Beruflich Dokumente
Kultur Dokumente
Epilepsy Center, Neurological Institute, Cleveland Clinic, 9500 Euclid Avenue, Cleveland, OH 44195, USA
Department of Psychiatry & Psychology, Neurological Institute, Cleveland Clinic, 9500 Euclid Avenue, Cleveland, OH 44195, USA
Department of Psychology, Butler University, 4600 Sunset Avenue, Indianapolis, IN 46208, USA
a r t i c l e
i n f o
Article history:
Received 20 March 2015
Revised 20 April 2015
Accepted 21 April 2015
Available online 28 May 2015
Keywords:
Epilepsy
Reliable change indices
Standardized regression-based change score
norms
Children
Neuropsychology
a b s t r a c t
Reliable change indices (RCIs) and standardized regression-based (SRB) change score norms permit evaluation of
meaningful changes in test scores following treatment interventions, like epilepsy surgery, while accounting for
testretest reliability, practice effects, score uctuations due to error, and relevant clinical and demographic
factors. Although these methods are frequently used to assess cognitive change after epilepsy surgery in adults,
they have not been widely applied to examine cognitive change in children with epilepsy. The goal of the current
study was to develop RCIs and SRB change score norms for use in children with epilepsy. Sixty-three children
with epilepsy (age range: 616; M = 10.19, SD = 2.58) underwent comprehensive neuropsychological evaluations at two time points an average of 12 months apart. Practice effect-adjusted RCIs and SRB change score norms
were calculated for all cognitive measures in the battery. Practice effects were quite variable across the neuropsychological measures, with the greatest differences observed among older children, particularly on the Children's
Memory Scale and Wisconsin Card Sorting Test. There was also notable variability in testretest reliabilities
across measures in the battery, with coefcients ranging from 0.14 to 0.92. Reliable change indices and SRB
change score norms for use in assessing meaningful cognitive change in children following epilepsy surgery
are provided for measures with reliability coefcients above 0.50. This is the rst study to provide RCIs and
SRB change score norms for a comprehensive neuropsychological battery based on a large sample of children
with epilepsy. Tables to aid in evaluating cognitive changes in children who have undergone epilepsy surgery
are provided for clinical use. An Excel sheet to perform all relevant calculations is also available to interested
clinicians or researchers.
2015 Elsevier Inc. All rights reserved.
1. Introduction
Neuropsychological assessment is an essential component of epilepsy
surgery programs. These evaluations help determine the cognitive risks
associated with epilepsy surgery and assess postsurgical neurobehavioral
outcomes. Change in cognitive abilities across time or in response to interventions has historically been evaluated by 1) examining differences in
cognitive outcome between groups of patients or 2) comparing change
scores in individual patients to some predetermined, yet often arbitrary,
difference believed to reect actual change based on conventional practice (e.g., 10 or 15 standard score points). These procedures for assessing
change are confounded by methodological artifacts (e.g., imperfect test-
Corresponding author at: Cleveland Clinic Epilepsy Center, 9500 Euclid Avenue, P57,
Cleveland, OH 44195, USA. Tel.: +1 216 444 2354; fax: +1 216 444 4525.
E-mail addresses: buschr@ccf.org (R.M. Busch), tlinewea@butler.edu
(T.T. Lineweaver), fergusl3@ccf.org (L. Ferguson), hautj@ccf.org (J.S. Haut).
http://dx.doi.org/10.1016/j.yebeh.2015.04.052
1525-5050/ 2015 Elsevier Inc. All rights reserved.
retest reliability, measurement error, practice effects, and regression toward the mean) that are likely to lead to erroneous conclusions regarding
cognitive outcome.
Beginning in the 1990s, two methods for assessing postsurgical cognitive change while controlling these confounding factors emerged in
the adult epilepsy literature: reliable change indices (RCIs) and standardized regression-based (SRB) change score norms [13]. These
methods have been developed for a wide range of cognitive measures
and are now routinely applied to assess cognitive outcome in adults following epilepsy surgery [14]. Despite the clear benets, RCIs and SRB
change score norms have not been developed to examine cognitive
change in children after epilepsy surgery across a wide range of cognitive measures.
Our prospective, longitudinal study was designed to address this gap
in the literature. Specically, this study provides RCIs and SRB change
score norms for children with epilepsy across a comprehensive neuropsychological battery using the same methods employed by Martin
and colleagues [4] for adults with epilepsy. These data allow clinicians
46
2.2. Measures
Participants completed a comprehensive neuropsychological evaluation that included measures of intelligence, memory, language,
visuospatial skills, executive functioning, and academic achievement.
