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Abstract

PURPOSE:

To describe language-based neuropsychological outcomes following brain injury in two pediatric populations commonly treated in rehabilitation settings, namely severe traumatic brain injury (sTBI) and stroke secondary to arteriovenous malformation (AVM).

METHODS:

Investigated were children between the ages of 6 and 16 who were admitted to a brain injury rehabilitation program in a pediatric rehabilitation hospital and who were diagnosed with a left-sided sTBI ( $n=$ 16; mean age $=$ 13.2) or a left-hemispheric stroke secondary to AVM ( $n=$ 16, mean age $=$ 10.7). Groups were compared on demographic information, as well as general cognitive and language-based neuropsychological measures, controlling for age.

RESULTS:

Children in the AVM group presented with greater deficits, at trend levels, relative to the sTBI group on measures of working memory, verbal fluency, and an aphasia screening tool.

CONCLUSIONS:

This study represents an initial step in understanding the language-based neuropsychological outcomes of children diagnosed with sTBI compared to those with stroke secondary to AVM, which will help inform the rehabilitation process. With this knowledge, clinicians, families, and educators will be better equipped to provide informed individual rehabilitation programs, recommendations, and education for children and adolescents with brain injuries.

Keywords

Acquired brain injury traumatic brain injury arteriovenous malformation left-laterality language neuropsychological outcome rehabilitation

1. Introduction

In pediatric rehabilitation settings, children and adolescents present with brain injuries of varying etiologies. Following both traumatic and acquired brain injuries, there are immediate and long-term impacts, with language difficulties commonly experienced [1, 2]. In a recent study, it was reported that 1 in 5 students in grades 7 to 12 had experienced a brain injury [3], with injury severity an important predictor of cognitive outcomes, in addition to physical and psychosocial factors [4]. For many children with a severe TBI (sTBI), special classroom assistance or specialized education placements are required following their injuries [5, 6, 7, 8, 9]. With regards to language outcomes, studies have reported verbal and language processing impairments, as well as high-level language discourse difficulties in children with sTBI [10]. Of note, these findings are typically discussed relative to children who have sustained mild or moderate TBI or between different developmental groups [11, 12]. As a result, there is a dearth of knowledge on language profiles following sTBI compared to those with different injury etiologies.

Another condition commonly treated in pediatric rehabilitation settings is arteriovenous malformation (AVM), a congenital abnormality that may result in intracranial hemorrhage as it involves an abnormal connection of cerebral blood vessels [13]. Childhood hemorrhagic strokes occur in approximately 2–3 per 100,000 children and account for nearly half of all acquired pediatric strokes [14], with 15 to 50 percent attributed to intracranial vascular anomalies, such as AVM [15]. Recent studies investigating the neuropsychological outcome of childhood stroke indicate that many domains of cognitive functioning are affected, including language difficulties [2, 16]. Within the rehabilitation setting, children who have a stroke secondary to AVM experience significant obstacles in both physical and cognitive domains. Similar to children with sTBI, these challenges often persist after the child is discharged home from the hospital. Despite the continued difficulties, few studies have investigated cognitive outcomes in hemorrhagic stroke within a pediatric population. Those that have yield mixed findings regarding lesion location and cognitive outcomes [14, 16, 17, 18]. Other studies have highlighted the effects of insult to dominant hemispheric systems such that, compared to right-hemispheric lesions, damage to the left-hemisphere later in childhood typically resulted in language deficits, such as acute aphasia, as well as challenges with reading, delayed verbal memory, and receptive language [13, 17, 19, 20]. Similar to the TBI research, the majority of these studies compared outcomes between different developmental subgroups or compared an AVM group to healthy controls.

