Children with Traumatic Brain Injury (TBI) may have post-injury deficits in mobility and physical function, which are generally more profound with increasing injury severity (Ewing-Cobbs et al., 1989; Jaffe et al., 1992; Kuhtz-Buschbeck, et al., 2003a). Children characterized as having moderate to severe injuries based on acute injury presentation are reported to have deficits in coordination, upper extremity function, strength, postural control, gait and other mobility skills (Drijkoningen et al.; Jaffe, et al., 1992; Katz-Leurer et al., 2009, Katz-Leurer et al., 2008; Kissane et al., 2015; Kuhtz-Buschbeck, et al., 2003a; Kuhtz-Buschbeck, et al., 2003b). Children with injuries on the milder end of the severity spectrum may demonstrate differences in balance, and aspects of gait and visuomotor response speed compared to uninjured children up to several months post injury (Gagnon et al., 2004a, 2004b; Sambasivan et al., 2015). The NIH Toolbox for Assessment of Neurological and Behavioral Function is a neurobehavioral outcome battery that assesses motor function, along with cognition, emotion, and sensation. The NIH Toolbox is brief, methodologically and psychometrically sound, and was designed for longitudinal assessments of people with various health conditions and ages (3 to 85 years) (Gershon et al., 2013). The NIH Toolbox Motor Battery (NIHTB-M) includes assessments of dexterity, strength, balance, endurance and locomotion (Reuben et al., 2013). The NIH Toolbox was developed for research applications but the motor battery may also have utility as an efficient clinical tool to assess physical function and mobility. The NIHTB-M has been studied in adults with TBI (Carlozzi et al., 2017), but has not been evaluated in children with TBI. Our objective was to examine the feasibility of administering the NIHTB-M to a small group of children who presented to the Emergency Department (ED) or hospital following TBI. Our evaluation focuses administration time and barriers to participation to inform the use of the NIHTB-M to assess physical function in children with TBI for either research or clinical applications. Additionally, we compare NIHTB-M performance of a small sample of children with TBI with the normative sample and describe TBI-affected children with poor NIHTB-M performance in terms of personal and injury factors, and scores on questionnaire-based assessments of somatic symptoms and physical health-related quality of life, to preliminarily examine these relationships and to guide future research.
Materials and Methods
Participants
We administered the NIHTB-M to a subset of children (n=32) enrolled at a single site of the Transforming Research and Clinical Knowledge in TBI (TRACK-TBI) study. TRACK-TBI is a multi-site observational cohort study which collects clinical, imaging, biomarker, and outcome data on hospital-presenting patients with TBI s of all ages and TBI severities using the National Institute of Neurologic Disorders and Stroke Common Data Elements (CDEs) (Yue et al., 2013). Inclusion criteria for TRACK-TBI are presentation to the ED of a study hospital with at least a ‘mild’ TBI (ACRM, 1993), completed acute clinical neuroimaging (computed tomography (CT) or magnetic resonance imaging (MRI)), and enrollment in the study within 24 hours of injury. Clinical neuroimaging was obtained based on the judgment of treating clinicians. As part of standard clinical practice to minimize unnecessary radiation, CT scan use generally was guided by Pediatric Emergency Care Applied Research Network (PECARN) algorithm, which foregoes CT imaging of children with the mildest clinical presentations. (Kuppermann et al., 2009) However, at our institution MRI is available in the ED, which has no risk of radiation and the PECARN algorithm is not applicable; thus, some children with injuries of various severities underwent rapid MRI scans at the discretion of treating clinicians. Nevertheless, the inclusion criteria requiring clinical neuroimaging, excludes those who were not deemed to require neuroimaging on clinical grounds, presumably those with the mildest acute injury presentations. Thus, our findings are not applicable to children at the mildest end of the injury severity spectrum, who do not present to the hospital, or do not require neuroimaging on clinical grounds.
Exclusion criteria for TRACK-TBI include major polytrauma likely to interfere with follow-up, spinal cord injury (ASIA C or worse), major debilitating baseline conditions (e.g., significant developmental delay or significant psychological conditions), or placement in child protective custody.
Eligible subjects for TRACK-TBI were identified using the hospital’s electronic medical record (EMR) and approached by either the primary investigator or trained research coordinators. Informed consent was obtained from parents/guardians for all subjects and children aged 14 to 16 years, with assent obtained for children aged 7 to 13 (when not precluded by the severity of the injury). The study protocol was approved by the local Institutional Review Board.
The NIHTB-M was added to the pediatric outcome assessment battery at a single site of the TRACK-TBI study in August of 2016. Children aged 3 to 16 years old enrolled in TRACK-TBI at this site and scheduled for a 2-week or 6-month follow up between August 2016 and June 2018 were included in this analysis. Children who remained acutely hospitalized at the time of the study assessment did not complete the NIHTB-M because of on-going clinical care. Children with orthopedic injuries completed those portions of the assessment that did not violate medical precautions (2 weeks, n=2, 6 months, n=1).
The median age of the 22 children completing at least part of the battery at 2 weeks post-TBI was 11 years (IQR=6-14), with a median Glasgow Coma Score (GCS) score of 15 (IQR=14-15, range 2T to 15 (“T” indicating intubation)). The median age of the 23 children completing at least part of the battery at 6 months post-TBI was 11 years (IQR=7-14), with a median GCS score of 15 (IQR=13-15, range 2T to 15). Similar to demographics of pediatric TBI overall (Faul et al., 2010), most of the children enrolled had milder injuries, but some had more severe injuries requiring hospitalization, including surgery and intensive care. Demographic and injury characteristics are detailed in Table 1.
Table 1.