The following instruments were administered on two separate occasions: Wechsler Intelligence Scale for Children Fourth Edition [5],
Children's Memory Scale [6], Expressive One-Word Picture Vocabulary
Test Revised [7], BeeryBuktenica Developmental Test of Visual
Motor Integration Fourth Edition [8], Test of VisualPerceptual Skills
Third Edition [9] (Visual Discrimination, Visual Memory, and Spatial
Relationships subtests), Wisconsin Card Sorting Test [10], DelisKaplan
Executive Function System [11] (Trail Making Test, Verbal Fluency Test,
and Tower Test), and the WoodcockJohnson III Tests of Achievement
[12] (LetterWord Identication, Reading Fluency, Calculation, Math
Fluency, Spelling, Writing Fluency, Passage Comprehension, Applied
Problems, Writing Samples, Word Attack, and Punctuation and Capitalization subtests). All measures were administered according to standardized instructions provided in the respective test manuals and
scored using age-adjusted norms.
Table 1
Demographic and seizure data for study patients.
Variable
Age (years)
Education (years)
Full Scale IQ (standard score)
Age at seizure onset (years)
Duration of epilepsy (years)
Intertest interval (months)
Sex
Male
Female
Race
Caucasian
African-American
Other
Handedness
Left
Right
Ambidextrous
Type of seizures
Generalized
Focal
Seizure focus
Temporal
Frontal
Parietal
Occipital
Multilobar
Younger group
Ages 610
n = 36
Older group
Ages 1116
n = 27
M (SD)
M (SD)
8.36 (1.38)
2.69 (1.31)
86.61 (17.27)
5.24 (2.24)
3.12 (2.13)
13.03 (8.47)
17 (47.2%)
19 (52.8%)
32 (88.9%)
2 (5.6%)
2 (5.6%)
6 (16.7%)
29 (80.6%)
1 (2.8%)
16 (44.4%)
20 (55.6%; 9 left,
11 right)
4
4
2
1
9
12.63 (1.60)
7.00 (1.66)
83.67 (16.06)
8.26 (3.18)
4.48 (3.03)
10.93 (2.97)
10 (37.0%)
17 (63.0%)
21 (77.8%)
3 (11.1%)
3 (11.1%)
4 (14.8%)
23 (85.2%)
0 (0%)
13 (48.1%)
14 (51.9%; 10 left,
4 right)
5
2
0
1
6
2.3. Analyses
2.3.1. Reliable change indices
Practice effect-adjusted RCI cutoff scores were calculated for each of
the neuropsychological measures in the test battery according to
the methods outlined by Jacobson and Truax [13]. First, testretest
reliability coefcients were computed for each of the neuropsychological measures. Then RCIs were developed for the two separate age
ranges (i.e., 610 and 1116). The standard error of measurement
(SEM) was used to calculate the standard error of the difference (SEdiff),
where SEdiff = 2(SEM)2. As noted by Jacobson and Truax [13], the SEdiff
describes the spread of the distribution of change scores that would be
expected if no actual change had occurred (p. 14), that is, based solely
on chance uctuations in test scores across time. Next, condence intervals were established at 80% and 90% by multiplying the SEdiff by 1.28
and 1.64, respectively. This provided two different distribution ranges
of change scores, with the 90% condence interval offering a more conservative estimate of testretest change and the 80% condence interval, a more liberal estimate. The resulting cutoff score ranges were
then adjusted for practice effects [3,14]. Average practice effects were
determined by calculating the mean change (i.e., Time 2 mean minus
Time 1 mean) for each cognitive measure. Finally, these practice effects
were added to the condence interval in order to center the range of
cutoff scores around the average testretest practice effect. Score changes outside of these condence intervals are considered uncommon in
children with epilepsy who have not undergone surgery during the
testretest interval since they occur in less than 80% (80% CI) of these
children or 90% (90% CI) of these children in the absence of surgical
intervention.
47
Table 2
Testretest means, SD, mean difference scores, and testretest reliability.
