Emotional Aspects of Pediatric Post-Intensive Care Syndrome Following Traumatic Brain Injury

Abstract

Children with traumatic brain injury (TBI) requiring neurocritical care are at risk for neurocognitive, emotional, physical, and psychosocial difficulties, collectively known as Post-Intensive Care Syndrome. Our study assessed parent-reported emotional functioning and identified risk factors for emotional sequelae in the acute recovery phase. Fifty-three children between 5 and 18 years old hospitalized for TBI were assessed 1-month following discharge. Relevant injury-, child-, and family-specific variables were collected. Emotional functioning was assessed using PROMIS Parent Proxy Report Short Forms for Anxiety and Depressive Symptoms. We used Chi-square tests to evaluate differences between children with and without elevations in anxiety and depressive symptoms. Logistic regression determined predictors of elevations in symptoms among significant variables. Parents frequently endorsed moderate or worse anxiety (45.2%) and depressive (32.1%) symptoms among children. Mechanism of injury and elevated parent post-traumatic stress disorder (PTSD) symptoms were associated with elevated anxiety and depressive symptoms, while direct family involvement in the accident/injury was associated only with elevated anxiety symptoms. Results from logistic regression indicated that only elevated parent PTSD symptoms were a significant predictor for child anxiety and depressive symptoms. Anxiety and depressive symptoms are prevalent in the acute recovery phase of TBI. Consistent with previous research, elevations in anxiety and depressive symptoms were more related to psychosocial factors than injury severity. High levels of parent PTSD symptoms and their relationship with children’s internalizing symptoms highlight the need for mental health treatment for TBI patients and their families.

Introduction

Traumatic brain injury (TBI) results in more than 30,000 pediatric neurocritical care admissions in the United States each year (Williams et al. 2019). TBI is the leading cause of mortality and morbidity in children over one year of age, accounts for billions of dollars in annual healthcare costs, and is a known risk factor for long-term disability. Children surviving TBI severe enough to require neurocritical care are at particularly high risk for long-term morbidities due to direct brain injury, as well as Pediatric Intensive Care Unit (PICU) interventions and secondary complications (Williams et al. 2019). Neurocognitive, emotional, physical, and psychosocial difficulties, collectively known as Post-Intensive Care Syndrome in pediatrics (PICS-P), are increasingly described (Manning et al. 2018), but the scope of PICS-P and risk factors for morbidities are less well understood, especially in the TBI population.

Our preliminary work in children following neurocritical care reports high rates of emotional disturbance in the acute phase of recovery, including anxiety (35%), depression (16%), and behavioral changes (26%), and significant correlation between measures of emotional functioning and sleep disturbance, fatigue, quality of life, and cognition (Poppert Cordts et al. 2019; Williams et al. 2017). These findings highlight the interrelatedness of functional domains within the PICS-P framework and indicate that emotional functioning is an important factor in multidimensional recovery in the acute phase. There is a vital need to understand emotional functioning after hospital discharge in children with TBI as anxiety and depression may have a profound impact on recovery trajectories.

Studies of pediatric mild TBI show that in most cases psychological symptoms occur early in recovery and decrease over time with greatest risk for long-term sequelae being those children with previous mild TBIs and/or pre-morbid psychopathology (Emery et al. 2016). The presence of psychological symptoms also predict delayed recovery across domains (Clarke et al. 2012; Grubenhoff et al. 2016). Limited studies including more complicated and severe TBI requiring hospital admission report a somewhat different trajectory for with psychosocial and behavioral difficulties gradually increasing over time (Anderson et al. 2005), highlighting the need for further exploration of risk factors among this subset of TBI patients requiring neurocritical care.

Anxiety and depression may manifest as a result of direct brain injury, from situational factors like mechanism of injury, specific patient factors before or after injury, or a combination. Many studies have suggested that severity of TBI is not predictive of novel anxiety (Max et al. 2011), depressive disorders (Max et al. 2012), internalizing behaviors (Catroppa et al. 2015; Peterson et al. 2013), or emotional/behavioral problems (Anderson et al. 2001). Additionally, neurocognitive impairment has been shown to be only weakly related to depressive symptoms following TBI (Kirkwood et al. 2000). With respect to child factors, younger age has been associated with increased anxiety symptoms (Max et al. 2011; Vasa et al. 2004), while older age, particularly adolescence, has been associated with increased depressive symptoms (Chrisman and Richardson 2014; Max et al. 2012). Despite a higher prevalence of internalizing disorders in females, no sex differences have been found in depressive symptoms after TBI (Chrisman and Richardson 2014; Max et al. 2011). Pre-injury status has also been shown to predict emotional and behavioral functioning following TBI in several studies (Anderson et al. 2001; Catroppa et al. 2015), although they are not always predictive of elevated mood and anxiety symptoms (Luis and Mittenberg 2002).

