Tbi School Assessment
Tbi School Assessment
Tbi School Assessment
Author Manuscript
J Int Neuropsychol Soc. Author manuscript; available in PMC 2009 August 27.
Published in final edited form as:
NIH-PA Author Manuscript
H. Gerry Taylor, Ph.D1, Maegan Swartwout, B.A2, Keith O. Yeates, Ph.D3, Nicolay C. Walz,
Ph.D4, Terry Stancin, Ph.D5, and Shari L. Wade, Ph.D6
1 Division of Developmental and Behavioral Pediatrics and Pediatric Psychology, Department of
Pediatrics, Case Western Reserve University and University Hospitals Case Medical Center,
Cleveland, Ohio
2 Department of Psychology, University of Houston, Columbus, Ohio
3Division of Pediatric Psychology, Department of Pediatrics, Columbus Children’s Hospital, The
Ohio State University & Children’s Research Institute, Columbus, Ohio
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Abstract
Previous studies have documented weaknesses in cognitive ability and early academic readiness in
young children with traumatic brain injury (TBI). However, few of these studies have rigorously
controlled for demographic characteristics, examined the effects of TBI severity on a wide range of
skills, or explored moderating influences of environmental factors on outcomes. To meet these
objectives, each of three groups of children with TBI (20 with severe, 64 with moderate, and 15 with
mild) were compared with a group of 117 children with orthopedic injuries (OI group). The children
were hospitalized for their injuries between 3 and 6 years of age and were assessed an average of 1½
months post injury. Analysis revealed generalized weaknesses in cognitive and school readiness
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skills in the severe TBI group and suggested less pervasive effects of moderate and mild TBI. Indices
of TBI severity predicted outcomes within the TBI sample and environmental factors moderated the
effects of TBI on some measures. The findings document adverse effects of TBI in early childhood
on post-acute cognitive and school readiness skills and indicate that residual deficits are related to
both injury severity and the family environment.
INTRODUCTION
Traumatic brain injury (TBI) is one of the most common causes of death and long-term
disability in the pediatric age range (Gotschall, 1993; Kraus, 1995). According to a report on
Emergency Department (ED) visit, hospitalizations, and deaths in the United States for the
years 1995–2001 (Langlois et al., 2006), nearly half a million children 0–14 years of age had
TBI each year during this period. Of this number, 91.6% were treated and released from an
Corresponding author: H. Gerry Taylor, PhD, Division of Developmental/Behavioral Pediatrics and Psychology, D.O. Walker Building
Suite 3150, 10524 Euclid Ave., Cleveland, OH 44106, FAX: 216-844-6276/PHONE: 216-844-6227; EMAIL: [email protected].
Taylor et al. Page 2
ED, 7.8 % were hospitalized, and .6% died. Hospitalization rates in this age range were higher
for males than females by a ratio of nearly 2:1. Of those cases for which the external cause of
injury was known, falls were a more common cause (39%) than motor vehicle-related events
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(11%), though these two causes were more equally distributed in children over 4 years of age.
Defining severity based on the Glasgow Coma Scale (GCS, Jennett & Teasdale, 1974) score,
Kraus (1995) estimated that most children sustain mild TBI (80–90%). Incidence rates are
lower for moderate (7%–8%) and severe (5%–8%) TBI, but these more serious injuries are
more often associated with long-term disability.
The consequences of TBI in children include physical conditions (e.g., neuromotor impairment,
seizures, trauma-related orthopedic injuries), lowered cognitive and academic skills relative to
age expectations or preinjury estimates, and problems in school performance, behavior,
socialization, and adaptive functioning (Anderson et al., 2006; Ewing-Cobbs et al., 2004b;
Stancin et al., 2002; Schwartz et al., 2003; Yeates & Taylor, 1997; Yeates, 2000). Studies of
cognitive sequelae document global reductions in ability as measured by IQ testing, as well as
impairments in the domains of language, memory, problem-solving, perceptual-motor skills,
and attention and executive function (Anderson et al., 2006; Ewing-Cobbs et al., 2004b; Fay
et al., 1994; Levin et al., 1995; Taylor et al., 1999; Yeates, 2000). Despite their pervasiveness,
investigations of outcomes after TBI in school-age children indicate that effects may be
especially pronounced on measures of perceptual and psychomotor speed, attention, planning
and mental flexibility, discourse processing, and verbal recall (Anderson & Catroppa, 2005,
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Bawden et al., 1985; Chadwick et al., 1981; Donders, 2001; Levin & Eisenberg, 1979; Rutter,
1981; Taylor et al., 1999; Tremont et al., 1999; Yeates, 2000). Relative deficits are also
observed on tasks with greater demands on self-organization, inferencing, or metacognition,
as opposed to those providing external structure or tapping the child’s existing knowledge base
(Dennis & Barnes, 2001; Dennis et al., 1996, 2001; Donders & Giroux, 2005; Ewing-Cobbs
& Barnes, 2002; Hanten et al., 2002).
More negative outcomes are predicted by more severe TBI and less advantaged family
environments (Anderson et al., 2006; Fletcher et al., 1995; Swartz et al., 2003; Taylor et al.,
1999; Taylor et al., 2001). Cognitive deficits have been observed in both younger and older
children with moderate to severe TBI (Anderson et al., 2004, 2005a, 2006; Taylor et al.,
1999). Studies of children with mild TBI have yielded less consistent findings, with some
studies demonstrating only transient cognitive deficits if any and others suggesting emerging
consequences over time post injury (Anderson et al., 2001; Gronwald et al., 1997; Keenan et
al., 2007; Ponsford et al., 1999). Children with more severe TBI show some recovery of
cognitive and academic abilities but this occurs primarily during the first year post injury after
which there is a slowing of any continued catch-up growth (Anderson et al., 2004; Chadwick
et al., 1981; Ewing-Cobbs et al., 2004b; Jaffe et al., 1995; Taylor et al., 2004; Yeates et al.,
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2004).
