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Classification of Traumatic Brain Injury Severity: A Neuropsychological


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Chapter 5
Classification of Traumatic Brain Injury
Severity: A Neuropsychological Approach

Daniel N. Allen, Nicholas S. Thaler, Chad L. Cross, and Joan Mayfield

Introduction

Traumatic brain injury (TBI) continues to be one of the most common causes of
disability and death among children and adolescents in the United States each
year, with many going on to have permanent disabilities (Faul, Xu, Wald, &
Coronado, 2010; Rivara et al., 2012). However, outcomes vary dramatically such
that some children demonstrate minimal long-term impairment, while others
evidence significant continuing disability. The classification of injury severity is
important then, because it may provide one means of predicting long-term out-
comes and prescribing treatment. In this way, severity classification may assist
in identifying those children who are at increased risk for long-term disability
following TBI and suggest specific interventions that might assist in the recovery
process.

D.N. Allen, Ph.D. (*) • N.S. Thaler, M.A.


Lincy Professor of Psychology, Department of Psychology, University of Nevada Las Vegas,
4505 Maryland Parkway, Box 455030, Las Vegas, NV 89154, USA
e-mail: daniel.allen@unlv.edu; nick.thaler@gmail.com
C.L. Cross, Ph.D., P.Stat®, L.C.A.D.C., M.F.T.
Veterans Health Administration, Office of Informatics and Analytics, Las Vegas, NV, USA
School of Community Health Sciences, University of Nevada, Las Vegas,
4505 Maryland Parkway, Las Vegas, NV 89154, USA
e-mail: chad.cross@rocketmail.com
J. Mayfield, Ph.D.
Our Children’s House at Baylor, 3301 Swiss Avenue, Dallas, TX 75204, USA
e-mail: JoanM@baylorhealth.edu

D.N. Allen and G. Goldstein (eds.), Cluster Analysis in Neuropsychological Research: 95


Recent Applications, DOI 10.1007/978-1-4614-6744-1_5,
© Springer Science+Business Media New York 2013
96 D.N. Allen et al.

Despite its importance, classifying the severity of TBI has presented unique
challenges from very early on. For some disorders, where neuropathology is rela-
tively uniform across patients and where disease progression follows a relatively
well-defined course, classification efforts have been successful in staging the dis-
ease as it progresses from mild to severe, including a prototypical characterization
of both symptom expression and cognitive decline. In contrast, for disorders where
neuropathology is not uniform or heterogeneous, classifying the severity of brain
injury or dysfunction has been particularly challenging. In Chap. 3 the case for
schizophrenia is discussed, which although not an acquired disorder or typically
considered a neurological condition, is characterized by heterogeneity across a
number of domains, such as symptoms and outcomes. More relevant to the current
discussion is the observation that schizophrenia is also characterized by heteroge-
neous neurocognitive deficits. As is apparent from studies of schizophrenia, cluster
analysis can be particularly useful in identifying profiles of performance on neuro-
psychological testing that may be related to important disorder-related variables
such as treatment outcomes, medication response, and longer-term prognosis. In the
current chapter, literature is reviewed that demonstrates cluster analysis is a useful
approach to investigate neurocognitive heterogeneity present in TBI and the case if
made for the potential usefulness of tests such as the Trail Making Test (TMT) to aid
in classifying the severity of the injury.

Heterogeneity and TBI Severity Classification

Saatman et al. (2008) recently underscored the problem that heterogeneity poses to
the classification of TBI through conventional methods. Their paper summarized
the preliminary deliberations of a workgroup tasked with developing a classification
system for TBI. They state, “The heterogeneity of traumatic brain injury (TBI) is
considered one of the most significant barriers to finding effective therapeutic inter-
ventions” with a pressing need to “….develop a reliable, efficient, and valid classi-
fication system for TBI that could be used to link specific patterns of brain and
neurovascular injury with appropriate therapeutic interventions” (p. 719). While the
focus of their efforts was primarily on developing classification for therapeutic
interventions, their point is more generally relevant to classification for other pur-
poses, such as to predict educational and vocational outcomes, which is similarly
troubled by heterogeneity. Heterogeneity in outcomes arises from a number of
sources, and variability in neuropathology resulting from TBI is a major contributing
factor. This heterogeneity can be seen in Fig. 5.1, which presents computed tomog-
raphy scans (CTs) of six individuals who sustained a severe TBI. Each case high-
lights a different pathology, ranging from localized contusions to diffuse axonal
injury, which in turn may or may not be indicative of subsequent cognitive impair-
ment and functional disability. Furthermore, some children who sustain injuries
with little to no corroborating evidence from neuroimaging indicating the presence
of cerebral damage may experience substantial declines, while others with profound
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 97

Fig. 5.1 Heterogeneity of severe traumatic brain injury (TBI). Note: computed tomography (CT)
scans of six different patients with severe TBI, defined as a Glasgow Coma Scale score of 8, high-
lighting the significant heterogeneity of pathological findings. CT scans represent patients with
epidural hematomas (EDH), contusions and parenchymal hematomas (contusion/hematoma), dif-
fuse axonal injury (DAI), subdural hematoma (SDH), subarachnoid hemorrhage and intraventricu-
lar hemorrhage (SAH/IVH), and diffuse brain swelling (diffuse swelling) (From: Saatman, K. E.,
Duhaime, A. C., Bullock, R., Maas, A. I., Valadka, A., & Manley, G. T. (2008). Workshop Scientific
Team and Advisory Panel Members. Classification of traumatic brain injury for targeted therapies.
Journal of Neurotrauma, 25(7), 719–738. Used with permission. All rights reserved)

visible injuries go on to make adequate recoveries (Suskauer & Huisman, 2009).


Therefore, classification methods should incorporate both clinical and neuroimag-
ing data as well as subsequent assessments of behavioral and cognitive functions,
which are typically obtained through neuropsychological evaluation.

Current Classification Approaches

As detailed by Saatman et al. (2008) and others, there are a number of different
approaches to classify TBI. For example, pathoanatomic classification focuses on
common neuropathological features of the injury, including both lesion location
and the underlying causative processes. This approach has identified four general
types of neuropathology associated with TBI that include (1) hematomas, (2) sub-
arachnoid hemorrhage, (3) contusions, and (4) diffuse axonal injury. To the extent
98 D.N. Allen et al.

that neuropsychological tests are differentially sensitive to these various types of


neuropathology, they may prove useful as part of a multidimensional classification
system.
The physical mechanism causing TBI has also been used to classify injury sever-
ity. This approach utilizes magnitude and direction of forces acting on the brain to
predict pattern of injury (Gennarelli & Thibault, 1985) and classifies injuries based
on whether they were caused by the head striking or being struck by an object
(impact loadings) or from the brain moving within the intracranial space (inertial
loadings). It has been observed that inertial loading is often associated with diffuse
injuries (e.g., DAI), while impact loading is more often associated with focal inju-
ries (brain contusion), providing some support for the validity of this approach.
Others have classified brain injury by distinguishing between primary and second-
ary injuries resulting from specific pathophysiological mechanisms, where primary
injuries result directly from the trauma (e.g., contusions), while secondary injuries
develop following the initial injury as a result of other mechanisms (e.g., edema
causing herniation). Of import, secondary injuries are particularly viable targets for
treatment, since some may be avoided with proper and timely intervention.
Finally, classifications have been developed based on clinical signs present at the
time of injury or soon thereafter in order to predict injury severity. These clinical
signs often include length of unconsciousness and post-traumatic amnesia (PTA),
neurological signs, and confusion and disorientation following injury (Ruff, Iverson,
Barth, Bush, & Broshek, 2009). Different professional organizations have used
combinations of these signs to develop criteria for classifying severity of brain
injury (e.g., American Congress of Rehabilitation Medicine, 1993; Carroll, Cassidy,
Holm, Kraus, & Coronado, 2004), although there is some variability in the criteria
used across disciplines and sites.
One of the most commonly used clinical indicators is the Glasgow Coma Scale
score (GCS; Teasdale & Jennett, 1974), which reflects the depth of coma. The GCS
is a 15-point scale with severe injury defined as a score of 8 or less, moderate injury
as a score of 9–12, and a mild injury as reflected by scores of 13 or greater. GCS
scores have demonstrated usefulness in predicting a number of important outcomes
including the probability of cognitive recovery and the development of cerebral
atrophy, among others (Cifu et al., 1997; Dikmen & Machamer, 1995; Ghosh et al.,
2009), although the GCS is not without limitations (Saatman et al., 2008). Another
clinical indicator is the length of PTA, or the time period following injury during
which continuous memory or the ability to store current events is impaired (Russell
& Smith, 1961; Wrightson & Gronwall, 1981). Russell first proposed the use of
PTA in 1932, and variations of this method continue to be used today to predict
clinical outcomes (e.g., Brown et al., 2010). Length of coma or unconsciousness has
been used in a similar manner, although criteria that identify when a person has
officially regained consciousness do vary. Some recommend a combination of these
and other indicators to improve prediction of outcomes (e.g., American Congress of
Rehabilitation Medicine, 1993; Carroll et al., 2004; Saatman et al., 2008; Sherer,
Struchen, Yablon, Wang, & Nick, 2008).
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 99

While these methods have proven useful, they do have limitations, including that
some individuals who are initially classified as having severe injuries demonstrate
minimal long-term impairments. For example, when severity classification is made
using the GCS or other similar procedures, some children initially classified as hav-
ing severe TBI do not demonstrate significant neurocognitive or behavioral deficits
when examined after a period of recovery, and other factors including age at injury
and premorbid functioning may account for more variance in neurocognitive out-
comes (Fay et al., 2009; Lieh-Lai et al., 1992; Wells, Minnes, & Phillips, 2009).
Indeed, the GCS has been described as only a gross predictor of TBI severity and
functional outcome (Ghosh et al., 2009; Hackbarth et al., 2002; Hiekkanen, Kurki,
Brandstack, Kairisto, & Tenovuo, 2009). Saatman et al. (2008) also point out that
the GCS relies primarily on acute behavioral responses post-injury including best
eye, verbal, and motor response, but provides little information about the patho-
physiologic mechanisms underlying injury, which may provide additional insights
on the nature and severity of the injury. They propose that an alternative, multidi-
mensional classification system that expands upon current qualitative observations
of behavior may be useful for future TBI clinical trials. In this regard, neuropsycho-
logical test results, particularly when used in combination with other indicators,
may afford a powerful method to help classify injury severity.

