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Differential Sensitivity of TOMAL Subtests and Index Scores

to Pediatric Traumatic Brain Injury


Nicholas S. Thaler and Sally J. Barney
Department of Psychology, University of Nevada-Las Vegas, Las Vegas, Nevada
Cecil R. Reynolds
Department of Educational Psychology, Texas A&M University, College Station, Texas
Joan Mayeld
Our Childrens House at Baylor University, Dallas, Texas
Daniel N. Allen
Department of Psychology, University of Nevada-Las Vegas, Las Vegas, Nevada
The objective of the present study was to examine and compare the subtest, index, and
factor scores of the Test of Memory and Learning (TOMAL), using receiver-operating
characteristic curves, to investigate their sensitivity and specicity to traumatic brain
injury (TBI) in children and adolescents. One hundred and fty participants who had
sustained TBI were compared to 150 controls matched on age and gender from the
TOMALs standardization sample. Results indicated that the greatest area under the
curve (AUC) was for the Object Recall (OR) subtest score, the Composite Memory
Index (CMI), and the attention factor score. The optimal CMI cutoff score for a TBI
diagnosis was 83. When factor scores were compared, the attention factor and two ver-
bal factors had signicantly larger AUCs than the three nonverbal factors. These nd-
ings suggest that the OR subtest and CMI are most sensitive to TBI, and that when
components were broken into factors with no overlapping subtests, attention and verbal
memory were optimal for classifying TBI.
Key words: memory, pediatric, ROC, TBI, TOMAL
In the last decade, there has been a substantial increase
in research on neuropsychological assessment for youth
who have sustained a traumatic brain injury (TBI). Out-
comes for this population have been well documented,
and TBI has been found to affect childrens cognitive,
behavioral, emotional, and academic functioning nega-
tively (Hooper, Alexander, & Moore, 2004; Lowther &
Mayeld, 2004; Max et al., 1998; Roberts & Furuseth,
1997; Wassenberg, Max, & Lindgren, 2004). Impaired
attention and memory have been reported routinely in
pediatric TBI (Dennis, Guger, Roncadin, Barnes, &
Schachar, 2001; Hooper et al., 2004; Max et al., 1998;
Wassenberg et al., 2004), with severity of these decits
serving as an important predictor of outcome
(Catroppa & Anderson, 2002, 2007). A number of neu-
ropsychological memory batteries including the
Wide-Range Assessment of Memory and Learning-
Second Edition (WRAML-2; Sheslow & Adams,
2003), the California Verbal Learning Test for Children
Address correspondence to Daniel N. Allen, Ph.D., Neuropsychol-
ogy Research Program, Department of Psychology, University of
Nevada-Las Vegas, 4505 Maryland Parkway, Las Vegas, NV 89154.
E-mail: daniel.allen@unlv.edu
APPLIED NEUROPSYCHOLOGY, 18: 168178, 2011
Copyright # Taylor & Francis Group, LLC
ISSN: 0908-4282 print=1532-4826 online
DOI: 10.1080/09084282.2011.595443
(CVLT-C; Delis, Kramer, Kaplan, & Ober, 1994), the
Childrens Memory Scale (Wechsler, 1995), and the Test
of Memory and Learning (TOMAL; Reynolds & Bigler,
1994) have been used to assess these decits in this popu-
lation with reliable and comparable ndings. However,
relatively few studies have examined the ability of scores
from these batteries to distinguish populations and spe-
cic decits in pediatric TBI.
Researchers have previously examined the ability of
scores from intelligence batteries to distinguish decits
in both child and adult TBI populations, and ndings
generally converge in identifying selectively impaired
performance on working memory and processing speed
subtests (Allen, Thaler, Donohue, & Mayeld, 2010;
Calhoun & Mayes, 2005; Donders & Janke, 2008;
Donders, Tulsky, & Zhu, 2001; Mayes & Calhoun,
2004). Although useful within the clinical setting, intelli-
gence batteries provided limited information on specic
cognitive processes such as memory. With regard to
memory batteries, researchers typically select subtests
within the battery for evaluation of specic constructs
such as working memory. However, a lack of criterion
validity studies on memory batteries may hinder their
application to the very clinical populations they were
designed to evaluate (Allen, Knatz, & Mayeld, 2006).
Existing criterion validity studies do conrm some
reliable ndings across batteries. For example, a study
of WRAML scores found that children with severe
injuries performed approximately one standard devi-
ation below the mean on verbal, visual, and general
indexes, while children with mild and moderate injuries
performed signicantly better than the severe group on
the visual memory index (Farmer et al., 1999). However,
none of the groups performed signicantly worse on the
Visual Learning Delayed subtests compared with the
controls. Additional validity studies have found that
adults with moderate-to-severe TBI perform signi-
cantly poorer on the Continuous Visual Memory Test
compared with controls (Strong & Donders, 2008) and
scored approximately one third to three quarters of a
standard deviations below the standardization sample
(SS) on the California Verbal Learning Test-II
(Jacobs & Donders, 2007). Studies on the CVLT-C have
found that both severity of injury and processing speed
appear to mediate the impact of performance in children