Younger age at injury is another predictor of more negative outcomes. Specifically, children
aged 2 to 7 years at the time of injury are more susceptible to deficits in expressive language,
attention, and academic achievement and show less recovery of IQ compared with children
injured at later ages (Anderson et al., 2005b; Barnes et al., 1999; Dennis et al., 1995; Ewing-
Cobbs et al., 1997, 2004b; Kaufmann et al., 1993; Verger et al., 2000). Deficits that emerge
over time are also reported in children injured at a young age (Anderson et al., 1999, 2000;
Ewing-Cobbs et al., 2004a). Postinjury development and expressive language skills are
particularly compromised in infants and toddlers (< 3 years) (Anderson et al., 2005b; Ewing-
Cobbs et al., 1989). Researchers have speculated that the poorer outcomes in younger children
may reflect a greater susceptibility to diffuse brain insult or abnormalities in neurogenesis, or
a greater effect of injury on post-injury skill development (Anderson & Moore, 1995; Barnes
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et al., 1999; Ewing-Cobbs et al., 1997, 2004a, 2004b; Taylor & Alden, 1997; Wetherington &
Hooper, 2006).
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The primary objective of the present study was to investigate the effects of TBI during early
childhood on post-acute neuropsychological and school readiness skills using methods that
rigorously control for non-injury influences on outcomes. To provide an estimate of the effects
of TBI that took into account pre-injury risk exposure as well as the experience of
hospitalization for injury, children admitted to hospitals for orthopedic injuries but without
TBI were recruited as a comparison group. Outcomes were assessed using comprehensive
measures of cognitive and early academic skills that were applicable across all or at least a
major portion of the 3- to 6-year-old age range. Findings suggesting that children’s self-
regulatory or executive functions may be vulnerable to TBI and may play an important role in
children’s ongoing development (Blair, 2002; Bronson, 2002; Anderson et al., 2005c; Ewing-
Cobbs et al., 2004a) prompted inclusion of several experimental measures of this skill domain.
Finally, group comparisons were made controlling for background factors.
We hypothesized deficits in young children hospitalized for TBI would have deficits in
cognitive and school readiness skills relative to children with orthopedic injuries only. We
anticipated that these deficits would be most pervasive in children with more severe TBI, but
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that impairments would also be found in children with moderate and mild TBI. Given the failure
of many previous studies to investigate a wide range of outcomes in young children with TBI,
we anticipated wide-ranging deficits and did not have expectations with respect to which skills
would be more or less affected. Based on previous studies, we also explored the possibility
that the effects of TBI severity would be exacerbated by less advantaged family environments
and younger age at injury.
METHODS
Design
Data were collected as part of a longitudinal investigation of TBI in young children that
employed a concurrent cohort/prospective research design. The study compared post-acute
neuropsychological and early academic skills in children hospitalized for TBI at varying levels
of severity with children hospitalized for orthopedic injuries not accompanied by TBI (OI
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group). The rationale for recruiting children with OI as a comparison group was to examine
the consequences of TBI in relation to outcomes for children who also experienced
hospitalization for their injuries and who, by virtue of being at risk for injury, were more likely
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that uninjured children to be have similar preinjury behavior and family characteristics
(Anderson et al., 2004; Goldstrohm & Arffa, 2005). The initial assessment was conducted in
the post-acute period and included tests of neuropsychological and early academic skills and
data from parents regarding the family environment.
Sample
Children were recruited from consecutive admissions of children with mild to severe TBI or
with OI at three tertiary care children's hospitals and a general hospital, all of which had Level
1 trauma centers. The study was approved by the ethics boards of all participating hospitals
and informed consent was obtained prior to participation. Eligibility criteria included age at
injury between 3 years, 0 months and 6 years, 11 months, no documentation in the medical
chart or in parent interview of child abuse as a cause of the injury, and English as the primary
spoken language in the home. Eligibility for the TBI group included a TBI due to blunt trauma
requiring overnight admission to the hospital and either a GCS score <15 (suggesting altered
neurological status) or evidence for TBI-related brain abnormalities from cortical tomography
(CT) or magnetic resonance imaging (MRI).
Consistent with previous investigations (Anderson et al., 2006; Fletcher et al., 1990; Yeates et
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al., 2004), severe TBI was defined as one resulting in a GCS score of 8 or less. Moderate TBI
was defined as a GCS score of 9–12 or a higher GCS score with abnormal neuroimaging. A
final group of children with mild TBI comprised those participants with GCS scores of 13–14
without neuroimaging abnormalities. To insure that evidence for TBI was based on direct
physical examination and not on history alone, children with GCS scores of 15 and normal
neuroimaging were not recruited. Inclusion in the OI required a documented bone fracture to
an area of the body other than the head that required an overnight hospital stay, and the absence
of any evidence of loss of consciousness or other findings suggestive of brain injury (e.g.,
symptoms of concussion). Children with TBI or OI with previous diagnoses of autism or other
developmental disabilities associated with generalized cognitive impairment were also
excluded.
