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Verbal and Nonverbal Skill Discrepancies in Hydrocephalic Children
Verbal and Nonverbal Skill Discrepancies in Hydrocephalic Children
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Journal of Clinical and Experimental NeuropsycholOgy 016&8634/92/1404-0593%3.00
1992,Vol. 14, NO.4, pp. 593-609 Q Swets & Zeitlinger
Jack M. Fletcher
Department of Pediatrics, University of Texas Medical School at Houston
David J. Francis
University of Houston
Downloaded by [Carnegie Mellon University] at 11:42 13 January 2015
Nora M. Thompson
Southwest Neuropsychiatric Institute
Kevin C. Davidson
University of Houston
Michael E. Miner
Division of Neurosurgery, Ohio State University
ABSTRACT
This study evaluated a large sample (N = 90) of 5- to 7-year-old children with hy-
drocephalus caused by aqueductal stenosis or prematurity-intravenmcdar hemorrhage
or associated with spina bifida. Comparison groups of normal controls, children
with spina bifida and no shunt, and premature children with no hydrocephalus were
also evaluated. Comparison of skill discrepancies at two occasions separated by 1
year revealed that hydrocephalic children, as a group, showed poorer nonverbal
than verbal skills on measures from the McCanhy Scales of Children’s Abilities,
neural tube. Many children are born with an obvious spinal defect, represented
by a myelomeningocele or meningocele, at the caudal end of the neural tube.
Cranial anomalies are multiple but generally include the Arnold-Chiari malfor-
mation, which introduces a barrier to CSF outflow from the ventricular system to
the subarachnoid space. SB is also often associated with corpus callosum defects
(Just, Swartz, Ludwig, Ermert, & Thelen, 1990).
These congenital abnormalities result from early disruptions in neuro-
embryogenesis, occurring between approximately the fourth and sixteenth weeks
(Barkovich, 1990). The presence of multiple anomalies indicates that there was a
prolonged, rather than a brief, disruption in neuroembryogenesis during the first
mmester and the early part of the second trimester. In contrast, noncommunicating
hydrocephalus develops in some premature infants due to blockage of CSF
reabsorptive mechanisms. The hemorrhages in the germinal matrix and parenchyma
lead to destruction of the brain and may result in the development of porencephalic
cysts. Specific neurological deficits may depend upon the laterality and severity
of the hemorrhages and the resulting porencephalic cyst. Since these destructive
lesions occur in what would normally be the late second and early third trimester
(Volpe, 1989), P-Hyd infants have late gestational disruptive lesions rather than
the early gestational anomalies that are seen in patients with SB and AS. Corpus
callosum abnormalitiesmay be present in the P-Hyd children because the destructive
lesion producing the hemorrhage and hydrocephalus may destroy the corpus
callosum. Abnormalities in the corpus callosum may also be related to stretching
and thinning of the corpus callosum as the ventricles enlarge (i.e., as the hydro-
cephalus worsens). However, hydrocephalus and premature birth are abnormal
events that occur in what is generally an otherwise normal brain.
If the effects of hydrocephalus per se are to lower nonverbal skills (Dennis et
al., 1981; Rourke, 1989), then hydrocephalic children without other neuro-
pathological lesions should present with preservation of verbal skills and impairment
of nonverbal skills. This may be particularly apparent in AS children, where the
major abnormalities are often restricted to the CSF obstruction that leads to
hydrocephalus and the corpus callosum anomalies. In contrast, SB and P-Hyd
can be considered spectrum disorders because of the variable presentation of
other CNS anomalies that have a diffuse effect on the CNS. The effect of these
other CNS anomalies may be to reduce verbal skills to the level of nonverbal
5% JACK M.FLETCHER ET AL.
METHODS
Subjects
The design of this study involved (a) two-group comparisons of three etiologies of hydro-
cephalus (SB-shunt, prematurity-hydrocephalus,and AS) with comparison groups addressing
treatment and handicap effects (SB-no shunt, p r e m d t y - n o hydrocephalus, and normals);
and (b) comparisons across the three etiologies of hydrocephalus. All children were initially
recruited for a longitudinal study at the ages of 60-84 months over a 2-year period,
representing a thorough combing of the Houston-Galveston metropolitan area and sup-
plementation from San Antonio and Dallas. Most children were followed 1 year later,
with additional subjects entering the study to increase sample size.