Neuropsychological Approaches

While acknowledged that neuropsychological testing cannot be used to classify


brain injury severity in the acute stages of moderate to severe injury for obvious
reasons, brief computerized neuropsychological batteries that are administered
shortly after mild TBI in athletes may show some promise in predicting protracted
recovery (e.g., Lau, Collins, & Lovell, 2012) and in this way may provide one
means for classifying severity of more mild injuries. Additionally, neuropsycho-
logical approaches to classification of severity of injury have been attempted and
progressed along a number of lines. Some advocate for the usefulness of impair-
ment indexes that represent an average of impaired scores across a battery of tests
sensitive to brain injury (Reitan & Wolfson, 2009; Russell, Neuringer, & Goldstein,
1970). Such approaches have been shown to be predictive of the presence or absence
of brain injury, as well as the severity of injury. Others have utilized scores from an
individual measure or a limited number of measures, to screen for brain impairment
following injury (e.g., Reitan & Wolfson, 1995, 2004). In this approach, neuropsy-
chological tests are administered some time after injury, and results are used to
establish the severity of impairment in specific abilities that are ostensibly the result
of brain injury. For TBI, the feasibility of this approach has support from studies
that demonstrate neuropsychological testing with brief test batteries can be con-
ducted within weeks following moderate to severe TBI (Boake et al., 2001; Sherer
et al., 2002), even before PTA has fully resolved in some patients (Kalmar et al.,
2008; Wilson et al., 1999). Kalmar and colleagues (2008) found that 32 % (n = 112)
100 D.N. Allen et al.

of their patients with moderate to severe TBI who were still experiencing PTA were
able to complete a brief battery of neuropsychological tests designed to take
60–75 min to administer. Performance on this battery was predictive of important
outcomes such as functional independence and disability (Hanks et al., 2008).
Neuropsychological approaches may also provide additional information on the
pathophysiological changes that occur post-injury through the repeated measure-
ment of cognition and behavior over time (Goethe & Levin, 1986). These approaches
are therefore useful for broadly classifying injury severity, but do not typically cap-
ture the heterogeneity of neurocognitive deficits that results from TBI. In contrast,
cluster analysis may provide a unique approach to reflect both severity and heteroge-
neity of injury. While we do not provide an exhaustive review of the TBI cluster
analysis literature here, some representative studies are helpful to illustrate this point.
To date, cluster analytic studies have provided a number of unique insights into
TBI, and one organizing theme to these studies is that they address the issue of neu-
ropsychological heterogeneity. Illustrative of this, a recent study by Allen et al.
(2010) investigated attention and memory heterogeneity in 150 children and adoles-
cents with TBI using the Test of Memory and Learning (TOMAL; Reynolds &
Bigler, 1994). The children with TBI were on average 11.7 years old (SD = 3.7),
52.1 % male, and 56.3 % Caucasian and were assessed 6.9 months (SD = 3.1) fol-
lowing injury. Clusters derived from this sample were compared to clusters derived
from 150 age- and sex-matched normal controls to determine whether differing
patterns of learning, memory, and attention/concentration would be evident among
the groups. Also, the TBI clusters were compared on a number of important clinical,
cognitive, and behavioral variables, to determine whether cluster membership might
be associated with unique patterns of cognitive and behavioral disturbances. Results
of the cluster analyses for the TBI and control groups are presented in Fig. 5.2a, b.
As can be seen from the figure, cluster analyses indicated that a four-cluster solu-
tion was optimal for the control group (Fig. 5.2a), while a five-cluster solution was
optimal for the TBI group (Fig. 5.2b). Not only were there differences in the number
of clusters, the profiles of performance differed between the groups with the control
group clusters being primarily differentiated by level of performance, while the TBI
clusters were characterized by both level and pattern of performance differences.
Differences were also present among the TBI clusters for neurocognitive, achieve-
ment, and behavioral variables not included in the cluster analysis, which provided
additional support for the validity of the cluster solution and its potential value in
predicting outcomes. Clusters characterized by impairment in verbal, nonverbal, or
global memory impairment generally had poorer neurocognitive and academic
achievement outcomes than clusters characterized by average memory performance
or attention deficits. In addition, the cluster characterized by global memory impair-
ment had increased parent- and teacher-reported behavioral problems. Thus, the
findings indicate that unique patterns of neurocognitive impairment are observed in
children with TBI that distinguish them from non-brain-injured children, these
patterns of impairment are not accounted for by expected variation in test perfor-
mance observed in normal populations, and cluster membership is associated with
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 101

Fig. 5.2 Normal control and traumatic brain injury clusters on the Test of Memory and Learning.
Panel (a): normal controls. Panel (b): traumatic brain injury (From: Allen, D. N., Leany, B. D.,
Thaler, N. S., Cross, C., Sutton, G. P., & Mayfield, J. (2010). Memory and attention profiles in
pediatric traumatic brain injury. Archives of Clinical Neuropsychology, 25(7), 618–633. Used with
permission. All rights reserved)

patterns of outcome on some important clinical variables. These neurocognitive


profiles identified using cluster analysis may prove useful for identifying homo-
geneous subgroups of children with TBI that are differentiated by a number of
important clinical, cognitive, and behavioral variables associated with treatment
and outcomes.
The validity and usefulness of cluster solutions such as those identified by Allen
et al. (2010) is dependent not only on demonstrating between-cluster differences on
external variables but also on the degree to which they are generalizable from one
sample to another. Comparison of two studies of the Wechsler Intelligence Scale for
Children, Third Edition (WISC-III; Wechsler, 1991) conducted at different sites by
different investigators on separate study samples provides some support for the gen-
eralizability of neuropsychological clusters (Donders & Warschausky, 1997; Thaler
et al., 2010). Figure 5.3a, b provide WISC-III profiles obtained in these two studies.
Figure 5.3a presents results reported by Donders and Warschausky (1997) who
examined WISC-III performance of 153 children who sustained mild, moderate, or
severe closed head injuries. The sample was on average 11.8 years old, 52 % male,
and 87 % Caucasian and had a Full Scale IQ of 91.1. When the WISC-III scores
102 D.N. Allen et al.

Fig. 5.3 WISC-III cluster analysis results from Donders & Warschausky (1997) and Thaler et al.
(2010). Panel (a): Donders et al. Panel (b): Thaler et al. (Panel (a) from: Donders, J., & Warschausky,
S. (1997). WISC-III factor index score patterns after traumatic head injury in children. Child
Neuropsychology, 3(1), 71–78. Used with permission. All rights reserved. Panel (b) from: Thaler,
N. S., Bello, D. T., Randall, C., Goldstein, G., Mayfield, J., & Allen, D. N. (2010). IQ profiles are
associated with differences in behavioral and emotional functioning following pediatric traumatic
brain Injury. Archives of Clinical Neuropsychology, 25(8), 781–790)

were subjected to cluster analysis, four clusters were identified (see Fig. 5.3a).
Three of the clusters were characterized by either above average, average, or low
average index scores and in this way were differentiated primarily by level of
performance differences. The fourth cluster exhibited low average scores on verbal
and attention indexes and impaired scores on the nonverbal and processing speed
indexes. No differences were present between the clusters on demographic vari-
ables, although significant differences were present on the GCS and neuroimaging
data, with the fourth cluster demonstrating more severe brain injury than the other
clusters. Thaler et al. (2010) also examined WISC-III clusters in 123 children with
TBI who were on average 11.6 years old, 58 % male, and had Full Scale IQ scores
of 82.4. The majority of these children sustained closed head injuries in the moder-
ate to severe range (Mean GCS = 7.1; median = 7). Cluster analysis of the WISC-III
scores also identified four clusters that were similar in many respects to those identi-
fied by Donders and Warschausky (1997), as can be seen in Fig. 5.3b. Comparisons
between the clusters on behavioral ratings generally indicated that
the most severely impaired cluster typically exhibited the most severe behavioral
disturbances. The samples for these two studies were comparable in many respects.
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 103

Both studies identified average and low average clusters, as well as a more severely
impaired cluster with selective impairment on perceptual organization and process-
ing speed. The Donders and Warschausky (1997) sample contained more children
with mild TBI, which may account for the overall higher performance and the high
average cluster identified in that study, which was not identified by Thaler et al.
(2010).
These studies illustrate the potential usefulness of neuropsychological tests in
addressing the question of neuropsychological heterogeneity in TBI and demon-
strate that in addition to differences in pattern of performance, there are also level of
performance differences between neuropsychological clusters. These level of per-
formance differences range from mild to severe impairment and may correspond to
injuries also ranging from mild to severe. For practical purposes as it pertains to
classifying severity of brain injury, a brief measure that is quickly and easily admin-
istered and also sensitive to brain damage has certain advantages over more exten-
sive assessments like the TOMAL and WISC. The TMT is one such measure and
the focus of the investigation described later in this chapter.