While there is minimal research examining the impact of mechanism of injury upon emotional functioning in the acute recovery phase, children with TBI requiring neurocritical care are more likely than non-hospitalized TBI patients to have been involved in a motor vehicle accident (McConnell et al. 2020). These high velocity injuries may increase anxiety and depression after TBI by increasing the risk of diffuse axonal injury and concurrent non-brain physical injuries like extremity fractures or abdominal trauma. Concurrent injuries (i.e., polytrauma) contribute to greater morbidity more broadly (Stewart et al. 2013) and may also lead to activity restrictions, which have also been shown to predict poorer emotional outcomes following TBI (Catroppa et al. 2015). MVAs are also more likely to involve other individuals, including parents, resulting in a greater impact to the family as a whole.

It is also critical to consider children within the context of their families. Pre-existing psychosocial factors, such as family environment and parenting style (Yeates et al. 2010), family functioning (Anderson et al. 2001), socioeconomic status (Kirkwood et al. 2000), and family history of anxiety (Max et al. 2012), may impact youth’s emotional and behavioral functioning during recovery from TBI. Given the reciprocal nature of child and family relationships, youth’s injuries and their experience in the PICU can have an impact upon family functioning, as highlighted in the PICS framework for families (PICS-F). Peterson et al. (2013) found elevated psychiatric symptoms in both mothers and fathers of children who have experienced complicated mild to severe TBI, with current parent anxiety symptoms being particularly correlated with adolescent internalizing behaviors. High levels of post-traumatic stress disorder (10–21%) and post-traumatic symptoms (84%) have been found in parents following children’s PICU admission for a broad range of injuries (Nelson and Gold 2012). In parents of children who have received neurocritical care more specifically, focus groups highlight that TBIs are a chronic illness that result in emotional, psychological, and social distress for the whole family (Williams et al. 2018).

Research suggests that ~30% of children have unmet healthcare needs in the year following TBI, with children with less severe TBI experiencing greater unmet needs, including about 1 in 5 with unmet mental health needs (Greenspan and MacKenzie 2000; Slomine et al. 2006). We developed our program, the Pediatric Critical Care and Neurotrauma Recovery Program (PCCNRP), to address this unmet need specifically for the ~90% of children who are discharged back into the community. The PCCNRP is a comprehensive and preventative model of multidisciplinary care that follows children from inpatient admission through their outpatient recovery. We see children shortly after discharge for paired (pediatric neuropsychologist and pediatric critical care physician) follow-up visits to identify concerns related to PICS-P and PICS-F and provide early intervention. See Hall et al. (2020) for more information regarding the PCCNRP clinic model.

The current paper focuses on our efforts to assess psychological and emotional functioning during the acute recovery phase after TBI to guide intervention. We used parent-reported screeners of anxiety and depressive symptoms, and identified risk factors for emotional dysfunction. We focused on examining injury-specific, child-specific, and family-specific variables. For injury-specific variables, we hypothesized that high velocity mechanism of injury would predict increased anxiety and depressive symptomatology. For child-specific variables, we hypothesized age and pre-existing mood/anxiety diagnoses would be associated with elevated anxiety and depressive symptoms. Finally, we hypothesized that elevations in parent PTSD symptoms and direct family involvement in the accident would be associated with elevated anxiety and depressive symptoms.

Method

Participants and Procedures

We conducted a retrospective chart review of 65 consecutive children aged 5 to 18 with a TBI hospitalization between July 2018 and February 2020. Children were included if they completed an acute follow-up visit through the PCCNRP and completed primary outcome measures of anxiety and depressive symptoms. Nine children were lost to follow-up, and three children were excluded for incomplete data. The final sample consisted of 53 children. Patients received a physical and neurological examination conducted by a pediatric critical care physician and a brief neuropsychological evaluation from a pediatric neuropsychologist. The Institutional Review Board at Oregon Health and Science University approved the study procedures with a waiver of informed consent.

