with a subset of children experiencing acute symptoms and a smaller subset reporting chronic symptoms. It is important to understand the presentation of PCS over time as the factors contributing to acute and chronic symptom expression also vary. Yeates and colleagues (2009)


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identified four distinct longitudinal PCS trajectories in a sample of children who presented to the emergency department (ED) after sustaining an injury. While the majority of children did not experience PCS, a subgroup of children experienced high levels of symptoms in the acute aftermath of injury. Of these children, one group continued to have symptoms persisting beyond 3 months, while another group experienced a significant decline in symptomatology within the 3 months after injury. The fourth group consisted of children who had a moderate level of PCS in the acute aftermath of injury and the symptoms remained stable over time. The current article will focus on the children who experience persistent symptoms lasting beyond 3 months after injury. There is a need for further study on long-term outcomes after pediatric mild TBI given its relevance to postinjury clinical management, which is not well understood in the subset of children with chronic PCS (Kirkwood et al., 2008). Acute PCS results from a combination of injury factors and noninjury factors following mild TBI. Children who initially experience high PCS levels that decline within 3 months tend to be those who sustain a more severe mild TBI (e.g., with posttraumatic amnesia, disorientation, and loss-of-consciousness; McNally et al., 2013; Yeates et al., 2009). Neurological factors are thought to account for many of the symptoms that comprise the somatic symptom cluster of acute PCS, as many of these symptoms (e.g., headaches, dizziness, and fatigue) are considered normal, transient reactions to brain injury (Anderson, Heitger, & Macleod, 2006). Unlike children with moderate and severe TBI, children with mild TBI show few, if any, acute or long-term impairments in neurocognitive domains (Babikian & Asarnow, 2009; Babikian et al., 2011; Babikian, McArthur, & Asarnow, 2013; Catroppa & Anderson, 2005). Residual problems with neurocognitive functioning following mild TBI are more likely due to a general injury effect rather than brain injury (Babikian et al., 2011). While factors such hyperactivity, impulsivity, and behavior problems predispose children to sustaining injury (Gulotta & Finney, 2000; Peterson & Stern, 1997), several other psychological factors, including premorbid PCS (McNally et al., 2013), parental distress (Olsson et al., 2013), cognitive ability (Fay et al., 2010), and younger age (Anderson et al., 2008; Verger et al., 2000) are associated with negative outcomes after mild TBI, including chronic PCS. Particularly relevant to the current article is the important role of coping in PCS outcomes as demonstrated in a study of children with mild TBI, which found that problem-focused disengagement coping strategies moderated the relationship between mild TBI and acute as well as chronic PCS outcomes (Woodrome et al., 2011). In addition, children with chronic pain report symptoms consistent with PCS (SmithSeemiller, Fow, Kant, & Franzen, 2003). Bias is also important to consider, as children and parents may underestimate their premorbid symptom levels and attribute all symptoms following the mild TBI to the injury (Brooks et al., 2013; Gunstad & Suhr, 2001). While infrequent, children may occasionally exaggerate their report of PCS for external benefit (e.g., school avoidance; Kirkwood, Kirk, Blaha, & Wilson, 2010) or litigation purposes (Kirkwood & Kirk, 2010). Finally, postinjury management (e.g., extended cognitive rest or prolonged activity restrictions) may adversely affect children’s recoveries following mild TBI by causing emotional distress due to falling behind in school, being away from friends, and lowered self-esteem (Kirkwood et al., 2008). Furthermore, there is evidence to suggest that children with high levels of preinjury anxiety are at risk for worse outcomes after mild TBI than nonanxious children (Mittenberg, Wittner, & Miller, 1997). Clinically speaking, children with preinjury anxiety


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are more likely to experience PCS after mild TBI (V. Anderson, personal communication, January 2, 2013). Preinjury anxiety is an established predictor of persistent PCS in adults after mild TBI (Ponsford et al., 2012; Meares et al., 2011). It may be that individuals with preinjury anxiety have greater anxiety sensitivity and less adaptive coping mechanisms, thereby leading to an increased likelihood of developing PCS after mild TBI (Ponsford et al., 2012). The role of psychological factors in the expression of PCS challenges the idea that symptoms solely result from neurological factors related to the mild TBI (Fay et al., 2010; McNally et al., 2013; Taylor et al., 2010; Yeates, 2010; Yeates et al., 2009, 2012).

