Behavior Problems following Childhood TBI: The Role of Sex, Age, and Time since Injury

Abstract

Objective:

To examine the frequency of behavioral problems after childhood traumatic brain injury (TBI) and their associations with injury severity, sex, and social environmental factors.

Setting:

Children’s hospitals in the Midwestern/Western United States.

Participants:

381 boys and 210 girls with moderate (n = 359) and severe (n = 227) TBI, with an average age at injury of 11.7 years (range 0.3-18) who were injured in ≤ 3 years ago.

Design:

Secondary data analysis of a multi-study cohort.

Main Measures:

Child Behavior Checklist (CBCL) administered pre-treatment.

Results:

Thirty-seven percent had borderline/clinical elevations on the CBCL Total Problem Scale, with comparable rates of Internalizing and Externalizing problems (33% and 31%, respectively). Less parental education was associated with higher rates of internalizing, externalizing, and total problems. Time since injury had a linear association with internalizing symptoms, with greater symptoms at longer post injury intervals. Younger boys had significantly higher levels of Oppositional Defiant symptoms than girls; whereas older girls had significantly greater ADHD symptoms than boys.

Conclusion:

Pediatric TBI is associated with high rates of behavior problems, with lower socioeconomic status predicting substantially elevated risk. Associations of higher levels of internalizing symptoms with greater time since injury highlights the importance of tracking children over time.

INTRODUCTION

Childhood traumatic brain injury (TBI) is linked to a range of emerging behavioral and emotional difficulties, including attention problems, conduct disorders, anxiety, post-traumatic stress, and depression. Secondary attention-deficit hyperactivity disorder (SADHD) occurs in an estimated 15-20% of children following moderate to severe TBI, particularly following more severe injury.^1,2 Internalizing difficulties affect up to 25% of school-aged children following TBI^3–6, with factors such as lower socioeconomic status, family history of anxiety disorders, and older age at injury conferring greater risk.^3,7 Neurocognitive and behavioral deficits contribute to impaired social competence, characterized by fewer friendships and lower levels of social participation.^8–11

Greater injury severity, earlier age at injury, and higher levels of social disadvantage and family dysfunction also are linked to higher levels of behavior problems following TBI. Some, but not all, studies indicate that children with severe TBI have higher rates of both internalizing and externalizing difficulties including SADHD^12–14 compared to those with less severe TBI. Although several studies link younger age at injury to poorer behavioral outcomes, including symptoms of anxiety, ADHD, and other externalizing behaviors,^4,15–18others have failed to detect significant associations between age at injury and behavioral impairments,^19,20 perhaps in part due to the timing of assessments and the potential for emerging deficits with increasing time post injury.^2,20 Although earlier age at injury has been associated with higher levels of behavior problems,^15,16 one study linked older age at injury to depression onset, potentially reflecting the increased incidence of depression in adolescents relative to younger children.³

Environmental factors have also been associated with behavioral functioning. Better family functioning and resources, including higher levels of income and education, have been consistently linked to fewer behavior problems and better functioning after childhood TBI.^21,22 Parental education is an important marker of the home environment and predictive of TBI outcomes, although proximal family characteristics such as parental disciplinary practices and parent-child interactions provide additional predictive value.^23–26

Evidence regarding sex differences in behavioral impairments after pediatric TBI is limited. Although females may experience more protracted acute recovery as indicated by significantly longer stays in the intensive care unit, and display a trend for more frequent admission to inpatient rehabilitation, longer-term studies have indicated few, if any, sex differences in recovery after pediatric TBI.^27–29 However, males may be more likely to develop clinically significant behavior problems than females several years after injury³⁰ and may be more likely to have problems at school.³¹ But findings are mixed, with differences disappearing at later time points post-injury or when outcomes are assessed using more rigorous diagnostic interviews.^29,32 In contrast, females may be more likely to develop new-onset internalizing problems, including post-traumatic stress²⁹ and obsessive-compulsive symptoms,³³ which may reflect female vulnerability to these conditions in the general population. Prior research has not considered how the presentation of behavior problems following pediatric TBI might vary in girls versus boys as a function of age at or time since injury; however, research on developmental psychopathology suggests the potential for higher rates of internalizing symptoms and depression in females during adolescence compared to earlier in childhood.³⁴

Using data collected from seven cohorts described in greater detail below, we examined the association of host (sex), injury (severity, age at injury, time since injury), and environmental characteristics (parent education) with parent-rated symptoms on the Child Behavior Checklist (CBCL). This uniquely large multi-study cohort of children with TBI allows for examination and characterization of common behavioral profiles following pediatric TBI and how they differ based on children’s age, sex, injury severity, and premorbid characteristics. To better understand how these factors acted in concert, we also examined the interactions of these factors in relation to our outcomes of interest.