Demographic and injury characteristics
| 2 weeks |
6 months |
|||
|---|---|---|---|---|
| Eligible participants n=34 | Participants with Partial NIHTB-M n=22 | Eligible participants n=33 | Participants with partial NIHTB-M n=23 | |
| Age (years) | ||||
| Median (IQR) | 12 (7-15) | 11 (6-14) | 11 (7-15) | 11 (7-14) |
| Mean (SD) | 10.9 (4.5) | 10.45 (4.6) | 10.6 (4.4) | 10.9 (4.2) |
| Race | ||||
| White, n (%) | 22 (64.7%) | 13 (59.1%) | 21 (63.6%) | 14 (60.9%) |
| Black, n (%) | 4 (11.8%) | 3 (13.6%) | 5 (15.2%) | 3 (13.0%) |
| Other, n (%) | 8 (23.5%) | 6 (27.3%) | 7 (21.2%) | 6 (26.1%) |
| Boys, n (%) | 23 (67.6%) | 16 (72.7%) | 22 (66.7%) | 18 (78.3%) |
| Ethnicity | ||||
| Hispanic, n (%) | 5 (14.7%) | 4 (18.2%) | 6 (18.2%) | 4 (17.4%) |
| Private Insurance, n (%) | 25 (73.5%) | 14 (63.6%) | 26 (78.8%) | 18 (78.3%) |
| ADHD, n (%) | 5 (14.7%) | 5 (22.4%) | 5 (15.2%) | 5 (21.7%) |
| Anxiety or Depression, n (%) | 2 (5.9%) | 2 (9.1%) | 2 (6.1%) | 1 (4.3%) |
| History of TBI, n (%) | 5 (14.7%) | 3 (13.6%) | 4 (12.1%) | 4 (17.4%) |
| Injury Mechanism | ||||
| Falls, n (%) | 14 (41.2%) | 8 (36.4%) | 15 (45.5%) | 11 (47.8%) |
| MVA, n (%) | 14 (41.2%) | 10 (45.5%) | 11 (33.3%) | 7 (30.4%) |
| Sports, n (%) | 5 (14.7%) | 3 (13.6%) | 5 (15.2%) | 4 (17.4%) |
| Other, n (%) | 1 (2.9%) | 1 (4.5 %) | 2 (6.1%) | 1 (4.3 %) |
| GCS1 Median (IQR) | 15 (14-15) | 15 (14-15) | 15 (14-15) | 15 (13-15) |
| LOC2, n (%) | 18 (52.9%) | 11 (50.0%) | 15 (45.5%) | 9 (39.1%) |
| Positive Neuroimaging3, n (%) | 18 (52.9%) | 12 (54.5%) | 16 (48.5%) | 11 (47.8%) |
| ICP monitoring, n (%) | 2 (5.9%) | 1 (4.5%) | 2 (6.1%) | 1 (4.3 %) |
| Neurosurgery, n (%) | 2 (5.9%) | 1 (4.5%) | 1 (3.0%) | 1 (4.3%) |
| Concomitant injury, n (%) | 8 (23.5%) | 3 (13.6%) | 7 (21.2%) | 4 (17.4%) |
| Time from Injury to Discharge | ||||
| < 24 hours, n (%) | 10 (29.4%) | 6 (27.3%) | 13 (39.3%) | 10 (43.5%) |
| 24 to 72 hours, n (%) | 15 (44.1%) | 13 (59.1%) | 13 (39.3%) | 8 (34.8%) |
| > 72 hours, n (%) | 9 (26.5%) | 3 (13.6 %) | 7 (21.2%) | 5 (21.7%) |
| Hospital Unit | ||||
| ED Only, n (%) | 5 (14.7%) | 2 (9.1%) | 5 (15.2%) | 2 (8.7%) |
| Hospital no ICU, n (%) | 13 (38.2 %) | 10 (45.5%) | 12 (36.4%) | 9 (39.1%) |
| Hospital ICU, n (%) | 16 (47.1%) | 10 (45.5%) | 16 (48.5%) | 12 (52.2%) |
Note: IQR=Interquartile range; ADHD=Attention-deficit/hyperactivity disorder; MVA= Motor Vehicle Accident; GCS= Glasgow Coma Scale; LOC=Loss of consciousness; ICP= Intracranial pressure; ED=Emergency department, ICU=Intensive Care Unit;
Worst in ED;
Observed LOC of any duration;
Any intracranial lesion noted in acute clinical imaging, or 2 week study scan;
Partial-Completed at least part of the NIHTB-M expected for age; Complete=Completed all of NIHTB-M expected for age.
Procedures
Participant demographics, socioeconomic information, medical history, and TBI history were obtained via parent/child interview. Injury details were obtained via the EMR and/or parent/child interview. Clinical care metrics, including GCS, surgical intervention, and intracranial pressure monitoring, were extracted from the EMR. Participants were considered to have “positive” (i.e., some finding of intracranial abnormality associated with the current injury, excluding injuries to skull or scalp only) or “negative” (i.e., no evidence of intracranial abnormality) neuroimaging based on neuroradiologic reports from acute clinical or 2 week study scans. All clinical data were stored on a secure and HIPAA-compliant database (maintained by QuesGen Systems, Inc.).
In-person outcome assessments occurred at 2 weeks (+/− 4 days) and 6 months (+/− 14 days) post-injury. The 2-week and 6-month assessments included the NIHTB-M and questionnaires selected from the CDEs for pediatric TBI (McCauley et al., 2012).
Measures
NIH Toolbox Motor Battery (NIHTB-M).
The NIHTB-M includes performance-based tasks which assess dexterity, strength, balance, endurance, and locomotion (see Table 2). The NIHTB-M tasks were selected based on expert consensus, feasibility, and criterion validation in a healthy population (Reuben, et al., 2013). The NIHTB-M was standardized for use in people aged 7-85, with an ‘Early Childhood’ version (excluding locomotion) for children aged 3 to 6 years (“NIH Toolbox® for Assessment,” 2016). Published NIHTB-M normative values are based on a stratified sample (age, sex, primary language) of 3413 community-dwelling, non-institutionalized 3 to 17 year-olds capable of following test instructions (English and Spanish) and providing informed consent (>/= 8 years old) or assent (< 8 years old), with accompanying parent/guardian consent. (Beaumont et al., 2013; Slotkin et al., 2012).
Table 2.
Description of NIH Toolbox Motor subdomain tasks
| Domain | Measures | Administration |
|---|---|---|
| Dexterity | 9-Hole Pegboard Dexterity Test | Separate scores for dominant and
non-dominant hand. Includes a practice trial and scored trial for each hand. |
| Strength | Grip Strength Test (hand-held dynamometer) | Separate scores for dominant and
non-dominant hand. Includes a practice trial and scored trial. |
| Balance | Standing Balance Test (Up to 5 positions for 50 seconds) |
Anterior/Posterior sway measured with iPod
accelerometer attached at waist. Two attempts to control each position for 50 seconds. Stop rules incorporated into application. Positions Eyes open, firm surface, feet together Eyes closed, firm surface, feet together Eyes open compliant surface, feet together Eyes closed, compliant surface, feet together Eyes open, firm surface, tandem stance. |
| Endurance | 2-Minute Walk Endurance Test | Performed at a “fast”
pace. Distance measured on a 50’ walkway. |
Note: A locomotion domain consisting of a 4-Meter Walk Gait Speed test (usual speed) is also included in the NIHTB-M, but is not included in this report.