with TBI (Donders & Minnema, 2004; Donders &
Nesbit-Greene, 2004). These ndings provide evidence
of general memory impairment in TBI cases and provide
support for the use of memory batteries when applied to
children with TBI, although additional research on these
batteries is necessary.
The TOMAL may be particularly salient for assessing
neuropsychological function in youth with TBI, as it is a
measure of broad-band verbal and nonverbal memory
as well as narrow-band memory skills, attention, and
learning (Schmitt & Decker, 2009). The TOMAL has
been used to evaluate neurocognitive decits in clinical
populations including attention-decit hyperactivity dis-
order (ADHD; Thaler, Allen, McMurray, & Mayeld,
2010), reading disabilities (Howes, Bigler, Lawson, &
Burlingame, 1999), genetic disorders (Lajiness-ONeill
et al., 2005), and TBI (Lowther & Mayeld, 2004),
and its large SS and high reliability ratings have estab-
lished the TOMAL as a psychometrically sound mem-
ory battery (Dumont, Whelley, Comtois, & Levine,
1994). However, only a few studies have examined the
TOMALs psychometric properties in children with
TBI. Lowther and Mayeld (2004) compared 70 chil-
dren who had sustained a moderate-to-severe TBI with
70 controls on their performance on the TOMAL. The
authors found that with the exception of two Nonverbal
Delayed Recall subtests, children with TBI performed
signicantly lower on indexes and subtests compared
with controls. Comparisons between children with mod-
erate and severe injuries indicated trends in the expected
direction, with the severe group generally performing
worse on subtests and indexes, although these
differences were not signicant.
A recent study by Allen, Leany, and colleagues (2010)
focused on neurocognitive heterogeneity in children
with TBI and identied six comparable TOMAL factors
in 150 children who had sustained TBI as well as 150
controls matched for gender and age from the
TOMALs SS. These factors were identied using prin-
cipal components analysis for both TBI and control
samples, and their structure differed from prior factor
solutions for the TOMAL (cf., Alexander & Mayeld,
2005; Reynolds & Bigler, 1994, 1996; Thaler et al.,
2010), possibly due to differences in the types of analyses
used, TOMAL subtests included in the analyses, the
populations under investigation, or some combination
of these factors. In any case, the factor structure ident-
ied by Allen, Leany, et al. (2010) approached simple
structure, was interpretable, and was stable across TBI
and control groups. As found in Lowther and Mayeld
(2004), signicant differences were present between con-
trols and TBI groups on the TOMAL subtest and index
scores, and as expected, similar differences were present
for factor score comparisons. Thus, the study by Allen,
Leany, et al. (2010) conrmed and extended the results
reported by Lowther and Mayeld, primarily by includ-
ing a larger sample and by examining factor score differ-
ences. In addition, while the extant ndings support the
TOMALs sensitivity to childhood TBI, further investi-
gation of its subtest, composite, and factor scores
sensitivities to TBI is warranted.
Signal detection theory has found wide application
in psychology through receiver-operating characteristic
(ROC) analyses (Swets, 1996). More specically, ROC
analyses assess the discriminative ability of test scores
DIFFERENTIAL SENSITIVITY OF TOMAL 169
in classication studies using a variety of instruments
and clinical populations (Basic et al., 2009; Horwitz,
Lynch, McCaffrey, & Fisher, 2008; Sagen et al., 2009;
Thaler et al., 2010). Therefore, the purpose of the
present study was to investigate scores at multiple levels
on the TOMAL in children who sustained TBI by calcu-
lating and comparing sensitivity and specicity rates of
scores across subtests, indexes, and factor scores using
ROC analyses. While prior research suggests that most
if not all subtests will differentiate those with TBI from
normal controls, differing sensitivities and specicities
among the scores may also be hypothesized. For
example, a meta-analysis of 28 publications on pediatric
TBI (Babikian & Asarnow, 2009) suggests that attention
and verbal memory appear to be the most impacted by
TBI, while visual memory and visual perception are
the most resilient. In consideration of this meta-analysis
and other criterion validity studies on memory batteries
(Farmer et al, 1999; Jacobs & Donders, 2007; Lowther &
Mayeld, 2004; Strong & Donders, 2008), we hypothe-
sized that given that our sample sustained moderate-to-
severe injuries, the TBI group would perform between
one and two standard deviations below the control
group. We also hypothesized that the Verbal Memory
Index (VMI) and Attention=Concentration Index
(ACI) would have greater classication rates than
the TOMALs Nonverbal Memory Index (NMI).
Finally, we compared the six factors identied by Allen,
Leany, and colleagues (2010) and anticipated that
an attention factor would be most sensitive to a diag-
nosis of TBI, followed by verbal factors, and then the
nonverbal factors.
METHOD
Participants
Participants included 150 children who had sustained
TBI (TBI group) and 150 children with no history of
TBI (control group) who were studied in the Allen,
Leany, et al. (2010) study. Children in the TBI group