Trail Making Test

In the investigation, we examined TMT performance as an indicator of brain injury


severity approximately one year following injury in children who sustained a TBI.
The TMT consists of Part A (TMT-A) and Part B (TMT-B). For adults, TMT-A
consists of a series of 25 numbered circles which the test subject is instructed to
connect in sequence by drawing a line from one circle to the next (i.e., start at 1,
draw a line to 2, then 3, and so on). TMT-B is similar to TMT-A, except that the 25
circles contain both letters and numbers. For TMT-B, the test subject is instructed to
connect the circles by alternating between the numerical and alphabetical sequences
(i.e., start at “1,” and then draw a line to “A,” then “2,” then “B,” and so on).
Performance is timed on both sections and the score is the amount of time (in sec-
onds) taken to complete each part. Errors are also recorded, although they are not
typically used when interpreting test performance.
Although well over 60 years old, the TMT continues to be one of the most fre-
quently administered neuropsychological tests in research and clinical practice
(Rabin, Barr, & Burton, 2005). The TMT was originally developed in 1938 as a test
of intelligence called the Test of Distributed Attention, and was then renamed the
Partington’s Pathways Test (Partington, 1949; Partington & Leiter, 1949; Watson,
1949). Later, it was included in the Army Individual Test of General Ability (U. S.
War Department, 1944) where it was called the TMT. The TMT was subsequently
incorporated into the Halstead–Reitan Neuropsychological Battery (Reitan &
Wolfson, 1992) but is also commonly used outside of this battery. In fact, a recent
survey of the members from the National Academy of Neuropsychology,
APA Division 40, and the International Neuropsychological Society found that the
TMT ranked third among the most frequently used instruments for clinical neuro-
psychological evaluation (Rabin et al., 2005). Consistent with its original design as
104 D.N. Allen et al.

a measure of intelligence, early studies indicated that the TMT was indeed signifi-
cantly correlated with tests of intelligence. For example, Partington and Leiter
(1949) found a correlation of 0.68 between the Standford–Binet 1937 Edition and
the Partington’s Pathways Test in a sample of 256 World War II veterans.
However, numerous studies thereafter established its sensitivity to brain dys-
function resulting from a wide variety of psychiatric and neurologic conditions,
including TBI in children and adults (Armitage, 1946; Barth et al., 1983; Levin,
Benton, & Grossman, 1982; Periáñez et al., 2007; Reitan, 1955, 1958, 1971; Reitan
& Wolfson, 1992). As recently reviewed by Allen, Thaler, Ringdahl, Barney, and
Mayfield (2012), the TMT in adults achieves overall correct classification rates of
approximately 84 % when normal controls are compared to mixed neurological
samples (Reitan, 1955, 1958). For older children, classification accuracies of 0.82
and 0.80 were found for TMT-A and TMT-B, respectively, when normal controls
were compared to children with mixed neurological disorders (Reitan & Herring,
1985). Similarly, a TMT-B cut score of 37/38 achieved a correct classification rate
of 78.0 % when normal children were compared to those with brain damage (Reitan
& Wolfson, 2004). Comparable classification rates were also obtained when chil-
dren classified as either slow or normal learners were examined (Mittelmeier, Rossi,
& Berman, 1989). Some alternative versions of the original TMT, such as the
Comprehensive TMT (Reynolds, 2002), also show comparable classification rates
(Allen et al., 2012; Armstrong, Allen, Donohue, & Mayfield, 2008).
As a result, rather than being considered a test of intelligence as originally envi-
sioned by Partington, a TMT has gained popularity and widespread use because of
its sensitivity to brain injury and the recognition that successful performance
requires a number of abilities, including psychomotor speed, complex attention,
visual scanning, and mental flexibility. Differential associations between Parts A
and B of the TMT with other neuropsychological tests provide evidence that the two
parts are assessing somewhat different constructs. These correlational studies sug-
gest TMT-A is more reliant on perceptual abilities, visuoperceptual processing
speed, and motor speed, while TMT-B is more reliant on working memory, inhibi-
tion, and executive functions (Langenecker, Zubieta, Young, Akil, & Nielson, 2007;
Ríos, Periáñez, & Muñoz-Céspedes, 2004; Sánchez-Cubillo et al., 2009; Thaler
et al., 2012).
The popularity of the TMT is based in part on its brief administration time and
ease of administration, as well as its well-documented sensitivity to brain dysfunc-
tion. Accordingly, despite its simplicity, the TMT may also be useful for establish-
ing the severity of brain injury. This is particularly true when one considers that
motor and sensory deficits are common following TBI, as is slowed information
processing, although deficits in attention, concentration, and memory are also com-
mon (Babikian & Asarnow, 2009; Felmingham, Baguley, & Green, 2004). Also,
because neurocognitive deficits can present great challenges for rehabilitation and
educational placement (Kraemer & Blancher, 1997; Lowther & Mayfield, 2004)
and the TMT requires abilities that are often impaired by TBI, TMT performance is
expected to have some predictive power in this regard.
We present the results of a study that examined classification of brain injury
severity via TMT performance in a sample of children with TBI. Given its
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 105

sensitivity to brain damage, the TMT was used as an indicator of brain injury sever-
ity, and cluster analysis was used as an empirical statistical approach to derive injury
severity subgroups. Following identification of an optimal cluster solution, compari-
sons were made among the clusters on important outcome domains including intel-
lectual, academic, and memory function to determine whether brain injury severity
classification derived from cluster analyzing the TMT scores would exhibit expected
associations with these outcomes. It was hypothesized that those classified as exhib-
iting greater severity of impairment would also demonstrate greater deficits in intel-
lect, poorer academic achievement, and greater impairment of memory abilities.
Comparisons were also made between the TMT clusters and classifications made at
the time of injury using the GCS. Given studies indicating inconsistent correspon-
dence between GCS scores at time of injury and later neurocognitive and functional
outcomes (Fay et al., 2009; Salorio et al., 2005), we did not anticipate that there
would be a high degree of consistency between the TMT and GCS classifications
and that the TMT classifications would be more strongly associated with intellec-
tual, academic, and memory functioning compared to the GCS classifications.

Method

Participants

Participants included 152 children and adolescents who had sustained a TBI that
were on average 12.9 years of age (SD = 2.8) with Full Scale IQ scores of 93.9
(SD = 14.8). They were 59.2 % male and 86.2 % right-hand dominant, and ethnicity
included 59.8 % Anglo/European, 20.6 % African American, 16.7 % Hispanic,
1.9 % Asian American, and 2.0 % others. They were assessed on average 13.8
months following injury. Of these children, 92.8 % had sustained closed head inju-
ries, with the most common causes of head injury including motor vehicle accidents
(50.7 %), pedestrian struck by a motor vehicle (21.1 %), four-wheeler accidents
(8.6 %), skiing accident (5.9 %), gunshot wound (3.3 %), bicycle accident (3.3 %),
falls (1.3 %), and other causes (6.0 %). The GCS (Teasdale & Jennett, 1974) had
been completed for 97 of the children, either by first responders or after the children
were transported to the hospital, and indicated that overall they had sustained mod-
erate to severe TBI (median = 7.0; mean = 7.2, SD = 2.9).

Measures

TMT Parts A and B

The TMT assesses psychomotor speed, visual scanning, complex attention, and
mental flexibility. As previously discussed, the adult version of the TMT consists of
two parts, A and B, and both parts include 25 circles that are distributed across an
106 D.N. Allen et al.

8.5 by 11 in. sheet of paper. For Part A, the circles are numbered 1 to 25. The test
subject is given a pencil and instructed to draw a line as quickly as possible that con-
nects the 25 numbered circles in order. The older child version of the test, which was
used in the current study, is designed for children aged 9–15 years. It is identical to
the adult version except that it includes only the first 15 circles for Parts A and B.

Wechsler Intelligence Scales

Intelligence was assessed using several versions of the Wechsler Intelligence Scales
because the children were tested over a number of years and were of different ages.
Most were administered the WISC-III (n = 129), although other versions of the test
were also administered. Because these versions of the Wechsler scales share many
common subtests and these subtests were designed to assess similar abilities, data
from the various versions were combined. Subtests that were selected for analysis
are strong indicators of their representative index scores, including Vocabulary (ver-
bal comprehension index), Block Design (perceptual organization/reasoning index),
Digit Span (working memory index), and Digit Symbol/Coding (processing speed
index). We also evaluated group differences for the Full Scale IQ.

The Woodcock–Johnson Psycho-educational Battery Tests of Achievement


(WJ; Woodcock & Johnson, 1989; Woodcock, McGrew, & Mather, 2001)

Academic achievement was assessed with the Woodcock–Johnson Psycho-


educational Battery Tests of Achievement Revised (Woodcock & Johnson, 1989) or
Third (Woodcock et al., 2001) Version. The Broad Reading and Broad Math cluster
scores were selected for analysis because these were completed by most partici-
pants and are generally consistent across the two versions of the test.

The Test of Memory and Learning (TOMAL; Reynolds & Bigler, 1994)

The TOMAL is a broad-based measure of memory and attention normed for children
between 5 and 19 years of age. Ten core subtests and four supplemental subtests
form indexes for verbal memory (VMI), nonverbal memory (NMI), delayed recall
(DRI), and attention/concentration (ACI), as well as an overall composite memory
(CMI). These indexes were compared across TMT clusters and GCS groups.

The Glasgow Coma Scale (Teasdale & Jennett, 1974)

The GCS is commonly used for assessing the severity of brain injury in TBI. The
GCS allows for ratings of three areas including Best Eye Response (score 1–4),
Best Verbal Response (score 1–5), and Best Motor Response (score 1–6). GCS
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 107

scores range between 3 and 15, with scores of 3–8 indicating severe injury, scores
of 9–12 indicating moderate injury, and scores of 13–15 indicating mild injury. The
GCS is popular for TBI severity classification for a number of reasons including
that it is objective and simple to complete. Furthermore, inter-rater reliability is
high. Changes in GCS scores from one assessment to the next suggest a corre-
sponding change in level of consciousness (Jennett & Teasdale, 1977; Teasdale &
Jennett, 1974).