Index/subtest
Younger group
Older group
Time 1 mean
(SD)
Time 2 mean
(SD)
Mean
change
Intelligence
Wechsler Intelligence Scale for Children Fourth Edition
Full Scale IQ
Verbal Comprehension Index
Perceptual Reasoning Index
Working Memory Index
Processing Speed Index
Similarities
Vocabulary
Comprehension
Word Reasoning
Block Design
Picture Concepts
Matrix Reasoning
Digit Span
LetterNumber Sequencing
Coding
Symbol Search
Cancellation
86.94 (17.40)
92.06 (16.06)
90.89 (14.55)
85.23 (17.71)
89.37 (16.02)
9.29 (3.39)
8.21 (3.07)
8.06 (2.98)
9.19 (3.30)
8.18 (2.96)
8.94 (3.42)
8.26 (2.85)
7.68 (3.52)
6.76 (3.55)
7.15 (3.12)
8.75 (3.79)
10.25 (2.72)
86.71 (16.84)
91.00 (15.91)
93.57 (17.08)
82.31 (14.37)
87.91 (16.02)
9.29 (3.13)
8.18 (3.40)
8.09 (2.80)
9.00 (3.44)
9.18 (3.14)
9.44 (3.17)
8.18 (3.57)
7.71 (3.18)
6.09 (3.22)
7.09 (3.03)
8.41 (3.29)
10.03 (2.78)
0.23
1.06
2.68
2.92
1.46
0.00
0.03
0.03
0.19
1.00
0.50
0.08
0.03
0.67
0.06
0.34
0.22
Memory
Children's Memory Scale
Visual Immediate
Visual Delayed
Verbal Immediate
Verbal Delayed
General Memory
Attention/Concentration
Learning
Delayed Recognition
Dot Locations Learning
Dot Locations Total Score
Dot Locations Short Delay
Dot Locations Long Delay
Stories Immediate
Stories Delayed
Stories Delayed Recognition
Faces Immediate
Faces Delayed
Word Pairs Immediate
Word Pairs Learning
Word Pairs Total Score
Word Pairs Long Delay
Word Pairs Delayed Recognition
Numbers Total Score
Sequences Total Score
Family Pictures Immediate
Family Pictures Delayed
Word List Learning
Word List Delayed
Word List Delayed Recognition
91.45 (13.45)
89.53 (13.61)
87.67 (23.07)
82.50 (22.40)
85.31 (22.45)
91.86 (21.66)
89.55 (18.12)
91.25 (21.42)
9.18 (2.89)
9.48 (2.92)
10.00 (3.10)
9.41 (3.00)
8.88 (3.70)
8.34 (4.24)
9.12 (3.78)
7.73 (2.96)
7.19 (2.76)
7.52 (3.65)
7.42 (4.48)
7.12 (4.20)
5.97 (3.85)
8.06 (4.09)
8.53 (3.84)
8.45 (3.80)
9.57 (3.09)
9.28 (3.25)
7.75 (5.37)
6.67 (3.53)
7.74 (3.81)
93.24 (14.92)
97.00 (15.00)
89.82 (25.96)
88.38 (22.97)
89.47 (23.66)
89.00 (20.70)
91.45 (19.00)
87.00 (19.26)
9.18 (3.32)
9.70 (3.39)
10.48 (2.82)
10.78 (2.57)
8.79 (4.34)
8.56 (4.33)
7.81 (2.79)
8.12 (2.74)
8.25 (3.40)
8.64 (4.15)
8.06 (4.51)
7.91 (4.73)
7.66 (3.79)
8.28 (4.18)
7.87 (3.30)
8.23 (3.79)
9.73 (3.03)
9.21 (3.06)
6.96 (3.93)
6.74 (3.46)
5.89 (3.25)
Language
Expressive One-Word Picture Vocabulary Test Revised
96.59 (17.49)
Visuospatial
Test of VisualPerceptual Skills Third Edition
Visual Discrimination
Visual Memory
Spatial Relationships
BeeryBuktenica Developmental Test of VisualMotor
Integration Fourth Edition
Executive functioning
Wisconsin Card Sorting Test
Categories completed
Total errors
Perseverative responses
DelisKaplan Executive Function System
Tower Test
Total achievement
Move accuracy ratio
Rule violations/item ratio
Time 1 mean
(SD)
Time 2 mean
(SD)
Mean
change
Testretest
reliability
83.67 (16.06)
90.52 (17.80)
87.11 (14.72)
85.70 (20.03)
83.78 (14.46)
8.63 (2.95)
8.52 (3.82)
7.78 (3.12)
8.92 (3.35)
6.89 (2.47)
9.04 (3.24)
7.78 (2.85)
7.96 (3.76)
7.19 (4.19)
6.81 (3.18)
6.93 (3.09)