Measures

Injury-Related Variables

Medical record review was used to obtain injury-related characteristics including evidence of intracranial findings on neuroimaging, mechanism of injury, first GCS at admission, and time since hospital discharge in months.

Intracranial Findings

The presence or absence of acute intracranial findings were determined by review of imaging records of either head Computed Tomography (CT) or Magnetic Resonance Imaging (MRI) and typically included intracranial hemorrhage, brain edema, diffuse axonal injury, or midline shift. Scalp injuries (e.g., subgaleal hematomas) and incidental findings were not considered an intracranial finding. Additionally, intracranial findings were ruled out if they initially presented on a head CT but were determined to be artifact during a follow-up MRI within 24 h. Three children did not undergo brain imaging during their hospitalization as they did not meet criteria for head CT in the emergency room according to the Pediatric Emergency Care Applied Research Network (PECARN; Kuppermann et al. 2009). These children were admitted to the PICU for polytrauma including mild TBI. The presence of intracranial findings was initially rated independently by three reviewers, who had high inter-rater reliability (ICC = .927). Discrepancies were reviewed and determined via expert consensus.

Mechanism of Injury

Mechanism of TBI was dichotomized into either high or low velocity injuries. High velocity injuries included accidents involving motor vehicles, bicycle or pedestrian versus automobile accidents, and bicycle or all-terrain vehicle (ATV) accidents, whereas low velocity injuries included falls and penetrating injuries.

Glasgow Coma Scale

The Glasgow Coma Scale (GCS; Teasdale and Jennett 1974) is a clinician-rated measure of level of consciousness in TBI consisting of three separate scales that measure eye, verbal, and motor responses. Ratings from each scale are summed to provide a final total score that ranges from three to 15, with higher scores indicating greater levels of consciousness. The GCS is a widely used as an indicator of injury severity, including defining mild (GCS = 13–15), moderate (GCS = 9–12) and severe (GCS = 3–8) TBI. GCS at hospital admission was used in analyses. Complicated mild TBI was defined as mild GCS and the presence of intracranial findings. Given the small number of children experiencing more severe TBIs, the sample was divided into two groups – children with mild (n = 21) or complicated mild (n = 22) TBI (total n = 43) and children with moderate (n = 6) or severe (n = 3) TBI (total n = 9).

Neurocognitive Impairment

Provisional diagnosis of Mild or Major Neurocognitive Disorder during the participant’s acute follow-up visit with the PCCNRP clinic was used to determine the presence of cognitive impairment (i.e., “impaired” or “not impaired”). Provisional diagnoses were made clinically based upon results from a brief neuropsychological screening battery taking into account premorbid functioning. The fixed battery included an estimate of premorbid functioning and assessment of domains of attention, processing speed, working memory, language, memory, and motor functioning. Please see Table 1 for a description of specific neuropsychological measures by domain and age.

Table 1.

PCCNRP neuropsychological screening battery

Neurocognitive domain	5 years	6–7 years	8–16 years	17 +
Estimate of premorbid functioning	WRAT-4 Word Reading	WRAT-4 Word Reading	WRAT-4 Word Reading	WRAT-4 Word Reading
EF: Attention	CMS Numbers - Forward	CMS Numbers - Forward	CMS Numbers - Forward	WAIS-IV Digits - Forward
EF: Processing speed	WPPSI-IV Bug search Cancellation	WISC-V Coding Symbol Search	WISC-V Coding Symbol Search Trails A - Total Time or D-KEFS Trails 2 - Total Time	WAIS-IV Coding Symbol Search Trails A - Total Time or D-KEFS Trails 2 - Total Time
EF: Working memory	CMS Numbers - Backwards	CMS Numbers - Backwards	CMS Numbers - Backwards	WAIS-IV Digits - Backwards
EF: Cognitive flexibility	N/A	N/A	Trails B - Total Time or D-KEFS Trails 2 - Total Time	Trails B - Total Time or D-KEFS Trails 2 - Total Time
EF: Self-monitoring	N/A	N/A	Trails B - Total Errors or D-KEFS Trails 4 - Total Errors	Trails B - Total Errors or D-KEFS Trails 4 - Total Errors
Memory & learning	ChAMP Lists (Im, Delayed, Recall) CMS Numbers - Total	ChAMP Lists (Im, Delayed, Recall) CMS Numbers - Total	ChAMP Lists (Im, Delayed, Recall) CMS Numbers - Total	ChAMP Lists (Im, Delayed, Recall) CMS Numbers - Total
Language	NEPSY-II Word Generation	NEPSY-II Word Generation	D-KEFS Letter Fluency Category Fluency	D-KEFS Letter Fluency Category Fluency
Visual-spatial	As-Needed	As-Needed	As-Needed	As-Needed
Fine motor dexterity	Grooved Pegboard	Grooved Pegboard	Grooved Pegboard	Grooved Pegboard
Parent completed measures	BRIEF-P (Age 5) or BRIEF-2 (Age 6+)