All five NIHTB-M tests were administered, but locomotion scores are not reported due to lack of normative data (“NIH Toolbox: Scoring,” 2016). The battery is administered via an iPad application which provides guided prompts for the examiner and score reports. Space and equipment requirements are described in the Administrator’s Manual, accessed at www.healthmeasures.net. (“NIH Toolbox® for Assessment,” 2016) The NIHTB-M was administered by a licensed physical therapist or trained research coordinator. Training to administer the battery included completion of the online NIH Toolbox administration tutorial modules, reading the NIH Toolbox Administrator’s Manual and conducting practice administrations.
Pediatric Quality of Life (PedsQL).
The PedsQL generic core is a health-related quality of life questionnaire (HRQoL) that has been used extensively in children and includes a physical sub-domain (PedsQL-Phys) (Varni and Limbers, 2009). In children with TBI, the PedsQL has demonstrated reliability, validity, and sensitivity to change, and is a supplemental measure of global outcome per the CDEs for TBI (McCarthy et al., 2005; McCauley, et al., 2012; Varni and Limbers, 2009). Parents of children aged 3 to 16 years and children aged 5-16 rate ‘how much of a problem’ a series of tasks have been on an ordinal scale. Raw scores are converted to a scaled score (ranging from 0 to 100), and higher scores indicate better HRQoL (Varni, 2012). Age-specific PedsQL forms are available and were selected based on the child’s age at the time of study enrollment. (Varni and Limbers, 2009)
Health and Behavior Inventory (HBI).
The HBI is a checklist of TBI-related symptoms, which has demonstrated favorable psychometric properties and is recommended as a basic CDE of TBI-related symptoms. (Ayr et al., 2009; Barry et al., 1996; McCauley, et al., 2012; Moran et al., 2011; Taylor et al., 2010; Yeates et al., 2012). Parents and children (aged 8 to 16 years) rate the frequency (i.e. never, rarely, sometimes, often) of common TBI-related symptoms over the last week, including eleven cognitive (e.g., trouble paying attention or gets confused; HBI-Cognitive) and nine somatic (e.g., has headaches, gets tired a lot; HBI-Somatic) symptoms. Cognitive domain and somatic domain symptom severity is calculated by summing symptom frequency ratings. Parents also complete a retrospective rating of their child’s pre-injury symptom severity (Ayr, et al., 2009). We report only parent HBI-ratings of symptoms due to availability of scores across the full age range of the sample.
Data Analysis
All statistical analyses were completed using IBM SPSS Statistics for Windows, Version 25.0 (Armonk, NY: IBM Corp). Sample characteristics were described using means, standard deviations, medians, and interquartile ranges. NIHTB-M performance, reported in age-referenced standard scores (mean 100, SD 15), was calculated automatically through the iPad application. Median sample scores were compared to standard scores using a one-sample Wilcoxon Signed Rank test, assuming a normative median of 100.
For NIHTB-M domains in which sample medians were significantly lower than the standardization sample, individual participants were characterized as having ‘low’ as compared to ‘broadly normal’ performance. Participants scoring ≤ 1.5 SD below the normative sample mean were considered ‘low’ for that domain, and remaining participants were considered ‘broadly normal.’ Mann Whitney U tests were used to examine median differences in PedsQL-Phys and HBI-somatic scores between ‘low’ and ‘broadly normal’ performers.
Results
At 2 weeks following injury, 28 (82%) of 34 eligible participants attended in-person follow-up. Of the 28, 15 (54%) completed the full NIHTB-M battery, seven (25%) completed a portion of the battery, and six (21%) did not participate in the NIHTB-M due to continued inpatient status (n=3) or time constraints (n=3) such as needing to return to school. At 6 months following injury, 23 (70%) of the 33 eligible participants attended in-person assessment. Of the 23, 17 (74%) completed the full battery, and six (26%) completed a portion of the battery. Details regarding full, partial, non-participation in the NIHTB-M tests at each time point are summarized in Figure 1. No differences in age, race or injury severity were noted between those who were eligible but did not participate and those who completed at least a portion of the NIHTB-M battery at either time point. At 6 months, the proportion of boys who participated in the NIHTB-M was higher than the proportion of girls who participated (82% versus 46%, p=0.05).
Figure 1.
TRACK-TBI participants with 2 week or 6month follow-up assessments scheduled between August 2016 and June 2018 with reasons for incomplete or partially complete assessments. 1 Injury sustained after the TBI. Ortho.=Orthopedic injury, direct.=direction, tech.=technological difficulties.
Time to Complete
The NIHTB-M Administrator’s Manual estimates that the battery requires about 21 minutes to complete, with the Early Childhood Motor Battery (for ages 3 to 6) expected to require 18 minutes. For our participants, including all administrations at either time point where participants completed all expected subdomains for their age, the median time to complete the performance-based tasks was 20 minutes (IQR=18-23 minutes; range=16-37 minutes). The median total time to complete the motor battery, including test transitions, was 23 minutes (IQR=20-26 minutes; range=18-37 minutes).
Barriers to Administration
Factors impacting completion of the NIHTB-M included ability to follow directions problems with technology, orthopedic injuries, and fatigue. (Figure 1).
Direction Following.
Children aged 5 and up consistently followed test instructions and engaged with the tasks per the administration guidelines; however, younger children (ages 3 and 4 years) had difficulty. At 2-weeks post injury, one of four children under age five was able to complete the NIHTB-M per administration guidelines, one completed the assessment but required repetitions of directions and frequent encouragement from the evaluator to persist resulting in a non-standard administration, and two were unable to complete the full assessment due to inability to follow the administration instructions sufficiently for accurate assessment. At 6 months post injury, one of the two children under age five was able to complete the NIHTB-M per administration guidelines, and one was unable to complete the full assessment due to inability to follow instructions. The balance subtest was the most difficult task for children under 5 years old to complete. Younger children had difficulty remaining still and keeping their eyes closed for 50 seconds due to limited attention span, rather than frank balance impairments. Younger children were also easily distracted by the iPod, even with it positioned on their back out of sight. Children attempted to grasp and remove the iPod during testing not out of discomfort but given familiarity with similarly shaped smartphones with which they were accustomed to playing.