Traumatic Stress after Injury Posttraumatic stress reactions are one of the most common and potentially impairing sequelae of pediatric unintentional injury (Kahana, Feeny, Youngstrom, & Drotar, 2006; Kassam-Adams & Winston, 2004; Landolt, Vollrath, Ribi, Gnehm, & Sennhauser, 2003; Winston, Kassam-Adams, Garcia-España, Ittenbach, & Cnaan, 2003). Posttraumatic stress disorder (PTSD) can occur after exposure to actual or threatened death or injury and is comprised of a constellation of intrusion symptoms, avoidance of trauma-related stimuli, negative alterations in cognition and mood, and hyperarousal (American Psychiatric Association, 2013). A significant percentage of children who develop posttraumatic stress reactions do not meet full criteria for PTSD but will have impairing subclinical symptoms, commonly referred to as PTSS in the pediatric injury literature (Carrion et al., 2001; Daviss et al., 2000; Iselin, Le Brocque, Kenardy, Anderson, & McKinlay, 2010; Kahana et al., 2006). Empirical evidence indicates the magnitude of the stressor is less relevant to outcomes following the event than is the perception of life threat. Results of a meta-analysis found little evidence to suggest that objective factors (e.g., injury severity and type of injury) significantly influence the development of PTSS (Fein et al., 2002; KassamAdams & Winston, 2004; Nugent, Christopher, & Delahanty, 2006; Trickey, Siddaway, Meiser-Stedman, Serpell, & Field, 2012). Additionally, the risk of developing PTSS does not vary depending on the mechanism of injury (MVRT, sports-related injuries, burns, falls; Nugent, Ostrowski, Christopher, & Delahanty, 2007). Rather, subjective factors, such as children’s strong sense of fear, life threat, and loss of control during or after injury put them at a higher risk for PTSS in the weeks and months following injury, compared to children who reported a lesser degree of subjective threat (Ehlers, Mayou, & Bryant, 2003; Langeland & Olff, 2008; Meiser-Stedman, Dalgleish, Glucksman, Yule, & Smith, 2009; Werba & Kazak, 2007). Other factors, not directly related to the injury event, may also contribute to the development of PTSS after mild TBI. Pediatric medical traumatic stress refers to children’s and parents’ reactions to pain, injury, serious illness, medical procedures, and frightening treatment experiences (National Child Traumatic Stress Network, 2004) and is related to posttraumatic stress outcomes (Kazak et al., 2006). In addition, parents are at risk for developing PTSS after a child sustains a traumatic injury (De Vries et al., 1999; Sturms et al., 2005), due to the potentially traumatic nature of seeing the child in danger. Consideration of parental psychopathology is critical given that children’s psychological recovery after injury is influenced by parental psychological well-being and ability to provide support (Nugent et al., 2007; Taylor et al., 1999).


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Additionally, children may experience anxiety related to surgical procedures, inadequate information about procedures, and disruption of daily routines during the peritraumatic period, which can cause distress (Coyne, 2006; Hildenbrand, Clawson, Alderfer, & Marsac, 2011; Kazak et al., 2005). Additional factors associated with the hospital experience (e.g., exposure to scary events like loud beeping alarms and the rush of staff down hospital hallways in response to emergency situations related to other patients) have also been found to contribute to the development of posttraumatic stress reactions (WardBegnoche, 2007). While the evidence above clearly points to factors contributing to the development of PTSS following injury, some researchers have questioned the likelihood of developing PTSS after TBI. It was thought that the occurrence of LOC following TBI precluded the encoding of mental representations of the traumatic event (Sbordone & Liter, 1995). However, empirical findings indicate that PTSS can develop from experiences acquired after the trauma, such as seeing accident photos or frequent retelling of the event (Bryant, 1996) or implicitly encoding sensory information that is retrieved automatically in the presence of appropriate cues (Ehlers & Clark, 2000; Schacter, Norman, & Koutstaal, 1997).