Adapted from Hartman et al. (2020) Table 1. WRAT-4 = Wide Range Achievement Test, Fourth Edition; CMS = Children’s Memory Scale; WAIS-IV = Wechsler Adult Intelligence Scale, Fourth Edition; WISC-V = Wechsler Intelligence Scale for Children, Fifth Edition; WPPSI-IV = Wechsler Preschool & Primary Scale of Intelligence, Fourth Edition; Trails A/B = Trail Making Test A/B; D-KEFS = Delis-Kaplan Executive Function System; ChAMP = Child and Adolescent Memory Profile; NEPSY-II = A Developmental NEuroPSYchological Assessment, Version 2; BRIEF-P = Behavior Rating Inventory of Executive Functioning, Preschool Version; BRIEF-2 = Behavior Rating Inventory of Executive Functinoing, Second Edition

Child-Specific Variables

Participant demographic characteristics collected included age, sex, race/ethnicity, and insurance status (public vs. commercial). Parent report during the evaluation was used to determine premorbid history of an anxiety or mood disorder diagnosis.

Family-Specific Variables

Family factors included involvement in the injury and parent self-report of post-traumatic stress symptoms.

Family Involvement in Injury

Medical record review was used to determine family involvement in the event resulting in the injury, and was characterized as either “direct” or “indirect/no involvement.” Direct involvement was defined as an immediate or extended family member being involved in the activity that directly resulted in the injury (e.g., being in or driving the car or ATV during the accident) or directly impacting the extent of the patient’s injury (e.g., providing cardiopulmonary resuscitation to the patient following an accident). Indirect or no involvement was defined as witnessing the injury or no immediate or extended family member being present during the event that resulted in injury. Ambiguous situations (n = 5) were reviewed by the authors and were determined by consensus. The parent informant may or may not have been the family member involved in the accident.

Parent Post-Traumatic Stress Symptoms

Parent Post-Traumatic Stress Disorder (PTSD) symptomology was assessed via self-report on the Primary Care PTSD Screen for DSM-5 (PC-PTSD-5; Prins et al. 2015). The PC-PTSD-5 is a 5-item screening tool designed to identify patients at risk for PTSD presenting in medical settings. Endorsement of three or more of the five items indicates heightened risk for PTSD. Given the non-normal distribution of scores, they were dichotomized as “elevated” or “not elevated.” Internal consistency for the PC-PTSD-5 in the current sample was deemed good (Cronbach’s α = .837).

Outcome Measures

Patient-Reported Outcomes Measurement Information System (PROMIS) Parent Proxy Short forms (Irwin et al. 2012) were used to assess anxiety and depressive symptoms in children. The PROMIS Parent Proxy Anxiety Short Form (Irwin et al. 2012) is an 8-item measure assessing parent-perceived youth anxiety over the past seven days, while the PROMIS Parent Proxy Depressive Symptoms Short Form (Irwin et al. 2012) is a 6-item measure assessing parent-perceived youth depressive symptoms over the past seven days. Items on each scale are ranked on a 5-point Likert scale that ranges from “1 = Never” to “5 = Almost Always.” Norm-referenced scores are presented as T-scores and categorize anxiety and depressive symptoms as Severe (T ≥ 65), Moderate (T = 55–64), Mild (T = 50–54), and Within Normal Limits (T < 50). These measures have shown good convergent and discriminant validity compared to legacy measures in a pediatric TBI population (Bertisch et al. 2017). As there was a notable floor effect, scores were dichotomized as “elevated” or “not elevated,” where scores falling in the moderate or severe ranges were considered elevated. High internal consistency was seen for both the Anxiety Short Form (Cronbach’s α = .966) and the Depressive Symptoms Short Form (Cronbach’s α = .926) in our study sample.