Taken together, there are significant cognitive declines following pediatric sTBI and AVM, however the unique neurocognitive profiles that differentiate these conditions are unknown. Within a pediatric rehabilitation centre, one of the main goals is to promote recovery and facilitate the development of appropriate skills in physical, cognitive, functional, and emotional domains [3]. The aim of the present study was to examine retrospective reports of neuropsychological performance in the acute stage of rehabilitation (e.g., post-acute care but within 12 months of their injury) following a left-sided traumatic brain injury or a left-sided AVM, with a specific focus on language-related neuropsychological outcomes. This information is essential from a rehabilitation perspective in order to inform best practices for clinical services, such as developing appropriate clinical treatment pathways, as well as to support clients and families in their transition home, back to school, and to their community.

2. Methods

2.1 Participants

Thirty-two children between the ages of 6 and 16 years were studied from an existing neuropsychological database; 16 with a diagnosis of left-sided laterality sTBI and 16 with a diagnosis of left-hemispheric stroke secondary to AVM. For the sTBI group, only participants with a Glasgow Coma Scale [21] score between 3 and 8, and a left-sided injury were included in analyses. For the AVM group, only participants who were diagnosed with a left-sided AVM were included in the analyses. For both groups, lesion lateralization was determined through brain imaging results and seizure activity was described in the medical records provided by the referring hospital, as well as rehabilitation hospital admission notes. Please see Table 1 for additional information. Exclusionary criteria for both groups were clients and/or legal guardians who declined consent to be included in the neuropsychological database; clients who participated in neuropsychological testing more than 12 months from the initial onset of their injury; were greater than 16 years of age at the time of assessment; or clients with a premorbid psychological disorder (e.g., attention deficit hyperactivity disorder, learning disability), previous brain injury, previously identified neurological disorder, or significant vision and/or hearing loss. All procedures were approved by the hospital Research Ethics Board.

Table 1
Mean and Standard Deviations (SD) demographic characteristics for children in the sTBI and AVM groups

Variables	sTBI $n=$ 16	AVM $n=$ 16	$p$ Value
Age at testing (years)	13.19 (2.69)	10.72 (2.81)	$<$ 0.05
Age at time of injury (years)	13.13 (2.63)	10.70 (2.78)	$<$ 0.05
Sex (% Male)	50	50	ns
Handedness (% Right)	71	80	ns
Seizure activity (% Yes)	31	6	$<$ 0.08
Lobes affected (%)
Frontal	44	31
Temporal	12	19
Parietal	0	12
Multiple lobe involvement	44	38
Lowest GCS score ${}^{1}$
3	14	–
4	14	–
5	21	–
6	7	–
7	7	–
8	5	–
Cause of TBI (%)
Passenger in MVA	50	–
Pedestrian/cyclist involved in MVA	44	–
Fall	6	–

Note: ${}^{1}$ Information missing for 2 cases. Lowest GCS score $=$ lowest Glasgow Coma Scale Score reported, GCS and cause only reported for TBI group.

2.2 Measures

Demographic variables that were examined included age at the time of injury, age at testing, sex, handedness, seizure activity, and brain injury location.

2.2.1 Wechsler Intelligence Scale for Children – fourth Edition (WISC-IV [22])

The WISC-IV has excellent reliability and validity [22]. Scores are presented as standard scores for the indices, with higher scores representing higher performance.

2.2.2 Children’s Memory Scale (CMS [23])

The reliability (internal consistency and test-retest) and validity (construct validity) of the CMS are reported to be high [23, 24, 25]. In the current analyses, standard scores for the composites were investigated, with higher scores representing higher performance.

2.2.3 Delis Kaplan Executive Function System (D-KEFS [26])

The reliability and validity of the measure have been well established [26, 27, 28]. The current study investigated the Verbal Fluency test, which includes letter fluency (speeded generation of words belonging to a specific letter), category fluency (speeded generation of words belonging to a specific category) and category switching (alternating between words in different categories) subtests. Scores are presented as scaled scores, with higher scores representing higher performance.