Based on the extant literature, we sought to test the following hypotheses: (1) Children injured at an earlier age and those from lower SES households will have higher rates of clinically significant behavior problems across domains; (2) Girls will be rated as having higher rates of internalizing problems and boys will be rated as having higher rates of externalizing problems and social competence deficits, particularly in adolescence.

METHOD

Overview.

This was a cross-sectional evaluation of data from the baseline visit of seven RCTs (including Online, CDC, TOPS-Original, CAPS, TOPS-RRTC, I2-Pilot, and I2-RRTC) of family-centered interventions for pediatric TBI involving 591 children between the ages of 3 and 18 years. This project was approved by the Institutional Review Board and de-identified data were used in all analyses. Data were collected between October 29 2003 and Jan 6 2015, and analyses were completed in 2017-2019. All data reported were collected after informed consent was obtained and prior to randomization and initiation of treatment. Members of the current analysis team significantly contributed to the design of all seven RCTs, which were conducted in the Midwestern/Western United States. The remarkable consistency of methods across studies minimizes potential difficulties typical of individual participant data meta-analyses of collections of observational data,³⁵ allowing us to focus on high-quality studies with readily available data and consistent recruitment and measurement procedures, as recommended by others.³⁶

Table 1 provides the recruitment criteria for the studies. Potentially eligible children were identified using the Trauma Registries of participating hospitals. Because the interventions targeted immediate and potential consequences of TBI, eligibility did not require current behavioral concerns. All participants were hospitalized overnight following TBI and met criteria for complicated mild (Glasgow Coma Scale score [GCS] of 13-15 with positive findings on imaging) to severe TBI (lowest GCS score of 3-8). We restricted the sample to those children whose baseline measurements were collected within three years of injury, excluding a small number (n=33) of children whose time since injury was substantially larger and age at injury younger than most other children in the analysis.

Table 1:

Recruitment Summary by Study

Characteristic	Online	CDC	TOPS-Original	CAPS	TOPS-RRTC	I2-Pilot	I2-RRTC
Full Study Name	Online Problem Solving	Group versus Individual Problem Solving	Teen Online Problem Solving	Counselor Assisted Problem Solving	Teen Online Problem Solving Multisite Study	Positive Parenting Skills Pilot	Positive Parenting Skills Multisite Study
Na	43	85	50	132	152	37	113
Datesb	2003-4	2005-6	2006-9	2007-11	2010-14	2009-11	2010-15
Typical Procedurec	Recruitment from a trauma registry or during inpatient hospitalization/rehabilitation, with potential participants contacted by letter with follow-up by phone or in person at a clinic
Procedure Anomaliesd	No inpatient recruitment or in-person follow-up	Additional recruitment at neurosurgery follow-up clinic, but no inpatient recruitment	No inpatient recruitment			Additional recruitment at a child abuse follow-up clinic	Additional recruitment at a child abuse follow-up clinic
Age (years)	5-18	5-18	11-18	12-17	11-18	3-9	3-9
Time Since Injury (months)	0-24	0-24	0-24	0-7	0-18	0-119	0-119
Injury Severityc,e	Overnight hospitalization, GCS score < 13 or 13-15 with positive neuroimaging findings
Typical Exclusionary Criteriac	Abusive head trauma, insufficient recovery for child to participate, significant pre-injury intellectual impairment, pre-injury psychiatric hospitalizations, parent hospitalized for psychiatric reasons in past year
Exclusionary Criteria Reductionsf	Pre-injury intellectual impairment, pre-injury psychiatric hospitalizations, and parent hospitalization for psychiatric reasons	Pre-injury psychiatric hospitalizations, and parent hospitalization for psychiatric reasons				Abusive head trauma	Abusive head trauma
Participation rate	0.55	0.39	0.48	0.72	0.47	0.43	0.46

^aN = number of participants assessed at baseline,

^bDates = dates of baseline assessment,

^cApplies to all studies,

^dProcedure Anomalies = recruitment in addition to typical procedures, or other deviations,

^eInjury Severity inclusionary criterion was identical for all studies,

^fExclusionary Criteria Reductions = typical exclusionary criteria that were not applied.