A total of 221 children (102 with TBI and 119 with OI) and their caregivers were enrolled in
the study. Comparison of participants with children listed in the trauma registries of the
participating hospitals who met age and injury severity criteria but were not enrolled indicated
that our sample was representative of the eligible cohort in income and race distribution. At
least a portion of the test battery was administered to 216 children (98%) at the baseline
assessment. The final sample comprised 99 children with TBI (20 severe, 64 moderate, and 15
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mild) and 117 with OI. Reasons for failure to test children included injuries that precluded
testing (2 with severe TBI) and difficulties in arranging for travel for the assessment (1 with
severe TBI and 2 with OI). Untested children did not differ from those assessed in parental
marital status, median income, race, or sex.
As shown in Table 1, the groups did not differ in age at assessment, median neighborhood
income based on the 2005 Census, distributions of sex, race, and maternal education levels, or
parent resources and stressors as measured by the Life Stressors and Social Resources
Inventory Adult Version (LISRES-A, Moos & Moss, 1994). Data collected in parent interview
also failed to suggest group differences in preinjury developmental status, though did point to
more pre-existing problems in boys than in girls. Parents reported special services prior to
injury for 2% of girls compared with 14% of boys, χ2 (df = 1, N = 213) = 8.61, p = .003.
Concerns regarding children’s preinjury development, behavior, or learning were noted for
11% of girls compared with 29% of boys, χ2 (df = 1, N = 214) = 9.93, p = .002.
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Table 2 lists injury and medical characteristics for each of the groups. The time between injury
and assessment was shorter for the OI group than for the TBI groups (significant for mild and
moderate TBI groups, nonsignificant trend for severe TBI group). This difference was likely
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related to our willingness to extend recruitment somewhat beyond 3 months post injury (our
initial recruitment window) in an effort to enroll as many of the children with TBI as possible.
The groups also differed in their mean New Injury Severity Score (NISS, Osler et al., 1997),
defined as the sum of the squares of the Abbreviated Injury Scale (AIS) scores for each child’s
three most severely injured body regions. Post-hoc tests indicated higher NISS for the severe
and moderate TBI groups compared with the mild TBI and OI groups. The groups also differed
in mean “non-head-injury” NISS, computed as the NISS minus the AIS for the head region.
According to post-hoc tests, the severity of injuries to regions other than the head was lower
in the TBI groups than in the OI group. The distribution of causes of injury for the TBI group
were consistent with national trends for young children, with a substantial proportion of both
the TBI and OI group sustaining injuries due to falls (Langlois et al., 2006). A significant group
difference in causes of injury reflects higher rates of transportation-related injuries in TBI
groups compared with the OI group.
As anticipated based on the criteria for group assignment, the mean GCS score and duration
of coma were higher for the severe TBI group than for the other TBI groups. Radiology reports
were unavailable for 2 children with TBI. The group assignments of these children were based
on information found elsewhere in the medical record. For the remainder of the TBI sample,
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these reports were used to classify neuroimaging findings into the categories of no lesion and
three grades of lesion severity. Mild abnormalities were defined as a single subdural,
subarachnoid or epidural hemorrhage, or a single intraparenchymal lesion, contusion or
hemorrhage; moderate abnormalities as multifocal lesions without diffuse abnormality as
identified by report of edema, mass effect, swelling, shift, volume loss, or diffuse axonal injury;
and severe abnormalities as any diffuse abnormality, with or without focal lesions. These
categories were consistent with research relating outcomes of TBI to the presence vs. absence
and type of brain lesions (Bowen et al., 1997; Filley et al., 1987; Levin et al., 1992; Levin et
al., 1997; Prasad et al., 2001; Williams et al. 1990). By definition, these abnormalities were
absent in the mild TBI and OI groups. Selection criteria likely accounted for the high percentage
of abnormalities in children with moderate TBI (81%).
Assessment Procedures
The child and family assessment procedures were administered as part of a more
comprehensive evaluation of the child and family that also included assessment of family
outcomes, ratings of child behavior, and video-taped parent-child interactions. Administered
via parent interview, the LISRES-A has satisfactory internal consistency and was used to assess
interpersonal supports and stressors experienced by the caregiver in a variety of social domains
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(e.g., with family members, friends, coworkers). Child tests were administered in a fixed order,
with three separate but overlapping test batteries given to children in the age ranges: 3 years,
0 months to 3 years, 5 months; 3 years, 6 months to 5 years, 11 months; and 6 years, 0 months
to 6 years, 11 months. Examiners were not aware of group assignment, and cross-site training
was undertaken to insure consistency in test administration. Child assessment procedures are
described below.
Intelligence—The Differential Ability Scales (DAS, Elliott, 1990) was used to assess global
intelligence. The DAS is a battery of cognitive tests for ages 2½ through 17 years. To obtain
a measure of general cognitive ability, we administered the core subtests needed to compute
the General Conceptual Ability score (GCA). Four subtests contributed to the GCA for children
ages 3 years, 0 months to 3 years, 5 months; and 6 subtests for older children. This measure
of intelligence was chosen for its excellent psychometric properties and because it has norms
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extending into the early childhood age range. Internal consistency indexes are .89 or higher
across this age range and test-retest reliability is .90 over a 4-week interval. Standard scores
for age were used in analysis of these and other measures with published norms.
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Memory—Tests of auditory and visual memory included DAS Recognition of Pictures and
Recall of Digits, the NEPSY Sentence Memory subtest, and the Story Recall subtest of the
Woodcock Johnson Tests of Achievement, Third Edition (WJ-III, Woodcock et al., 2001).