Table 2
Neuropsychological Measures mean (SD) for the sTBI and AVM groups

Measure	sTBI		AVM		$p$ Value	$\eta^{2}$
WISC-IV ${}^{1}$	$n=$ 15		$n=$ 14
Verbal comprehension	96.13	(15.61)	90.21	(13.74)	ns	ns
Perceptual reasoning	102.33	(14.69)	102.00	(14.84)	ns	ns
Working memory index	96.07	(10.00)	87.21	(15.88)	$<$ 0.09	0.11
Processing speed	90.73	(12.60)	87.50	(16.24)	ns	ns
Full scale IQ	95.07	(12.33)	89.79	(11.15)	ns	ns
CMS ${}^{1}$	$n=$ 13		$n=$ 13
Visual immediate	94.85	(15.38)	103.54	(12.48)	ns	ns
Visual delayed	99.13	(12.01)	101.39	(10.29)	ns	ns
Verbal immediate	89.00	(16.14)	91.54	(18.90)
Verbal delayed	87.85	(15.43)	88.92	(15.05)	ns	ns
General memory	89.92	(17.11)	95.31	(12.67)	ns	ns
Learning	90.31	(13.01)	98.46	(12.30)	ns	ns
Delayed recognition	87.92	(16.66)	91.69	(13.44)	ns	ns
DKEFS ${}^{2}$	$n=$ 9		$n=$ 11
Letter fluency	9.67	(3.00)	6.64	(3.41)	$<$ 0.06	0.19
Category fluency	10.22	(2.33)	8.73	(1.68)	ns	ns
Category switching-total correct	9.78	(3.73)	9.09	(2.39)	ns	ns
Reitan-Indiana Aphasia Screening Test ${}^{3}$	$n=$ 6		$n=$ 7
Anomia	0.67	(0.53)	0.86	(1.07)	ns	ns
Spelling	0.83	(1.33)	1.14	(1.46)	ns	ns
Dysgraphia	0.33	(0.52)	0.14	(0.38)	ns	ns
Dysarthria	1.00	(0.63)	1.43	(0.54)	ns	ns
Dyslexia	0.17	(0.41)	0.14	(0.38)	ns	ns
Dyspraxia	0.67	(0.82)	2.0	(1.63)	$<$ 0.10	0.23
Dyscalculia	0.83	(0.75)	0.71	(0.76)	ns	ns
Auditory agnosia	0.00	(0)	1.00	(1.16)	$<$ 0.06	0.29
CVLT-C ${}^{4}$	$n=$ 14		$n=$ 15
Learning slope	$-$ 0.25	(1.09)	0.13	(1.09)	ns	ns
Short delay free recall	$-$ 0.61	(1.53)	$-$ 0.57	(1.27)	ns	ns
Short delay cued recall	$-$ 0.57	(1.69)	$-$ 0.30	(1.25)	ns	ns
Long delay free recall	$-$ 0.25	(1.00)	$-$ 0.33	(1.05)	ns	ns
Long delay cued recall	$-$ 0.11	(0.79)	$-$ 0.23	(1.12)	ns	ns

Note: ${}^{1}$ standard scores; ${}^{2}$ scaled scores; ${}^{3}$ raw scores; ${}^{4}$ z scores.

2.2.4 Reitan-Indiana Aphasia Screening Test (AST [29])

This screening tool assesses a wide range of general language-related deficits, including Anomia (inability to name common geometric shapes, familiar items, and other objects), Spelling (written spelling of common geometric shapes), Dysgraphia (inability to write words and sentences from picture cues or oral dictation), Dysarthria (difficulty with speech articulation), Dyslexia (inability to read letters, numbers, words, and short sentences), Dyspraxia (inability to draw simple and more complex shapes and objects and difficulty performing a motor response), Dyscalculia (inability to complete 2-digit subtraction and multiplication questions), and Auditory Agnosia (difficulty repeating simple and more complex words and sentences) [29]. The AST is not a comprehensive test of language ability, but rather a screening test used to elicit responses that are indicative of pathognomic signs of brain impairment. This measure has proved to be helpful in understanding basic academic abilities and also can assist in intervention planning [30]. Scores are presented as raw scores, with lower scores representing better performance.