Measures

Background Interview.

Using consistent procedures across studies, the primary caregiver completed a background interview regarding the child’s medical and educational history, including premorbid ADHD and other emotional and behavioral problems. They also provided information regarding the highest level of education completed by the primary caregiver, which served as our proxy measure of SES.

Injury Information:

Using consistent procedures across studies, a trained research coordinator reviewed the medical chart and abstracted information regarding injury mechanism, length of stay, and lowest GCS score. Any discrepancies regarding injury severity or mechanism were resolved through discussion among the investigative team for that study.

Child Behavior Checklist (CBCL).

At baseline and follow up assessments, parents completed the CBCL,³⁷ reporting on their child’s behavior problems and overall competence during the previous six months. The CBCL has high validity and reliability and was selected by the NINDS Common Data Elements Working Group to assess behavior problems following pediatric TBI.³⁸ The 99-item preschool form was used for children < 6, and the 112-item school age form was used for children ≥ 6. Both versions have similar items providing continuity between forms.³⁷ We report rates of borderline or clinically elevated problems using age-specific norms that make results consistent across versions.^15,16,30,39 The Internalizing and Externalizing scales comprise several individual subscales. Specifically, the Internalizing scale includes the Withdrawn, Somatic Complaints, and Anxiety/Depressed Problems subscales, whereas the Externalizing scale includes the Delinquent and Aggressive behavior subscales. The Total Competence scale reflects participation in activities, academic functioning, and social engagement. We describe rates of Internalizing, Externalizing, and Total Problems, as well as Total Competence deficits and elevations on syndrome (anxious/depressed, somatic complaints, withdrawn, attention problems, and aggressive behaviors) and DSM-oriented scales (Affective Problems, Anxiety Problems, Attention Deficit/Hyperactivity Problems, Oppositional Defiant Problems). Based on the CBCL manual and prior research^15,16,30,39, we defined scores on the Total, Internalizing and Externalizing scales as borderline if the T score was between 60 and 63, and as elevated if it exceeded 63. For the DSM-oriented subscales, scores of 65 to 69 were considered borderline and scores of 70 and greater were clinically elevated. For Total competence, where lower scores reflected poorer functioning, T scores of 37 to 40 were considered borderline and those less than 37 were considered to fall in the clinical range. Multivariable models examined correlates of CBCL DSM- and summary scales.

Home and Community Social Behavior Scale (HCSBS).

Child prosocial adaptive behaviors were measured via the Social Competence Scale of the Home and Community Social Behavior Scales (HCSBS) parent rating form. Parents completed this well-validated instrument (relative to other social behavior measures).⁴⁰

Statistical Analysis

To characterize the nature and frequency of behavior problems in children who sustained TBI, we dichotomized the CBCL outcomes (internalizing and externalizing problems, total competence), syndrome, and DSM-oriented scales as borderline or clinically significant deficit versus no deficit based on recommended cutoffs.³⁷ The proportion of children with deficits were estimated with two-stage random-effects meta-analysis techniques,⁴¹ both overall and within characteristic groups. To increase statistical power, we combined children with complicated mild and moderate TBI in these analyses based on previous findings suggesting similar outcomes in these two groups.⁴²

We examined associations of continuous CBCL and DSM-oriented scale T-scores as well as HCSBS social competence T-score with child age, time since injury, parental education, and injury severity via generalized linear models with study-specific random intercepts as required to account for cross-study heterogeneity.⁴³ Normal distributions were utilized for the CBCL scales and HCSBS social competence, and data transformation using gamma distributions with the identity link were used to accommodate the right skew of the DSM-oriented scales. Study-specific random covariate effects, quadratic terms for time since injury, and second-order interactions were initially included, and iterative backward elimination was used to remove nonsignificant terms. Post-hoc univariate analyses examined statistically significant effects via random effects logistic regression. We assessed model adequacy through residual diagnostics. All analyses were conducted using SAS version 9.4 (SAS Institute, Cary, NC). Results with p<0.05 were considered statistically significant, without formal adjustments for multiple testing. The statistical computing environment R was used to create figures.⁴⁴

RESULTS

Sample Characteristics

As reported in Table 1, study participants ranged from 3-18 years of age at time of the assessment. Of the 578 participants for whom CBCL data were available, 71 were rated on the early childhood version and 507 were rated on the school-age version. All but two studies focused on children injured within the past 24 months, with an average time since injury of 0.5 years (SD = 0.5). Approximately 40% of participants across studies had severe TBI, while the remaining 60% had complicated mild or moderate injuries. Table 2 also describes preinjury history of ADHD and/or other emotional/behavioral problems.