were selected from a consecutive series of cases referred
for neuropsychological evaluation. Structural brain
damage resulting from TBI was conrmed using appro-
priate neuroimaging, laboratory, and examination nd-
ings. On average, injuries were severe in nature as
indicated by Glasgow Coma Scale (GCS) scores that
were available for 101 of our participants with TBI
(median 7). Children were selected for the TBI group
if they had a diagnosis of TBI and no other neurological
or neurodevelopmental disorders (including stroke,
ADHD, and anoxic brain injury) and if they had been
administered the TOMAL as part of their evaluation.
Participants in the control group were selected from
the TOMAL SS to match the TBI group on age and
gender. When more than one case matched a TBI par-
ticipant on age and sex, one case from the viable cases
was included via random selection. Using these criteria,
133 participants were matched on age and sex, with the
remaining cases randomly selected from the SS. Demo-
graphic and clinical information for both groups is
available in Table 1. Comparisons between the groups
found no signicant differences due to age, F(1,
299) 1.68, p .20, or gender, v
2
.66, p .42.
Measures
The TOMAL (Reynolds & Bigler, 1994) is a broad mea-
sure of memory, learning, and attention for children
aged 5 to 19 years and is composed of 10 core and 4 sup-
plementary subtests. Core subtests include Memory for
Stories (MFS), Facial Memory (FM), Word Selective
Reminding (WSR), Visual Selective Reminding (VSR),
Object Recall (OR), Abstract Visual Memory (AVM),
Digits Forward (DF), Visual Sequential Memory
(VSM), Paired Recall (PR), and Memory for Location
(MFL). Four of these subtests have a delayed compo-
nent including Memory for Stories Delayed (MFSD),
Facial Memory Delayed (FMD), Word Selective
Reminding Delayed (WSRD), and Visual Selective
Reminding Delayed (VSRD). Supplemental subtests
include Letters Forward (LF), Digits Backward, Letters
Backward, and Manual Imitation (MI). Subtests have a
standard score mean of 10 and a standard deviation of 3
TABLE 1
Demographic and Clinical Information
Variables
TBI group
(n 150)
Control Group
(n 150)
Age M11.7 (SD3.7) M11.5 (SD3.1)
Months Since Injury M7.0 (SD3.1)
% Male 57.3 52.7
% Ethnicity
Caucasian 54.5 74.7
African American 22.8 11.0
Hispanic=Latino 14.0 8.9
Asian American 0.7 3.4
Other 0.7 2.1
% Closed Head Injury 93.3
% Mechanism of Injury
Motor Vehicle
Accident
56.7
Struck by Motor
Vehicle
20.0
Gunshot 4.0
Fall 2.7
4-Wheeler Accident 5.3
Bike Accident 2.2
Skiing 3.3
Other 6.0
170 THALER ET AL.
and combine to produce several indexes including the
VMI, the NMI, a Composite Memory Index (CMI), a
Delayed Recall Index (DRI), and the ACI. All indexes
have a mean of 100 and a standard deviation of 15. A
more recent version (TOMAL-2; Reynolds & Voress,
2007) contains the same subtests and the same organiza-
tion of subtests into scales and indexes, and has more
than 90% item overlap with the TOMAL.
Data Analysis
Comparisons initially were made between the SS and
TBI groups on demographic variables to determine the
success of group matching based on the case selection
method. To establish the sensitivity of the TOMAL to
TBI, SS and TBI between-group comparisons were
made using multivariate analysis of variance
(MANOVA) for the TOMAL subtest and index scores,
with post-hoc univariate analyses used to examine spe-
cic subtest and composite score differences between
the groups when overall MANOVAs were signicant.
TOMAL indexes were then compared between the
TBI group and control group using ROC curves to
establish the sensitivity, specicity, and optimal cutoff
scores of TOMAL subtests and indexes for TBI. In
addition, ROC analyses were used to compare the two
groups using the factor scores derived from the
six-factor structure rst identied by Allen, Leany, and
colleagues (2010). In that study, the rst factor (atten-
tion) was composed of the digit and letter span tasks
and primarily assessed attention=concentration. The
second factor (verbal memory) consisted of the WSR,
WSRD, PR, and OR subtests. The third factor (memory
for stories) also assessed verbal memory and was com-
posed of MFS and MFSD. The fourth factor (nonverbal
learning) consisted of nonverbal learning subtests
including VSR and VSRD, while the fth factor
assessed facial memory with the FM and FMD subtests.
Finally, the sixth factor (abstract nonverbal) was com-
posed of abstract nonverbal subtests including AVM
and MFL. ROC analyses also were conducted for these
six factors because, unlike the TOMAL Supplementary
Index scores, the factors, like the primary TOMAL
indexes, share no subtests in common and so may be
more specic and sensitive than either the Supplemen-
tary Index or subtest scores. As in Allen, Leany, et al.
(2010), factor scores were calculated by summing the
standard scores of each factors subtests and then calcu-
lating the average of these subtests. Prior studies (e.g.,
Allen, Strauss, Kemtes, & Goldstein, 2007) have demon-
strated that such methods produce factor scores compa-
rable to regression-based scores calculated through
TABLE 2
TOMAL Data for the Standardization Sample (SS) and Traumatic Brain Injury (TBI) Groups
SS (N150) TBI (N150)
F
Variable Mean SD Mean SD (df 1,298) d
TOMAL Subtest Scores
Memory for Stories 10.6 2.5 8.1 3.0 39.2