Statistical Approach

We conducted separate analyses for parent-rated anxiety and depressive symptoms. We utilized chi-square tests, with Fischer Exact correction as needed for expected cell counts less than five, to evaluate differences on all injury-specific, child-specific, and family-specific variables between children with and without elevations in anxiety and depressive symptoms. We then entered significant variables (p < .05) in a binary logistic regression to determine association with elevations in anxiety and depressive symptoms. Results are reported as adjusted Odds Ratios (OR) with 95% Confidence Interval (95% CI).

Results

Children (N = 53; M = 10.7 years, SD = 3.7) were seen for an acute follow-up visit an average of 2 months (SD = .75) after injury. The majority of children had public insurance (58.5%). More than half (64.2%) of the participants identified as Caucasian, while others identified as multiracial (9.4%), Black (7.5%), American Indian/Pacific Islander (7.5%), or Asian (5.7%). Hispanic or Latino ethnicity was endorsed by 13.2% of the sample. Half (52.8%) of children had intracranial findings, 62.3% sustained a high velocity injury, and 41.5% received a provisional neurocognitive disorder diagnosis at follow-up. Half (52.8%) of the participants were male and 18.9% of children had a pre-existing diagnosis of an anxiety or mood disorder. Approximately one quarter (27.8%) of parents self-reported elevated symptoms of PTSD, and approximately one quarter (24.5%) of patients had a family member directly involved in the accident. Parents endorsed elevations in anxiety in 45.2% and depressive symptoms in 32.1% of children.

Association between Risk Factors and Elevated Anxiety Symptoms

Children who experienced a high velocity injury were more likely than children who experienced a low velocity injury to have elevated anxiety symptoms (p = .021) with a medium effect size (ϕ = .317). No associations between anxiety symptoms and other injury characteristics including GCS, presence of intracranial findings, or presence of neurocognitive impairment were found. Child-specific factors, such as age, sex, or premorbid diagnosis, were not associated with elevated anxiety symptoms. In contrast, parents with elevated PTSD symptoms were more likely to rate their child as having elevated anxiety symptoms (p < .001) with a large effect (ϕ = .519). Similarly, when a family member was directly involved in the accident, parents were more likely to endorse elevated anxiety than parents who were not (p = .008) with a medium effect size (ϕ = .362). See Table 2.

Table 2.

Injury-specific, child-specific, and family-specific variables in children with and without elevations in anxiety symptoms

Anxiety symptoms
	No elevation (n = 29)	Elevation (n = 24)	Test value	n	p	ϕ
Injury-specific factors
Glasgow coma score (n, %)a
Mild or complicated mild	25 (86.2%)	18 (78.3%)
Moderate or severe	4 (13.8%)	5 (21.7%)	–	–	.486	–
Intracranial findings (n, %)b
No	12 (44.4%)	10 (43.5%)
Yes	15 (55.6%)	13 (56.5%)	.005	50	.945	.010
Mechanism of Injury (n, %)b
Low velocity injury	15 (51.7%)	5 (20.8%)
High velocity injury	14 (48.3%)	19 (79.2%)	5.33	53	.021	.317
Neurocognitive Impairment (n, %)
No	16 (55.2%)	15 (62.5%)
Yes	13 (44.8%)	9 (37.5%)	.290	53	.590	−.074
Child-specific factors
Age at evaluation (n, %)b
Under 12 years	19 (65.5%)	13 (54.2%)
12 years and older	10 (34.5%)	11 (45.8%)	.707	53	.400	.116
Sex (n, %) b
Male	16 (55.2%)	12 (50%)
Female	13 (44.8%)	12 (50%)	.141	53	.707	.052
Previous diagnosis (n, %)a
No	26 (89.7%)	17 (70.8%)
Yes	3 (10.3%)	7 (29.2%)	–	–	.156	–
Family-specific factors
Parent PTSD symptoms (n, %)b
Not elevated	24 (88.9%)	8 (40%)
Elevated	3 (11.1%)	12 (60%)	12.64	47	<.001	.519
Direct family involvement (n, %)b
No	26 (89.7%)	14 (58.3%)
Yes	3 (10.3%)	10 (41.7%)	6.96	53	.008	.362