Table 2:

Baseline Characteristics by Study; Count (%) or Mean (SD)

characteristic	All	Online	CDC	TOPS_Original	CAPS	TOPS_RRTC	I2_Pilot	I2_RRTC
Na	591	43	85	50	132	152	26	103
Site
Cincinnati	280 (47.4)	43 (100.0)	66 (77.6)	25 (50.0)	45 (34.1)	41 (27.0)	26 (100.0)	34 (33.0)
Cleveland	87 (14.7)	0 (0.0)	0 (0.0)	0 (0.0)	41 (31.1)	35 (23.0)	0 (0.0)	11 (10.7)
Columbus	104 (17.6)	0 (0.0)	0 (0.0)	25 (50.0)	0 (0.0)	47 (30.9)	0 (0.0)	32 (31.1)
Denver	91 (15.4)	0 (0.0)	0 (0.0)	0 (0.0)	36 (27.3)	29 (19.1)	0 (0.0)	26 (25.2)
Mayo Clinic	10 (1.7)	0 (0.0)	0 (0.0)	0 (0.0)	10 (7.6)	0 (0.0)	0 (0.0)	0 (0.0)
Pittsburgh	19 (3.2)	0 (0.0)	19 (22.4)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)
Male	381 (64.5)	26 (60.5)	58 (68.2)	27 (54.0)	86 (65.2)	107 (70.4)	16 (61.5)	61 (59.2)
Caucasian	471 (79.7)	32 (74.4)	72 (84.7)	44 (88.0)	106 (80.3)	122 (80.3)	15 (57.7)	80 (77.7)
Child Ethnicity
Hispanic/Latino	32 (5.4)	0 (0.0)	0 (0.0)	2 (4.0)	6 (4.5)	12 (7.9)	2 (7.7)	10 (9.7)
Not Hispanic/Latino	558 (94.6)	43 (100.0)	84 (100.0)	48 (96.0)	126 (95.5)	140 (92.1)	24 (92.3)	93 (90.3)
Primary Caregiver
Father	46 (7.8)	5 (11.6)	1 (1.2)	4 (8.0)	13 (9.8)	18 (11.8)	1 (3.8)	4 (3.9)
Mother	528 (89.3)	38 (88.4)	80 (94.1)	45 (90.0)	115 (87.1)	132 (86.8)	24 (92.3)	94 (91.3)
Other	17 (2.9)	0 (0.0)	4 (4.7)	1 (2.0)	4 (3.0)	2 (1.3)	1 (3.8)	5 (4.9)
Parental Educationb
<HSc	44 (7.4)	10 (23.3)	6 (7.1)	3 (6.0)	9 (6.8)	9 (5.9)	2 (7.7)	5 (4.9)
HSc/GEDd	217 (36.7)	13 (30.2)	43 (50.6)	16 (32.0)	52 (39.4)	53 (34.9)	14 (53.8)	26 (25.2)
>HSc	330 (55.8)	20 (46.5)	36 (42.4)	31 (62.0)	71 (53.8)	90 (59.2)	10 (38.5)	72 (69.9)
Married	354 (59.9)	20 (46.5)	56 (65.9)	33 (66.0)	82 (62.1)	89 (58.6)	14 (53.8)	60 (58.3)
Age at Injury (years)	11.7 (4.3)	10.2 (3.2)	11.5 (3.6)	13.8 (2.4)	14.5 (1.7)	14.4 (2.1)	4.2 (2.1)	5.7 (2.0)
Time Since Injury (me)	0.5 (0.5)	1.1 (0.6)	0.4 (0.3)	0.8 (0.4)	0.3 (0.1)	0.5 (0.3)	1.2 (0.9)	0.5 (0.4)
TBI Severityf
Moderate/ComplMildg	359 (61.3)	28 (70.0)	53 (63.9)	30 (60.0)	81 (61.4)	85 (55.9)	20 (76.9)	62 (60.2)
Severe	227 (38.7)	12 (30.0)	30 (36.1)	20 (40.0)	51 (38.6)	67 (44.1)	6 (23.1)	41 (39.8)
ADHD Premorbidf
Yes	77 (13.0)	5 (11.6)	17 (20.0)	3 (6.0)	19 (14.4)	22 (14.5)	2 (7.7)	9 (8.7)
No	510 (86.3)	36 (83.7)	68 (80.0)	47 (94.0)	112 (84.8)	130 (85.5)	24 (92.3)	93 (90.3)
Other E/Bh Premorbidf
Yes	35 (5.9)	0 (0.0)	7 (8.2)	4 (8.0)	9 (6.8)	12 (7.9)	0 (0.0)	3 (2.9)
No	509 (86.1)	0 (0.0)	78 (91.8)	46 (92.0)	122 (92.4)	138 (90.8)	26 (100.0)	99 (96.1)