8.88 (2.79)
84.56 (14.86)
88.63 (13.83)
88.67 (13.73)
88.41 (19.28)
84.22 (12.46)
8.26 (2.44)
8.41 (3.19)
7.56 (2.68)
9.08 (3.43)
7.78 (2.90)
8.22 (3.07)
8.44 (2.49)
8.56 (3.94)
7.48 (3.98)
6.81 (2.79)
7.59 (2.72)
9.24 (3.14)
0.89
1.89
1.56
2.71
0.44
0.37
0.11
0.22
0.16
0.89
0.82
0.66
0.60
0.29
0.00
0.66
0.36
0.92
0.88
0.78
0.80
0.76
0.82
0.87
0.71
0.78
0.79
0.54
0.51
0.73
0.69
0.76
0.61
0.73
100.15 (14.08)
98.56 (15.43)
94.07 (22.59)
95.85 (21.28)
96.54 (22.37)
89.76 (18.73)
94.52 (17.97)
93.22 (18.39)
9.58 (2.89)
10.04 (2.65)
10.08 (2.66)
9.70 (3.04)
9.93 (4.09)
9.52 (4.20)
8.92 (3.76)
10.00 (3.14)
9.85 (3.39)
7.60 (3.65)
8.31 (4.01)
8.19 (3.98)
9.11 (3.69)
8.73 (3.54)
7.60 (3.70)
9.04 (3.12)
10.21 (2.75)
9.88 (3.42)
6.77 (3.28)
6.82 (3.62)
7.23 (3.69)
9.85
11.41
5.66
8.07
12.62
0.39
1.06
1.12
0.64
0.79
1.69
0.22
0.66
0.22
0.16
0.07
0.79
0.07
1.85
90.30 (12.97)
87.15 (13.84)
88.41 (22.29)
87.78 (22.30)
83.92 (21.08)
90.40 (16.80)
86.52 (13.88)
89.26 (22.91)
7.92 (2.48)
8.33 (2.63)
8.88 (2.73)
8.56 (2.79)
8.56 (3.81)
8.11 (4.42)
7.92 (4.44)
8.48 (3.09)
7.26 (3.35)
8.32 (3.68)
7.46 (4.09)
7.67 (4.09)
7.93 (3.75)
8.27 (4.14)
7.88 (3.18)
8.92 (2.97)
9.21 (3.18)
9.50 (3.40)
6.14 (2.88)
6.41 (3.33)
6.68 (3.21)
0.72
0.85
0.52
1.18
0.46
0.28
0.12
1.00
0.38
0.63
0.41
0.55
0.53
0.54
0.90
0.83
0.85
0.89
0.69
0.66
0.19
0.21
0.15
0.17
0.82
0.83
0.60
0.52
0.56
0.71
0.82
0.82
0.60
0.68
0.79
0.84
0.52
0.57
0.62
0.57
0.44
97.06 (16.50)
0.47
93.68 (16.08)
94.48 (19.41)
0.80
0.86
7.33 (3.08)
7.07 (4.12)
9.52 (4.42)
89.77 (10.01)
6.89 (2.81)
7.48 (3.27)
9.81 (4.29)
88.20 (11.18)
0.44
0.41
0.29
1.57
5.82 (3.03)
4.77 (3.44)
8.14 (3.31)
85.11 (12.36)
6.50 (3.22)
6.45 (3.08)
7.77 (3.89)
84.96 (14.28)
0.68
1.68
0.37
0.15
0.48
0.16
0.45
0.70
3.75 (1.62)
89.92 (13.10)
93.08 (14.35)
4.79 (1.53)
95.71 (15.23)
98.50 (13.51)
1.04
5.79
5.42
3.80 (1.83)
85.91 (12.00)
87.22 (14.81)
4.60 (1.63)
94.00 (17.21)
97.04 (18.06)
0.80
8.09
9.82
0.32
0.48
0.50
9.24 (2.20)
8.47 (3.56)
8.06 (3.03)
10.71 (2.20)
9.53 (2.27)
10.41 (1.18)
1.47
1.06
2.35
7.45 (3.24)
9.05 (2.70)
8.65 (2.21)
9.90 (3.63)
9.60 (2.39)
10.10 (1.07)
2.45
0.55
1.45
0.67
0.66
0.42
1.79
7.47
2.15
5.88
4.16
2.86
1.90
4.25
0.00
0.22
0.48
1.37
0.09
0.22
1.31
0.64
8.00
3.96
1.66
1.71
1.20
1.14
1.37
1.41
1.00
1.52
2.59
48
Table 2 (continued)
Index/subtest
Executive functioning
Delis-Kaplan Executive Function System
Verbal Fluency Test
Letter uency
Category uency
Category switching total correct
Category switching accuracy
Set-loss errors
Repetition errors
Trail Making Test
Visual scanning
Number sequencing
Letter sequencing
Numberletter switching
Motor speed
Total errors
Academic achievement
WoodcockJohnson III Tests of Achievement
Broad Reading
Broad Math
Broad Written Language
Academic Fluency
LetterWord Identication
Reading Fluency
Calculation
Math Fluency
Spelling
Writing Fluency
Passage Comprehension
Applied Problems
Writing Samples
Word Attack
Punctuation and Capitalization
Younger group
Older group
Time 1 mean
(SD)
Time 2 mean
(SD)
Mean
change
Time 1 mean
(SD)
Time 2 mean
(SD)
8.67 (2.93)