Relationship between PTSS and PCS While a significant body of literature exists supporting the relationship between PTSS and chronic PCS in adults (Bryant & Harvey, 1999; Hoge et al., 2008; Ponsford et al., 2012), less is known about the relationship between these constructs in children. However, findings from a study conducted by Hajek et al. (2010) provided sufficient evidence to conclude that a relationship between chronic PCS and PTSS in children may exist. To explore the relative roles of TBI-related factors and non-TBI-related factors on the development of PCS, children with mild TBI and those with orthopedic injury (OI), or injury to a body part other than the brain, were assessed for symptoms of PTSD and PCS. They found evidence indicating that parents of children with mild TBI reported higher levels of PCS than the OI group when controlling for PTSD, suggesting that neurological factors are important in the reporting of PCS. However, the authors also found that the somatic and cognitive symptom clusters were correlated with PTSD symptom clusters in children with mild TBI and those with OI. These relationships were found immediately following the injury, as well as 3 and 12 months later. Notably, while Hajek and colleagues (2010) found that the correlations between symptom clusters of PCS and PTSS were significant for both groups of children, the relationship was slightly stronger for those with OI. The authors concluded that the stronger relationship between these two constructs in children with OI suggests that additional factors influence the expression of PCS in children with mild TBI. This finding was substantiated by the fact that a larger percentage of variance was left unaccounted for in the group with mild TBI. Surprisingly, the authors did not articulate the potential implications of this novel finding. That is, they did not emphasize the possible role of psychological factors, such as PTSS, on the expression of PCS in children after mild TBI. The current article builds on the informative findings from Hajek and colleagues’ research to explore a possible relationship between PTSS and PCS following pediatric mild TBI.


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Developmental Considerations It is important to consider developmental differences when evaluating the empirical evidence related to PCS and PTSS in children following mild TBI, given that children’s maturity levels rapidly change throughout childhood and adolescence. Empirical evidence indicates that no significant differences exist in the manifestation of PTSS among children ranging in age from 7–18 years. Conversely, PTSS manifests differently in preschool-aged children due to their inability to accurately report traumatic stress reactions (i.e., helplessness, horror) and their immature cognitive abilities (Scheeringa, Zeanah, & Cohen, 2011; Trickey et al., 2012). The DSM-V recognized this developmental difference by including preschool-aged children under a separate diagnostic criterion (American Psychiatric Association, 2013). Furthermore, children have relatively stable brain development between the age of 7 and early adulthood (Anderson, Jacobs, & Anderson, 2008), suggesting that the deficits they experience from brain injury are more similar among children in this age group than compared to young children, who are more likely to experience global deficits (Anderson et al., 2010). Given that there is only slight variation in PTSS and brain development among school-aged children ranging from 7–18, and the majority of PCS research has been conducted with school-aged children, the present discussion will be targeted toward children in this age range. APPLYING A TRAUMATIC STRESS APPROACH TO PCS While there are multiple pathways leading to the persistence of PCS (e.g., premorbid cognitive functioning, coping style, and bias), one underrecognized but potentially important pathway is through PTSS. The topic of pediatric mild TBI has received considerable attention in the empirical literature as well as in the lay press, often leading parents and children to the conclusion that it has a dire prognosis (Rivara et al., 2011). Effective communication with families and children after TBI is important because they may assume PCS results from brain damage, dismissing the potential role of psychological factors. Allowing children to believe that the nonspecific symptoms characteristic of PCS result from long-lasting and impairing neurological damage may lead to hypervigilance to benign symptoms and the ways in which these symptoms may pose a threat to future well-being. This type of catastrophic interpretation is a key characteristic of PTSS (Bryant, 2001, 2011). The following discussion will use a levels of analysis framework to explore brain mechanisms and neuropsychological factors involved in the development and maintenance of PTSS. The levels of analysis approach accounts for the contribution of factors from various origins (i.e., etiological, brain mechanisms, neuropsychological, and symptom level factors) in the development of pathology, rather than differentiating between the mind and body (Pennington, 1991). Examining the complementary roles of brain mechanisms (neurobiological factors) and neuropsychological factors (cognitive processes), as well as the role of preinjury anxiety in etiology, can provide the foundation for understanding the development and the continuation of symptoms following mild TBI. Contribution of Brain Mechanisms to Outcomes Early stress responses may be precipitating factors for the expression of symptom level factors, such as persistent PCS and the development and maintenance of PTSS. The