2.2.5 California Verbal Learning Test – Children’s Version (CVLT-C [31])

The CVLT-C is a measure of verbal learning and memory, demonstrating good construct validity, criterion validity and sensitivity [31, 32, 33, 34]. The following subtests were included in current analyses: learning slope, short delay free recall, short delay cued recall, long delay free recall and long delay cued recall. Scores are presented as z-scores, with higher scores representing higher performance.

2.3 Analyses

For analyses, descriptive statistics were used to investigate demographic data, including one-way analyses of variance (ANOVA) for continuous variables and chi-square analyses for categorical variables. To compare sTBI and AVM groups and to examine for the effects of age, multivariate analyses of covariance (MANCOVA) was used. Where age was not significant, this variable was removed and MANOVA was conducted accordingly. For all comparisons, effect sizes were determined using partial eta-squared ( $\eta^{2}$ ). Statistical significance was set at $p<$ 0.05; however results between $p<$ 0.06 and $<$ 0.10 were considered trends in the data.

3. Results

With regards to demographics (Table 1), groups differed in age, with the sTBI group significantly older than the AVM group. The sTBI group also experienced more seizure activity, at a trend level, than the AVM group. For the neuropsychological measures (Table 2), although there were no statistically significant findings, analyses revealed trends towards the AVM group performing more poorly relative to the sTBI group on measures of verbal working memory (i.e., sequencing of letters and numbers), letter fluency (i.e., quickly generating words), auditory agnosia (i.e., repeating back verbal information and following simple verbal commands), as well as dyspraxia (i.e., drawing simple and more complex shapes.

4. Discussion

Although TBI and AVM represent two of the more common clinical populations treated in pediatric rehabilitation hospitals, there remains a paucity of knowledge on the acute cognitive and language profiles following these injuries [3], as well as how profiles differ between these groups. The current study therefore sought to compare children and adolescents with sTBI to those with stroke secondary to AVM, in order to gain an initial understanding of the unique language-based neuropsychological profiles. Overall, we found that the AVM group performed more poorly, at trend levels, compared to the sTBI group in areas of verbal working memory, verbal fluency, repeating verbal information and following verbal commands, as well as visual-motor drawings. These preliminary profiles provide important information for clinicians and educators working in pediatric rehabilitation, as they suggest differing acute profiles depending on the nature of brain injury and will help inform program planning.

Importantly, the Heart and Stroke Foundation recently updated their Canadian stroke best practice recommendations, with specific guidelines for pediatric rehabilitation [35]. The best practices propose evidence-based recommendations in areas of prevention, hyperacute, acute, rehabilitation, and transition periods, as well as mood, cognition, and fatigue. Hospital and community resources therefore have a reference for what standards of care should be implemented for all youth following a stroke, as well as how these standards can be best applied to promote positive outcomes and recovery. Together with the current findings, these standards may include early admission screening of specific language and verbal processing domains. Within our pediatric rehabilitation setting, speech and language pathologists and neuropsychologists comprehensively assess language and cognitive communication skills immediately upon a child’s hospital admission. Although rehabilitation goal planning and programing are tailored to individual needs, conducting these screening measures early help to identify specific challenges and aid in setting targeted therapy goals. Early identification and targeted therapy goals are essential, especially with time-limited hospital admissions. In addition, further understanding of cognitive and language-based profiles can occur through more thorough assessments (e.g., neuropsychological, and speech and language assessments) to determine the youth’s unique profile of strengths and areas of difficulty as they approach discharge and transition to their home and community. This information is essential in arranging the necessary academic and community-based referrals. Although the assessment and treatment resources are generally the same within a rehabilitation hospital, regardless of the type of brain injury sustained, there can often be differences within the community due to available and attainable supports. In Ontario, for example, a survivor of a motor vehicle accident who has sustained a TBI may be eligible for medical and rehabilitation benefits such as private speech therapy. Unfortunately, private resources that support an individual’s ongoing recovery following the acute rehabilitation phase are not available to all individuals and their families, including those with AVM. There may also be limited hospital-based neuropsychological and speech and language follow-up services to address any ongoing concerns. This potential discrepancy in resources raises questions of differing inpatient lengths of stay, depending on the type of brain injury sustained and individual needs required, as well as creating specialized outpatient rehabilitation programs that fill the gap between the acute hospital admission and long term follow up.