10.11 (3.23)
10.00 (3.18)
10.11 (3.16)
9.78 (2.88)
7.28 (2.05)
8.39 (3.40)
9.94 (3.62)
9.44 (3.05)
9.83 (2.31)
11.00 (1.94)
6.89 (2.25)
0.28
0.17
0.56
0.28
1.22
0.39
7.77 (2.84)
8.86 (3.71)
8.82 (2.94)
8.86 (2.59)
10.45 (2.04)
7.32 (2.68)
8.82 (3.38)
9.23 (3.70)
9.14 (3.06)
9.56 (2.58)
11.45 (1.74)
7.64 (2.01)
10.33 (2.64)
7.94 (3.57)
7.78 (4.01)
7.06 (4.33)
10.00 (2.03)
8.56 (4.32)
10.11 (3.23)
9.56 (3.45)
8.28 (4.10)
8.00 (4.56)
10.00 (2.57)
10.12 (2.28)
0.22
1.62
0.50
0.94
0.00
1.56
9.77 (2.53)
8.50 (2.96)
8.41 (3.38)
6.86 (4.28)
8.45 (3.16)
8.95 (3.63)
10.50 (2.41)
8.59 (2.67)
8.14 (4.04)
7.64 (3.53)
8.91 (2.93)
10.50 (1.44)
98.83 (21.65)
94.58 (15.53)
97.65 (21.13)
94.36 (20.79)
99.00 (18.44)
97.96 (22.48)
94.25 (16.11)
85.32 (16.59)
96.41 (20.96)
96.38 (19.80)
94.59 (17.28)
95.31 (17.27)
96.88 (15.99)
98.26 (15.61)
87.58 (19.43)
97.04 (19.70)
95.42 (15.19)
97.00 (18.61)
95.16 (20.72)
95.00 (18.19)
98.36 (23.41)
95.71 (13.17)
85.92 (19.53)
96.37 (19.17)
94.62 (18.38)
91.59 (15.45)
95.85 (17.16)
98.96 (16.19)
96.22 (13.49)
84.31 (22.32)
1.79
0.84
0.65
0.80
4.00
0.40
1.46
0.60
0.04
1.76
3.00
0.54
2.08
2.04
3.27
92.76 (15.68)
93.30 (17.60)
99.74 (14.10)
91.92 (16.26)
95.15 (13.52)
93.46 (15.98)
93.56 (17.88)
89.96 (17.93)
102.36 (14.36)
94.84 (15.17)
90.42 (13.59)
93.80 (15.15)
93.84 (14.85)
98.12 (10.21)
85.26 (21.11)
95.84 (17.51)
89.78 (14.96)
100.26 (14.07)
95.12 (17.60)
95.96 (11.17)
97.96 (19.71)
87.96 (16.07)
91.00 (17.30)
102.72 (15.33)
95.32 (13.37)
90.19 (12.59)
91.40 (12.46)
93.92 (15.49)
95.85 (7.58)
88.87 (19.18)
Mean
change
1.05
0.37
0.32
0.70
1.00
0.32
Testretest
reliability
0.74
0.63
0.51
0.53
0.30
0.14
0.73
0.09
0.27
0.78
0.46
1.55
0.48
0.17
0.68
0.73
0.43
0.46
3.08
3.52
0.52
3.20
0.81
4.50
5.60
0.95
0.87
0.91
0.90
0.91
0.90
0.74
0.85
0.92
0.79
0.88
0.83
0.69
0.85
0.71
1.04
0.36
0.48
0.23
2.40
0.08
2.27
3.61
p b 0.01.
p b 0.05.
49
Table 3
Adjusted reliable change indices (80% and 90% condence intervals).
Index/subtest
Younger group
Practice
Older group
Adjusted RC
80%
Adjusted RC
90%
Practice
Adjusted RC
80%
Adjusted RC
90%
Intelligence
Wechsler Intelligence Scale for Children Fourth Edition
Full Scale IQ
Verbal Comprehension Index
Perceptual Reasoning Index
Working Memory Index
Processing Speed Index
Similarities
Vocabulary
Comprehension
Word Reasoning
Block Design
Picture Concepts
Matrix Reasoning
Digit Span
LetterNumber Sequencing
Coding
Symbol Search
Cancellation
0
1
3
3
1
0
0
0
0
1
1
0
0
1
0
0
0
9, 9
11, 9
10, 15
17, 11
16, 13
3, 3
2, 2
3, 3
3, 3
1, 3
4, 5
4, 4
3, 3
4, 3
3, 3
5, 4
3, 2
12, 11
14, 12
13, 18
21, 15
20, 17
3, 3
3, 3
4, 4
4, 3
2, 4
5, 6
5, 5
4, 4
5, 4
4, 3
6, 5
3, 3
1
2
2
3
0
0
0
0
0
1
1
1
1
0
0
1
0
8, 9
13, 9
11, 14
13, 19
12, 13
3, 2
3, 2
3, 3
3, 3
1, 3
5, 3
3, 4
3, 4
4, 5
3, 3
3, 4
2, 3
10, 12
16, 12
14, 17
18, 23
16, 17
3, 3
3, 3
4, 4
3, 4
2, 3
6, 4
4, 5
4, 5
5, 6
4, 4
4, 5
3, 4
Memory
Children's Memory Scale
Visual Immediate
Visual Delayed
Verbal Immediate
Verbal Delayed
General Memory
Attention/Concentration
Learning
Delayed Recognition
Stories Immediate
Stories Delayed