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initial vulnerability to stress occurs when the injury event causes changes in brain metabolism by disrupting axonal functioning (Inglese et al., 2005), which may contribute to changes in information processing leading to enhanced threat perception and changes in the brain’s ability to manage stress (Bay & Liberzon, 2009). This process begins with strong peritraumatic perceptions of life threat, which then initiate a series of neurobiological and neuroendocrinological stress responses, which ultimately result in PTSS (Olff et al., 2005a, 2005b). Individual differences are important to consider when attempting understanding of why some individuals experience maladaptive outcomes after mild TBI and others do not. Strong emotional responses during or directly after trauma can alter physiological responses and subsequently lead to pathology. Perceptions of loss, threat, harm, and uncontrollability may increase the risk of subsequent PTSS (Ehlers & Clark, 2000; Olff et al., 2005a). The initial subjective perception of life threat leads to a cascade of neurobiological responses that are associated with subsequent PTSS (Olff et al., 2005b). Stressors perceived as threatening are associated with perceptions that one cannot adequately cope with the event, leading to increased peripheral vascular resistance and higher reactive levels of cortisol (Olff et al., 2005a; Suendermann, Ehlers, Boellinghaus, Gamer, & Glucksman, 2010). Stress appraisals mediate the magnitude of the neuroendocrine stress response after trauma, and the response is stronger when stressors are appraised as more threatening (Olff et al., 2005a). Two primary neuroendocrine system responses are activated when a person attempts to manage his or her emotional response to threat in a stressful event. The sympathetic nervous system (SNS) releases neurotransmitters, which in turn cause increases in heart rate, blood pressure, and blood glucose levels. The energy generated by the SNS activation enables individuals to flee in the “fight or flight” response to trauma. Additionally, the hypothalamus pituitary adrenocortical (HPA) system functioning is a critical factor for adaptive responding to stressful situations. It is activated only when individuals perceive uncertainty or emotional distress in response to stressors (Olff et al., 2005a, 2005b). Dysregulation of the SNS and HPA-axis systems is consequential because it lowers the threshold required to stimulate the stress response systems. Simply the anticipation of threat is enough to stimulate these systems and leads to a consistent anticipatory stress response and vigilance to threats of survival (Grogan & Murphy, 2011). The initial emotional and neurobiological reactions to a traumatic stressor then begin a maladaptive cycle of negative expectancies about future events and negative cognitive appraisals about the meaning of the trauma and trauma sequelae, which serve to maintain PTSS. Role of Neuropsychological Factors in PTSS The Cognitive Model of PTSD is considered to be one of the most well-accepted theories of the maintenance of PTSS over time and will serve as the framework for the present discussion of the role of cognitive factors in chronic PTSS. The model posits that PTSS persists when individuals perceive a sense of serious current threat. One source of current threat is derived from excessive negative appraisals about the traumatic event, its sequelae, and symptoms. Another source of current threat is the poorly integrated trauma memory that facilitates the spontaneous triggering of reexperiencing symptoms. The perceived threat stimulates the utilization of behavioral and cognitive strategies, which