Recall of Digits is a test of verbal working memory that requires the child to repeat back
increasingly long strings of digits, first forward and then in reverse. In Sentence Memory, the
child is asked to repeat orally presented sentences of increasing length. In Recognition of
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Pictures, the child is shown a picture of one or more objects for 5 or 10 seconds and is then
asked to pick out these objects from a display that includes both target and distractor pictures.
In Story Recall, the child is required to retell a series of brief stories.
to switch between color and shape names according to learned contingencies. An efficiency
score was computed for each condition (Simple Naming, Inhibition, Switch, and Both
inhibition and switching) using the formula number correct divided by completion time. In
DA, the child is asked to retrieve a reward (e.g., an M&M or a Cheerio) hidden under one of
two cups placed side by side. The contingency is then reversed with the reward hidden under
the other cup. The child is not allowed to see where the reward is placed, but can learn to
anticipate placement because the placement side is reversed after each correct response.
Performance was defined in terms of number of consecutively correct alternations. Delay of
Gratification requires the child to inhibit opening an attractive gift, with performance defined
in terms of contact vs. no contact with the gift.
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Basic Concept Scale - Revised (Bracken, 1998), as well as the WJ-III Letter/Word
Identification, Spelling, and Applied Problems subtests. In addition, DAS Early Number
Concepts was administered to the younger two age groups. The SRC assesses content found
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in most preschool and primary grade curricula (e.g., recognition of colors, letters, numbers,
sizes, comparisons and shapes). The assessment is brief and requires only that the child point
to the correct response. The WJ-III subtests administered measure letter/word recognition,
pencil control and written spelling of letters and words, and knowledge of early math concepts.
The latter subtests have test-retest reliabilities ranging from .85 to .96 for young children, with
established validity in relation to other achievement tests. Early Number Concepts assesses the
child’s ability to count, compare, and solve elementary number problems.
Data Analysis
Prior to analysis, raw scores on the outcome measures were converted to age-standardized
scores using published norms. Because published age norms were unavailable for Shape School
and DA, age-expected scores on these tests were generated based on regression analysis of
data from the OI group. Age-adjusted z scores were then computed for each measure by
dividing the differences between each observed and age-predicted score by the standard error
of the estimate. Potential influences of extreme scores on results were limited by truncating,
or windsorizing, standard scores to within 3 standard deviations of the mean score (Tabachnick
& Fidell, 1989). Examination of the scores revealed normal distributions for all continuous
measures with acceptable levels of skewness and kurtosis.
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Group comparisons on the continuous measures of outcome were made using analysis of
covariance (ANCOVA). Group effects were defined by preplanned contrasts of each TBI group
with the OI group. Covariates included a measure of socioeconomic status (SES), sex, and race
(white/non-white) as justified by evidence for associations of these factors with cognitive
abilities in children (McDermott, 1995). Covariate-adjusted logistic analysis was used to
examine group differences in odds of contact vs. no contact on the Delayed Gratification Task,
with age at assessment entered as an additional covariate in analysis of this measure. To assess
the dose-response relationship of TBI presence and severity with outcome, a further set of
secondary analyses examined the linear trend between degree of TBI (none or 0 = OI; 1 = mild
TBI, 2 = moderate TBI, and 3= severe TBI) and covariate-adjusted scores.
Preliminary analysis revealed that primary caregiver education level and median census tract
income were positively correlated with each other and with most neuropsychological
outcomes. SES was thus defined as the mean of the sample z-scores for these two variables.
Additional sociodemographic variables (e.g., parent marital status and occupation) were
examined but were excluded after initial analyses failed to reveal associations with outcomes
independent of parent education and census income. Time since injury was not considered as
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analysis failed to reveal associations with the performance of the TBI sample.
Regression analysis was used to examine moderating effects of SES, LISRES-A stressors and
resources scores, and age at injury on the group differences. To test for moderation, each of
these factors was entered separately into a regression along with the TBI-OI group contrast
terms and the interaction of each contrast with that factor. Models that included the covariates
were used to subsequently examine the moderating effects of LISRES-A resources and
stressors and age at injury. Moderating effects of race and sex were not examined due to small
cell sizes for the severe and mild TBI groups. Logistic regression was conducted to investigate
moderating effects on the Delayed Gratification Task, with age at assessment again included
as an additional covariate.
Classification of children into mild, moderate, and severe TBI groups was based on traditional
distinctions but did not permit empirical examination of the combined effects of different
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dimensions of TBI severity. To further investigate the relation of injury severity to outcomes
for the children with TBI, we conducted regression analyses of data from the three TBI groups
combined. Severity measures included the GCS score, coma duration (none, <24 hours, ≥24
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hours), NISS, and the presence and severity of neuroimaging abnormality as defined above.
The combined effects of these indices on outcomes, the GCS score, NISS, and neuroimaging
abnormality were examined by entering these factors into a hierarchical regression following
entry of SES, race, and sex. Because the GCS score was closely related to coma duration (r = .
85, p < .001), the latter variable was not included in these regressions. The NISS and
neuroimaging abnormality were also correlated (r = .60, p < .001) but analysis did not indicate
high levels of collinearity.
Sample size for each measure varied due to a restricted age range for some of the tests and the
inability of some children to complete some of the tests. An alpha of .05 for all comparisons
was justified by our interest in examining the effects of TBI on specific measures rather than
testing a study-wide hypothesis (Brandt, 2007). Effect sizes provided an indication of the
magnitude of group differences.
