Caregiver-report of symptoms following traumatic brain injury in a small clinical sample of preschool-aged children

1. Introduction

Traumatic brain injury is prevalent in preschool-aged children and has important repercussions. The incidence of traumatic brain injury (TBI) is higher in children under the age of five years than in any other age group [1]. According to the Center for Disease Control, in 2009–2010, in the United States, the number of TBI-related emergency department (ED) visits in children 4 years of age or younger was 2193.8 per 100,000 [2]. Several studies have documented that preschool-aged children with moderate-severe TBI often show adverse cognitive-behavioral sequelae years after the injury [3, 4, 5, 6, 7]. Even mild brain injury in this population has been associated with weaknesses in cognitive and emotional functioning within the first year post-injury [8, 9, 10] and later [11, 12], highlighting the importance of identification and treatment of TBI in young children.

Given the importance of TBI in preschool-aged children, it is critical that TBI is accurately diagnosed in this age group. For children, parental report of post-injury symptoms plays an important role in diagnosis and management of TBI [13]. For older children with TBI, parents and providers typically reference symptoms listed on post-concussive symptom inventories, given that symptoms commonly associated with concussion, or mild TBI (mTBI), are applicable to children with more severe injuries as well [14, 15]. However, the parent-report pediatric TBI symptom inventories have only been validated with parents of children as young as 5 or 6 years old [16, 17], and applicability of common post-TBI symptom measures to preschool-aged children has not been fully explored.

While parent-report post-concussion symptom chec- klists have not been formally validated in preschool-aged children, some investigators have applied them to this age group, providing some preliminary information on how they perform. McKinlay and colleagues conducted a comparison of parent report of symptoms following mTBI in preschool versus school-aged children as assessed by a mailed version of the Rivermead Post-Concussion Symptom Questionnaire (RPCSQ) [18]. They found that parents of preschool-aged children reported fewer symptoms than parents of school-aged children. Using the Post Concussion Symptoms Inventory (PCSI) by telephone interview, Barlow et al. found that children under age 6 years with mTBI had faster resolution of post-concussive symptoms than older children, though in their study the younger children also had less severe injuries [19]. While it is possible that younger children have fewer symptoms and symptom duration is shorter after mTBI compared to older children, poor sensitivity of the current symptom inventories to the experience of younger children with mTBI could also underlie the findings reported by both McKinlay and Barlow.

The concern that standard pediatric post-concussion symptom inventories are not adequately sensitive for preschool-aged children was identified by Barlow et al. [19]. They identified that parents of younger children often report symptoms post-injury which are not typically thought of as TBI-associated symptoms and are not captured by the current standardized assessments. Barlow et al. specifically listed “change in feeding” and “being fussy” as symptoms identified by parents of preschool-aged children with mTBI; it is a gap in the literature that there is no further qualitative description of symptoms reported by caregivers of young children with TBI.

The purpose of the present study was to begin to address this gap by providing further qualitative description of symptoms experienced following TBI in preschool-aged children based not only on use of a standard post-concussive symptom inventory but also as reported by caregivers in response to open-ended questions, in order to capture symptoms that are not identified by current standardized assessments. We report post-injury symptoms manifested by preschool children with brain injury who received care in an outpatient brain injury specialty clinic based on interview with the child’s caregiver. We hypothesized that, in addition to endorsement of symptoms contained in a post-concussive symptom inventory, a constellation of other post-TBI symptoms would be identified through caregiver report.

2. Methods

This retrospective medical record review study was approved by the local Institutional Review Board.

3. Results

Table 2 summarizes the percentage of participants who experienced one or more symptoms in each of the ACE domains. Physical, emotional, and sleep symptoms as detailed by the ACE were commonly reported to have occurred at some point after injury, whereas the ACE cognitive symptoms were less commonly endorsed. Report of symptoms in all domains was less frequent when considering only the week preceding the clinic visit; however, the majority of caregivers reported at least one current emotional or physical symptom. Cognitive symptoms remained the least frequently reported symptoms.