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are intended to manage the sense of threat and accompanying distress in the short term but which ultimately end up preventing cognitive change and maintaining PTSS over time (Ehlers & Clark, 2000). Although the Cognitive Model was initially proposed with an adult population in mind, Dalgleish, Meiser-Stedman, and Smith (2005) concluded that it is appropriate to apply this model to children given the similarities they observed between cognitive variables and PTSS in adults and children. The model proposes that individuals may have negative appraisals of the trauma and trauma sequelae that lead to a sense of serious current threat. In some cases, individuals’ appraisals center on the traumatic event and involve overgeneralizing the event and subsequently perceiving a range of additional events as being more threatening than they are in reality. Other appraisals may involve the trauma sequelae. Specifically, the interpretations of others’ reactions in the aftermath of trauma and appraisals of the trauma’s consequences in other domains of life (e.g., physically, academically, socially) may be perceived as threatening. According to the model, one area on which maladaptive appraisals may center is physical health consequences, including cognitions such as “My body is ruined” or “I will never be able to lead a normal life again.” The authors explain that common symptoms after trauma, such as flashbacks, irritability, emotional lability, concentration difficulties, and numbing, may be misinterpreted as threatening to physical or psychological well-being (Ehlers & Clark, 2000). The influence of maladaptive cognitive appraisals on the maintenance of PTSS is well established in the pediatric injury literature (Bryant, Salmon, Sinclair, & Davidson, 2007; Meiser-Stedman et al., 2009, 2007; Stallard & Smith, 2007). Meiser-Stedman et al. (2007) found that children who experienced physical assaults or MVRT reported higher levels of PTSS 1 month after the injury when they endorsed subjective appraisals of threat surrounding the trauma, experienced higher levels of trait anxiety, employed ruminative coping strategies, endorsed worry as being adaptive and reported sensory-based memories of the trauma. After 6 months, maladaptive appraisals, specifically those related to permanent change and future vulnerability, predicted unique variance in PTSS even when accounting for early PTSS (Meiser-Stedman et al., 2009). Based on these results, the authors concluded that maladaptive appraisals play a causal role in the development and maintenance of PTSS over time (Meiser-Stedman et al., 2009). Similarly, Bryant et al. (2007) explored the relationship between maladaptive appraisals and PTSS in children who were admitted to the hospital following injury. They found that maladaptive appraisals, specifically, perceptions of future vulnerability, accounted for unique variance in PTSS 6 months later. Stallard and Smith (2007) also found that cognitive appraisals, including a negative interpretation of symptoms (e.g., “I might go crazy”), injustice (e.g., “This isn’t fair), permanent change (e.g., “This has ruined my life” or “Things are never going to be right again”), and a heightened sense of future danger (e.g., “Bad things always happen to me”), were associated with higher levels of PTSS in children 8 months after being admitted to the emergency room following an MVRT. The findings from these studies provide support for the conclusion that children who continue to have maladaptive cognitions related to the traumatic event and its sequelae are also the children who experience higher levels of PTSS. Furthermore, many of the maladaptive cognitions endorsed by these children relate to the perception that their lives will never be the same again and that they are vulnerable to future harm.

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This is consistent with what children who are concerned about the possible negative impact of TBI on their daily lives may believe about their futures.

Maladaptive Cognitive Coping Maintains PTSS. Stress outcomes are also influenced by an individual’s ability to manage the maladaptive cognitions that maintain symptoms. The use of cognitive strategies, such as avoidance, is considered maladaptive because they serve to maintain PTSS by preventing the acquisition of information incongruent with the fear structures (Ehlers & Clark, 2000). Other examples of maladaptive cognitive coping strategies include rumination, suppression of intrusive memories, distraction, and selective attention to threat. The use of these strategies was associated with high levels of PTSS in children after MVRT (Ehlers et al., 2003; Stallard & Smith, 2007). Furthermore, children’s selective attention to threat also serves to maintain PTSS over time. Paying selective attention to threat cues is a unique cognitive coping strategy because it is a relatively automatic; it arises from the activation of fear networks in the immediate aftermath of a trauma, which results in these fear responses becoming highly accessible (Ehlers & Clark, 2000). Individuals tend to interpret even benign stimuli as threatening. The overemphasis on detecting fear-related information prevents nonthreatrelated information from being adequately processed, which subsequently maintains high levels of anxiety and perpetuates the biases towards potential threats in the environment (Dalgleish, Moradi, Taghavi, Neshat-Doost, & Yule, 2001; Hayes, VanElzakker, & Shin, 2012).