^aN = number of participants assessed at baseline with time since injury less than 3 years,

^bParental Education = reported education of the primary caregiver,

^cHS=High School,

^dGED = General Education Diploma,

^em = months,

^fUnknown values omitted from display but included in percentage calculation,

^gModerate/Compl = Moderate or Complicated Mild TBI,

^hE/B = Emotional/Behavioral.

As reported in Table 3, 37% of children had borderline or clinical elevations on the Total Problem Scale, with comparable rates of Internalizing and Externalizing problems (33% and 30%, respectively). Forty-four percent had significant deficits in total competence. Approximately 1 of 5 children had elevated scores on the DSM-oriented Affective (24%), Somatic (21%), Conduct scales (21%), and Attention Problems subscales (21%).  

Table 3:

Borderline/Clinical Behavioral Problems by Gender and Injury Severity; Number/Total (% based on meta-analysis)

Subscale	All	Female		Male
		Moderate/ComplMilda	Severe	Moderate/ComplMilda	Severe
Internalizing	186/576 (32.5%)	37/127 (30.5%)	31/76 (43.0%)	68/222 (31.4%)	49/147 (34.0%)
Externalizing	173/576 (30.4%)	33/127 (26.6%)	25/76 (34.4%)	65/222 (31.1%)	48/147 (34.3%)
Total Problems	211/576 (37.0%)	44/127 (34.5%)	35/76 (46.9%)	73/222 (33.5%)	58/147 (43.0%)
Total Competence	191/447 (44.4%)	37/96 (38.7%)	22/64 (35.2%)	80/181 (45.8%)	51/102 (50.2%)
Syndrome Scales
AnxiousDep	79/576 (14.0%)	12/127 (10.3%)	13/76 (18.7%)	31/222 (14.7%)	22/147 (16.0%)
WithdrawnDep	90/576 (16.1%)	18/127 (16.2%)	16/76 (22.6%)	32/222 (14.9%)	23/147 (17.6%)
SomaticCompl	116/576 (20.6%)	30/127 (24.9%)	18/76 (25.8%)	36/222 (17.0%)	31/147 (21.9%)
SocialProb	89/505 (17.9%)	19/110 (19.2%)	11/69 (19.9%)	31/195 (17.8%)	28/127 (23.5%)
ThoughtProb	107/505 (21.4%)	19/110 (18.5%)	16/69 (24.5%)	37/195 (19.5%)	35/127 (28.3%)
AttentionProb	118/576 (20.7%)	27/127 (22.8%)	23/76 (33.8%)	39/222 (18.5%)	29/147 (20.9%)
RuleBreakingBeh	78/505 (15.7%)	14/110 (14.5%)	13/69 (20.8%)	29/195 (16.4%)	22/127 (17.9%)
AggressiveBeh	99/576 (17.7%)	17/127 (14.4%)	17/76 (25.1%)	37/222 (19.1%)	27/147 (19.4%)
DSM-Scales
Affective	134/576 (23.7%)	25/127 (22.0%)	26/76 (35.1%)	44/222 (20.5%)	38/147 (27.0%)
Anxiety	86/576 (15.2%)	13/127 (11.9%)	8/76 (12.6%)	37/222 (17.7%)	27/147 (20.0%)
Somatic	106/505 (21.1%)	24/110 (22.7%)	17/69 (27.5%)	39/195 (20.7%)	24/127 (20.1%)
ADHD	109/576 (19.4%)	27/127 (22.6%)	18/76 (25.3%)	37/222 (17.6%)	26/147 (18.9%)
OppDefiant	94/576 (16.6%)	17/127 (15.3%)	12/76 (17.6%)	36/222 (17.5%)	27/147 (19.2%)
Conduct	105/505 (21.4%)	20/110 (19.4%)	16/69 (25.2%)	39/195 (22.4%)	29/127 (23.5%)

^aModerate/Compl = Moderate or Complicated Mild TBI, Numerator represents participants with borderline or clinical score across all studies. Denominator represents all participants with the corresponding measure across all studies. Percentage represents the average percent of participants with a borderline or clinical score, as estimated via random effects meta-analysis with a logistic transformation.