Technology.
We found administration using the iPad application and the examiner prompts to be user-friendly and were able to use the application to generate score reports. However, Bluetooth disconnection between the iPod and iPad occurred in several instances. When disconnection occurs, the examiner is provided an option to ‘reconnect’ on the iPod, however, reconnection attempts were not always successful. If the ‘reconnect’ is not successful, the assessment is not scored and all raw data from completed components of the balance assessment are lost. Bluetooth disconnection during balance assessment resulted in lost data for three subjects at each time point.
Orthopedic Injuries and Fatigue.
At the 2-week assessment, two of 22 subjects were unable to participate in the full NIHTB-M due to orthopedic injuries sustained at the time of trauma. At 6 months, one child had an orthopedic injury, sustained after the qualifying TBI, which prevented completion of all subtests. Children were informed that they could stop assessment at any time. Of 45 total administrations, one participant requested to stop due to fatigue during the 6 month assessment.
Comparison to a normative sample and description of ‘low’ performers
We compared the performance of the 5 to 16-year-old children in our sample to the NIHTB-M normative sample for each motor subtest (Table 3). We did not include children under 5 years due to the difficulties with test administration, described above. At 2 weeks post injury, balance (median=85, IQR=68-101, p=0.04) and endurance (median=79, IQR=71-91, p<0.01) scores were significantly lower than the normative sample median, with five participants (36%) in the balance domain and six participants (35%) in the endurance domain scoring ≤ 1.5 standard deviations below the normative sample mean. Of note, 80% of subjects with ‘low’ balance performance had intracranial lesions on neuroimaging, whereas 33% of the group with ‘broadly normal’ balance scores had intracranial lesions. No significant differences were found between children with TBI and the normative sample for dexterity or grip strength, although a substantial minority of children (17% to 28%) scored more than 1.5 standard deviations below the normative sample mean in these domains. When considering subtest performance in isolation, the expected base rate of scoring more than 1.5 standard deviations below the normative sample mean is 7%. At 2 weeks post injury, median parent (U=10.5, z=−2.28, p=0.02) and child (U=10.0, z=−1.99, p=0.05) PedsQL-Physical scores were lower in participants with ‘low’ endurance performance compared to the ‘broadly normal’ group, but no difference in HBI-somatic scores was noted between endurance (U=24.5, z=−0.87, p=0.40). No difference in PedsQL or HBI-somatic scores was found between ‘low’ and ‘broadly normal’ balance subgroups two weeks post injury (see Table 4).
Table 3.
Performance on the NIHTB-M at 2 weeks and 6 months post injury (ages 5-16)
| 2 weeks |
6 months |
|||||||
|---|---|---|---|---|---|---|---|---|
| Domain (Test) | n | Median (IQR) Mean (SD) |
% 1.5SD ≤ Normative Sample | Results of one sample Wilcoxon Signed Rank test | n | Median (IQR) Mean (SD) |
% 1.5 SD ≤ Normative Sample | Results of one sample Wilcoxon Signed Rank test |
| Dexterity (9-Hole Pegboard Test Dominant Hand) | 18 | 100 (83-109) 94 (21) |
3 (16.7%) | z=−0.802 r=0.19 p=0.422 |
21 | 101 (88-106) 100 (15) |
1 (4.7%) | z=−0.131 r=0.03 p=0.896 |
| Dexterity (9-Hole Pegboard Test Non-Dominant Hand) | 171 | 96 (82-109) 94 (23) |
3 (17.6%) | z=−.758 r=0.18 p=0.449 |
201 | 104 (89-120) 104 (16) |
1 (5%) | z=1.188 r=0.27 p=0.235 |
| Strength (Grip Strength Dominant Hand) | 18 | 99 (75-108) 93 (22) |
5 (27.7%) | z=−0.697 r=0.17 p=0.486 |
21 | 97 (90-111) 100 (18) |
1 (4.7%) | z=−0.278 r=0.06 p=0.781 |
| Strength (Grip Strength Non-Dominant Hand) | 171 | 100 (83-110) 97 (24) |
3 (16.7%) | z=−0.310 r=0.08 p=0.756 |
201 | 99 (91-111) 102 (16) |
0 (0%) | z=0.093 r=0.21 p=0.926 |
| Balance (Standing Balance Test) | 141,2 | 85 (68-101) 86 (20) |
5 (35.7%) | z=−2.040 r=0.55 p=0.041* |
172,3 | 98 (82-105) 93 (17) |
4 (23.5%) | z=−1.375 r=0.33 p=0.169 |
| Endurance (2-Minute Walk Endurance Test) | 171 | 79 (71-91) 81 (13) |
6 (35.3%) | z=−3.466 r=0.84 p=.001* |
203 | 88 (77-98) 87 (14) |
6 (30.0%) | z=−3.086 r=0.69 p=0.002* |
Note: IQR= Interquartile Range; SD=Standard Deviation
Excludes one participant due to orthopedic injury;
Excludes three participants with missing data due to technological difficulties;
Excludes one participant due to fatigue; and
Significant at p<0.05
Table 4.