Stories Delayed Recognition
Faces Immediate
Faces Delayed
Word Pairs Immediate
Word Pairs Learning
Word Pairs Total Score
Word Pairs Long Delay
Word Pairs Delayed Recognition
Numbers Total Score
Sequences Total Score
Family Pictures Immediate
Family Pictures Delayed
Word List Learning
Word List Delayed
2
7
2
6
4
3
2
4
0
0
1
0
1
1
1
1
2
0
1
0
0
0
1
0
15, 19
9, 24
11, 16
11, 23
12, 20
16, 10
16, 20
27, 18
3, 3
3, 3
6, 3
3, 4
2, 4
2, 5
3, 4
2, 4
3, 6
4, 4
4, 3
3, 3
4, 4
4, 4
7, 5
4, 4
20, 23
14, 29
15, 19
16, 28
16, 24
20, 14
22, 25
33, 25
4, 4
4, 4
7, 4
4, 5
3, 5
3, 6
4, 5
3, 5
4, 7
5, 6
5, 3
4, 3
5, 5
5, 5
8, 7
5, 5
10
11
6
8
13
1
8
4
1
1
1
2
3
1
1
1
1
0
0
0
1
0
1
0
6, 26
6, 28
7, 19
9, 25
2, 27
11, 9
6, 22
20, 28
2, 4
2, 5
4, 6
2, 5
1, 7
4, 3
2, 4
3, 4
3, 5
4, 5
3, 2
2, 2
3, 5
4, 4
3, 4
4, 4
11, 31
10, 33
11, 22
14, 30
6, 32
14, 12
10, 26
27, 35
2, 5
3, 6
6, 8
3, 7
3, 8
5, 4
3, 5
4, 5
4, 7
5, 6
4, 3
3, 3
4, 6
5, 6
4, 5
5, 6
11, 12
15, 16
10, 12
13, 15
12, 8
14, 11
13, 12
16, 16
13, 24
18, 29
10
9, 29
14, 34
0
1
4, 5
3, 5
5, 6
4, 6
0
1
4, 3
3, 5
5, 4
4, 6
0
0
1
0
3, 2
4, 3
5, 3
4, 4
4, 3
5, 4
6, 5
5, 5
1
0
0
1
2, 4
4, 4
3, 4
3, 4
2, 4
5, 6
4, 5
3, 5
1
1
1, 4
3, 5
1, 4
4, 6
2
1
1, 6
2, 3
2, 7
3, 4
10, 7
9, 11
13, 9
12, 14
3
4
3, 9
15, 8
5, 11
18, 11
Language
Expressive One-Word Picture Vocabulary Test Revised
Visuospatial
BeeryBuktenica Developmental Test of VisualMotor Integration Fourth Edition
Executive functioning
Wisconsin Card Sorting Test
Perseverative responses
DelisKaplan Executive Function System
Trail Making Test
Letter sequencing
Numberletter switching
Verbal Fluency Test
Letter uency
Category uency
Category switching total correct
Category switching accuracy
Tower Test
Total achievement
Move accuracy ratio
Academic achievement
WoodcockJohnson III Tests of Achievement
Broad Reading
Broad Math
2
1
50
Table 3 (continued)
Index/subtest
Younger group
Practice
Academic achievement
WoodcockJohnson III Tests of Achievement
Broad Written Language
Academic Fluency
LetterWord Identication
Reading Fluency
Calculation
Math Fluency
Spelling
Writing Fluency
Passage Comprehension
Applied Problems
Writing Samples
Word Attack
Punctuation and Capitalization
1
1
4
0
1
1
0
2
3
1
2
2
3
Older group
Adjusted RC
80%
Adjusted RC
90%
Practice
Adjusted RC
80%
Adjusted RC
90%
12, 11
11, 13
14, 6
12, 13
13, 16
11, 12
11, 10
18, 15
14, 8
13, 14
14, 18
13, 9
22, 16
16, 14
14, 16
17, 9
16, 17
17, 20
14, 16
14, 13
23, 19
17, 11
16, 17
19, 23
16, 12
28, 21
1
3
1
5
6
1
0
0
0
2
0
2
4
7, 8
6, 12
7, 8
5, 14
22, 11
12, 14
7, 8
12, 13
9, 8
14, 9
15, 15
9, 5
17, 24
9, 10
9, 15
9, 10
7, 16
27, 15
15, 17
9, 10
16, 17
11, 11
17, 12
19, 19
12, 7
23, 30
RC = reliable change. Results are only reported for cognitive measures with testretest reliabilities above .50. When interpreting an individual patient's pattern of scores, testretest differences falling at or below the lower limit of the RC interval or at or above the upper limit of the RC interval would be indicative of clinically meaningful change.
51
Table 4
Regression equations for neuropsychological measures.