Associations with SES, Injury Severity, Age, Sex, and Time Since Injury

In multivariable models (see Table 4), higher levels of parent education were associated with lower levels of Total, Internalizing and Externalizing problems, as well as lower levels of symptoms across the DSM-oriented subscales. Parental education level was also positively associated with Social Competence. In post hoc univariate analysis comparing those with some post-secondary education, a high school degree or equivalent, or less than high school degree, children of parents with less than high school education had more than twice the odds of elevated internalizing [OR = 2.82; CI 1.27-6.28], externalizing [OR = 2.31; CI = 1.02-5.24] and total problems [OR = 2.90; CI 1.30- 6.44] compared to children of parents with at least some postsecondary education. Children of parents with at least some postsecondary education had significantly better social competence than those children of parents with HS/GED (diff = 4.60, CI = 2.69-6.60), and those children of parents with less than high school education (diff = 7.10, CI = 3.68-10.52).

Table 4:

Estimated Coefficients (p-values)

Covariate	Affective	Anxiety	ADHD	Opposition/Defiant	PTSD	Total Problems	Internalizing	Externalizing	Social Competence
ParentEd
>HS	−4.05 (0.0036)	−2.57 (0.0303)	−2.51 (0.0357)	−2.80 (0.0212)	−4.03 (0.0038)	−6.65 (0.0004)	−6.38 (0.0005)	−6.98 (0.0001)	7.10 (<.0001)
HS/GED	−1.11 (0.4378)	−1.05 (0.3845)	−0.33 (0.7890)	−0.75 (0.5442)	−1.38 (0.3357)	−1.99 (0.2999)	−2.57 (0.1705)	−2.54 (0.1738)	2.50 (0.1633)
<HS	reference	reference	reference	reference	reference	reference	reference	reference	reference
Sex
Female	0.44 (0.5388)	−0.61 (0.3190)	−2.75 (0.1187)	−4.51 (0.0116)	−8.29 (0.0025)	−4.90 (0.0892)	0.92 (0.3485)	−6.79 (0.0155)	1.48 (0.1276)
Male	reference	reference	reference	reference	reference	reference	reference	reference	reference
TBI Severity
Moderate/ComplMild	−1.66 (0.0193)	−0.51 (0.4015)	−0.32 (0.6069)	−0.19 (0.7622)	−1.17 (0.1044)	−1.51 (0.1298)	−0.81 (0.4016)	−0.88 (0.3631)	−0.01 (0.9889)
Severe	reference	reference	reference	reference	reference	reference	reference	reference	reference
Time Since Injury	0.75 (0.3372)	0.83 (0.2235)	0.80 (0.2507)	0.86 (0.2227)	0.92 (0.2977)	17.7 (0.0012)	2.45 (0.0235)	15.7 (0.0031)	−8.35 (0.0142)
Time Since Injury squared	--	--	--	--	--	−4.72 (0.0132)	--	−4.59 (0.0131)	5.43 (0.0063)
Age at Injury	0.21 (0.0101)	0.041 (0.5577)	−0.05 (0.5608)	−0.11 (0.2055)	−0.17 (0.2145)	0.44 (0.0256)	0.40 (0.0004)	0.22 (0.2579)	0.095 (0.5668)
Age at Injury * Time Since Injury	--	--	--	--	--	−0.73 (0.0065)	--	−0.62 (0.0175)	--
Age at Injury * Female sex	--	--	0.32 (0.0250)	0.34 (0.0193)	0.60 (0.0040)	0.48 (0.0393)	--	0.53 (0.0188)	--

Severe injury was associated with higher problem ratings on the DSM-oriented Affective Scale than moderate TBI. Injury severity displayed no significant interactions with SES or sex for the CBCL summary measures or DSM-oriented scales.