^aFisher’s Exact Test; ^bChi-Square Test; PTSD = Post-Traumatic Stress Disorder

We utilized binary logistic regression to assess risk factors for parent-reported elevated anxiety symptoms. Mechanism of injury, parent PTSD symptoms, and family involvement were entered into the model as predictors. The model explained 39.2% (Nagelkerke R²) of the variance in anxiety symptoms, and correctly classified 76.6% of cases. As shown in Table 3, only elevated parent PTSD made a unique statistically significant contribution to the model (OR 9.23; 95% CI 1.79–47.4). This indicated that parents with elevated PTSD symptoms had nine times increased odds of reporting that their child is experiencing elevated anxiety symptoms.

Table 3.

Binary logistic regression analyses predicting elevations in parent-reported anxiety and depressive symptoms

	B	p	Odds ratio (95% confidence interval)
Elevations in anxiety symptoms
Parent PTSD symptoms	2.22	.008	9.23 (1.79–47.4)
Mechanism of injury	1.25	.107	3.50 (.76–16.1)
Direct family involvement	.19	.841	1.21 (.19–7.70)
Elevations in depressive symptoms
Parent PTSD symptoms	1.43	.043	4.16 (1.04–16.6)
Mechanism of injury	1.23	.110	3.42 (.76–15.5)

PTSD = Post-Traumatic Stress Disorder

Association between Risk Factors and Elevated Depressive Symptoms

Children who experienced a high velocity injury were more likely to experience elevated depressive symptoms than those who experienced a low velocity injury (p = .038) with a small to medium effect size (ϕ = .285). Other injury related factors, such as GCS, presence of intracranial findings, and presence of neurocognitive impairment, were not associated with elevated depressive symptoms. Child-specific factors, such as age, sex, and premorbid diagnosis, were also not associated with elevated depressive symptoms. Parents with elevated PTSD symptoms were more likely to have children with elevated depressive symptoms (p = .010) with a medium effect size (ϕ = .375). No association was found between direct family involvement in the accident and elevations in depressive symptoms. See Table 4.

Table 4.

Injury-specific, child-specific, and family-specific variables in children with and without elevations in depressive symptoms

Depressive symptoms
	No elevation (n = 36)	Elevation (n = 17)	Test Value	n	p	ϕ
Injury-specific factors
Glasgow coma score (n, %)a
Mild or complicated mild	29 (82.9%)	14 (82.4%)
Moderate or Severe	6 (17.1%)	3 (17.6%)	–	–	>.999	–
Intracranial findings (n, %)b
No	15 (45.5%)	7 (41.2%)
Yes	18 (54.5%)	10 (58.8%)	.083	50	.773	.041
Mechanism of injury (n, %) b
Low velocity injury	17 (47.2%)	3 (17.6%)
High Velocity Injury	19 (52.8%)	14 (82.4%)	4.29	53	.038	.285
Neurocognitive impairment (n, %) b
No	21 (58.3%)	10 (58.8%)
Yes	15 (41.7%)	7 (41.2%)	.001	53	.973	.005
Child-specific factors
Age at evaluation (n, %) b
Under 12 years	24 (66.7%)	8 (47.1%)
12 years and older	12 (33.3%)	9 (52.9%)	1.86	53	.173	.187
Sex (n, %) b
Male	17 (47.2%)	11 (64.7%)
Female	19 (52.8%)	6 (35.3%)	1.42	53	.234	.163
Previous diagnosis (n, %) a
No	31 (86.1%)	12 (70.6%)
Yes	5 (13.9%)	5 (29.4%)	–	–	.734	–
Family-Specific Factors
Parent PTSD symptoms (n, %) b
Not elevated	25 (80.6%)	7 (43.8%)
Elevated	6 (19.4%)	9 (56.2%)	6.61	47	.010	.375
Direct family involvement (n, %) a
No	28 (77.8%)	12 (70.6%)
Yes	8 (22.2%)	5 (29.4%)	–	–	.734	–

^aFisher’s Exact Test; ^bChi-Square Test; PTSD = Post-Traumatic Stress Disorder

We utilized binary logistic regression to assess the impact of elevated parent PTSD symptoms and mechanism of injury on the likelihood that parent-reported depressive symptoms would be elevated. The model explained 24.7% (Nagelkerke R²) of the variance in depressive symptoms, and correctly classified 74.5% of cases. As shown in Table 3, only elevated parent PTSD symptoms made a unique statistically significant contribution to the model (OR = 4.16; 95% CI = 1.04–16.6). This indicated that parents with elevated PTSD symptoms had 4 times increased odds of reporting that their child is experiencing elevated depressive symptoms.