Domain/measure
SEest
Intelligence
Wechsler Intelligence Scale for Children Fourth Edition
Full Scale IQ
Verbal Comprehension Index
Perceptual Reasoning Index
Working Memory Index
Processing Speed Index
Processing Speed Index w/ modier (4%)
Similarities
Vocabulary
Comprehension
Word Reading
Block Design
Picture Concepts
Picture Concepts w/ modier (5%)
Matrix Reasoning
Digit Span
LetterNumber Sequencing
Coding
Symbol Search
Symbol Search w/ modier (5%)
Cancellation
.916
.873
.790
.813
.769
.797
.826
.869
.687
.788
.788
.536
.581
.534
.730
.695
.754
.649
.687
.705
6.537
7.402
9.916
10.035
9.531
9.087
1.627
1.669
1.973
2.125
1.906
2.681
2.608
2.716
2.538
2.559
1.904
2.367
2.285
2.075
12.299
18.519
15.837
23.765
21.854
28.281
2.224
1.167
3.060
1.715
1.997
4.393
7.261
3.580
2.500
2.491
2.049
3.504
4.853
2.628
.858
.781
.847
.723
.737
.731
.727
.852
.613
.804
.858
.501
.490
.589
.720
.623
.693
.565
.559
.733
Memory
Children's Memory Scale
Visual Immediate
Visual Immediate w/ modier (7%)
Visual Delayed
Verbal Immediate
Verbal Delayed
General Memory
General Memory w/ modier (2%)
Attention/Concentration
Learning
Delayed Recognition
Stories Immediate
Stories Delayed
Stories Delayed Recognition
Stories Delayed Recognition w/ modier (6%)
Faces Immediate
Faces Delayed
Word Pairs Immediate
Word Pairs Immediate w/ modier (8%)
Word Pairs Learning
Word Pairs Total Score
Word Pairs Long Delay
Word Pairs Delayed Recognition
Numbers Total Score
Sequences Total Score
Family Pictures Immediate
Family Pictures Delayed
Word List Learning
Word List Delayed
.525
.585
.569
.897
.822
.854
.867
.900
.699
.685
.823
.843
.535
.590
.432
.501
.687
.743
.828
.821
.607
.701
.794
.851
.527
.591
.594
.553
12.238
11.770
12.400
10.673
12.764
11.875
11.501
8.752
13.147
13.663
2.385
2.261
2.786
2.689
2.430
2.837
2.877
2.676
2.404
2.512
3.074
2.753
2.147
1.887
2.485
2.581
2.879
2.929
45.132
31.308
42.511
8.967
23.078
17.395
4.532
8.223
25.044
38.397
1.344
2.318
4.585
1.055
5.798
4.985
2.317
6.407
2.106
1.700
4.222
3.373
1.448
1.354
5.475
4.337
3.521
2.988
.566
.559
.628
.943
.806
.891
.888
.896
.773
.586
.913
.802
.447
.480
.398
.557
.733
.761
.825
.866
.594
.652
.769
.856
.481
.560
.468
.577
Language
Expressive One-Word Picture Vocabulary Test Revised
.851
9.316
11.825
.885
Visuospatial
BeeryBuktenica Developmental Test of VisualMotor Integration Fourth Edition
.701
9.419
17.028
.789
.487
14.170
52.027
.516
.669
.812
.661
2.279
1.846
1.784
4.564
1.160
5.307
.678
.797
.488
.748
.640
.474
.451
2.258
2.664
2.495
1.958
1.578
3.239
5.311
6.568
.874
.703
.435
.348
Executive functioning
Wisconsin Card Sorting Test
Perseverative responses
DelisKaplan Executive Functioning System
Tower Test
Total achievement
Total achievement w/ modier (9% and 12%)
Move accuracy ratio
Verbal Fluency Test
Letter uency
Category uency
Category switching total correct
Category switching accuracy
Bbaseline
Bage
Bonset
Btestinterval
.493
.270
.107
1.404
1.266
.314
.419
.304
.228
52
Table 4 (continued)
Domain/measure
Executive functioning
DelisKaplan Executive Functioning System
Trail Making Test
Letter sequencing
Numberletter switching
Academic achievement
WoodcockJohnson III Tests of Achievement
Broad Reading
Broad Reading w/ modier (1%)
Broad Math
Broad Math w/ modier (3%)
Broad Written Language
Academic Fluency
LetterWord Identication
Reading Fluency
Calculation
Calculation w/ modier (4.1%)
Math Fluency
Spelling
Writing Fluency
Passage Comprehension
Applied Problems
Writing Samples
Word Attack
Punctuation and Capitalization
SEest
Bbaseline
.618
.761
3.061
2.630
2.559
2.816
.695
.746
.953
.957
.864
.880
.912
.899
.904
.903
.733
.761
.840
.923
.798
.873
.830
.706
.854
.713
5.807
5.600
7.907
7.551
7.122
8.639
6.588
.811
10.313
9.962
10.266
7.042
9.940
6.993
.681
11.163
5.924
14.938
7.742
.981
16.242
27.636
15.850
9.308
14.424
3.366
30.876
44.585
8.552
11.014
24.469
17.549
18.958
29.876
26.723
23.861
.927
.945
.818
.807
.840
.923
.835
.993
.652
.639
.912
.889
.738
.791
.793
.708
.707
.725
Bage
Bonset
Btestinterval
.656
.998
1.183
Results are only reported for cognitive measures with testretest reliabilities above .50. Numbers in parentheses after equations with modiers represent the percent of variance accounted
for by that particular modier. R = reliability coefcient, SEest = standard error of the estimate, C = constant, Bbaseline = unstandardized beta (slope) for baseline test score, Bage = age at
baseline testing, Bonset = age at recurrent seizure onset, and Btestinterval = interval between baseline testing and repeat testing measured in months.
for regression to the mean or other potential modiers and, in the case
of our study, are based on smaller samples than the SRB change score
norms because they were calculated for two separate age groups.