Older age at injury was associated with higher levels of DSM-oriented Affective symptoms, whereas the influence of age at injury on ADHD, Opposition/Defiant and PTSD symptoms varied for boys and girls. Post hoc examination (Figure 1) shows that the sex differences in ADHD symptoms were more pronounced among children injured at older ages, but for Opposition/Defiant and PTSD differences were more pronounced for children injured at younger ages. Formal contrasts at the 10th and 90th percentiles of age at injury (ages 5.05 and 16.66) revealed significant sex differences at age 16.66 for ADHD symptoms (t =2.69, p=.01), with girls with TBI demonstrating more symptoms relative to age-corrected female norms than boys with TBI relative to their age-corrected norms. Significant sex differences also were found at age 5.05 for Opposition/Defiant (t=−2.48 , p=0.01) and PTSD symptoms (t=−3.01, p<0.01), with girls demonstrating significantly fewer symptoms than boys, relative to their respective norms. In exploratory, post hoc analyses examining the types of ADHD symptoms reported in boys and girls, adolescent girls were rated as having more inattentive symptoms than younger girls, whereas hyperactivity symptoms were slightly lower in adolescent versus younger girls.

Figure 1:

Model-based expected subscale scores for ADHD, Opposition/Defiant and PTSD subscales, evaluated at parental education of HS/GED, moderate/complicated mild TBI Severity, and median time since injury (0.4).

Age at injury had a more complex relationship with time since injury in predicting Total Problems and Externalizing scales, as shown in Figure 2. The curvilinear pattern indicates that at longer times post injury, children injured at younger ages had higher Total Problems and Externalizing scale scores than those injured at older ages. As depicted in Figure 2, sex also interacted with age at injury, resulting in significant age-related contrasts for males at longer times since injury and for females at shorter times since injury. In males evaluated at a longer time since injury (1.16 years, 90th percentile), older age (16.66 years, 90th percentile) was associated with significantly lower externalizing problems (t=−2.28, p = 0.02) than younger age (age of 5.05 years old, 10th percentile); this comparison was not significant for females. In females with a short time since injury (0.13 years, 10th percentile), older age (16.66 years, 90th percentile) was associated with significantly higher levels of externalizing problems (t = 3.06, p <0.01) than younger age (age of 5.05 years old, 10th percentile); in contrast, males did not show significant age-related differences at shorter times since injury.

Figure 2:

Model-based expected subscale scores for Externalizing and Total Problems, evaluated at parental education of HS/GED, moderate/complicated mild TBI Severity, and various fixed values sex and age at injury (10^th percentile [P10=5], 1^st quartile [25^th percentile, Q1=8], median [12.8], 3^rd quartile (75^th percentile, Q3=15], and 90^th percentile [P90=16.7]).

The association of internalizing symptoms with age at injury and time since injury is more straightforward, characterized by a simple linear trend for more internalizing symptoms at older ages and with greater time since injury, without interaction with other variables (see Table 4). Time since injury had a significant curvilinear association with the Social Competence scale. As shown in Figure 3, longer times since injury were associated with higher Social Competence scores, and the increase occurred more rapidly as time since injury progressed past one year. (See Figure 3.)

Figure 3:

Model-based expected subscale scores for Social Competence, evaluated at parental education of HS/GED, moderate/complicated mild TBI Severity, and median age at injury (12.8).

DISCUSSION

Findings from a large cohort of children with moderate to severe TBI suggest that clinically-significant symptoms of internalizing and externalizing problems are common, affecting nearly one third of participants. Deficits in total competence are even more prevalent, with more than 40% rated as having difficulties. These findings suggest that social and behavioral challenges following TBI cut across domains.

Consistent with hypotheses and a sizable literature linking SES with cognitive and behavioral outcomes following TBI, parent education level was a strong correlate of every dimension of behavior examined. Two-thirds of children from households with less than high school degrees had significant social competence difficulties, placing these children at substantial risk for functional impairments in school and community. Thus, identifying and tracking these vulnerable children may be crucial, because they may be less likely to receive regular follow-up care.^45–47 Although we found no interaction between injury severity and SES, other research has noted that the effects of social-environmental variables may be amplified in the context of severe TBI.^15,25,48,49 Limited intervention research supports the utility of family-centered interventions for low-SES families,^50–53 underscoring the potential value of identifying and treating children with TBI at elevated social risk.