Data Analysis

In order to develop severity classifications based on TMT performance, Part A and


Part B raw scores (time in seconds) were submitted to hierarchical cluster analysis
using Ward’s method with squared Euclidean distance as the distance measure.
Ward’s method of cluster analysis was selected because it is consistent with the
cluster analytic methodology of previous studies of neuropsychological variables in
children with TBI (Allen et al., 2010; Curtiss, Vanderploeg, Spencer, & Salazar,
2001; Mottram & Donders, 2006; Thaler et al., 2010), its results are consistent with
those produced by other agglomerative clustering methods, and compared to these
other methods, it is less affected by outliers (Morris, Blashfield, & Satz, 1981). The
squared Euclidian distance coefficient was selected because it provides a direct
measure of distance between objects in Euclidean space and is sensitive to both pat-
tern and level of performance differences (Everitt, Landau, & Leese, 2001). Three-,
four-, and five-cluster solutions were specified, and we followed the approach sug-
gested by Aldenderfer and Blashfield (1984) to determine the appropriate number
of clusters. DFA was used to examine the proportion of cases correctly classified
into their cluster solutions as well as to determine the overlap between clusters. By
graphing the clusters in discriminant function space, the overlap between each clus-
ter was inspected (as suggested by Aldenderfer & Blashfield, 1984). In this case, the
clusters should be fairly well separated when plotted in discriminant function space,
though there will often be some overlap. Additionally, Beale’s F statistic was used
as a measure of parsimony to determine if more complex cluster solutions accounted
for significantly more variance. Finally, cluster solutions that yielded clusters that
had <5 % of the sample were discarded, as such clusters are unlikely to be general-
izable or meaningful for other samples.
The stability of each of the cluster solutions were examined using K-means itera-
tive partitioning cluster analysis, with the number of clusters and initial cluster cen-
ters specified based on results from the Ward’s method solutions. Degree of
correspondence between the cluster solutions derived using Ward’s method and
K-means iterative partitioning method was then evaluated using Cohen’s kappa.
Based on these methods, the most appropriate number of clusters was identified for
the children with TBI.
After identifying the appropriate number of TMT clusters, comparisons among
the clusters were conducted on variables that were not included in the cluster
108 D.N. Allen et al.

analysis, but that represented outcomes in other important domains, including


intelligence, academic achievement, and memory. This was accomplished to deter-
mine the extent to which the TMT severity clusters identified using cluster analysis
were associated with other variables of interest. It was hypothesized that if the TMT
clusters represented a reliable method of classifying the sample, those with more
severe injuries would demonstrate greater impairment on these other indicators of
outcome. These comparisons were made using analysis of variance (ANOVA) or
multivariate ANOVA (MANOVA) in which cluster membership served as a
between-subjects variable and test scores as the dependent variables.
Finally, in order to examine the correspondence between severity classifications
produced by cluster analysis of the TMT and those produced by the GCS that was
completed at the time of injury, the sample was divided into three groups based on
GCS scores using accepted cutoffs. For mild, moderate, and severe brain injury
(Jennett & Teasdale, 1977; Teasdale & Jennett, 1974). Correspondence between the
TMT and GCS classifications was accomplished using chi-squared analysis and
kappa coefficients, and comparisons were also made among the GCS groups on the
intellectual, academic, and memory variables with ANOVA or MANOVA to deter-
mine whether similar differences would be present for the GCS classifications as for
the TMT classifications.

Procedure

Participants in the TBI group were selected from a consecutive series of cases that
were referred for neuropsychological assessment to a pediatric specialty care hospi-
tal. Children from this series were included in this study if they had sustained a TBI,
completed the TMT as part of the neuropsychological evaluation, and had evidence
of structural brain damage based on appropriate neuroimaging, laboratory, and
other examinational findings including neurological evaluation. All tests were
administered according to standard procedures by a pediatric neuropsychologist or
by doctoral-level technicians under the supervision of the neuropsychologist.
Children were evaluated 3–98 months following TBI (mean = 13.8; SD = 15.3). The
study was conducted in compliance with IRB regulations.

Results

Cluster Analysis of the TMT

Overall results for the measures used in the study are presented in Table 5.1. As can
be seen from the table, not all variables were available for all participants. When
data were missing, comparisons were made on the reduced number of cases.
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 109

Table 5.1 Results Variable N Mean SD


on primary variables
TMT-A (sec) 152 31.0 14.3
for all participants
TMT-B (sec) 152 70.2 42.8
Full Scale IQ 151 85.3 14.5
Vocabulary 151 7.7 3.1
Block Design 151 8.1 3.8
Digit Span 151 8.5 2.7
Coding 151 6.7 3.5
WJ Broad Reading 136 94.6 14.1
WJ Broad Math 136 96.8 16.7
TOMAL verbal 134 82.3 16.4
TOMAL nonverbal 134 84.0 16.1
TOMAL composite 134 82.7 15.1
TOMAL delayed 134 87.2 13.5
TOMAL attention 129 83.5 13.0
Note: Results are reported in standard scores except where
noted. TMT-A Trail Making Test Part A, TMT-B Trail Making
Test Part B, WJ Woodcock–Johnson

Fig. 5.4 Three-, four-, and five-cluster solutions for the Trail Making Test Parts A and B

The three-, four-, and five-cluster solutions for the TMT are presented in Fig. 5.4.
Examination of the profiles based on TMT-A and TMT-B indicates that clusters in
the three-cluster solution were differentiated primarily by level of performance.
Discrepancies between the clusters were larger for TMT-B than for TMT-A,
although each cluster maintained its position with regard to overall performance.
The cluster that performed the best obtained scores that were in the average range,
and it was the largest cluster (n = 80). The second cluster was similar to the first on
TMT-A, but performed almost four SDs poorer on TMT-B (n = 42). The third cluster
was the smallest of the clusters (n = 30) and exhibited the worst performance over-
all, obtaining scores in the impaired range on both TMT-A and TMT-B. In the four-
cluster solution, the impaired cluster (C3) was divided into two clusters with the
fourth cluster (C4) exhibiting marked impairment on TMT-B and comparable or
somewhat better performance on TMT-A. However, this cluster consisted of only
110 D.N. Allen et al.

three participants. Finally, for the five-cluster solution, C4 was maintained and the
impaired cluster (C3) was divided again to form a fifth cluster (C5) that demon-
strated worse performance on TMT-A and TMT-B compared to C3. This cluster
consisted of only six participants.
Discriminant function analysis (DFA) results indicated that when the TMT
scores were used to predict cluster membership, there was a negligible difference in
the correct classification rates for the three-, four-, and five-cluster solutions, with
correct classification rates of 96.1 %, 95.4 %, and 97.4 %, respectively. The K-means
iterative partitioning method was then used to examine the stability of the three-,
four-, and five-cluster solutions. Cohen’s kappa indicated that the level of agreement
between the Ward’s and K-means results for the three-, four-, and five-cluster solu-
tions were 0.90, 0.92, and 0.96, respectively. Kappas above 0.80 are considered to
indicate excellent agreement (Landis & Koch, 1977), suggesting that all solutions
are stable as indicated by level of agreement between the Ward’s and K-means
methods. Beale’s F tests were nonsignificant when comparing the three-cluster
solution to the four-cluster solution, F = 1.66, p = 0.19; the three-cluster to the five-
cluster solution, F = 1.58, p = 0.18; or the four-cluster to the five-cluster solution,
F = 1.29, p = 0.28. The Beale’s F test results suggest that compared to the three-
cluster solution, the four- and five-cluster solutions did not explain significantly
more variance. Finally, the additional clusters in the four- and five-cluster solutions
(C4 and C5) only accounted for 2.0 % and 3.9 % of the entire sample, respectively.
Considering these results, we turned our attention to the three-cluster solution.
While we considered the other clusters (particularly C5) theoretically interesting,
given what appears to be somewhat unique impairment on TMT-A relative to TMT-
B, we decided that grouping these more severely impaired clusters into one “severe”
cluster (C3) would provide a better approach with regard to cluster stability, gener-
alizability to other samples, and power to make comparisons between the clusters
on external validity variables. Also, from a parsimony perspective, the three-cluster
solution appeared to be the best given the negligible differences between the three-,
four-, and five-cluster solutions from the DFA and K-means analyses, as well as
from the Beale’s F test results. A straightforward interpretation of the clusters based
on the TMT Part B scores would suggest that C1 could be considered a mild severity
cluster, as scores for this cluster are generally in the normal range. Mild severity is
used to characterize this cluster rather than “normal” because of the fact that they
had sustained a TBI. A moderate cluster is also present (C2), as well as a more
severely impaired cluster (C3).