Relevance of Preinjury Anxiety Prior to beginning the discussion about the influence of PTSS on post-TBI outcomes, it is crucial to emphasize the importance of considering preinjury characteristics, particularly preinjury anxiety, in understanding the development and maintenance of PCS. Consideration of preinjury anxiety is particularly relevant to the understanding of PTSS and PCS following mild TBI. Anxious children may be predisposed to have negative appraisals and expectancies about information in their environments prior to the traumatic event. These automatic and deeply engrained processes may facilitate the later development of PTSS (Kimble, Batterink, Marks, Ross, & Fleming, 2012). Empirical evidence consistently supports the relationship between high levels of trait anxiety, defined as the general tendency to perceive stressful situations as dangerous or threatening (Hensley & Varela, 2008), and elevated levels of posttraumatic stress (Hensley & Varela, 2008; Kılıç, Kılıç, & Yılmaz, 2008; Levi, Drotar, Yeates, & Taylor, 1999; Meiser-Stedman et al., 2009; Smith, Perrin, Yule, & Clark, 2010). Individuals with high trait anxiety may respond to stressors with more fear and distress (Kılı, Kılıç, & Yılmaz, 2008; Smith et al., 2010) and demonstrate enhanced fear conditioning (Hayes et al., 2012). It may be the case that high trait anxiety burdens cognitive resources and interferes with the ability to adequately process traumatic events and associated emotions (Hensley & Varela, 2008). As such, anxious children’s use of reappraisal strategies and the ability to sustain comfort from reassurance and safety efforts may be inadequate, decreasing the likelihood that they will be able to successfully cope with PTSS (Smith et al., 2010).


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PROPOSED MODEL Given the extant literature indicating that psychological factors are important contributors to the expression of PCS beyond 3 months after injury, it is questionable whether persistent symptoms should be labeled as PCS. This is consistent with the World Health Organization’s identified concern about attributing the nonspecific residual symptoms following mild TBI to PCS. Simply, the term “PCS” indicates that symptoms arise following a head injury, which we know is not the case, as many children with OI also experience significant symptoms. As it is well established that injury-related factors (e.g., expected, transient consequences of mild TBI) primarily contribute to PCS within 3 months of TBI, it may be more appropriate to identify these acute symptoms as PCS and to reconceptualize our thinking about chronic symptoms. Traumatic stress reactions are a plausible explanation for why children may report chronic PCS and can explain the presence of chronic PCS in children who have sustained an acute physical injury, both with and without brain trauma. Considering that many injured children develop PTSS after the traumatic injury and maladaptive cognitive appraisals are a primary contributing factor to the persistent sense of serious current threat characteristic of PTSS, it is plausible that health-related fears specific to TBI may be the focus of negative cognitive appraisals. Children who are suffering from PTSS will be attentive to information perceived as threatening and are likely to attribute physical, cognitive, and emotional responses to the TBI (Bryant, 2011). This notion, initially suggested by Bryant (2011) to help explain the expression of PCS in adults, posits that high levels of PCS may result from an information processing bias toward threat to well-being. The sense of uncertainty about health states represents a key part of children’s reactions to trauma that may lead to PTSS (Smith et al., 2010). While these children may not actually experience higher PCS levels, they are more attuned to the potential threat that the symptoms pose to well-being, and they tend to catastrophize the meaning of the symptoms, thereby resulting in reports of chronic PCS. Given that children with preinjury anxiety are most likely to experience persistent PCS and anxiety predisposes children to develop significant stress responses after a potentially traumatic event, PCS may well represent a stress reaction after sustaining a TBI. Children with anxiety are more likely to perceive events as life threatening and thereby are prone to experiencing interrelated neurobiological responses and cognitive appraisals of threat, which serve to engender the development of PTSS. Symptoms of PCS persist over time when children are unable to adequately cope with their posttraumatic stress reactions. Cognitive factors, such as maladaptive appraisals and the use of dysfunctional coping strategies, maintain stress reactions and perpetuate PCS. See Figure 1 for a model explaining how premorbid anxiety influences stress reactions, which, if they endure over time, may be mislabeled as chronic PCS. The model accounts for the role of brain mechanisms (neurobiological factors) and neuropsychological factors (cognitive appraisal processes) that subsequently lead to PTSS and the expression of persistent PCS. The model also includes preinjury anxiety as a possible factor contributing to the expression of symptoms.