Characteristics of participants with ‘low’ versus ‘broadly normal’ NIHTB-M Endurance and Balance scores
| Endurance | Balance | |||||||
|---|---|---|---|---|---|---|---|---|
| 2 weeks |
6 months |
2 weeks |
6 months |
|||||
| Low | Broadly normal | Low | Broadly normal | Low | Broadly normal | Low | Broadly normal | |
| n | 6 | 11 | 6 | 14 | 5 | 9 | 4 | 13 |
| Age Median (IQR) | 14 (11-15) | 14 (10-15) | 11 (9-16) | 13 (8-14) | 14 (10-16) | 14 (8-15) | 12 (9-16) | 14 (9-16) |
| Predominant Injury Type, % (n) | MV 67% (4) | Fall 46% (5) | MV 50% (3) | Fall 62% (8) | MV 40% (2) | MV 44% (4) Fall 44% (4) |
MV 50% (2) Fall 50% (2) |
Fall 38% (5) |
| Intracranial Lesion, % (n) | 33% (2) | 55% (6) | 33% (2) | 50% (7) | 80% (4) | 33% (3) | 75% (3) | 39% (5) |
| GCS <13 % (n) | 17% (1) | 18% (2) | 17% (1) | 29% (4) | 20% (1) | 22% (2) | 50% (2) | 15% (2) |
| Observed LOC, % (n)1 | 83% (5) | 50% (4) | 60% (3) | 46% (5) | 50% (2) | 71% (5) | 67% (2) | 46% (5) |
| Prior TBI, % (n) | 33% (2) | 9% (1) | 0% (0) | 21% (3) | 40% (2) | 11% (1) | 25% (1) | 15% (2) |
| ADHD, n (%) | 50% (3) | 18% (2) | 33% (2) | 14% (2) | 40% (2) | 11% (1) | 50% (2) | 8% (1) |
| PedsQL-Phys Child Median (IQR), Mean (SD) | 72 (52-80) 67 (16) |
90 (72-94) 85 (13) |
75 (59-88) 75 (16) |
94 (91-100) 91 (14) |
81 (73-89) 81 (9) |
91 (64-97) 81 (19) |
91 (81-98) 90 (9) |
95 (73-95) 87 (18) |
| PedsQL-Phys Parent, Median (IQR), Mean (SD) | 53 (34-78)* 55 (20) |
81 (60-88) 76 (19) |
78 (70-98) 81 (16) |
97 (94-100) 91 (16) |
78 (44-89) 69 (25) |
78 (47-83) 67 (22) |
95 (94-99) 96 (3) |
94 (77-98) 86 (17) |
| HBI-Somatic, Median (IQR) Mean (SD) | 7 (3-14) 8 (6) |
5 (0-9) 5 (4) |
2 (0-7) 3 (5) |
0 (0-2) 1 (2) |
4 (1-8) 4 (4) |
4 (2-8) 5 (4) |
1 (0-3) 1 (1) |
1 (0-5) 3 (4) |
Note: ‘Low’ scores were defined as ≤1.5 SD below normative sample mean (≤ standard score of 77.5). ‘Broadly normal’ scores were defined as >1.5 SD below normative sample mean (>Standard score of 77.5). IQR=Interquartile range; GCS=Glasgow Coma Score; LOC=Loss of Consciousness; ADHD=reported history of attention deficit hyperactivity disorder; PedsQL-Phys=Pediatric Quality of Life-Physical; Child=Child rated; Parent=Parent rated; HBI=Health and Behavior Inventory, current symptoms; MV=Motor vehicle accident;
Excludes unwitnessed injuries.
=significant difference in median score compared to the ‘broadly normal’ group via Mann-Whitney U test at p<0.05.
At 6 months post injury, endurance of children with TBI (median= 88, IQR= 77-98, p<0.01) was significantly below the normative sample median, with six (30%) participants obtaining ‘low’ endurance scores. No significant differences were found between children with TBI and the normative sample for dexterity, grip strength, or balance. However, in the balance domain, 4 out of 17 (24%) children had ‘low’ balance scores. At 6 months post injury, no significant difference in PedsQL-child (U=17.0, z=−1.97, p=0.06), PedsQL-Parent (U=27.5, z=−1.22, p=0.24) or HBI-somatic (U=29.0, z=−1.15, p=0.31) ratings was observed between those with ‘low’ endurance versus ‘broadly normal’ endurance scores. Similarly, no differences in PedsQL-child (U=21.0, z=−0.37, p=0.80), PedsQL-Parent (U=21.5, z=−0.52, p=0.62), or HBI-somatic (U=22.5, z=−0.42, p=0.70) ratings was seen between those with ‘low’ versus ‘broadly normal’ balance scores (see Table 4).
Discussion
To our knowledge, this is the first study to examine the feasibility of using the NIHTB-M to assess motor function performance in children with TBI. In our sample of hospital-presenting children with TBI, who required neuroimaging on clinical grounds, the NIHTB-M was well tolerated by all but the youngest children and typically completed in less than 25 minutes. We encountered certain barriers to administration including very young children (i.e., 3 and 4-year-olds) having difficulty following test instructions and being distracted by the technology used for data capture, lost data due to disconnection between the iPod and iPad, orthopedic injuries, medical complexity, or fatigue.
Our experience with very young children is inconsistent with results of feasibility and normative studies of the balance assessment with healthy 3- and 4–year-old children (Beaumont, et al., 2013; Reuben, et al., 2013; Rine et al., 2013), although our observations are based on a very small sample. Given that attention and behavioral problems are common following pediatric TBI, it is possible that difficulty with direction-following was injury-related, at least during the subacute (2 week) assessment (Crowe et al., 2015).
Another factor impacting feasibility of test administration among young children may have been technological. According to the test developers, validation of the NIHTB balance assessment was completed using specific accelerometer technology (ADXL213AE, 61.2 g; Analog Devices, Inc., Norwood, MA) (Rine, et al., 2013) and not an iPod accelerometer. Even if technologically equivalent, the iPod resembles a smartphone, which seemed to make it more familiar, attractive, and distracting to some young children. Younger children may benefit from incorporating developmentally appropriate motivational techniques and strategies by the examiner, to increase their engagement in the NIHTB-M tests (without, of course, modifying the standardized administration of the tests). Finally, 2 weeks following injury, several patients remained acutely hospitalized or had co-occurring orthopedic injuries, which may be an important consideration for timing initial early post-acute assessments.
The endurance and balance subtests were most likely to identify ‘low’ motor performance following TBI. Specifically, 35% of children at 2 weeks and 30% of children at 6 months demonstrated low endurance performance and 36% of children at 2 weeks and 24% of children at 6 months demonstrated low balance performance on the NIHTB-M. Among patients with moderate to severe TBI, limited endurance may be a consequence of prolonged immobility, but is also noted in people with milder brain injuries, who exhibit exercise intolerance (Bell and Shenouda, 2013; Quatman-Yates et al., 2018). Balance impairments are also commonly reported following TBI and are hypothesized to be caused by difficulty integrating visual, vestibular, and somatosensory information, and/or peripheral vestibular dysfunction (Alhilali et al., 2014; Guskiewicz, 2011; Shepard et al., 2013). The proportion of subjects with ‘low’ performance in these domains could be a consequence of the sample including participants with markers of increased injury severity (GCS<12, intracranial abnormalities, ICU use) who would be expected to have more significant motor impairments than those with milder injuries. (Ewing-Cobbs, et al., 1989; Jaffe, et al., 1992). However, inspection of individual case data (see Table 5) reveals that balance and endurance impairments were present in a small number of children with milder presentations in the ED albeit those warranting clinical neuroimaging.. Even in this small sample, ‘low’ endurance performance appeared associated with parent and self-report measures of physical function (PedsQL-Phys). Conversely, we found that ‘low’ balance performance was not associated with parent or self-report measures of physical function or worse somatic symptoms. Differences between performance-based tests and subjective report measures highlight the potential value of incorporating both types of measures into outcome assessment of children following TBI.