Frequency of report of individual symptoms within the physical, cognitive, emotional, and sleep ACE domains are also displayed in Table 2. Within the physical domain, the most commonly reported symptom ever observed was headache, followed by fatigue and vomiting. Within the week prior to evaluation, headache remained the most commonly reported symptom and was reported for approximately one third of the children. The two children with repeat TBI comprised 40% of the children for whom balance concerns persisted at the time of evaluation. Within the emotional domain, irritability was most commonly reported ever after injury and within the last week prior to evaluation. Sleeping more than usual was the most commonly reported symptom within the sleep domain ever after injury; however, by the time of evaluation sleeping less than usual was more common. While few symptoms were endorsed within the cognitive domain, difficulty remembering was reported by 18% of the caregivers at some point after injury.

In addition to the ACE physical, cognitive, emotional, and sleep symptoms, 82% of caregivers reported other symptoms. The descriptions of these other symptoms are presented in Table 3 along with the percentage of children who displayed each symptom. The other symptoms which were most frequently reported as occurring ever after injury were decreased engagement, behavioral dysregulation, and increased dependence. In the week prior to the evaluation, behavioral dysregulation and increased dependence remained common (reported for 25% and 18% of children respectively); however, decreased engagement was not reported for any children.

4. Discussion

This study of children 3 to 5 years old presenting to an outpatient specialty brain injury clinic after sustaining a TBI indicates that preschool-aged children display many of the symptoms commonly exhibited by older children and adolescents across the spectrum of severity of TBI, such as headaches, fatigue, and irritability [15, 20]. In addition, as hypothesized, we found that caregivers of preschool-aged children with TBI commonly report other symptoms which are not captured on traditional TBI symptom inventories. This is consistent with the concern raised by Barlow et al. [19], and the current work advances the field by beginning to describe “atypical” symptoms reported across a small cohort of young children. It is possible that not accounting for these less traditional symptoms accounts for reports of quicker recovery/less symptom reporting in this age group [18, 19, 21] despite later adverse outcomes reported for even mild injuries in preschool-aged children [11, 12].

Many of the common post-TBI symptoms listed on the ACE form may represent abstract concepts that preschool-aged children would not be expected to understand or express, for example, “balance difficulties” or “difficulty concentrating”, such that in this age group, symptom report is dependent on caregiver observation/report. Some of the other symptoms reported for these young children may be relatively straightforward in representing a different presentation of an otherwise common post-TBI symptom. For example, stomachaches and appetite changes may be manifestations of nausea, anxiety, or more generalized malaise. Similarly, increased dependence, including behaviors such as being more clingy and requesting more help, may signify that a child is anxious or doesn’t feel well but may be unable to verbalize that information.

Of symptoms not captured by the ACE, behavioral concerns were most common. Atypical behaviors fell on both sides of a spectrum, from decreased engagement with being quieter than usual to behavioral dysregulation with temper tantrums, non-compliance, and physically aggressive behaviors. A pattern commonly observed was that decreased engagement was reported earlier post-injury; no caregivers reported that decreased engagement persisted in the week prior to evaluation. Following the phase of decreased engagement, behavior dysregulation often emerged and persisted, being among the mostly commonly reported symptoms still present at the time of the evaluation, on average one month post-injury. Given the association of TBI in this age group with later difficulties with cognitive-behavioral regulation [6, 22, 23], behavioral dysregulation may be particularly important to monitor closely over time. As with some of the physical symptoms reported, these behavioral symptoms too may overlap with more traditionally described symptoms, with decreased engagement perhaps representing fatigue or feeling slowed down and behavioral dysregulation including aspects of irritability and increased emotionality. Alternatively, these behavioral symptoms may be important markers of injury severity, with decreased engagement reflecting presentation of the decreased initiation observed early after more severe injury in older children and behavioral dysregulation heralding persisting difficulties with cognitive and behavioral control [24]. Another possibility is that these symptoms, as reported by the child’s caregiver, are a marker of changes in parent-child interactions following a child’s injury. As the quality of parent-child interactions has been proposed as a contributor to outcomes after injury [7, 25, 26], this too represents an important piece of the clinical picture. Further work is needed to understand the implication of these symptoms for later outcomes.