RESULTS
Group Differences
Table 3 summarizes group performance on the tests by domain. Significant group contrasts
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from the ANCOVAs are also reported. As shown in the table, the severe TBI group had lower
scores than the OI group on the GCA, contrast estimate (CE) (standard error [se]) = −10.58
(3.25), p = .001, Sentence Memory, CE = −1.62 (0.68), p = .018, Story Recall, CE = −8.75
(3.60), p = .016; Recognition of Pictures, CE = −6.22 (2.62), p = .018, Recall of Digits, CE =
−6.40 (2.51), p = .012, Pattern Construction, CE = −9.46 (2.35), p < .001, Copying Designs,
CE = −5.52 (2.22), p = .014, Early Number Concepts, CE = −6.63 (2.31), p = .005, and SRC,
CE = −11.40 (3.36), p = .001. The moderate TBI group had lower scores than the OI group on
Pragmatic Judgment, CE = −4.62 (2.03), p = .024, Sentence Memory, CE = −1.19 (0.44), p = .
007, Recall of Digits, CE = −4.55 (1.66), p = .007, Shape School Both condition, CE = −0.37
(0.18), p =.044, and SRC, CE = −4.56 (2.14), p = .034. The only test on which the mild TBI
group had lower scores than the OI group was Pragmatic Judgment, CE = −4.62 (2.03), p =.
037. It is unclear why adverse effects on Pragmatic Judgment were found for children with
moderate and mild TBI but not for those with severe TBI. However, the ordering or group
means for most measures were in the expected direction.
Many of the effect sizes for the severe TBI-OI group contrasts were of medium magnitude
(Cohen’s d = .5-.8), whereas most effects for the moderate TBI-OI group contrasts were small
(Cohen’s d = .2-.5). Effect sizes for several of the mild TBI-OI group contrasts were in the
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medium range and in the hypothesized direction despite a lack of statistical significance, with
nonsignificant trends (p < .1) for Verbal Fluency, Recall of Digits, and the Shape School Simple
Naming and Switch conditions.
Results from the multiple regressions also revealed that all three covariates accounted from
unique variance in at least some outcomes. Higher SES was associated with better performance
on all tests except for the Gift Delay, DA, and the Shape School Both condition. Whites scored
higher than nonwhites on Verbal Comprehension, Naming Vocabulary, and the Shape School
Both condition. Females outperformed males on all the GCA, Pragmatic Judgment, Verbal
Fluency, Verbal Comprehension, all four memory tests, Pattern Construction, Shape School
Simple Naming and Inhibition conditions, Letter/Word Identification, and Spelling.
In regressions examining the effect of group along a continuum from OI to severe TBI,
significant linear trend effects were found for GCA, unstandardized beta (B) (se) = −2.08
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(0.84), p = .014, Sentence Memory, B = −0.57 (0.18), p = .001, Story Recall, B = −2.25 (0.87),
p = .011, Recall of Digits, B = −2.21 (0.66), p = .011, Pattern Construction, B = −1.38 (0.63),
p = .029, Shape School Switch condition, B = −0.17 (0.07), p = .015, Shape School Both
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condition, B = −0.21 (0.07), p = .004, Early Number Concepts, B = −1.36 (0.66), p = .039, and
SRC, B = −2.99 (0.86), p = .011. For each of these outcomes, scores decreased with increasing
TBI severity.
of Pictures, R2 change = .09, F (3, 84) = 10.45, p < .025, Pattern Construction, R2 change = .
22, F (3, 69) = 8.78, p < .001, Copying, R2 change = .16, F (3, 50) = 4.97, p = .004, Applied
Problems, R2 change = .10, F (3, 81) = 4.14, p = .009, Early Number Concepts, R2 change = .
15, F (3, 51) = 4.91, p = .004, and SRC, R2 change = .08, F (3, 87) = 3.92, p = .011.
Group differences in some outcomes were also moderated by LISRES-A stressors. These
effects included a stressors x severe TBI-OI group contrast for Pattern Construction, B = 0.66
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(0.28), p = .021, and stressors x moderate TBI-OI group contrast interactions for Spelling, B
= −0.78 (0.29), p = .008, and SRC, B = −0.72 (0.30), p = .018. According to results from follow-
up analyses, the source of the moderating effect on Pattern Construction was an association of
increasing stressors with lesser effects of severe TBI. The negative consequences of severe
TBI on Pattern Construction were nevertheless evident at both lower and higher levels of
stressors. In contrast, increasing stressors were associated with more negative consequences
of moderate TBI on Spelling and SRC. Further follow-up analyses these effects indicated
adverse effect of moderate TBI for children at high stressors (1 SD below the sample mean)
for both Spelling (p = .022) and SRC (p = .002).
The only moderating effects of age at injury were on the mild TBI-OI group contrasts for
Pragmatic Judgment, B = 7.83 (3.56), p = .029, and Letter/Word Identification, B = −10.63
(4.36), p = .016. Follow-up analyses of these interactions revealed that younger age at injury
predicted lower scores for the mild TBI group on Pragmatic Judgment, while older age at injury
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predicted lower scores on Letter/Word Identification. Similar but less dramatic age-at-injury
effects were evident for the other TBI groups. In contrast, age at injury was unrelated to scores
on these tests for the OI group. Follow-up tests revealed an adverse effect of mild TBI on
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Pragmatic Judgment only in younger children (defined as 1 SD below the sample mean age)
(p = .005), and a trend for an adverse effect on Letter/Word Identification only in older children
(defined as 1 SD above the sample mean) (p = .09).