Comparisons Between the GCS Groups and TMT Clusters

One of the primary goals of the study was to compare the severity classifications of
the TBI sample that resulted from the GCS scores and the TMT clusters. This goal
was addressed in two ways, including a direct comparison of agreement between
the two different approaches to severity classification, as well as a comparison of the
GCS and TMT groups on the external validity variables.
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 111

Table 5.2 Cross-tabulation of severity classification for the Trail Making Test (TMT) clusters and
Glasgow Coma Scale (CGS) severity groups
TMT clusters
Mild Moderate Severe
GCS group Mild 2 (2.1%) 2 (2.1%) 1 (1.0%)
Moderate 12 (12.4%) 7 (7.2%) 4 (4.1%)
Severe 37 (38.1%) 19 (19.6%) 13 (13.4%)

Agreement Between the TMT and GCS Classifications

To form GCS severity groups, the GCS scores were used to classify the 97 partici-
pants with available GCS data based on established cutoffs. When classified in this
manner, 71.1 % were identified as “severe,” 23.7 % were identified as “moderate,”
and 5.2 % were identified as “mild.” Given that GCS scores were missing for 55 of
the children, we compared those with GCS scores to those without GCS scores on
all of the demographic, clinical, and neuropsychological variables used in this study,
in order to determine if the groups were comparable. No significant differences
were present for any of the variables, with the exception of the Coding subtest of the
Wechsler scales,
F(1, 149) = 9.18, p < 0.01. The group without GCS scores was lower on this variable
than the group with GCS scores (means = 5.6 and 7.4, respectively), suggesting that
the group without GCS scores may have had more severe neurocognitive impair-
ment. If that was the case, then the group might be most accurately characterized as
having sustained severe injuries. However, there were no significant differences on
TMT-A and TMT-B, which is arguably the most sensitive test to brain dysfunction
that we administered.
Table 5.2 presents the severity classification agreement rates between the TMT
clusters and the GCS. Visual inspection of the table indicated low agreement
between the TMT and GCS groups, which was confirmed using Cohen’s kappa,
which suggested very poor agreement between the two methods (kappa = 0.02,
p = 0.98). For example, cases in the mild TMT cluster (C1) were distributed across
all GCS levels, while cases classified as severe by the GCS were distributed across
all of the TMT clusters, with most (n = 37) falling in the mild TMT cluster.
In addition to the low correspondence between the two approaches, examination
of the mean TMT and GCS scores for the classification groups also demonstrates
expected absence of differences. Table 5.3 presents descriptive statistics for each
classification approach as well as results of between-group analyses (ANOVA). For
the TMT clusters, there were large between-group differences for TMT Part A and
B, with similar results for the GCS scores of the GCS groups. These differences
were expected because the TMT and GCS scores were used to develop the TMT
clusters and GCS groups, respectively. However, the analyses further indicated that
the TMT clusters did not significantly differ with regard to GCS scores, while the
GCS clusters did not differ on TMT variables. The absence of differences provides
additional evidence that the TMT and GCS approaches are yielding quite different
classification results.
112 D.N. Allen et al.

Table 5.3 Differences between Trail Making Test (TMT) clusters and Glasgow Coma Scale
(CGS) groups on classification variables
Mild Moderate Severe
Mean SD Mean SD Mean SD F p
TMT clusters
GCS 7.0 2.8 7.6 2.9 7.0 3.0 0.41 0.67
TMT-A 23.7 7.8 35.1 11.5 44.9 18.5 39.56 <0.01
TMT-B 40.8 11.1 75.5 10.5 141.2 37.6 299.93 <0.01
GCS groups
GCS 13.4 0.9 10.2 1.1 5.7 1.8 108.42 <0.01
TMT-A 30.4 9.8 29.0 8.9 30.5 12.8 0.13 0.88
TMT-B 67.0 21.4 64.7 29.9 67.7 36.9 0.07 0.94
Note: TMT-A Trail Making Test Part A, TMT-B Trail Making Test Part B

TMT and GCS Classification Comparisons on Demographic


and Clinical Variables

Next, the TMT clusters and GCS groups were compared across demographic, clini-
cal, intellectual, achievement, and memory variables. These variables are consid-
ered external validity variables in this analysis since they were not included in the
cluster analysis, and differences between groups on these variables would provide
support for the validity of the two classification approaches. Comparisons on demo-
graphic and clinical variables are presented in Table 5.4. None of the differences
between the groups were significant, suggesting that TMT cluster membership and
GCS group membership is not substantially influenced by these variables.

TMT and GCS Classification Comparisons on IQ Variables

Descriptive statistics for IQ variables are presented in Table 5.5 for the TMT clus-
ters and GCS groups. For the TMT clusters, significant differences emerged for all
the Wechsler subtests as well as the Full Scale IQ. However, no differences were
present for the GCS groups on the Wechsler subtests, although there was a signifi-
cant difference for Full Scale IQ. Figure 5.5 presents the Wechsler subtest profiles
for the GCS groups (Fig. 5.5a) and the TMT clusters (Fig. 5.5b). As seen in the
figure, there was some overlap across the four subtests among GCS groups, particu-
larly with the Digit Span subtest in which all three groups converged in level of
performance. The mild group otherwise appeared to perform better than the moder-
ate and severe groups, which exhibited little distinction from each other with the
exception of the Digit Symbol subtest where clearer distinction between the three
groups was apparent. Post hoc analyses indicated that for the Full Scale IQ, the
severe and moderate groups performed significantly worse than the mild group, but
did not differ from each other. Regarding the TMT clusters, the overlap was reduced
and particularly differentiated the severe cluster from the mild and moderate
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 113

Table 5.4 Demographic and clinical variables for the Glasgow Coma Scale (GCS) groups and
Trail Making Test (TMT) clusters
Variable Mild Moderate Severe X2 p
TMT clusters
Gender (% male) 57.5 61.9 60.0 0.23 0.89
Ethnicity (%) 12.39 0.13
Caucasian 64.6 50.0 63.6
African American 12.5 31.3 4.5
Hispanic 20.8 18.8 22.7
Other 2.1 0 9.0
Closed HI (%) 94.9 95.2 86.7 2.73 0.26
GCS groups
Gender (% male) 40.0 65.2 56.5 1.21 0.55
Ethnicity (%) 6.01 0.65
Caucasian 100.0 50.0 63.8
African American 0.0 16.7 21.3
Hispanic 0.0 33.3 10.6
Other 0.0 0.0 4.2
Closed HI (%) 80.0 100.0 92.8 3.30 0.19
Mean SD Mean SD Mean SD F p
TMT clusters
Age (years) 12.6 2.3 13.4 3.3 12.9 3.1 1.29 0.28
Months since injury 14.6 16.1 13.3 12.7 12.5 17.0 0.24 0.79
GCS groups
Age (years) 14.7 2.3 11.9 2.7 12.9 2.7 2.52 0.09
Months since injury 12.0 7.5 9.5 7.0 13.5 14.3 0.85 0.43
Note: GCS Glasgow Coma Scale, TMT Trail Making Test, HI head injury

Table 5.5 IQ variables for the Glasgow Coma Scale (GCS) groups and Trail Making Test (TMT)
clusters
Mild Moderate Severe
Variable Mean SD Mean SD Mean SD F p ηp2
TMT clusters
Vocabulary 8.3 3.2 7.5 2.8 6.2 2.8 5.63 <0.01 0.073
Block Design 9.1 3.6 8.5 3.1 5.0 3.6 15.67 <0.01 0.176
Digit Span 9.0 2.8 8.4 2.6 7.3 2.4 4.34 0.02 0.058
Coding 7.6 3.2 6.8 2.9 4.2 4.0 11.65 <0.01 0.136
Full Scale IQ 89.8 13.4 86.7 10.4 71.4 13.6 23.03 <0.01 0.238
GCS clusters
Vocabulary 9.6 2.6 7.0 2.9 7.5 2.9 1.58 0.21 0.033
Block Design 10.6 1.9 7.4 4.2 8.5 3.5 1.70 0.19 0.035
Digit Span 8.8 2.6 8.4 3.2 8.4 2.2 0.07 0.94 0.001
Coding 10.2 2.3 8.1 3.1 6.9 3.6 2.96 0.06 0.060
Full Scale IQ 99.6 9.07 84.8 14.8 84.7 11.6 3.44 0.04 0.068
114 D.N. Allen et al.

Fig. 5.5 Comparison of the GCS and Trail Making Test severity groups on selected subtests from
the Wechsler Intelligence Scales. Panel (a): GCS groups. Panel (b): TMT clusters. Note: VO
Vocabulary, BD Block Design, DS Digit Span, CD Coding

clusters. Inspection of the severe cluster indicates that children in this cluster had
general cognitive impairment with even greater deficits on the Block Design and
Coding subtests. This pattern of performance resembles a pattern that was identified
in studies of children with TBI that examined the WISC-III. In those studies there
was a subgroup of severely impaired children who exhibited relative deficits on the
Perceptual Organization and Processing Speed indexes (Donders & Warschausky,
1997; Thaler et al., 2010; see Fig. 5.3). Post hoc comparisons indicated that for all
of the subtests, the mild cluster (C1) significantly differed from the severe cluster
(C3), and for the Block Design and Coding subtests, as well as the Full Scale IQ, the
moderate cluster (C2) also significantly differed from the severe cluster. There were
no significant differences between the mild and moderate clusters on any of the
Wechsler subtests.

TMT and GCS Classification Comparisons on Achievement Variables

Result for the Woodcock–Johnson achievement variables are presented in Table 5.6
and Fig. 5.6. For the TMT clusters, significant differences were found for both the
Broad Reading and Broad Math, while the GCS groups significantly differed only on
the Broad Math score. Plots of achievement variables are present on Fig. 5.6. Again
children with mild injuries were distinct from children with moderate and severe inju-
ries when grouped into GCS scores, while children with severe injuries were distinct
from children with mild and moderate injuries when grouped into TMT clusters. Post
hoc analyses indicated that for the GCS clusters, there were no significant differences
among the groups on the Broad Math score, although there was a trend difference
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 115

Table 5.6 Achievement test variables for the Glasgow Coma Scale (GCS) groups and Trail
Making Test (TMT) clusters
Mild Moderate Severe
Variable Mean SD Mean SD Mean SD F p ηp2
TMT clusters
WJ Broad Reading 97.1 14.1 95.2 9.4 87.4 16.9 5.16 <0.01 0.072
WJ Broad Math 102.7 16.3 97.0 10.2 81.8 15.5 20.37 <0.01 0.234
GCS clusters
WJ Broad Reading 103.4 7.3 89.2 18.6 94.5 11.1 2.76 0.07 0.061
WJ Broad Math 106.4 10.7 97.1 15.5 94.9 11.9 1.92 0.15 0.043

Fig. 5.6 Comparison of the GCS and Trail Making Test severity groups on selected subtests from
the Woodcock-Johnson tests of achievement. Panel (a): GCS groups. Panel (b): TMT clusters

between the mild and severe group (p = 0.059) for the Broad Reading Score. For the
TMT clusters, the mild and moderate groups significantly differed from the severe
group for both Reading and Math, and there was a trend toward significant differences
between the mild and moderate group on the Math score (p = 0.052).