The current preliminary results also highlight the need to prepare children, adolescents, and their families for discharge in ways that are tailored to their child’s specific pattern of cognitive strengths and difficulties as a result of their brain injury. The need for long term support once the child and family returns home and back to school is an important aspect to discuss early in the rehabilitation stage. As an example, effective communication and verbal processing skills are essential for academic success. Challenges in these domains are often observed beyond the acute rehabilitation period [11] and may contribute to ongoing academic challenges. Within TBI, academic outcomes are often related to injury severity, as well as other family and environmental factors [36]. Although there are some reports that children show improvement in cognitive functioning one year post injury [37], school success can remain hindered years after recovery. Children and adolescents with a brain injury may continue to fall behind, and the gap between their performance and their healthy peers may continue to widen as they may not acquire academic gains at the same rate [4, 38]. One initiative to help combat this is creating individual education plans where accommodations, modifications, and behaviour interventions for the individual are outlined and identified based on their brain injury [39]. In addition, standardized assessments (i.e., neuropsychological and speech and language assessments), as well as school-based recommendations should be shared between rehabilitation teams and the student’s community school to specifically inform the educational needs required for academic success. It is possible that students with such support, regardless of their injury type, may have better recovery outcomes, which may help lessen the impact of language-based cognitive deficits.

Taken together, the information provided in this preliminary report is informative not only for clinicians, but also educators and families following discharge from a rehabilitation centre, as the rehabilitation process does not end when the child returns to their community. Although these findings represent an initial step to understanding unique profiles following brain injury, it is not without limitations. One of the main limitations is the sample size, which is often the case when investigating clinical populations in rehabilitation settings. This study also focused on specific language-based measures from a retrospective database. Although this is a first step to characterizing specific clinical outcomes in two populations not commonly compared, future research would benefit from investigating additional neuropsychological domains. Furthermore, given the trend towards greater seizure activity in the sTBI group, additional investigation is necessary to determine the impact of seizure activity on language-based neuropsychological performance. Finally, some of the datasets were incomplete due to updated test versions and some participants not being able to complete all measures administered. Despite these limitations, this study represents a first step in describing the unique language-based neuropsychological profiles from a rehabilitation perspective of children with sTBI and children with stroke secondary to AVM. By understanding these profiles, families, educators and clinicians will be better equipped to recognize and support the needs of these individuals and understand the unique sequelae of brain injury [40].

Footnotes

Acknowledgments

The authors are especially grateful to the clients and their parents/caregivers for their participation in this study.

Conflict of interest

The authors have no conflicts of interest to report.

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Informing pediatric rehabilitation: Language-based neuropsychological profile following traumatic brain injury and stroke secondary to arteriovenous malformation

Abstract

PURPOSE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

1. Introduction

2. Methods

2.1 Participants

Table 1 Mean and Standard Deviations (SD) demographic characteristics for children in the sTBI and AVM groups

2.2.1 Wechsler Intelligence Scale for Children – fourth Edition (WISC-IV [22])

2.2.2 Children’s Memory Scale (CMS [23])

2.2.3 Delis Kaplan Executive Function System (D-KEFS [26])

Table 2 Neuropsychological Measures mean (SD) for the sTBI and AVM groups

2.2.5 California Verbal Learning Test – Children’s Version (CVLT-C [31])

2.3 Analyses

3. Results

4. Discussion

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Mean and Standard Deviations (SD) demographic characteristics for children in the sTBI and AVM groups

Table 2
Neuropsychological Measures mean (SD) for the sTBI and AVM groups