Table 5.
Characteristics of participants tested with the NIH Toolbox Motor Battery 2 weeks or 6 months following injury
| Participant | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | 12 | 13 | 14 | 15 | 16 | 17 | 18 | 19 | 20 | 21 | 22 | 23 | 24 | 25 | 26 | 27 | 28 | 29 | 30 | 31 | 32 |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Age | 8 | 16 | 14 | 10 | 5 | 7 | 11 | 12 | 4 | 13 | 6 | 14 | 8 | 15 | 15 | 3 | 16 | 6 | 7 | 14 | 16 | 7 | 10 | 4 | 11 | 16 | 14 | 14 | 16 | 14 | 3 | 11 |
| Sex | M | M | M | M | F | F | M | M | F | M | M | M | M | F | M | M | F | M | M | F | M | M | M | F | M | F | M | M | M | M | M | F |
| ADHD | No | No | No | Yes | No | No | Yes | No | No | Yes | No | No | No | No | No | 0 | No | No | No | No | No | No | No | No | Yes | Yes | No | No | No | No | No | Yes |
| Prior TBI | No | No | Yes | No | No | No | No | Yes | No | Yes | No | No | No | No | No | 0 | No | No | No | No | No | No | No | No | No | No | Yes | No | Yes | No | No | No |
| Mechanism of Injury | Fall | Fall | Sp | Fall | Fall | MV | Fall | Fall | MV | Sp | MV | Fall | Sp | MV | Fall | Fall | MV | Fall | MV | MV | Oth | Fall | MV | Fall | Sp | MV | MV | MV | Sp | MV | Fall | MV |
| Loss of Consciousness | Unk | Yes | No | Yes | No | Yes | No | No | No | Yes | Yes | No | No | Yes | Unk | no | Unk | Unk | Yes | Yes | No | Unk | Yes | No | Yes | No | Yes | Yes | Yes | Yes | Yes | No |
| Glasgow Coma Scale | 15 | 14 | 15 | 4 | 15 | 2T | 12 | 15 | 15 | 14 | 14 | 10T | 15 | 14 | 15 | 15 | 13 | 15 | 2T | 14 | 15 | 15 | 15 | 15 | 15 | 15 | 12 | 15 | 14 | 14 | 15 | 15 |
| Intracranial Abnormality (CT or MRI) | + | − | + | − | − | + | − | − | + | − | − | + | − | − | − | + | + | + | + | − | + | + | − | + | − | + | + | − | + | − | − | + |
| Hospitalization | ED | Hos | ICU | ICU | Hos | ICU | ICU | Hos | Hos | Hos | ICU | ICU | Hos | Hos | ICU | ICU | ICU | Hos | ICU | ICU | Hos | Hos | Hos | ICU | ED | Hos | ICU | Hos | ICU | ED | Hos | ICU |
| Two Weeks Following Injury | ||||||||||||||||||||||||||||||||
| PedsQL Child-Physical | 63 | 94 | 100 | 88 | 75 | 70 | 100 | 88 | NA | 84 | 44 | 94 | 94 | 66 | 100 | NA | 9 | 63 | IP | MM | 81 | 94 | 91 | NA | 59 | 75 | 72 | TC | 91 | 81 | NA | 72 |
| PedsQL Parent-Physical | 56 | 78 | 100 | 97 | 88 | 84 | 84 | 53 | ER | 31 | 34 | 81 | 91 | 59 | 31 | ER | 0 | 59 | 100 | MM | 97 | 81 | 78 | ER | 50 | 78 | 56 | 78 | 81 | 91 | ER | 88 |
| HBI Parent-Somatic, pre-injury symptoms | 1 | 3 | 3 | 0 | 1 | 1 | 0 | 6 | 2 | 0 | 0 | 0 | 0 | 10 | 3 | 0 | 0 | 1 | 0 | MM | 0 | 0 | 0 | 0 | 6 | 2 | 0 | 0 | 0 | 0 | 0 | 0 |
| HBI-Parent-Somatic, current symptoms | 13 | 10 | 5 | 3 | 2 | 8 | 0 | 6 | 1 | 9 | 4 | 4 | 3 | 13 | 4 | 4 | 12 | 5 | 12 | MM | 0 | 6 | 6 | 0 | 17 | 1 | 4 | 13 | 0 | 9 | 2 | 9 |
| 9-Hole Pegboard Test Dominant Hand | NA | NA | NA | NA | NA | 49 | 100 | TC | 77* | 66 | 122 | 109 | TC | 119 | 89 | 99* | IP | 104 | IP | MM | 100 | 96 | 84 | 107 | 53 | 83 | 109 | 103 | 83 | 103 | 110* | 117 |
| 9-Hole Pegboard Test Non-Dominant Hand | NA | NA | NA | NA | NA | 38 | 121 | TC | 86* | 70 | 105 | 128 | TC | OI | 88 | 87* | IP | 96 | IP | MM | 111 | 107 | 99 | 107 | 60 | 81 | 122 | 96 | 93 | 102 | 109* | 82 |
| Grip Strength Dominant Hand | NA | NA | NA | NA | NA | 61 | 80 | TC | 51 | 99 | 77 | 126 | TC | 94 | 103 | 105 | IP | 103 | IP | MM | 99 | 106 | 67 | 97 | 50 | 99 | 64 | 108 | 127 | 108 | 94 | 109 |
| Grip Strength Non-Dominant Hand | NA | NA | NA | NA | NA | 38 | 66 | TC | 85 | 100 | 102 | 135 | TC | OI | 111 | 75 | IP | 90 | IP | MM | 99 | 106 | 80 | 119 | 86 | 92 | 73 | 117 | 134 | 108 | 104 | 109 |
| Standing Balance Test | NA | NA | NA | NA | NA | OI | 101 | TC | DF | 56 | 100 | 102 | TC | 126 | 106 | DF | IP | 100 | IP | MM | 60 | 72 | 88 | 78 | TN | 66 | 69 | TN | 79 | 82 | 91* | TN |
| 2-Minute Walk Endurance Test | NA | NA | NA | NA | NA | OI | 94 | TC | 71* | 62 | 77 | 84 | TC | 79 | 100 | DF | IP | 103 | IP | MM | 91 | 79 | 90 | 92 | 54 | 75 | 67 | 67 | 80 | 78 | 90* | 89 |
| Six Months Following Injury | ||||||||||||||||||||||||||||||||
| PedsQL-Child-Physical | 100 | 94 | 100 | 78 | 50 | MM | 84 | 100 | MM | 81 | 56 | ER | 97 | MM | 94 | NA | 72 | MM | 100 | 100 | 100 | 94 | 78 | NA | 59 | 91 | 91 | NA | NA | NA | NA | NA |