TMT and GCS Classification Comparisons on Memory Variables

For the TOMAL indexes, descriptive statistics and between-group comparisons are
presented in Table 5.7. Again, for the TMT clusters significant differences emerged
for all of the memory variables, while for the GCS groups, no statistically signifi-
cant differences were present although there was a trend toward significance for the
Delayed Recall Index (p = 0.09). The pattern of performance for the TOMAL
116 D.N. Allen et al.

Table 5.7 Memory variables for the Glasgow Coma Scale (GCS) groups and Trail Making Test
(TMT) clusters
Mild Moderate Severe
Variable Mean SD Mean SD Mean SD F p ηp2
TMT clusters
TOMAL VMI 85.7 16.0 86.2 11.7 67.0 14.9 16.68 <0.01 0.179
TOMAL NMI 88.6 15.3 86.6 12.6 67.1 11.7 22.82 <0.01 0.231
TOMAL CMI 86.7 14.5 85.9 10.8 66.2 11.4 24.65 <0.01 0.248
TOMAL DRI 90.5 13.7 88.4 10.3 76.1 11.9 12.63 <0.01 0.146
TOMAL ACI 85.0 12.9 85.0 11.2 76.0 13.6 4.72 0.01 0.070
GCS groups
TOMAL VMI 94.4 9.9 81.8 18.5 81.1 15.3 1.62 0.21 0.036
TOMAL NMI 94.8 4.7 83.8 14.6 82.6 15.5 1.54 0.22 0.033
TOMAL CMI 94.6 5.7 83.0 13.7 81.1 14.2 2.26 0.77 0.048
TOMAL DRI 97.2 4.7 87.9 13.7 84.0 13.0 2.84 0.06 0.060
TOMAL ACI 84.8 16.0 82.2 12.8 83.1 10.3 0.12 0.88 0.003
Note: TOMAL Test of Memory and Learning, VMI verbal memory index, NMI nonverbal memory
index, CMI composite memory index, DRI delayed recall index, ACI attention/concentration
index

Fig. 5.7 Comparison of the GCS and Trail Making Test severity groups on selected subtests from
the Test of Memory and Learning. Panel (a): GCS groups. Panel (b): TMT clusters

indexes is presented in Fig. 5.7. Similar to the IQ and achievement variables, the
TMT clusters overall appeared to better identify children with severe injuries from
those with mild and moderate injuries, while the GCS groups appeared to better
identify children with mild impairment from those with moderate and severe impair-
ment. Post hoc analyses indicated that the significant differences for the TMT clus-
ters on all TOMAL indexes were accounted for by significant differences between
the severe group, compared to the mild and moderate groups, who did not differ
from each other.
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 117

Discussion

Results of the current study provide support for the usefulness of the TMT as a
method to classify severity of TBI in children and adolescents. The TMT clusters
correspond in a general way with mild, moderate, and severe classifications,
although the best performing cluster obtained scores that were in the average range.
However, in this context they are considered to be in the mild severity group rather
than normal because they did sustain a brain injury, which was well documented
and, in some cases, classified as severe based on GCS scores. Whether these were
children who had high levels of premorbid function for whom normal performance
still represented a decline from baseline functioning or might have actually experi-
enced substantial recovery of function to near premorbid levels could not be directly
evaluated here.
Inspection of the figures indicates that the TMT clusters appear to differenti-
ate the severe cluster from the mild and moderate clusters, which is consistent
with the statistical analyses of cluster differences on the IQ, achievement, and
memory variables. TMT clusters differed on all intellectual, academic, and
memory variables, with the severe cluster consistently performing below the
moderate and mild clusters, and these differences appeared unrelated to demo-
graphic or clinical variables such as age, time since injury, and GCS scores. Our
results provide strong evidence that children who perform in the “severe” range
on both the TMT-A and TMT-B following TBI exhibit cognitive and academic
impairment across a number of domains that have implications for real-world
outcomes. Children who perform in the “moderate” range had less distinction
from those in the “mild” range, although certain IQ domains and Full Scale IQ
did differentiate between the moderate and severe groups. Additionally, the
moderate group consistently performed below the mild group on many of the
outcomes that were examined. The absence of significant differences between
the mild and moderate clusters may have been accounted for by the relatively
severe nature of injury sustained by the current sample, with few mild injury
cases included. If mild cases were included, then the distinction between the
mild and moderate group is expected to be larger, or another cluster may have
appeared composed primarily of cases with mild initial injuries who performed
average or above on the TMT.
It is also worth noting that while there were minimal statistical differences among
the GCS groups, when visually plotted they appear to differentiate the mild group
from the moderate and severe groups. Severe scores as measured by the GCS had
little correspondence with TMT clusters, and, as might be expected, there was mini-
mal correspondence between the GCS groups with neuropsychological variables,
particularly between those initially classified with moderate and severe injuries.
Only Full Scale IQ differentiated among the GCS groups, which like the GCS may
be considered a more general indicator of overall functioning. There was clear sepa-
ration between the mild GCS group and the moderate and severe groups, although
these differences did not achieve statistical significance, probably because of the
118 D.N. Allen et al.

small number of cases in the mild GCS group. The TMT clusters could therefore be
interpreted as a more refined classification system particularly with regard to neuro-
psychological and academic outcomes for the moderate and severe clusters and so
may have greater relevance for predicting persisting deficits across neurocognitive
and academic domains. This is not totally unexpected, as the TMT was adminis-
tered at the same time as the tests of intelligence, achievement, and memory, so
higher correspondence would be anticipated between the TMT clusters and these
measures than would be expected for the GCS groups and neuropsychological mea-
sures. Nonetheless, the results clearly demonstrate a lack of correspondence between
severity ratings made at the time of injury using the GCS and later classification
using the TMT.
Since the patients were tested with the TMT well after the acute phase of injury,
the low correspondence between GCS scores and TMT may be largely accounted
for by this factor since the GCS is typically administered during the acute phase of
injury, often by first responders at the scene of the accident, or by the ER staff as
was the case for the children in this study. As such, it is a measure of acute injury,
while the TMT is generally administered during a follow-up exam some weeks after
injury. However, the finding is consistent with longitudinal studies of neuropsycho-
logical recovery following TBI that have demonstrated that initial GCS classifica-
tions are limited with regard to predicting post acute recovery of neurocognitive
abilities. For example, Fay et al. (2009) followed a sample of children for four years
who were classified according to GCS scores as having moderate or severe TBI.
They found that while the moderate group had fewer children with no neuropsycho-
logical deficit at follow-up (81 %) compared to the severe group (67 %), a similar
number demonstrated persistent deficits (14 % and 17 %, respectively). Also, dura-
tion of unconsciousness but not lowest GCS score predicted neuropsychological
outcomes. Direct comparisons between the moderate and severe injury groups were
not made, so it is unclear whether the differences in number of children with
moderate and severe injuries who demonstrated neuropsychological deficits were
significant, but studies such as this suggest a lack of correspondence between
neuropsychological and GCS scores.
Thus, some children who are classified as severely impaired at the time of
injury based on the GCS will attain normal levels of neuropsychological function-
ing at some point in the future (Fay et al., 2009; Salorio et al., 2005). The TMT may
be a better predictor of longitudinal functioning as it is typically assessed at a time
when patients have been medically stabilized and cognitive functioning is unlikely
to abruptly change. In contrast, the GCS is more appropriate for classification during
the acute stage of injury, as it loses its effectiveness as patients regain conscious-
ness. In this way, the TMT and GCS may be viewed as complimentary approaches.
Although both TMT-A and TMT-B significantly differed among the three TMT
clusters, inspection of the figure clearly reveals that the TMT Part B had a greater
sensitivity to brain damage, which is consistent with other studies comparing
TMT-A and TMT-B scores (Demery, Larson, Dixit, Bauer, & Perlstein, 2010; Stuss
et al., 2001). As suggested by Reitan and Wolfson (2004), TMT-B is particularly
useful as a screen for brain dysfunction. Our mild cluster had a mean TMT Part B
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 119

score of 40.8 (SD = 11.1), our moderate cluster had a mean score of 75.5 (SD = 10.5),
and our severe cluster a mean score of 141.2 (SD = 37.6). These scores may repre-
sent approximate cutoff points for classifying TBI severity with the TMT Part B,
although results need to be replicated with additional outcome variables before
conclusively establishing their validity. In our sample the moderate and severe TMT
clusters identified only those children with residual deficits (given time since injury
was 13.8 months on average). In this regard, these data provide evidence that
clusters are useful in predicting other important domains of functioning (intellect,
achievement, and memory) and so may prove useful in documenting recovery of func-
tion and for predicting more general outcomes throughout the recovery process.
The current study has a number of limitations. First, generalizability of results is
limited by the nature of the TBI sample, which was composed of children and
adolescents referred to a pediatric specialty care hospital for neuropsychological
evaluation following TBI. They were included in this study if they had been admin-
istered the TMT as part of that evaluation, and the large majority had sustained
moderate to severe TBI. Thus, it is not clear whether the TMT clusters would have
been more distinct, particularly the mild and moderate clusters, if children with
mild TBI were included in the study, although one would suspect that this would be
the case. Similarly, inclusion of cases with mild injuries may have resulted in addi-
tional clusters that were not identified here. Also, while this sample was large
enough for cluster analysis particularly for the TMT variables, the number of cases
with GCS scores was more limited, making direct comparisons between the GCS
groups and TMT clusters difficult. Cross-validation of the current results is there-
fore necessary in other TBI samples.
As a related concern, the mild GCS group only had a few participants. Therefore,
some variables that approached significance, such as the WISC Digit Symbol
Coding and the Woodcock–Johnson Broad Reading cluster, might have been dif-
ferentiated among the GCS groups with larger and balanced sample sizes. However,
the TMT cluster effect sizes were consistently larger than those of the GCS groups,
suggesting that even with equal sample sizes, the TMT clusters may be more effec-
tive in classifying severity of neurocognitive impairments. In addition, analysis of
only those cases with GCS scores did indicate that the general pattern noted for the
TMT clusters remained, particularly with regard to the external validity variables,
where there was clear distinction of the severe cluster from the mild and moderate
clusters. Finally, children in our sample were evaluated with the TMT an average of
13.8 months after they were injured, so it may be that better separation between the
groups and higher predictive power on outcome variables might have been achieved
if the evaluation occurred closer to the time of injury.
Future studies should investigate whether or not the TMT demonstrates similar
usefulness in classifying severity of brain injury and dysfunction in other clinical
populations, as well as adults. Studies should also further establish appropriate cut-
off scores for the TMT-A and TMT-B clusters that might be useful in demarcating
severity of injury. Along with additional neurocognitive variables, these clusters
should be compared across behavioral variables and other outcome measures that
are relevant for TBI rehabilitation. It may also be informative to examine the utility
120 D.N. Allen et al.