0.91
Word Selective Reminding 10.1 2.8 7.8 3.4 27.9

0.74
Object Recall 9.8 3.0 5.8 3.3 29.7

1.27
Digits Forward 9.8 3.6 6.7 2.6 6.0

0.99
Paired Recall 10.0 3.0 7.4 3.8 25.0

0.76
Letters Forward 9.9 3.2 6.7 2.7 7.3

1.08
Digits Backward 10.9 3.6 8.2 2.3 16.5

0.89
Letters Backward 10.4 3.7 7.9 2.6 13.7

0.78
Facial Memory 10.4 2.8 7.6 3.0 13.3

0.97
Visual Selective Reminding 10.2 3.5 6.5 3.2 16.7

1.10
Abstract Visual Memory 10.1 3.0 7.3 3.5 36.1

0.86
Visual Selective Reminding 10.5 2.9 8.3 2.7 12.6

0.79
Memory for Location 9.8 4.0 7.7 4.3 31.0

0.51
Memory for Stories Delayed 9.9 2.8 6.5 3.3 40.2

1.11
Facial Memory Delayed 9.6 2.5 8.9 2.4 5.7

0.29
Word Selective Reminding Delayed 9.5 2.4 7.8 2.9 30.0

0.64
Visual Selective Reminding Delayed 9.7 1.7 8.4 2.3 19.6

0.64
TOMAL Index Scores
Verbal Memory Index 100.4 13.4 80.4 16.1 73.3

1.37
Nonverbal Memory Index 101.0 13.2 82.6 15.4 90.8

1.31
Composite Memory Index 101.0 12.1 80.8 14.8 130.7

1.49
Delayed Recall Index 97.8 8.8 86.0 12.9 48.9

1.06
Attention=Concentration Index 101.0 18.9 82.6 13.2 16.9

1.13

Bonferroni correction p <.0023 for signicance at the .05 level.