Discussion

Following pediatric TBI, parents in our study identified elevated anxiety symptoms in nearly half of patients as well as elevated depressive symptoms in one quarter of patients. One quarter of parents reported experiencing elevated PTSD symptoms themselves. These findings demonstrate that psychological and emotional adjustment difficulties are common following TBI for patients and families. Few injury and child characteristics were associated with increased risk of anxiety and depressive symptoms. However, our study did identify high velocity mechanism of injury and family involvement in the trauma as risk factors that could be assessed prior to discharge. Most importantly, our study highlighted the importance of assessing parent stress and PTSD symptoms when evaluating anxiety and depressive symptoms in children during the acute recovery phase of TBI.

Our study found higher prevalence of anxiety (45.2%) and depression (32.1%) symptoms among a subset of PICU survivors with TBI, compared to the 16–28% of the general PICU population which experiences a deterioration in emotional functioning according to a recent review (Rennick and Rashotte 2009), indicating TBI may be a unique risk factor for emotional distress. Our rates were also higher than prior TBI research suggesting prevalence rates of 17–28% for anxiety symptoms (Luis and Mittenberg 2002; Max et al. 2011) and 11–20% of depressive symptoms (Luis and Mittenberg 2002; Max et al. 2012), which may be related to the use of screening measures to capture elevations in symptoms compared to structured interviews to detect novel disorders. Shorter time since injury in the current study may have also contributed to the higher rates of anxiety and depressive symptoms. Consistent with prior TBI research, our study identified greater rates of anxiety symptoms than depressive symptoms. Of note, almost 20% of the participants in the current study had a pre-existing anxiety or mood disorder, which is notably higher than the lifetime prevalence rate for anxiety or depression (8.4%) in the general pediatric population (Bitsko et al. 2018). However, rates of pre-existing diagnoses did not differ between children with elevations in anxiety and depressive symptoms and those without indicating that this alone does not account for our findings. Contrary to our hypothesis, a pre-existing mood or anxiety diagnosis was not associated with elevated anxiety or depressive symptoms in the current study, as has been seen in some previous studies (Anderson et al. 2001; Catroppa et al. 2015).

Consistent with our hypothesis, anxiety and depressive symptoms were more common in high velocity injury than low velocity injury group with a large effect size. The high velocity injury group includes injuries resulting from MVAs, which may have a broader impact on the family. It is easy to imagine why a high velocity injury may lead to increased symptoms of depression, anxiety, and PTSD for the patient and family given the potential for perceived danger of dying, legal ramifications, and high rates of multiple injuries. These factors may explain higher rates of emotional distress in this patient group compared to other mechanisms of TBI.

Factors such as age at injury and severity of injury are inconsistently associated with chronic morbidities following TBI, and our study similarly showed emotional morbidity across injury- and child-specific variables. Consistent with past research (Anderson et al. 2001; Catroppa et al. 2015; Max et al. 2011, 2012; Peterson et al. 2013), neither severity of TBI (i.e., GCS and intracranial findings) nor neurocognitive impairment were associated with elevations in anxiety and depressive symptoms. Of note, the small sample of children with more severe TBIs may have limited our ability to see an impact of TBI severity upon emotional functioning. Child-specific factors, such as age and gender, were also not associated in the current sample. Similar to our findings, Luis and Mittenberg (2002) found no significant relationship between age and novel onset of mood or anxiety disorders, despite associations seen in some studies (Chrisman and Richardson 2014; Max et al. 2011, 2012). Our study found no sex differences in emotional outcomes after TBI, similar to prior work (Chrisman and Richardson 2014; Max et al. 2011).