of the TMT when it is administered closer to the acute phase of injury, as it may
better have better predictive validity and provide a better comparison to the GCS.
Finally, the role of environmental factors on cluster membership was not examined,
which may help explain differences in TMT performance following injury and be
useful in understanding the recovery process (Taylor et al., 2008). The current find-
ings do provide evidence that the TMT can serve as a brief classification instrument,
though continued research is necessary to replicate these findings with other sam-
ples with differing demographic and clinical characteristics.

References

Aldenderfer, M. S., & Blashfield, R. K. (1984). Cluster analysis. Beverly Hills, CA: Sage.
Allen, D. N., Leany, B. D., Thaler, N. S., Cross, C., Sutton, G. P., & Mayfield, J. (2010). Memory
and attention profiles in pediatric traumatic brain injury. Archives of Clinical Neuropsychology,
25(7), 618–633.
Allen, D. N., Thaler, N. S., Ringdahl, E. N., Barney, S., & Mayfield, J. (2012). Comprehensive trail
making test performance in children and adolescents with traumatic brain injury. Psychological
Assessment, 24(3), 556–564.
American Congress of Rehabilitation Medicine; Mild Traumatic Brain Injury Committee. (1993).
Definition of mild traumatic brain injury. The Journal of Head Trauma Rehabilitation, 8(3),
86–87.
Armitage, S. G. (1946). An analysis of certain psychological tests used for the evaluation of brain
injury. Psychological Monographs, 60(1), 1–48. Whole No. 277.
Armstrong, C., Allen, D. N., Donohue, B., & Mayfield, J. (2008). Sensitivity of the comprehensive
trail making test to traumatic brain injury in adolescents. Archives of Clinical Neuropsychology,
23, 351–358.
Babikian, T., & Asarnow, R. (2009). Neurocognitive outcomes and recovery after pediatric TBI:
Meta-analytic review of the literature. Neuropsychology, 23(3), 283–296. doi:10.1037/
a0015268.
Barth, J. T., Macciocchi, S. N., Giordani, B., Rimel, R., Jane, J. A., & Boll, T. J. (1983).
Neuropsychological sequelae of minor head injury. Neurosurgery, 13, 529–533.
Boake, C., Millis, S. R., High, W. M. Jr., et al. (2001). Using early neuropsychologic testing to
predict long-term productivity outcome from traumatic brain injury. Archives of Physical
Medicine and Rehabilitation, 82, 761–768.
Brown, A. W., Malec, J. F., Mandrekar, J., Diehl, N. N., Dikmen, S. S., Sherer, M., et al. (2010).
Predictive utility of weekly post-traumatic amnesia assessments after brain injury: A multicen-
tre analysis. Brain Injury, 24(3), 472–478.
Carroll, L. J., Cassidy, J. D., Holm, L., Kraus, J., & Coronado, V. G. (2004). Methodological issues
and research recommendations for mild traumatic brain injury: the WHO Collaborating centre
task force on mild traumatic brain injury. Journal of Rehabilitation Medicine, 43(Suppl),
113–125.
Cifu, D. X., Keyser-Marcus, L., Lopez, E., Wehman, P., Kreutzer, J. S., Englander, J., et al. (1997).
Acute predictors of successful return to work 1 year after traumatic brain injury: A multicenter
analysis. Archives of Physical Medicine and Rehabilitation, 78, 125–131.
Curtiss, G., Vanderploeg, R. D., Spencer, J., & Salazar, A. M. (2001). Patterns of verbal learning
and memory in traumatic brain injury. Journal of the International Neuropsychological Society,
7(5), 574–585. doi:10.1017/S1355617701755051.
Demery, J. A., Larson, M. J., Dixit, N. K., Bauer, R. M., & Perlstein, W. M. (2010). Operating
characteristics of executive functioning tests following traumatic brain injury. The Clinical
Neuropsychologist, 24(8), 1292–1308. doi:10.1080/13854046.2010.528452.
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 121

Dikmen, S., & Machamer, J. (1995). Neurobehavioral outcomes and their determinants. The
Journal of Head Trauma Rehabilitation, 10, 74–86.
Donders, J., & Warschausky, S. (1997). WISC-III factor index score patterns after traumatic head
injury in children. Child Neuropsychology, 3(1), 71–78.
Everitt, B. S., Landau, S., & Leese, M. (2001). Cluster analysis (4th ed.). London: Arnold.
Faul, M., Xu, L., Wald, M. M., & Coronado, V. G. (2010). Traumatic brain injury in the United
States: Emergency department visits, hospitalizations and deaths 2002–2006. Atlanta, GA:
Centers for Disease Control and Prevention, National Center for Injury Prevention and Control.
Fay, T. B., Yeates, K., Wade, S. L., Drotar, D., Stancin, T., & Taylor, H. (2009). Predicting longi-
tudinal patterns of functional deficits in children with traumatic brain injury. Neuropsychology,
23(3), 271–282. doi:10.1037/a0014936.
Felmingham, K. L., Baguley, I. J., & Green, A. M. (2004). Effects of diffuse axonal injury on speed
of information processing following severe traumatic brain injury. Neuropsychology, 18(3),
564–571. doi:10.1037/0894-4105.18.3.564.
Gennarelli, T. A., & Thibault, L. E. (1985). Biomechanics of head injury. In R. H. Wilkins & S. S.
Rengachary (Eds.), Neurosurgery (pp. 1531–1536). New York: McGraw-Hill.
Ghosh, A., Wilde, E. A., Hunter, J. V., Bigler, E. D., Chu, Z. L., Li, X. Q., et al. (2009). The relation
between Glasgow Coma Scale score and later cerebral atrophy in paediatric traumatic brain
injury. Brain Injury, 23(3), 228–233.
Goethe, K. E., & Levin, H. S. (1986). Neuropsychological consequences of head injury in children.
In G. Goldstein & R. E. Tarter (Eds.), Advances in clinical neuropsychology (Vol. 3, pp. 213–
242). New York: Plenum Press.
Hackbarth, R. M., Rzeszutko, K. M., Sturm, G., Donders, J., Kuldanek, A. S., & Sanfilippo, D. J.
(2002). Survival and functional outcome in pediatric traumatic brain injury: A retrospective
review and analysis of predictive factors. Critical Care Medicine, 30(7), 1630–1635.
Hanks, R. A., Millis, S. R., Ricker, J. H., Giacino, J. T., Nakese-Richardson, R., Frol, A. B., et al.
(2008). The predictive validity of a brief inpatient neuropsychologic battery for persons with
traumatic brain injury. Archives of Physical Medicine and Rehabilitation, 89, 950–957.
Hiekkanen, H., Kurki, T., Brandstack, N., Kairisto, V., & Tenovuo, O. (2009). Association of
injury severity, MRI-results and ApoE genotype with 1-year outcome in mainly mild TBI: A
preliminary study. Brain Injury, 23(5), 396–402. doi:10.1080/02699050902926259.
Jennett, B., & Teasdale, G. (1977). Aspects of coma after severe head injury. The Lancet, 1(8017),
878–881.
Kalmar, K., Novack, T. A., Nakase-Richardson, R., Sherer, M., Frol, A. B., Gordon, W. A., et al.
(2008). Feasibility of a brief neuropsychologic test battery during acute inpatient rehabilitation
after traumatic brain injury. Archives of Physical Medicine and Rehabilitation, 89, 942–949,
doi:10.1016/j.apmr.2008.01.008.
Kraemer, B. R., & Blancher, J. (1997). An overview of educationally relevant effects, assessment,
and school reentry. In A. Glang, G. H. S. Singer, & B. Todis (Eds.), Students with acquired
brain injury: The school response (pp. 3–31). Baltimore, MD: Paul H. Brookes.
Landis, J. R., & Koch, G. G. (1977). The measurement of observer agreement for categorical data.
Biometrics, 33(1), 159–174.
Langenecker, S. A., Zubieta, J., Young, E. A., Akil, H., & Nielson, K. A. (2007). A task to manipu-
late attentional load, set-shifting, and inhibitory control: Convergent validity and test-retest
reliability of the parametric Go/No-Go test. Journal of Clinical and Experimental
Neuropsychology, 29(8), 842–853. doi:10.1080/13803390601147611.
Lau, B. C., Collins, M. W., & Lovell, M. R. (2012). Cutoff scores in neurocognitive testing and
symptom clusters that predict protracted recovery from concussions in high school athletes.
Neurosurgery, 70(2), 371–379, doi:10.1227/NEU.0b013e31823150f0.
Levin, H. S., Benton, A. L., & Grossman, R. G. (1982). Neurobehavioral consequences of closed
head injury. New York: Oxford University Press.
Lieh-Lai, M. W., Theodorou, A. A., Samaik, A. P., Meert, K. L., Moylan, P. M., & Canady, A. L.
(1992). Limitations of the Glasgow Coma Scale in predicting outcome in children with
traumatic brain injury. The Journal of Pediatrics, 120(2), 195–199.
122 D.N. Allen et al.