Although the effects of injury severity were less prominent than those of SES, children with severe TBI had higher levels of affective problems compared to children with mild-moderate TBI. Although affective symptoms may, in some cases, be driven by the brain insult, they may also reflect the child’s reaction to emerging deficits in cognition and executive function, which are also likely more pronounced following severe TBI. Given the high rates of social competence difficulties in this sample as a whole, screening for these concerns among children with severe TBI may be especially important.^54–57

Contrary to our hypotheses, we did not find evidence that younger age at injury was associated with higher rates of behavioral problems. Instead, we found that children injured in adolescence were rated as having higher levels of DSM Affective symptoms. This finding may be partly attributable to the difficulties parents have reporting on affective symptoms in younger children. However, adolescence is a time of tremendous physical and social-emotional development, accompanied by expectations for increasing autonomy. TBI during adolescence may be especially stressful given that its effects, which include activity restrictions and need for supervision, run counter to developmental expectations. Moreover, considerable evidence suggests that adolescence itself is associated with higher rates of depression, making this a time of heightened vulnerability.^58,59

We found higher rates of externalizing and total behavior problems with increasing time since injury (i.e., latent effects) in children injured at earlier, versus later, ages. In other words, children who sustained early injuries were rated as having higher levels of behavioral difficulties further out from injury than those who sustained injuries in adolescence. These findings are consistent with evidence suggesting that problems following early TBI may not be apparent until the child faces greater social and academic demands.^60–62 Although our data are cross-sectional, they underscore the potential value of tracking children over time and assessing for emerging challenges.

Consistent with expectations, we also found that the effects of age at injury on mental health outcomes were different for boys than for girls. However, our findings contrasted with previous research, which had indicated that females have higher rates of internalizing problems and males have higher rates of externalizing conditions such as ADHD.⁶³ Instead, we found no significant association between sex and internalizing problems, and complex associations of sex with ADHD and externalizing symptoms. In our study, scores on ADHD, Oppositional/Defiant, and PTSD symptoms tended to be higher for girls with older ages at injury. We observed this same trend for the externalizing composite scale – particularly over shorter times since injury. These findings may reflect an increased vulnerability among adolescent girls to the effects of TBI. At a symptom level, adolescent girls were rated as having difficulties with inattention rather than hyperactivity, suggesting that the symptom profile also differs among adolescent girls versus boys. Taken together, our findings provide preliminary evidence that the consequences of TBI may manifest differently in boys versus girls depending on their age and developmental status. The concussion literature has shed light on the potential vulnerability of adolescent girls to prolonged post-concussive symptoms on self-report^64,65 and our findings provide further evidence that this may be a time of risk for more severe TBI as well. Consistent with new NIH mandates and our limited understanding of sex differences on behavioral recovery following pediatric TBI, these will be important questions to examine in future research. Understanding the potential associated biologic correlates associated with sex differences also will be important, especially the hormonal changes that occur during puberty.^66–68

The association of time since injury with social competence was curvilinear, with more social competence problems noted in the post-acute recovery period (around 6 months) and higher levels of social competence reported with increasing time since injury after that time. These findings indicate that social competence increases steadily with increasing time since injury once past the acute recovery period. Given the high rates of social competence deficits in this cohort and the critical importance of social competence for everyday functioning and quality of life, our findings suggest that addressing these concerns should be a focus of the early recovery period.

This study is the first to examine influences of pediatric TBI on behavioral outcomes in a large, multi-cohort sample. Given the methods of the contributing studies, we were limited to a single, parent-report measure of behavior problems; diagnostic interviews or reports from other sources (self, peers, teachers) may have yielded different results. A portion of the sample had data from the early childhood version of the CBCL; as a consequence, we were unable to examine subscales that were unique to either the older or younger versions. This was also a cross-sectional evaluation, so the analyses did not incorporate longitudinal outcomes. Finally, because our study sample consisted of cohorts recruited for participation in randomized trials, our results may be biased by any systematic differences between families who do and do not participate in trials. Despite these limitations, the study provides important new information about the influences of injury, host, and social/SES factors on behavior problems post pediatric TBI.

CONCLUSIONS

Findings from a large cohort of children and adolescents highlight the high rates of internalizing and externalizing problems and total competence deficits following pediatric TBI. Low SES places children at substantially elevated risk. Associations with age at injury, time since injury, and sex are more complex but suggest the importance of considering each of these factors in identifying children at heightened risk for behavior problems after TBI. Given evidence that some problems peak years post injury, following children beyond the acute injury period will be important. Family problem solving interventions may provide an avenue for improving outcomes in children identified as at risk.⁴⁸