Our finding of parent PTSD symptoms in one quarter of respondents and strong association with child and adolescent internalizing symptoms following TBI is consistent with prior literature (Peterson et al. 2013). Our results further demonstrate the reality of PICS-F and that youth TBI, hospitalization, PICU interventions, and associated sequelae are a significant life event in the story of an entire family with the potential to negatively and reciprocally impact the well-being of all family members (Williams et al. 2018). Prior research in hospitalized TBI patients also shows that the emotional difficulties identified in our study are persistent and may increase over time (Anderson et al. 2005). Children with TBI and their families require monitoring, follow-up, and support for the entire family system, especially when the circumstances of injury involve family members.

Emerging research has demonstrated that parents especially value neuropsychological consultation in the months following TBI (Dodd et al. 2018; Kirkwood et al. 2017), and our program has built on this research to implement clinical evaluations and interventions to address the psychological domains of PICS-P and PICS-F. Based upon feedback from focus groups (Williams et al. 2018), our clinic hosts a monthly family support group for patients and their family members to connect with other families who have experienced similar traumas. We are also in the process of developing a brief treatment protocol based upon Acceptance and Commitment Therapy principles to help patients and their families adjust to and cope with life after injury. Whether these targeted interventions will be successful is unclear, but this study builds on prior work showing the need for research on interventions to combat the emotional disturbances seen after neurocritical care for TBI in children and their families.

Strengths and Limitations

This study has a number of important strengths. The study benefited from a diverse sample in terms of sex, race/ethnicity, and socio-economic status. Additionally, this study focuses on a unique TBI sample, namely children who received critical care yet were primarily discharged home. The large majority of our clinical sample (86.2%) completed follow-up, which is notably higher than in most research studies. Our sample was representative of the TBI population with regard to severity (81.1% had mild TBI, while 17% had moderate to severe TBI) and premorbid diagnoses of mood or anxiety disorders (18.9% of the sample). Reviewers demonstrated high inter-rater reliability on relevant variables, and various domains were assessed by experts in their respective fields (i.e., a critical care physician and a board-certified neuropsychologist specializing in pediatric TBI). Lastly, outcome variables were assessed using well-established and norm-referenced measures of depressive symptoms and anxiety that have shown good convergent and divergent reliability in a pediatric TBI sample (Bertisch et al. 2017).

There are several important limitations that should be noted. First, this study utilized a relatively small sample size. All of the patients included in the study were served at a single tertiary care center with a unique follow-up program. While this hospital serves a large geographic region of the northwestern United States, generalization of findings to the national or global population of pediatric TBI patients should be made cautiously. Second, this study relied exclusively on parent report of mental health outcomes. Parent and youth agreement on ratings of depressive symptoms and anxiety disorders is poor, and utilizing parent report for internalizing symptoms could contribute to under-detection of symptoms among teens (Cantwell et al. 1997). On the other hand, the current results indicated that parents reporting greater post-traumatic stress symptoms for themselves reported higher depressive and anxious symptoms in their children. While there is likely a bidirectional relationship between parent and child distress, some of the increased symptoms reported in children may be due to parent distress influencing their perception of distress in their child. Third, the same informant was utilized for both predictor and outcome variables, which may contribute to the higher correlations seen in the current study. Last, this study included internalizing symptoms at only one time point in the acute phase of healing after TBI. While this study does not allow for a longitudinal perspective on internalizing symptoms following TBI, this work is critical for the identification and timely intervention for youth that are experiencing mental health challenges following injury.

Conclusions and Future Directions

The current study highlights the identification of elevated anxiety and depressive symptoms that warrant treatment in children following hospitalization for TBI. Brief assessment and consultation in the acute phase of healing is an efficient way to identify emotional difficulties early, triage as appropriate, and potentially alter the long-term trajectory of these patients. Patients with high velocity mechanisms of injury and with concurrent family involvement and stress may be particularly at risk for these emotional sequelae. We recommend acute follow-up care for all patients and parents seen in the PICU for TBI and future research studies should investigate optimal assessment procedures and triaging of these patients, as well as optimal intervention strategies.

Funding

This work was supported by the Agency for Healthcare Research and Quality (grant number K12HS022981 to CW); and the National Heart, Lung, and Blood Institute (grant number K12HL133115 to JP).

Compliance with Ethical Standards

Conflict of Interest

On behalf of all authors, the corresponding author states there is no conflict of interest.