| PedsQL-Parent-Physical | 94 | 94 | 94 | 94 | 44 | MM | 100 | 100 | MM | 81 | 56 | 97 | 100 | MM | 100 | 81 | 78 | MM | 69 | 97 | 78 | 97 | 97 | 91 | 75 | 97 | 100 | NA | NA | NA | NA | NA |
| HBI Parent-Somatic, pre-injury symptoms | 4 | 1 | 3 | 2 | 0 | MM | 1 | 0 | MM | 3 | 0 | 0 | 0 | MM | 0 | 0 | 0 | MM | 0 | 1 | 1 | 0 | 0 | 2 | 4 | 2 | 1 | NA | NA | NA | NA | NA |
| HBI Parent-Somatic, current symptoms | 3 | 1 | 5 | 0 | 0 | MM | 2 | 0 | MM | 1 | 0 | 0 | 0 | MM | 1 | 4 | 0 | MM | 8 | 0 | 5 | 0 | 1 | 2 | 12 | 1 | 0 | NA | NA | NA | NA | NA |
| 9-Hole Pegboard Test Dominant Hand | 79 | 77 | 101 | 103 | 104 | MM | 87 | 92 | MM | 78 | 130 | 103 | 107 | MM | 100 | DF | 89 | MM | 115 | 115 | 94 | 105 | 82 | 107 | 131 | 99 | 103 | NA | NA | NA | NA | NA |
| 9-Hole Pegboard Test Non-Dominant Hand | 80 | 81 | 125 | 103 | 125 | MM | 121 | 85 | MM | 77 | 107 | 122 | 100 | MM | 87 | DF | 105 | MM | 125 | 115 | 111 | 98 | OI | 107 | 118 | 98 | 96 | NA | NA | NA | NA | NA |
| Grip Strength Dominant Hand | 88 | 134 | 111 | 97 | 112 | MM | 90 | 85 | MM | 108 | 93 | 143 | 97 | MM | 106 | 74 | 92 | MM | 110 | 82 | 120 | 93 | 62 | 108 | 97 | 90 | 90 | NA | NA | NA | NA | NA |
| Grip Strength Non-Dominant Hand | 88 | 113 | 111 | 86 | 111 | MM | 101 | 86 | MM | 108 | 93 | 152 | 110 | MM | 106 | 104 | 92 | MM | 97 | 91 | 120 | 106 | OI | 119 | 97 | 84 | 91 | NA | NA | NA | NA | NA |
| Standing Balance Test | 63 | 105 | 93 | 70 | 114 | MM | TN | 91 | MM | F | TN | 109 | 113 | MM | 98 | DF | 98 | MM | 97 | 89 | 105 | TN | 98 | 87 | 98 | 60 | 75 | NA | NA | NA | NA | NA |
| 2-Minute Walk Endurance Test | 98 | 96 | 100 | 83 | 117 | MM | 77 | 89 | MM | F | 66 | 89 | 82 | MM | 86 | DF | 75 | MM | 101 | 89 | 65 | 111 | 66 | 106 | 77 | 87 | 89 | NA | NA | NA | NA | NA |
Note: ADHD=Attention Deficit Hyperactivity Disorder; CT=Computerized Tomography; MRI=Magnetic Resonance Imaging; PedsQL-Phys=Pediatric Quality of Life-Physical; Child=Child rated; Parent=Parent rated; HBI=Health and Behavior Inventory; M=Male; F=Female; Sp=Sports Injury; MV=Motor Vehicle Accident. Unk=unknown; ED=Discharged from emergency department; Hos=Admitted to hospital ward; ICU=Admitted to ICU; ‘+’= positive intracranial neuroimaging findings on CT or MRI , ‘−’=negative intracranial neuroimaging findings on CT or MRI. Reasons for Incomplete or Partially Complete assessments: TC=Time Constraint; OI=Orthopedic Injury; IP=Inpatient; DF=Direction Following. TN=Technology, MM=Missed Full TRACK-TBI Follow-up; ER=Administration Error. NA= Not Available: Outside of study time frame (NIHTB-M) or Not Completed due to the child’s age (PedsQL).
Non-standard administration, scores may not be valid.
These observations should be considered in light of several limitations. Our sample did not include children at either end of the severity spectrum. We excluded children who did not require neuroimaging on clinical grounds, likely those with the mildest clinical presentations, and although half of the sample had evidence of structural brain injury and nearly half were admitted to the intensive care unit, all children were ambulatory without use of an assistive device at the time of their assessment. We do not anticipate additional barriers to administration among children with milder presentations than seen in our sample; however, severe mobility limitations could be additional barrier to participation. Exploration of the NIHTB-M’s use and ceiling and floor effects in children at the extremes of the injury severity spectrum are needed. Second, because no control group or pre-injury performance assessments were performed, motor impairments seen in this sample cannot be attributed solely to TBI, particularly in light of evidence of balance impairments in groups of uninjured children (such as those with ADHD), who were represented in this sample (Buderath et al., 2009; Goetz et al., 2017). Finally, we report the percentage of “low” performers in each domain within our sample; however, this should not be interpreted to represent proportion of subjects with deficits among children with TBI in general or any subgroup of children with TBI. The sample was not sufficiently representative to draw definitive conclusions about the nature and severity of performance-based physical function and mobility deficits in children following TBI.