Lowther, J. L., & Mayfield, J. (2004). Memory functioning in children with traumatic brain injuries:
A TOMAL validity study. Archives of Clinical Neuropsychology, 19(1), 89–104. doi:10.1016/
S0887-6177(02)00222-6.
Mittelmeier, C., Rossi, J. S., & Berman, A. (1989). Discriminative ability of the trail making test
in young children. International Journal of Clinical Neuropsychology, 11(4), 163–166.
Morris, R., Blashfield, R., & Satz, P. (1981). Neuropsychology and cluster analysis: Potentials and
problems. Journal of Clinical Neuropsychology, 3(1), 79–99. doi:10.1080/01688638108403115.
Mottram, L., & Donders, J. (2006). Cluster subtypes on the california verbal learning test-
children’s version after pediatric traumatic brain injury. Developmental Neuropsychology,
30(3), 865–883. doi:10.1207/s15326942dn3003_6.
Partington, J. E. (1949). Detailed instructions for administering Partington’s pathways test. The
Psychological Service Center Journal, 1, 46–48.
Partington, J. E., & Leiter, R. G. (1949). Partington’s pathways test. The Psychological Service
Center Journal, 1, 11–20.
Periáñez, J. A., Ríos-Lago, M., Rodríguez-Sánchez, J. M., Adrover-Roig, D., Sánchez-Cubillo, I.,
Crespo-Facorro, B., et al. (2007). Trail making test in traumatic brain injury, schizophrenia,
and normal ageing: Sample comparisons and normative data. Archives of Clinical
Neuropsychology, 22, 433–447.
Rabin, L., Barr, W., & Burton, L. (2005). Assessment practices of clinical neuropsychologists in
the United States and Canada: A survey of INS, NAN, and APA Division 40 members. Archives
of Clinical Neuropsychology, 20(1), 33–65.
Reitan, R. M. (1955). The relation of the trail making test to organic brain damage. Journal of
Consulting Psychology, 19, 393–394.
Reitan, R. M. (1958). Validity of the trail making test as an indicator of organic brain damage.
Perceptual and Motor Skills, 8, 271–276.
Reitan, R. M. (1971). Trail making test results for normal and brain-damaged children. Perceptual
and Motor Skills, 33, 575–581.
Reitan, R. M., & Herring, S. (1985). A short screening device for identification of cerebral
dysfunction in children. Journal of Clinical Psychology, 41(5), 643–650.
Reitan, R. M., & Wolfson, D. (1992). The Halstead-Reitan neuropsychological test battery:
Theory and clinical interpretation (2nd ed.). Tucson, AZ: Neuropsychology Press.
Reitan, R. M., & Wolfson, D. (1995). The category test and the trail making test as measures of
frontal lobe functions. The Clinical Neuropsychologist, 9, 50–56.
Reitan, R. M., & Wolfson, D. (2004). The trail making test as an initial screening procedure for
neuropsychological impairment in older children. Archives of Clinical Neuropsychology, 19,
281–288.
Reitan, R. M., & Wolfson, D. (2009). The Halstead-Reitan neuropsychological test battery for
adults—Theoretical, methodological, and validational bases. In I. Grant, K. M. Adams, I.
Grant, & K. M. Adams (Eds.), Neuropsychological assessment of neuropsychiatric and neuro-
medical disorders (3rd ed., pp. 3–24). New York: Oxford University Press.
Reynolds, C. R. (2002). Comprehensive trail making test (CTMT). Austin, TX: PRO-ED, Inc.
Reynolds, C. R., & Bigler, E. D. (1994). Test of memory and learning: Examiner’s manual. Austin,
TX: Pro-Ed.
Rivara FP, Koepsell TD, Wang J, Temkin N, Dorsch A, Vavilala MS, Durbin D, Jaffe KM.
Incidence of disability among children 12 months after traumatic brain injury. Am J Public
Health. 2012, 102(11):2074-9. doi: 10.2105/AJPH.2012.300696.
Ríos, M., Periáñez, J. A., & Muñoz-Céspedes, J. M. (2004). Attentional control and slowness of
information processing after severe traumatic brain injury. Brain Injury, 18(3), 257–272. doi:1
0.1080/02699050310001617442.
Ruff, R. M., Iverson, G. L., Barth, J. T., Bush, S. S., & Broshek, D. K. (2009). Recommendations
for diagnosing a mild traumatic brain injury: A National Academy of neuropsychology educa-
tion paper. Archives of Clinical Neuropsychology, 24, 1–8.
Russell, E. W., Neuringer, C., & Goldstein, G. (1970). Assessment of brain damage: A neuropsy-
chological key approach. Oxford: Wiley-Interscience.
5 Classification of Traumatic Brain Injury Severity: A Neuropsychological Approach 123

Russell, W. R., & Smith, A. (1961). PTA in closed head injury. Archives of Neurology, 5, 16–29.
Saatman, K. E., Duhaime, A. C., Bullock, R., Maas, A. I., Valadka, A., Manley, G. T., et al. (2008).
Classification of traumatic brain injury for targeted therapies. Journal of Neurotrauma, 25(7),
719–738.
Salorio, C. F., Slomine, B. S., Grados, M. A., Vasa, R. A., Christensen, J. R., & Gerring, J. P.
(2005). Neuroanatomic correlates of CVLT-C performance following pediatric traumatic brain
injury. Journal of the International Neuropsychological Society, 11(6), 686–696. doi:10.1017/
S1355617705050885.
Sánchez-Cubillo, I., Periáñez, J. A., Adrover-Roig, D., Rodríguez-Sánchez, J. M., Ríos-Lago, M.,
Tirapu, J., et al. (2009). Construct validity of the trail making test: role of task-switching,
working memory, inhibition/interference control, and visuomotor abilities. Journal of the
International Neuropsychological Society, 15(3), 438–450.
Sherer, M., Sander, A. M., Nick, T. G., High, W. M. Jr., Malec, J. F., & Rosenthal, M. (2002). Early
cognitive status and productivity outcome after traumatic brain injury: findings from the TBI
model systems. Archives of Physical Medicine and Rehabilitation, 83, 183–192.
Sherer, M. M., Struchen, M. A., Yablon, S. A., Wang, Y. Y., & Nick, T. G. (2008). Comparison of
indices of traumatic brain injury severity: Glasgow Coma Scale, length of coma and post-
traumatic amnesia. Journal of Neurology, Neurosurgery & Psychiatry, 79(6), 678–685.
doi:10.1136/jnnp. 2006.111187.
Stuss, D. T., Bisschop, S. M., Alexander, M. P., Levine, B., Katz, D., et al. (2001). The trail making
test: A study in focal lesion patients. Psychological Assessment, 13, 230–239.
Suskauer, S. J., & Huisman, T. M. (2009). Neuroimaging in pediatric traumatic brain injury:
Current and future predictors of functional outcome. Developmental Disabilities Research
Reviews, 15(2), 117–123. doi:10.1002/ddrr.62.
Taylor, H. G., Swartwout, M. D., Yeates, K. O., Walz, N. C., Stancin, T., & Wade, S. L. (2008).
Traumatic brain injury in young children: Postacute effects on cognitive and school readiness
skills. Journal of the International Neuropsychological Society, 14(5), 734–45.
Teasdale, G., & Jennett, B. (1974). Assessment of coma and impaired consciousness: A practical
scale. The Lancet, 2, 81–84.
Thaler, N. S., Allen, D. N., Hart, J. S., Boucher, J. R., McMurray, J. C., & Mayfield, J. (2012).
Neurocognitive correlates of the trail making test for older children in patients with traumatic
brain injury. Archives of Clinical Neuropsychology, 27(4), 446–452.
Thaler, N. S., Bello, D. T., Randall, C., Goldstein, G., Mayfield, J., & Allen, D. N. (2010). IQ
profiles are associated with differences in behavioral functioning following pediatric traumatic
brain injury. Archives of Clinical Neuropsychology, 25(8), 781–790.
U. S. War Department, Adjutant General’s Office. (1944). Manual of the army individual test.
Author: Washington D. C.
Watson, N. (1949). A qualitative check list for the clinical use of Partington’s pathways test in the
evaluation of brain injury. Psychological Service Center Journal, 1, 49–51.
Wechsler, D. (1991). Wechsler intelligence scale for children (3rd ed.). San Antonio, TX: The
Psychological Corporation.
Wells, R., Minnes, P., & Phillips, M. (2009). Predicting social and functional outcomes for
individuals sustaining paediatric traumatic brain injury. Developmental Neurorehabilitation,
12(1), 12–23. doi:10.1080/17518420902773109.
Wilson, B. A., Evans, J. J., Emslie, H., Balleny, H., Wason, P. C., & Baddeley, A. D. (1999).
Measuring recovery from post traumatic amnesia. Brain Injury, 13, 505–520.
Woodcock, R. W., & Johnson, M. B. (1989). Woodcock–Johnson psycho-educational battery-
revised. Allen, TX: DLM Teaching Resources.
Woodcock, R. W., McGrew, K. S., & Mather, N. (2001). Woodcock–Johnson III tests of achievement.
Itasca, IL: Riverside.
Wrightson, P., & Gronwall, D. (1981). Time of work and symptoms after minor head injury. Injury,
12, 445–454.

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