Some symptoms, such as enuresis representing a regression in toilet-training, may have multiple contributions. While difficulty concentrating was not strongly endorsed for this sample, perhaps due to limited expectations for the same in this age group, enuresis may occur because a child attends less or responds less quickly to their bodily signals regarding need to void. Alternatively, a diffuse brain injury, as occurs in TBI, may temporarily disrupt the relatively newly learned coordination required for continence.

Many of the typical post-TBI symptoms were reported with similar frequency to that described for preschoolers with mTBI by McKinlay et al. [18], despite the inclusion of children with more severe injuries in the current sample. The symptoms reported for the two children with repeat TBI generally appeared similar to those of the children with a single injury, though both children were among the 18% of children for whom balance remained a concern at the time of the clinic visit. There were some symptoms which are commonly reported by older children with TBI that were identified with low frequency in this sample. Physical symptoms that were infrequently reported included dizziness, sensitivity to light and noise, and numbness/tingling. The experience of these symptoms is likely hard for a young child to describe, and a caregiver may be more apt to notice generalized irritability rather than identifying a link between behavior and specific environmental stimuli. Additionally, cognitive symptoms, specifically ‘feeling mentally foggy’ and ‘difficulty concentrating’, were never/rarely reported, respectively, again likely due to these being concepts that a young child is unlikely to express and due to lack of demands/expectation for sustained attention in this age group.

While the descriptions of other symptoms reported by caregivers of preschool-aged children with TBI may reflect different expression of well-recognized post-TBI phenomena, it remains critical to raise awareness that young children and their caregivers may report physical symptoms and changes in behavior which clinicians and researchers may not readily associate with TBI. For example, in the absence of observed trauma, a mTBI may not be suspected in a child presenting with behavioral withdrawal and enuresis. Even in the setting of a known trauma, these symptoms may be attributed to other etiologies, such as a change in the child’s routine, rather than TBI. Failure to recognize a mTBI would result in not modifying a child’s activities as needed to manage symptoms and prevent repeat injury during recovery and thus may result in additional morbidity. Alternatively, it is possible that some or all of the identified symptoms represent a child’s response to trauma more globally, rather than being specific to TBI, although other recent work focused on sleep symptoms showed that sleep problems were more common in young children after TBI compared to children with orthopedic injuries [27]. Clarifying what symptoms in this age group are related to the experience of trauma but not TBI in particular will be a critical next step in this line of work. Future work including a non-TBI injury control group is needed to identify the specificity of these symptoms in order to optimize evaluation and management of TBI in this age group. Future work should also consider inclusion of a non-injury control group to determine the baseline frequency of these symptoms in this age group.

In addition to the primary limitation of the lack of a control group, the retrospective nature of this work limits the ability to provide a detailed timeline for presence and resolution of the symptoms described. Furthermore, the small, clinical, convenience sample did not allow exploration of the impact of child (e.g. age, pre-injury diagnoses/behaviors), family (e.g. caregiver demographics, caregiver/child interactions, litigation), and injury (e.g. severity) factors on symptom reporting. Symptom report was not obtained from other caregivers, such as daycare providers, though doing this in future work may help discern the possible role of change in parent-child interactions in parent-report of child’s symptoms.

5. Conclusion

Preschool-aged children with TBI exhibit many of the commonly described post-concussive symptoms. In addition, these children appear to show behavioral and physical symptoms which may not be readily associated with TBI. The current findings highlight the need for additional attention to the presentation of TBI in preschool aged children. Further work is needed to evaluate symptoms of TBI in this age group, including the specificity of symptoms for TBI in comparison to other forms of trauma, in order to optimize detection and management of TBI in young children.