Despite these study limitations, overall, the NIHTB-M was relatively brief to administer, generally well tolerated by school-aged children and, despite occasional technological challenges, is a feasible battery of tests for the assessment of children with TBI for clinical and research purposes. Given the NIHTB-M’s feasibility, future investigations are needed to examine reliability, validity, and sensitivity to change in children with TBI, with particular focus on inpatient populations, children with severe mobility limitations, and pre-school-aged children.
Acknowledgements
The TRACK-TBI Investigators: Opeolu Adeoye, MD, University of Cincinnati; Neeraj Badjatia, MD, University of Maryland; Kim Boase, University of Washington; Yelena Bodien, PhD, Massachusetts General Hospital; M. Ross Bullock, MD PhD, University of Miami; Randall Chesnut, MD, University of Washington; John D. Corrigan, PhD, ABPP, Ohio State University; Karen Crawford, University of Southern California; Ramon Diaz-Arrastia, MD PhD, University of Pennsylvania; Sureyya Dikmen, PhD, University of Washington; Richard Ellenbogen, MD, University of Washington; V Ramana Feeser, MD, Virginia Commonwealth University; Adam R. Ferguson, PhD, University of California, San Francisco; Brandon Foreman, MD, University of Cincinnati; Raquel Gardner, University of California, San Francisco; Etienne Gaudette, PhD, University of Southern California; Joseph Giacino, PhD, Spaulding Rehabilitation Hospital; Dana Goldman, PhD, University of Southern California; Luis Gonzalez, TIRR Memorial Hermann; Shankar Gopinath, MD, Baylor College of Medicine; Rao Gullapalli, PhD, University of Maryland; J Claude Hemphill, MD, University of California, San Francisco; Gillian Hotz, PhD, University of Miami; Sonia Jain, PhD, University of California, San Diego; Frederick K. Korley, MD, PhD, University of Michigan; Joel Kramer, PsyD, University of California, San Francisco; Natalie Kreitzer, MD, University of Cincinnati; Harvey Levin, MD, Baylor College of Medicine; Chris Lindsell, PhD, Vanderbilt University; Joan Machamer, MA, University of Washington; Christopher Madden, MD, UT Southwestern; Geoffrey T Manley, MD PhD, University of California, San Francisco; Alastair Martin, PhD, University of California, San Francisco; Thomas McAllister, MD, Indiana University; Michael McCrea, PhD, Medical College of Wisconsin; Randall Merchant, PhD, Virginia Commonwealth University; Pratik Mukherjee, MD PhD, University of California, San Francisco; Lindsay Nelson, PhD, Medical College of Wisconsin; Laura B. Ngwenya, MD, PhD, University of Cincinnati, Florence Noel, PhD, Baylor College of Medicine; David Okonkwo, MD PhD, University of Pittsburgh; Eva Palacios, PhD, University of California, San Francisco; Daniel Perl, MD, Uniformed Services University; Ava Puccio, PhD, University of Pittsburgh; Miri Rabinowitz, PhD, University of Pittsburgh; Claudia Robertson, MD, Baylor College of Medicine; Jonathan Rosand, MD, MSc, Massachusetts General Hospital; Angelle Sander, PhD, Baylor College of Medicine; Gabriella Satris, University of California, San Francisco; David Schnyer, PhD, UT Austin; Seth Seabury, PhD, University of Southern California; Sabrina Taylor, PhD, University of California, San Francisco; Nancy Temkin, PhD, University of Washington; Arthur Toga, PhD, University of Southern California; Alex Valadka, MD, Virginia Commonwealth University; Mary Vassar, RN MS, University of California, San Francisco; Paul Vespa, MD, University of California, Los Angeles; Kevin Wang, PhD, University of Florida; John K. Yue, CCRC, PMP, University of California, San Francisco; Esther Yuh, MD PhD, University of California, San Francisco; Ross Zafonte, Harvard Medical School
The authors also thank Research Coordinators, Scott Haire and Carla Fortes-Monteiro and lab members: Beth Costine-Bartell, Eleanor Crawford, George Price, John Shen, Madeline Perlewitz, Natalie Escobar, Jacqueline Andrews, Scott Henderson, Zoe Silsby, Andrew Bourque, and Madeline Karsten for their invaluable contributions.
Disclosure Statement
General Disclosure: Grant Iverson has received research support from test publishing companies including Psychological Assessment Resources, Inc. and CNS Vital Signs in the past (not in the past 5 years). He acknowledges unrestricted philanthropic support from ImPACT Applications, Inc., the Mooney-Reed Charitable Foundation, Heinz Family Foundation, and the Spaulding Research Institute. He receives royalties for one neuropsychological test (Wisconsin Card Sorting Test-64 Card Version).
Sources of Funding:
This project was supported by the National Institutes of Health (NIH), National Institute of Neurological Disorders and Stroke (NINDS), and Department of Health and Human Services, through U01NS086090-01. NIH had no role in the design, or conduct of the study including collection, management, analysis, or interpretation of the data; or preparation, review, or approval of the manuscript. Emily Evans receives funding through the Center on Health Services Training and Research (CoHSTAR).
Footnotes
No other conflict of interest or competing financial interests exist.
Contributor Information
Emily A. Evans, Department of Neurosurgery, Massachusetts General Hospital, MGH-Institute of Health Professions.
Nathan E. Cook, Department of Physical Medicine and Rehabilitation, Harvard Medical School; MassGeneral Hospital for Children™ Sports Concussion Program; Massachusetts General Hospital; Spaulding Rehabilitation Hospital; Boston, MA
Grant L. Iverson, Department of Physical Medicine and Rehabilitation, Harvard Medical School; Spaulding Rehabilitation Hospital and Spaulding Research Institute; MassGeneral Hospital for Children™ Sports Concussion Program; Home Base, A Red Sox Foundation and Massachusetts General Hospital Program, Boston, MA
Elise L. Townsend, Department of Physical Therapy, School of Health and Rehabilitation Sciences, MGH Institute of Health Professions, Boston, MA.
Ann-Christine Duhaime, Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA.
The TRACK-TBI Investigators, University of California, San Francisco, San Francisco General Hospital and Trauma Center, San Francisco, CA.
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