IMPLICATIONS AND FUTURE DIRECTIONS The current article is largely theoretical given the lack of data examining PCS and PTSS in children. Indeed, only one study has directly compared PCS and PTSS after

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PTSS

Premorbid anxiety

Cognitive coping strategies

Neurobiological responses Negative appraisals of the trauma/sequelae


Perception of life threat

Mild TBI

PCS

Figure 1 Theoretical model for understanding the development of PCS following pediatric mild TBI from a traumatic stress perspective.

Note: Dotted lines denote indirect relationship.

pediatric mild TBI, making it difficult to ascertain the nature of this relationship. Future programmatic research will be necessary to evaluate the extent to which the model is empirically supported. Methodologically rigorous studies of pediatric PCS include a longitudinal design, given the distinction between acute and chronic PCS, as well as a control group of children with OI to determine the relative effects of injury- and noninjury-related factors on outcomes. To empirically evaluate the model proposed in this article, a study should be designed to examine PTSS as a mediating variable between mild TBI and PCS. This model also assumes that subjective perceptions of life threat related to the specific injury event and subsequent acute neurobiological responses mediate the relationship between mild TBI and PTSS. A number of relevant moderators, such as premorbid anxiety and cognitive coping strategies (e.g., vigilance to threat that serves to maintain maladaptive cognitive appraisals) may influence relationships within the model and should be examined scientifically. Recognizing the important role of maladaptive cognitive appraisals in the maintenance of PCS allows clinicians to select treatments to specifically target these cognitions. A number of psychoeducational interventions, including parent training (Antonini et al., 2014; Brown, Whittingham, Boyd, & Sofronoff, 2013) and provision of information booklets (Ponsford et al., 2001), have shown to be effective in reducing children’s behavioral and emotional symptoms following pediatric TBI. Interventions comprised of psychoeducation, reassurance, and reattribution of symptoms to nonthreatening causes are effective for reducing chronic symptoms of PCS, which may occur by normalizing symptoms and assuring individuals that they are not a result of long-term cognitive impairment (Mittenberg, Canyock, Condit, & Patton, 2001). Cognitive therapy is also an empirically sound treatment approach for adults with the potential to address the catastrophic appraisals that may lead to the exaggeration of PCS severity. In turn, this may subsequently alleviate anxiety and arousal related to the posttraumatic stress reactions and may reduce symptoms of persistent PCS (Walter, Kiefer, & Chard, 2012).