DIFFERENTIAL SENSITIVITY OF TOMAL 171
principal component or maximum likelihood factor
analyses but have the advantage of retaining similar
characteristics to the original TOMAL standard scores.
This also is a reasonable approximation to unit weight-
ing in the calculation of a factor score and is more likely
to generalize outside of the sample.
Procedure
The TOMAL was administered as part of a clinical
neuropsychology evaluation at a pediatric restorative
care facility by either a pediatric neuropsychologist
or trained doctoral-level graduate students under
supervision of the neuropsychologist.
RESULTS
Subtest and Index Differences
The SS groups performance on the TOMAL subtest
and index scores approximated the SS mean, and the
TBI group performed approximately 1.3 standard devia-
tions below the SS group on most TOMAL scores.
Although introducing some redundancy into the analy-
ses, we tested group differences for both subtest and
index scores because of a relative lack of information
on TOMAL performance in children with TBI. MANO-
VAs indicated signicant differences between the groups
on the subtest scores, F(68, 528) 5.59, p <.001,
g
2
p
.419, and index scores, F(68, 528) 12.4, p <.001,
g
2
p
.31. Following Bonferroni correction for multiple
comparisons, signicant differences were present
between the TBI and SS groups on all of the TOMAL
scores (see Table 2).
ROC analyses were then conducted to determine the
sensitivity and specicity of TOMAL subtest and index
scores to brain damage. The area under the ROC curve
(AUC) serves as an indicator of a test scores ability to
distinguish groups, with an AUC of 1.00 indicating per-
fect classication and an AUC of 0.50 indicating a rate
no greater than chance. Therefore, the more an AUC
approaches 1.00, the better overall classication rate of
the test, and AUCs between 0.80 and 0.90 are regarded
as good classication accuracy (Hosmer & Leme-
show, 2000). By comparing AUCs for different tests,
in this case the TOMAL scores, signicant improvement
in classication can be identied. The method described
by Hanley and McNeil (1983) was used to make pair-
wise comparisons and detect signicant differences
between AUCs of the various subtest, index, and factor
scores.
Table 3 contains the AUCs, standard error of the
curves, and 95% condence intervals for 17 TOMAL
subtests (the MI subtest was not included in the analysis
because it was infrequently administered due to the
levels of motor impairment in much of the TBI sample)
as well as pairwise contrasts for the six most sensitive
subtests. Inspection of the curves indicates that the
OR subtest had the highest AUC at 0.82, a good classi-
cation rate, followed by the MFSD, VSR, LF, DF, and
FM subtests. See Figure 1 for subtest ROC curves.
Next, classication accuracy was calculated for the
top six subtests scores using discriminant function
analysis (DFA). DFA indicated that the OR subtest cor-
rectly classied 76.0% of the cases, the MFSD subtest
72.0% of the cases, the VSR subtest 71.0% of the cases,
the DF subtest 71.0% of the cases, the LF subtest 68.7%
of the cases, and the FM subtest 68.0% of the cases.
Pairwise comparisons indicated that the ORs AUC
was not signicantly greater than the MFSD, VSR,
LF, and DF subtests but was signicantly greater than
TABLE 3
ROC Analyses for the TOMAL Subtest Scores (Subtests Ordered
from Greatest to Least AUC)
Subtest AUC SE 95% CI of Area
Object Recall 0.82 .024 0.770.87
Memory for Stories Delayed 0.78 .026 0.730.83
Visual Selective Reminding 0.78 .026 0.730.83
Letters Forward 0.77 .027 0.720.82
Digits Forward 0.76 .028 0.700.81
Facial Memory 0.75 .028 0.700.81
Memory for Stories 0.74 .029 0.680.79
Digits Backward 0.72 .029 0.660.78
Abstract Visual Memory 0.71 .029 0.660.77
Visual Sequential Memory 0.71 .030 0.650.77
Letters Backward 0.71 .030 0.650.77
Word Selective Reminding 0.70 .030 0.640.76
Paired Recall 0.69 .030 0.630.75
Word Selective Reminding Delayed 0.68 .031 0.620.74
Visual Selective Reminding Delayed 0.68 .031 0.620.74
Memory for Location 0.64 .032 0.580.71
Facial Memory Delayed 0.57 .033 0.510.64
Contrasts z score SE p
OR vs. MFSD 1.16 .031 .25
OR vs. VSR 1.30 .030 .19
OR vs. LF 1.47 .031 .14
OR vs. DF 1.83 .032 .07
OR vs. FM 2.12 .031 .03
MFSD vs. VSR 0.11 .035 .91
MFSD vs. LF 0.28 .035 .78
MFSD vs. DF 0.67 .035 .50
MFSD vs. FM 0.90 .034 .37
VSR vs. LF 0.19 .032 .85
VSR vs. DF 0.58 .035 .57
VSR vs. FM 0.74 .036 .46
LF vs. DF 0.56 .025 .58
LF vs. FM 0.58 .035 .57
DF vs. FM 0.17 .039 .86
ORObject Recall; MFSDMemory for Stories Delayed;
VSRVisual Selective Reminding; LFLetters Forward; DF
Digits Forward; FMFacial Memory.
172 THALER ET AL.
the FM subtest. Therefore, it can be inferred that the
rst ve subtests have comparable classication accura-
cies with each other while the FM is signicantly less
accurate than the OR subtest. When the rst ve sub-
tests were analyzed together, they correctly classied
82.0% of the cases.
Next, ROC curves were examined for TOMAL index
scores. Table 4 displays the AUC curves, standard
errors, and condence intervals for the VMI, NMI,
CMI, DRI, and ACI scores.
As seen in the table, the CMI had the highest AUC at
0.857. Pairwise comparisons indicated that the CMIs
AUC was signicantly greater than the VMIs AUC.
However, the VMIs AUC was not signicantly greater
than the NMIs AUC nor was it signicantly greater
than the ACIs AUC. The VMIs AUC was signicantly
greater than the DRIs AUC. However, the NMI, ACI,
and DRI did not signicantly differ from each other.
Figure 2 displays the ve index scores ROC curves
and their comparisons.
DFA next calculated overall classication rates for