DISCUSSION
Effects of Severe, Moderate, and Mild TBI in Young Children
Consistent with findings from past research on young children, the participant’s in this study
with either severe or moderate TBI performed more poorly than the OI group on a wide range
of neuropsychological and achievement tests (Anderson et al., 1997, 2006; Anderson &
Catroppa, 2005; Ewing-Cobbs et al., 1989, 1997, 2004a, 2004b; Morse et al., 1999). Compared
with the OI group, children with severe TBI had poorer general cognitive ability as measured
by the GCA and lower scores on tests of memory, spatial reasoning, executive function, and
school readiness skills. Although group comparisons failed to indicate deficits on some verbal
tests, a negative effect of severe TBI on Naming Vocabulary was observed in children with
low SES. The moderate TBI group performed more poorly than the OI group on tests of
pragmatic language, memory, executive function, and school readiness concepts, but not in
general ability. The effect sizes for the latter differences were generally smaller than those for
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the severe TBI vs. OI group contrasts. Similar to previous findings, moderate TBI in young
children thus had more selective and less pronounced consequences than severe TBI (Anderson
et al., 1997, 2005; Ewing-Cobbs et al., 1997; Goldstrohm & Arffa, 2005).
The only measure on which the mild TBI group performed significantly less well than the OI
group was Pragmatic Judgment. However, this difference yielded a medium effect size, as did
differences between the mild TBI and OI groups on Verbal Fluency, Recall of Digits, and the
Shape School Simple Naming condition. In view of the small size of the mild TBI group, these
results are interpreted as at least tentative support for post-acute neurocognitive effects of these
injuries. Previous studies have yielded inconsistent effects of mild TBI, with some studies
demonstrating adverse consequences for cognition or achievement (Anderson et al., 2001;
Dennis & Barnes, 2001; Gronwall et al., 1997) and others not (Anderson et al., 2005a; 2006).
Results may vary depending on when after injury children are assessed and criteria used to
define mild TBI (Satz et al., 1997). We recruited children who were hospitalized for at least 1
day and had some impairment in consciousness as defined by a GCS score of 13 or 14. For
this reason, our mild TBI group may have had more significant trauma than children discharged
from out-patient emergency departments or with GCS scores of 15.
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Taylor et al. Page 11
findings indicating that multiple measures of TBI severity are useful in predicting outcomes
of TBI (Bowen et al., 1997; Foreman et al., 2007; Levin, 1995; Levin & Eisenberg, 1979;
Prasad et al., 2002).
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The findings also documented moderating influences of non-injury factors on some of the
group differences. In keeping with results of our previous study of older children with TBI
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(Taylor et al., 1995, 2002; Yeates et al., 1997), weaknesses in Naming Vocabulary in the severe
TBI group were evident only at lower levels of SES, and weaknesses in Spelling and the SRC
in the moderate TBI group were found only at higher levels of parent stressors. At least for
measures of verbal and early academic skills, the sequelae of TBI appeared to be exacerbated
by environment disadvantage. Possible explanations for these findings are that these skills were
not as well established in children from less advantaged backgrounds and thus more easily
disrupted by TBI, or that fewer resources were available after injury to support postinjury
recovery (Taylor et al., 2002). The fact that all three measures involve knowledge-based skills
is consistent with these interpretations. Contrary to expectations, the adverse effects of severe
TBI on Pattern Construction and Spelling were more evident in children with higher SES.
Similar moderating effects have been found in studies of cognitive outcomes of very low birth
weight (Taylor et al., 2006) and can be explained in two ways: either children with severe TBI
are less able to benefit from environmental supports than children without TBI, or the effects
of severe TBI are dampened or obscured by social disadvantage.
Findings revealed little support for our expectation that outcomes of TBI would be worse for
children injured at younger ages. An adverse effect of mild TBI on Pragmatic Judgment was
found only in the children injured at younger ages. However, this finding is difficult to explain
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in isolation and may be an artifact of the lower mean age at injury of the mild TBI group. Such
an age disparity could arise because younger children are generally more difficult to engage
in testing (Anderson et al., ) or because the expressive language skills tapped by Pragmatic
Judgment may only be emerging these children. Analysis also revealed that age at injury
moderated differences between the mild TBI and OI groups on Letter/Word Identification. For
this measure, the adverse consequences of mild TBI were more evident with increasing age at
injury. Because the initial items on this test require only that the child point to a named symbol
whereas the later items require name retrieval, this finding may be another artifact of the group
differences in age at injury. The lack of evidence for age at injury effects contrasts with results
from previous studies that have examined TBI across wider age spans (Anderson et al.,
2005; Barnes et al., 1999; Dennis et al., 1995; Ewing-Cobbs & Barnes, 2002; Levin et al.,
1995; Verger et al., 2000), suggesting that age at injury may be less consequential in children
injured before 7 years of age (Ewing-Cobbs et al., 1997). Alternatively, the impact of younger
J Int Neuropsychol Soc. Author manuscript; available in PMC 2009 August 27.
Taylor et al. Page 12
age at injury may become more pronounced with increasing time since injury (Anderson et al.,
2000; Ewing-Cobbs et al., 2004).
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range, and a sample of children with TBI who were representative of admissions to the
participating hospitals.
One major study limitation is that the only clinical neuroimaging, in most instances CT scans,
were available to determine the presence and nature of the brain insults in the TBI sample.