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Finally, there are also important implications for secondary prevention efforts after pediatric mild TBI. Currently, usual care practices do not include the provision of psychoeducational materials about TBI sequelae or information concerning mental health problems in the aftermath of injury. As TBI is a medical event, it is unlikely that most children and families are aware that their symptoms may be psychologically induced rather than indicative of worsening physical health. Providing psychoeducational materials about possible reactions to TBI as well as common causes of these reactions (e.g., PTSS) could be beneficial to children and families. This approach would have the added benefit of reducing burden on medical professionals. Future Directions An important area of future research should center on the role of parental pathology and how it may influence children’s symptoms of persistent PCS. For example, further examination of possible risk factors for the development of parental PTSS, including feelings of guilt about their children’s injuries and maladaptive cognitive appraisals about the trauma (Ostrowski, Christopher, & Delahanty, 2007), is warranted. The impact of parent’s coping style should also be examined. It may also be the case that parents’ PTSS and associated behaviors, such as avoidance, influence children’s stress reactions (Nugent et al., 2007). Furthermore, a primary concern in the study of PCS is the discrepancy in diagnostic criteria between the DSM-V and the International Statistical Classification of Diseases and Related Health Problems, 10th revision (ICD-10; World Health Organization, 1993). The DSM-IV research criteria for PCS places emphasis on objective factors (i.e., decline in cognitive functioning and loss of consciousness after injury, which may be accompanied by changes in emotional functioning), while the ICD-10 criteria accounts for subjective factors as well. The ICD-10 criteria, which state, in part, that individuals must fear they will have permanent brain damage, are particularly relevant to the present article as they posit that PCS is maintained by an exaggerated vigilance to physical symptoms or worsening brain damage. Future research should examine relationships among mild TBI in children, PTSS, and PCS according to the ICD-10 criteria and should evaluate the findings in light of the current DSM-V criteria. CONCLUSION The persistence of PCS is a serious public health concern given the high numbers of children who sustain mild TBI. Persistent PCS is associated with negative outcomes months and even years after TBI. Children who develop PCS after brain injury miss an average of one week of school as a result of their injury and associated sequelae (Babcock et al., 2013), and children with higher levels of cognitive PCS report impaired psychosocial quality of life (Moran et al., 2012), highlighting the importance of understanding the etiology and maintenance factors of PCS. The primary goal of the current article was to examine potential factors contributing to the expression of PCS in children after mild TBI with specific emphasis on the contribution of PTSS. More specifically, the current article proposed a levels-of-analysis approach to understanding the influence of posttraumatic stress reactions on pediatric PCS. It may be the case that children experience PTSS, which is labeled as PCS in the absence of an appropriately thorough physical and psychological assessment. This may


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arise via stress responses resulting from the injury, which initiate a complex series of processes involving neurobiological and cognitive variables that eventually lead to persistent physical, cognitive, and emotional symptoms after mild TBI. A variety of factors, including premorbid PCS, parental distress, premorbid anxiety, cognitive ability, coping, pain, bias, and symptom exaggeration are thought to contribute to the persistence of PCS. The current model proposes that PTSS may also be a factor in chronic PCS. Specifically, children’s premorbid anxiety levels may influence the development of PTSS and their report of persistent PCS. Children with high levels of anxiety are more likely to respond to stressors with fear and distress. Additionally, high levels of anxiety are associated with a selective attention to threat and maladaptive cognitive coping strategies, both of which can serve to maintain PTSS and result in reporting PCS. In addition, children who sustain mild TBI may also be influenced in their reactions to brain trauma because of inconsistencies in how researchers, medical professionals, and lay people portray the consequences of TBI. The outcomes of pediatric mild TBI are unknown in a subset of children, though much attention has been placed on the potential serious negative outcomes of injury. This in itself may lay the groundwork for heighted levels of awareness concerning the possible consequences of sustaining TBI. It should be emphasized that the proposed model is not intended to suggest that PTSS reactions are the only means by which children experience PCS outcomes nor is it intended to convey that PTSS accounts for all noninjury-related variance in symptomatology. The degree to which specific factors and mechanisms influence outcomes varies among children, and the current article sought to identify PTSS as an important factor to consider when conceptualizing and diagnosing a child with these symptoms. The present review calls attention to the validity of labeling chronic physical, cognitive, and emotional symptoms after mild TBI as PCS. PCS may be a more appropriate label for the symptoms experienced within 3 months of injury but falsely implies that lasting symptoms are predominantly neurologically related. This exploration of PCS and PTSS highlights the importance of considering chronic symptoms from a psychological perspective and urges healthcare providers and parents to consider traumatic stress as a possible factor in pediatric chronic PCS. Original manuscript received November 25, 2013 Revised manuscript accepted July 9, 2014 First published online August 11, 2014

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