the indexes. The CMI correctly classied 77.3% of the
cases, the VMI 75.3% of the cases, the NMI 72.0% of
the cases, the ACI 73.5% of the cases, and the
DRI 71.3% of the cases. When all ve indexes were
selected as predictors, they correctly classied 76.9% of
the cases.
Table 5 contains sensitivity and specicity estimates,
and true positives (TP), true negatives (TN), false posi-
tives (FP), and false negatives (FN) for the CMI index
score curve presented in Figure 2. The CMI was selected
TABLE 4
ROC Analyses for the TOMAL Index Scores (Indexes Ordered from
Greatest to Least AUC)
Index AUC SE 95% CI of Area
Composite Memory 0.86 .021 0.820.90
Verbal Memory 0.83 .024 0.780.88
Nonverbal Memory 0.82 .024 0.770.87
Attention=Concentration 0.80 .026 0.750.86
Delayed Recall 0.76 .028 0.710.82
Contrasts z score SE p
VMI vs. NMI 0.66 .024 .50
VMI vs. CMI 2.16 .011 .03
VMI vs. DRI 2.52 .024 .01
VMI vs. ACI 1.02 .025 .31
NMI vs. CMI 2.90 .014 <.01
NMI vs. DRI 1.71 .026 .09
NMI vs. ACI 0.35 .027 .73
CMI vs. DRI 3.76 .023 <.01
CMI vs. ACI 2.19 .023 .03
DRI vs. ACI 1.08 .033 .28
VMI Verbal Memory Index; NMI Nonverbal Memory Index;
CMI Composite Memory Index; DRI Delayed Recall Index;
ACI Attention=Concentration Index.
FIGURE 2 ROC curves of the TOMAL VMI, NMI, CMI, DRI, and
ACI.
FIGURE 1 ROC curves of the TOMAL OR, MFSD, DF, LF, VSR,
and FM subtests.
DIFFERENTIAL SENSITIVITY OF TOMAL 173
for display, as it had the best AUC of all indexes. There
is a tradeoff between sensitivity and specicity in that as
one increases, the other typically decreases. Therefore,
the optimal cutoff score is best determined by adding
sensitivity and specicity percentages of each score and
seeing which pair yields the highest sum. TP, TN, FP,
and FN represent the actual number of cases in each
category.
As seen in the table, the optimal cutoff score for the
CMI is 83, and this had the highest TP rate for TBI,
with the smallest tradeoff in FP rate. Additional cutoff
rates were examined for the VMI, NMI, ACI, and
DRI. The VMI detected the most TBI cases at a cutoff
score of 89, the NMI at a score of 89, the ACI at a score
of 92, and the DRI at a score between 90 and 92.
To determine the likelihood that a child with such a
prole would have TBI, children who had TOMAL
index scores below all established cutoff points were
further investigated. Of the original 150 TBI children,
57 (38%) had proles below the cutoff scores of the ve
indexes. Thirty-six of these children had GCS with a
mean of 5.9 (SD2.4), capturing children in our sample
with severe injuries. Of the original 150 controls, only 4
(7%) performed below the cutoff scores.
Factor Score Differences
The six factors rst identied by Allen, Leany, and
colleagues (2010) were next analyzed using ROC curves.
Table 6 displays the AUCs, standard errors, condence
errors, and pairwise contrasts for the six factors.
As seen in the table, the attention factor had the
greatest AUC, followed by the verbal factor, which
TABLE 5
ROC Curve Details for the TOMAL Composite Memory Index
CMI Score Sn (%) Sp (%) TP TN FP FN
46 1.00 0.01 150 1 149 0
51 1.00 0.01 150 2 148 0
52 1.00 0.02 150 3 147 0
54 1.00 0.03 150 5 145 0
55 1.00 0.04 150 6 144 0
56 1.00 0.05 150 8 142 0
57 1.00 0.07 150 10 140 0
58 1.00 0.07 150 11 139 0
59 1.00 0.10 150 15 135 0
61 1.00 0.11 150 17 133 0
62 1.00 0.12 150 18 132 0
63 0.99 0.13 148 19 131 2
64 0.99 0.14 148 21 129 2
65 0.99 0.15 148 22 128 2
66 0.99 0.17 148 25 125 2
67 0.99 0.19 148 29 121 2
68 0.99 0.21 148 32 118 2
69 0.99 0.24 148 36 114 2
70 0.99 0.26 148 39 111 2
71 0.98 0.31 147 47 103 3
72 0.98 0.35 147 52 98 3
73 0.98 0.35 147 53 97 3
74 0.98 0.36 147 54 96 3
75 0.98 0.37 147 55 95 3
76 0.97 0.41 146 62 88 4
77 0.97 0.42 146 63 87 4
79 0.97 0.50 145 75 75 5
80 0.96 0.51 144 76 74 6
81 0.96 0.52 144 78 72 6
82 0.95 0.55 143 82 68 7
83 0.95 0.55 142 83 67 8
84 0.92 0.57 138 86 64 12
85 0.91 0.59 136 88 62 14
86 0.88 0.60 132 90 60 18
87 0.85 0.62 128 93 57 22
88 0.85 0.63 128 95 55 22
89 0.84 0.71 126 106 44 24
90 0.83 0.72 124 108 42 26
91 0.80 0.76 120 114 36 30
92 0.76 0.76 114 114 36 36
93 0.72 0.78 108 117 33 42
94 0.69 0.81 103 122 28 47
95 0.67 0.83 101 124 26 49
96 0.64 0.85 96 128 22 54
97 0.63 0.87 94 130 20 56
98 0.62 0.89 93 133 17 57
99 0.57 0.89 85 134 16 65
100 0.55 0.91 83 136 14 67
101 0.52 0.93 78 139 11 72
102 0.49 0.93 74 140 10 76
103 0.44 0.95 66 142 8 84
104 0.39 0.97 58 146 4 92
105 0.34 0.97 51 146 4 99
106 0.28 0.98 42 147 3 108
107 0.27 0.98 41 147 3 109
108 0.27 0.99 40 148 2 110
109 0.25 0.99 38 148 2 112
110 0.23 0.99 34 148 2 116
111 0.19 0.99 28 148 2 122
(Continued )
TABLE 5
Continued
CMI Score Sn (%) Sp (%) TP TN FP FN
112 0.16 0.99 24 148 2 126
113 0.14 0.99 21 148 2 129
114 0.11 0.99 16 148 2 134
115 0.10 0.99 15 148 2 135
116 0.08 0.99 12 148 2 138
117 0.07 0.99 10 148 2 140
118 0.06 0.99 9 148 2 141
120 0.05 0.99 8 149 1 142
121 0.04 1.00 6 150 0 144
124 0.03 1.00 5 150 0 145
126 0.01 1.00 2 150 0 148
128 0.00 1.00 0 150 0 150
CMI Composite Memory Index; SnSensitivity; Sp
Specicity; TPTrue Positives; TNTrue Negatives; FPFalse
Positives; FNFalse Negatives.
Specicity and sensitivity are reported in decimal form, while TP,
TN, FP, and FN are the number of individuals in the TBI group
(n 150) or control group (n 160) who are correctly or incorrectly
classied.
174 THALER ET AL.
did not have a signicantly smaller AUC. The attention
and verbal factors had signicantly larger AUCs com-
pared with facial memory and abstract nonverbal
factors, but otherwise, factors did not differ from
each other. See Figure 3 for the ROC curves of the six
factors.
DFA indicated that the attention factor correctly