Imaging methods with greater sensitivity to white matter damage and focal lesions would likely
have provided information useful in enhancing prediction of variations in outcomes of TBI
(Scheibel & Levin, 1997; Wilde et al., 2006). A further limitation is that the mild and severe
TBI groups were relatively small despite recruitment from multiple hospitals. Larger group
sizes would have increased statistical power for detection of moderating effects of
environmental variables and age at injury. Analysis of individual tests rather than ability
constructs is another potential weakness. Although this approach was justified by the lack of
established methods for assessing ability constructs in this age range, the use of multiple-
indicator latent constructs would have allowed us to more clearly distinguish the skills most
and least affected by TBI and reduced the probability of Type I error.
Conclusion
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Study findings suggest several conclusions with respect to the post-acute effects of TBI on
young children. While these conclusions are tentative given the exploratory nature of the study,
they provide a basis for formulating more specific hypotheses about how TBI affects young
children:
1. Severe TBI sustained during early childhood can result in generalized cognitive
impairment and deficits in school readiness skills. Furthermore, memory, spatial
reasoning, and executive function may be more affected than some language skills.
2. Children with moderate TBI have more specific impairments than those with severe
TBI, and similar impairments may be present in children with mild TBI.
3. Specific cognitive measures are sensitive to injury consequences. Based on effect
sizes, the DAS GCA, DAS Pattern Construction, Copying Designs, Recall of Pictures,
and Recall of Digits subtests, NEPSY Sentence Memory subtest, WJ-III Story Recall
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Taylor et al. Page 13
subtest, and Shape School Switch and Both conditions are useful in detecting
cognitive impairment in children with severe TBI. The memory measures and Shape
School are also sensitive to less severe TBI. In light of the lack of group differences
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on the DA and Delay of Gratification Task, these tasks are less likely to be useful in
examining injury effects.
4. Indices of TBI severity, including the GCS score, NISS, coma duration, and
neuroimagining abnormality, are related to cognitive and school readiness skills.
5. Age at injury is not a critical factor in predicting outcomes of TBI sustained during
the early childhood years.
6. Although measures of environmental disadvantage predict lower scores on most tests
in children with and without TBI, these factors may amplify the effects of TBI on
some tests but dampen or obscure effects on other measures.
The major clinical implication of these findings is that young children with TBI are at risk for
post-acute deficits in cognition and school readiness skills and that measures used in this study,
or similar ones, are sensitive to these deficits. The results also encourage examination of both
injury-related and environmental factors as determinants of injury consequences. We can only
speculate about the reasons for environmental moderation of injury effects, but they underscore
the complexity of influences on recovery (Taylor, 2004). Additional research is needed to better
understand the nature of the effects mild to severe TBI in young children on brain development
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and how brain pathology maps onto neurobehavioral outcomes (Taylor, 2004). Larger scale
studies of outcome will also be required, especially in examining the consequences of mild
TBI. Further research on this subset of children might explore factors contributing to the
decision to hospitalize these children and track acute changes in cognitive functioning. Based
on the presumption that mild TBI results in residual deficits in only a minority of children with
mild TBI (Bigler, 2007; Kirkwood et al., in press), it may be more helpful to find ways to
distinguish affected from unaffected individuals than to demonstrate group differences. The
development of tests that clarify the effects of TBI at all levels of severity and the study of the
factors that contribute to skill development following injury will be essential in improving our
capacity to identify and treat the sequelae of TBI in young children. We are currently following
the present cohort to determine the nature of changes in cognitive and achievement outcomes
over time post injury, evaluate behavioral sequelae, and investigate the effects of family factors
on outcomes.
Acknowledgments
Supported by grant R01 HD42729 to Dr. Wade from NICHD, in part by USPHS NIH Grant #M01 RR 08084, and by
Trauma Research grants from the State of Ohio Emergency Medical Services. The authors wish to acknowledge the
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contributions of Christine Abrahamin, Andrea Beebe, Lori Bernard, Anne Birnbaum, Beth Bishop, Tammy Matecun,
Karen Oberjohn, Elizabeth Roth, and Elizabeth Shaver in data collection and coding. The Cincinnati Children’s
Medical Center Trauma Registry, Rainbow Pediatric Trauma Center, Rainbow Babies & Children’s Hospital,
Columbus Children’s Hospital Trauma Program, and MetroHealth Center Department of Pediatrics and Trauma
Registry provided assistance with recruitment.
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Table 1
Sample Demographic Characteristics.
Group
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Age at assessment in years, M 4.86 (0.88) 5.19 (1.20) 4.68 (1.00) 5.21 (1.08)
(SD)
Males n (%) 14 (70%) 37 (58%) 6 (40%) 67 (57%)
Non-white race, n (%) 7 (35%) 22 (44%) 6 (40%) 27 (33%)
Census median family income in 52,767 (16,435) 57,096 (26,539) 51,556 (25,874) 63,888 (23,410)
dollars, M (SD)
Maternal education, n (%):
<2 years high school 0 (0%) 3 (5%) 0 (0%) 2 (2%)
2 years high school 5 (25%) 7 (11%) 1 (7%) 6 (5%)
High school degree/GED 10 (50%) 24 (38%) 7 (50%) 45 (38%)
2 years college 4 (20%) 11 (17%) 3 (21%) 23 (20%)
4 years college 1 (5%) 12 (19%) 3 (21%) 29 (25%)
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Note: TBI = traumatic brain injury; OI = orthopedic injury; SD = standard deviation; GED = General Education Diploma. All group differences non-
significant.