While SRB change score norm methodology is more complicated to
use, it corrects for multiple confounding factors that RCIs do not. Statistically, SRB change score norms correct for practice effects by using an
individual's baseline score as a predictor of postoperative performance.
This provides more accurate adjustment of practice effects than RCIs because practice effects can be estimated differently at different levels of
baseline performance. Standardized regression-based change score
norms also allow for correction of demographic- and disease-related
variables that could potentially impact cognitive performance over
time. Finally, SRB change score norms convert changes in test scores
to a common metric (i.e., z-scores), permitting direct comparison of
cognitive change across a wide range of neuropsychological measures.
Studies that have compared RCI and SRB change score norm methodologies head-to-head suggest that predictive accuracy is similar for both
measures [15,16]. This has led many clinicians to utilize the easily
employed RCI cutoffs rather than calculating SRB change score norms
for individual patients. Nevertheless, we have created a Microsoft Excel
calculator that calculates SRB change score norms to facilitate the interpretation of cognitive change in individual patients for clinicians and
Table 5
Select neuropsychological test results for case example.
Cognitive measure
Preop
Postop
Change score
RCI cutoffs
81
98
103
79
98
94
2
0
9
16, 12
14, 17
16, 17
82
99
98
0.38
0.84
0.40
94
109
70
67
77
112
70
91
17
+3
0
+24
14, 30
10, 33
13, 15
16, 16
99
111
74
70
1.72
0.08
0.41
2.24
a
z-Scores exceeding 1.28 are signicant with an 80% condence interval, and those exceeding 1.64 are signicant with a 90% condence interval. Change values in bold indicate
those that demonstrate clinically meaningful change using RCIs or SRB change score norms.
53
Fig. 1. Plot of the z-scores demonstrating magnitude of postoperative cognitive change on each of the cognitive measures for the child in the case example. Note that bars exceeding the red
lines (z 1.28 for 80% CI or z 1.64 for 90% CI) reect those postoperative measures for which the change scores reect signicant and meaningful cognitive change.
surgical delays or other factors, most of the patients in our control group
had a conrmed diagnosis of epilepsy for at least one year but were not
surgical candidates. Second, our study did not include any children
under the age of 6. Therefore, our results should not be applied to younger children. Only children aged 6 to 16 were included primarily to enable the use of the same neuropsychological battery with ageappropriate normative data for all children. The neuropsychological
measures for children younger than 6 and older than 16 are different
and use different normative groups. Third, to control for age-specic differences in test items and developmental factors, we stratied patients
into younger (ages 610) and older (ages 1116) age groups before developing the RCIs. This resulted in reduced sample sizes (n = 36 and 27,
respectively) for the RCI calculations compared to SRB change score
norm calculations (n = 63) with relatively small numbers of patients
with different seizure foci. Finally, despite attempts to have a rather
consistent 9-month testretest interval for all children, there was
some variability in the length between baseline neuropsychological
testing and repeat neuropsychological testing because of limited availability of the families to return for testing and/or other scheduling limitations. While not ideal, this is likely to reect clinical practice as test
retest intervals often vary among our surgical patients as well. Further,
the vast majority of patients (80%) in our sample completed both assessments within a 5- to 12-month interval.
5. Conclusions
The establishment of RCIs and SRB change score norms for use in
evaluating cognitive change in children with epilepsy is an important
step toward improving their care. These methods allow clinicians to
more accurately assess cognitive change after surgery or to evaluate
other treatment interventions while taking into account the effects of
epilepsy on the developing brain. These methodologies also permit researchers to compare cognitive outcomes across studies in order to further our understanding of the true cognitive changes associated with
epilepsy surgery in children. Finally, use of these methodologies can aid
54
clinicians in advising parents and physicians about the potential cognitive outcomes of epilepsy surgery on an individual level and may result
in more targeted and relevant cognitive and school interventions for
children with epilepsy regardless of whether or not they undergo
surgery.
Acknowledgments
This project was supported by the Epilepsy Foundation through the
Partnership for Pediatric Epilepsy Research (award ID 189351 and
122693) and the Targeted Research Initiative for Youth (award ID
246507) (to J.S.H. and R.M.B.).
Additional support for this research was provided by the Cleveland
Clinic Epilepsy Center and the Clinical and Translational Science
Collaborative of Cleveland (KL2TR000440) from the National Center
for Advancing Translational Sciences (NCATS) component of the
National Institutes of Health and NIH roadmap for Medical Research
(to R.M.B.). The contents are solely the responsibility of the authors
and do not necessarily represent the ofcial views of the NIH.
Conict of interest
None of the authors has any conicts of interest to disclose.
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