classied 76.0% of the cases, the verbal factor 71.0%
of the cases, the memory for stories factor 70.7% of
the cases, the nonverbal learning factor 67.3% of the
cases, the abstract nonverbal factor 65.0% of the cases,
and the facial memory factor 63.3% of the cases. All
six factors correctly predicted 77.3% of the cases.
DISCUSSION
This study provides additional evidence concerning the
psychometric properties of the TOMAL when used to
evaluate children with TBI by identifying those subtests,
indexes, and factor scores that are most sensitive to
brain damage via ROC analyses. Similar to previous
reports (e.g., Lowther & Mayeld, 2004), the current
TBI sample obtained universally lower scores than the
controls on the TOMAL subtests and indexes. The
DRI had the smallest difference between the two groups,
although the TBI group still scored approximately two
thirds of a standard deviation below the controls on this
index.
ROC analyses of the TOMAL subtests, indexes, and
factors indicated that OR scores were the most sensitive
to TBI, with the greatest AUC and DFA classication
accuracy, although the AUC for OR was not signi-
cantly greater than the four subtests with the next high-
est AUCs. The OR subtests high ROC curve may be
related to its content; when administering this subtest,
examiners show a series of pictures and verbally name
the pictures for the participants and subsequently
prompt the participants to verbally recall the stimuli at
a later time. Therefore, this subtest relies on both visual
and verbal memory processing to complete successfully.
Left and right hippocampal damage is signicantly asso-
ciated with verbal and nonverbal memory decits,
respectively (Ariza et al., 2006), and furthermore, diffuse
axonal injury may result in poor interhemispheric trans-
fer of information in moderate and severe TBI cases
(Fork et al., 2005; Salorio et al., 2005). As our sample
was predominantly classied with moderate and
severe injuries, it is likely that both intrahemispheric
and interhemispheric damage occurred in a majority of
the children, who consequently had memory-processing
difculties in both verbal and nonverbal modalities. The
FIGURE 3 ROC curves of the six factors.
TABLE 6
ROC Analyses for the TOMAL Factor Scores (Factors Ordered from
Greatest to Least AUC)
Index AUC SE 95% CI of Area
AF 0.80 .026 0.750.85
VF 0.78 .027 0.720.83
MFSF 0.77 .027 0.720.82
NLF 0.77 .027 0.710.82
FMF 0.70 .030 0.640.75
ANF 0.71 .030 0.650.77
Contrasts z score SE p
AF vs. VF 0.99 .029 .32
AF vs. MFSF 1.06 .033 .29
AF vs. NLF 1.27 .031 .20
AF vs. FMF 3.05 .036 <.01
AF vs. ANF 3.05 .031 <.01
VF vs. MFSF 0.23 .030 .82
VF vs. NLF 0.35 .031 .72
VF vs. FMF 2.38 .034 .02
VF vs. ANF 2.01 .033 .04
MFSF vs. NLF 0.12 .035 .91
MFSF vs. FMF 2.08 .036 .04
MFSF vs. ANF 1.75 .033 .08
NLF vs. FMF 1.84 .038 .07
NLF vs. ANF 1.68 .032 .09
FMF vs. ANF 0.41 .037 .68
AFAttention Factor; VFVerbal Factor; MFSFMemory for
Stories Factor; NLFNonverbal Learning Factor; FMFFacial
Memory Factor; ANFAbstract Nonverbal Factor.
DIFFERENTIAL SENSITIVITY OF TOMAL 175
concept that tasks that rely on both verbal and visual
processing are the most sensitive to TBI is also sup-
ported by the CMI, which includes both verbal and non-
verbal subtests in a composite score and is the index
with the greatest AUC in our study.
Other sensitive subtests include the MFSD, VSR,
LF, and DF. With the exception of the LF and DF
subtests, these subtests share little in common in con-
tent, method of administration, and type of memory
assessed. The MFSDs high AUC is of interest, as other
delayed subtests of stimuli (WSRD, VSRD, and FMD)
were relatively insensitive to TBI. Lowther and May-
eld (2004) found that the VSRD and FMD subtests
were the only ones for which scores did not signicantly
differ from the controls, and we have found similar nd-
ings in our sample. Perhaps most striking is the separ-
ation between the VSR and VSRD, and the FM and
FMD subtests, as the immediate subtests had relatively
high AUCs (0.78 and 0.75), while the delayed subtests
detected brain injury at a rate only slightly better than
chance. Other studies have found that adults with TBI
performed signicantly lower than controls on a num-
ber of visual learning tasks but not on tasks of delayed
retention as measured by the Shum Visual Learning
Test (Shum, Harris, & OGorman, 2000), while children
with moderate or severe TBI did not signicantly differ
from controls on the WRAML Visual Learning
Delayed subtest yet differed on numerous other subtests
including the Visual Learning Immediate and Verbal
Learning Delayed subtests (Farmer et al., 1999).
Whether or not these ndings are truly indicative of
an immediate=delayed nonverbal difference in TBI
populations requires further and more rigorous
evaluation.
TOMAL index scores also exhibit differential sensi-
tivity to TBI. As previously stated, the CMI stands
out as the most sensitive index and highlights the global
impairments of brain damage on both verbal and non-
verbal memory tasks. The VMI, NMI, and ACI all have
AUCs that did not signicantly differ from each other,
indicating that when verbal, nonverbal, and attention=
concentration tasks are considered separately, they have
comparable sensitivity to brain damage. This is contrary
to our hypothesis that the VMI and ACI would be more
sensitive than the NMI to brain damage. It may be that
the CMI has the largest AUC specically because it is
composed of subtests from these three indexes, thereby
accounting for the heterogeneous cognitive deciencies
that may be present in brain injury. The DRI has an