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Table 2
Injury and Medical Characteristics.
Group
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Age at injury in years, mean 4.74 (0.88) 5.06 (1.20) 4.55 (1.03) 5.11 (1.07)
(SD)
Length of hospital Stay in 6.70 (7.24) 2.89 (1.86) 1.60 (0.63) 1.63 (1.08)
days, mean (SD)*
NISS total, mean (SD)* 12.47 (8.57) 15.08 (7.81) 7.40 (5.87) 7.04 (2.66)
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NISS non-head- related, 1.24 (2.11) 2.44 (5.25) 1.60 (2.53) 7.04 (2.66)
mean (SD)*
Lowest GCS score, mean 3.95 (1.79) 13.45 (2.00) 13.60 (0.51)
(SD)*
Time since injury in months, 1.51 (0.75) 1.51 (0.76) 1.62 (0.82) 1.16 (0.50)
mean (SD)*
Note: TBI = traumatic brain injury; OI = orthopedic injury; SD = standard deviation; NISS = New Injury Severity Score; GCS = Glasgow Coma Scale.
*
Significant difference between groups at p < .05.
a
Injuries due to “other” causes included those related to sports and recreation, rough-housing, and falling objects.
b
See text for definition of severity of neuroimaging abnormality. Abnormality was absent in the mild TBI and OI groups by definition.
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Table 3
Neuropsychological Variables
Group
General ability: GCAb* 85.00 (15.63) 0.68 97.37(16.49) 0.10 95.36(11.78) 0.19 101.78 (15.11)
Language:
Pragmatic Judgmentb†‡ 101.00 (13.59) 0.01 99.16(14.75) 0.34 97.29(14.49) 0.56 105.10 (12.95)
Verbal Fluencyd 7.89 (2.02) 0.29 8.42 (2.93) 0.21 7.67 (2.74) 0.53 9.21 (3.00)
Verbal Comprehensionc 38.53 (10.03) 0.34 43.05 (9.88) 0.11 42.92 (7.61) 0.09 45.87 (10.86)
Naming Vocabularyc 47.35 (12.17) 0.22 50.26(11.07) 0.06 50.77 (8.60) 0.04 52.45 (10.16)
Memory:
Recognition of Picturesc* 42.05 (10.73) 0.56 49.26(12.22) 0.04 45.93 (9.75) 0.34 51.09 (10.70)
Recall of Digitsc*† 44.45 (11.88) 0.61 47.75(10.23) 0.43 47.46 (6.91) 0.50 53.07 (10.69)
Story Recallb* 101.93 (14.60) 0.65 108.72(13.62) 0.26 108.00(13.06) 0.38 113.18 (13.29)
Sentence Memoryd*† 7.95 (3.08) 0.59 8.74 (2.01) 0.43 9.50 (1.51) 0.17 10.20 (3.12)
Spatial reasoning:
Pattern Constructionc* 41.78 (10.37) 0.97 53.76 (9.81) 0.07 52.50 (7.57) 0.11 54.47 (9.77)
Copying Designsc* 39.31 (5.45) 0.63 48.27(10.16) 0.15 50.60 (8.76) 0.37 48.08 (8.59)
Picture Similaritiesc 42.41 (11.81) 0.47 49.19(11.81) 0.01 50.08(11.26) 0.10 50.61 (11.47)
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Executive Function:
Gift Delay, no contact, n (%) 8 (44%) ---- 23 (38%) ---- 7 (50%) ---- 32 (29%)
DA, consecutive alternationse −0.06 (0.90) 0.01 0.11 (1.02) 0.14 0.08 (1.16) 0.13 0.00 (1.00)
Switch condition* −0.76 (0.68) 0.61 −0.44 (0.88) 0.35 −0.61 (0.65) 0.62 −0.02 (0.97)
Page 22
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Group
Both condition*† −0.82 (0.71) 0.76 −0.47 (0.83) 0.40 −0.62 (0.80) 0.57 −0.00 (0.99)
Letter/Word Identificationb 101.21 (13.55) 0.06 103.30(16.18) 0.07 108.43(17.98) 0.15 105.64 (16.74)
Spellingb 93.58 (10.90) 0.29 98.10(13.21) 0.06 101.00(11.28) 0.07 99.46 (13.47)
Applied Problemsb 94.10 (13.25) 0.46 102.47(13.55) 0.01 106.70(13.57) 0.32 103.81 (13.71)
Early Number Conceptsc* 38.59 (7.30) 0.70 46.66(10.29) 0.02 44.82 (6.76) 0.27 48.38 (9.92)
SRCb*† 89.20 (15.20) 0.73 99.34(17.47) 0.29 103.93(14.88) 0.03 106.50 (14.80)
Note: TBI = traumatic brain injury; OI = orthopedic injury; SD = standard deviation; GCA: Differential Ability Scales General Conceptual Composite; SRC = Bracken Basic Concept Scale School
Readiness Composite.
a
Effect sizes defined by Cohen’s d: difference between estimated (covariate-adjusted) means/estimate of pooled within-group SD.
b
standard score
c
T score
d
scaled score
e
age-standardized z score
*
Significant difference, severe TBI vs. OI (p<.05).
†
Significant difference, moderate TBI vs. OI (p<.05).
J Int Neuropsychol Soc. Author manuscript; available in PMC 2009 August 27.
‡
Significant difference, mild TBI vs. OI (p<.05).
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