AUC that was signicantly lower than the CMI and
VMIs AUC, implicating it as the index that correctly
classied the fewest TBI cases. This is a reection of
the relatively insensitive delayed recall subtests, as only
the MFSD subtest had an AUC approaching a good
classication status.
Optimal cutoff index scores were estimated by sum-
ming the sensitivity and specicity percentiles of each
TOMAL index for each available score. From this, we
nd that the CMI has the best classication accuracy
at a score of 83, which is approximately one standard
deviation below the mean. At this score, 94.7% of the
TBI cases were correctly identied, while 55.3% of the
control cases were correctly excluded. The high TP yet
comparatively weak TN rate provides insight on the nat-
ure of neurocognitive proles in pediatric TBI, though it
also establishes that the TOMAL by itself is not suf-
cient to accurately rule out controls. When all parti-
cipants with scores below the ve indexes cutoff
scores were examined, nearly all had a diagnosis of
TBI, though the majority of the TBI cases did not meet
these criteria. This low-sensitivity=high-specicity rate
has been found in other screening tools for brain dam-
age (e.g., Horwitz et al., 2008) and suggests that very
few unimpaired youth would score below the indexes
cutoff scores, although several brain-injured youth
might score above the cutoffs on at least one of the
indexes.
The TOMAL factors have the advantage of repre-
senting purer constructs than the indexes, and indeed,
the rank order of AUC curves agree with the existing
literature on domains most impaired by TBI. Numerous
studies have evidenced that attention is adversely affec-
ted in brain injury (Anderson, Catroppa, Morse,
Haritou, & Rosenfeld, 2005; Catroppa, Anderson,
Morse, Haritou, & Rosenfeld, 2008; Dennis et al.,
2001; Thaler, Allen, Park, McMurray, & Mayeld,
2010; Willmott, Ponsford, Hocking, & Scho nberger,
2009), while the meta-analysis of outcomes in pediatric
TBI has suggested that nonverbal memory is more pre-
served in TBI than verbal memory is (Babikian &
Asarnow, 2009). In our study, the attention factor had
the largest AUC, followed by the two verbal factors
and then the three nonverbal factors. Though the atten-
tion factor and verbal factors did not signicantly differ
in AUC curves, the general trends t with our hypoth-
esis on memory performance. That the index scores
and the factors differed on AUC rank order may be
because the factors represent independent and quantitat-
ively derived constructs directly from the data set while
the indexes were based on theoretical knowledge of
memory and have some overlap with each other; for
example, the Digit Span subtest is shared by both the
VMI and the ACI. For this reason, the ROC analyses
on the index scores may be best viewed from a clinical
perspective in that the CMI may have the most sensi-
tivity to TBI, while the analyses on the factor scores
provide further insight on the cognitive domains most
affected by brain damage.
Although these ndings are promising and provide
insight regarding the TOMALs sensitivity to TBI, some
176 THALER ET AL.
limitations should be addressed. First, most of our sample
sustained moderate-to-severe brain damage, and so subt-
est and index score classication accuracies for mild TBI
cases remain unknown. This is an issue, as recent litera-
ture suggests that mild pediatric cases also exhibit cogni-
tive impairment (Catroppa & Anderson, 2007; Hessen,
Nestvold, & Anderson, 2007). Further, all children were
assessed between 3 and 21 months after injury, and
further longer-term outcomes for our sample were una-
vailable. Finally, the factor structure obtained from
Allen, Leany, and colleagues (2010) may not be generaliz-
able toother samples, althoughthis may not be as muchof
an issue because the factors chiey served to identify dis-
tinct components of attention and verbal and nonverbal
memory abilities. Regardless, the examination of the fac-
tors indicated differential impairment in the constructs
they assessed in directions that agree with previous nd-
ings (e.g., Babikian & Asarnow, 2009). Finally, the cur-
rent sample was one of convenience, and participants
were selected for inclusion in the current study based on
whether or not they had been referred for clinical neurop-
sychological evaluation following TBI.
The current study used ROC analyses to establish the
TOMAL subtests, indexes, and factors that are most
sensitive to brain damage. The overall ndings suggest
that the OR subtest and CMI are the most sensitive, while
delayed tasks of visual memory are the least affected.
When factors were considered independently of index
composition, the attention factor emerged as most affec-
ted by brain injury, followed by verbal memory factors
and nally nonverbal memory factors. A further investi-
gation of the TOMAL-2s (Reynolds & Voress, 2007) sen-
sitivity to brain damage when used for adults is warranted,
given that the TOMAL-2 was standardized to include an
adult sample. Neither the TOMAL nor the TOMAL-2
provide clinical norms for TBI populations, and so the
ndings from this and other studies (Allen, Leany, et al.,
2010; Lowther & Mayeld, 2004) provide the greatest
insight on TOMAL prole performance at this time.
ACKNOWLEDGEMENTS
Normal comparison data were from the TOMAL stan-
dardization sample. Copyright 1994 by PRO-ED,
Austin, TX. Used with permission. All rights reserved.
We thank the TOMAL publisher for allowing access
to the standardization data.
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178 THALER ET AL.
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