Children were included in the hydrocephalus groups based on standard clinical d e f i -
tions and procedures for establishing diagnosis, including magnetic resonance imaging,
medical record review, and neurologic examination. Children who presented with hydro-
cephalus not secondary to dysraphic anomalies, prematurity, or AS were excluded. In
addition, any hydrocephalic child with additional complications, including meningitis.
other neurological anomaly (e.g., trauma, tumor, or stroke), uncontrolled epilepsy, primary
sensory loss (deafness, blindness), severe behavioral disorder (e.g.. autism, childhood
psychosis), or evidence of abuse or neglect, was excluded. Single or multiple shunt revi-
sions did not exclude a child from study. Subjects were also required to have either a
Verbal or Perceptual-Performance IQ on the McCarthy Scales of Children’s Abilities
(McCarthy, 1972) above 69 to avoid spurious results, since the relationship of VIQ and
PIQ changes with overall level of intelligence as a property of the test (Dennis et al.,
1981; Matarazzo, 1972).
The SB-shunt (SB-S) group consisted of 19 meningomyeloceles and 1 meningocele,
all of whom were shunted for hydrocephalus. The SB-no shunt (SB-nos) comparison
group (n = 13) consisted of 4 meningomyeloceles, 4 meningoceles, 3 spinal lipomas, and
2 children with disastomyelia. Although these children were recruited with the understanding
that they were all nonhydrocephalic, a careful review of medical records and, in 10 cases
(excluding two spinal lipoma and one disastomyelia cases), concurrent MFU of the brain,
revealed ventricular enlargement in two meningomyelocelesand two meningoceles. Hence,
this group did not uniformly represent a nonhydrocephalic comparison group. To maintain
sample size, these cases were not eliminated and were kept in a nonshunted SB compari-
son group. None of these cases demonstrated more than mild hydrocephalus.
The prematurity-hydrocephalus group (P-Hyd) consisted of 20 children with a history
of Grade III (n = 12) and Grade IV (n = 8 ) intraventricular hemorrhage (NH). Eight of
these children were shunted and the other 12 had received medication treatment for
progressive hydrocephalus shortly after birth. In this group, hydrocephalus was defined as
a Grade 111 or IV IVH persisting for at least 3 weeks after admission, with evidence of
VERB AL-NONVERBAL 597
which they were shunted. In each case, concurrent MRI was consistent with AS. Normal
children ( n = 13) were siblings ( n = 5), cousins ( n = 2). or were recruited from parents who
had a SB or premature child not eligible for the study ( n = 6). This approach to recruitment
prevented the selection of a markedly different group of normals in terms of demographic
characteristics. Any child meeting the exclusionary criteria for the hydrocephalic groups
was not included. All normal children demonstrated complete absence of acquired neu-
rological disorder, including normal MRI in 12 cases.
Table 1 summarizes demographic data at the time of the initial recruitment (Year l),
Variable Group
Aqueductal
Spina Bifida Premature Stenosis Normal
Shunt NoShunt Hyd NoHyd Shunt
N 20 13 20 16 8 13
Age (mos.)
M 74.4 77.0 76.7 73.4 73.2 77.0
SD 4.3 5.4 5.0 5.10 6.4 4.6
SES (%)
Low (4-5) 60 23 40 31 37 39
Middle (3) 20 23 15 31 13 23
High (1-2) 20 54 45 38 50 38
Gender (%)
Male 30 38 45 56 75 69
Female 70 62 55 44 25 31
Race (%)
White 65 84 80 63 62 84
Black 10 0 5 24 25 0
Hispanic 20 8 10 13 13 16
Other 5 8 5 0 0 0
McCarthy
GCI
M 76.0 103.7 90.0 100.6 93.8 102.5
SD 10.8 16.8 24.3 7.6 18.1 14.9
598 JACK M.FLETCHER ET AL.
revealing patterns that parallel the epidemiology of the disorders. Chi-square analyses
across the six groups and in the three two-group comparisonswere not statistically significant
(p > .05), although some trends are apparent. In particular, there is a trend for more
females and fewer Blacks in both SB groups. However, these trends are consistent with
the epidemiology of SB (Wiswell, Tuttle, Northam, & Simonds, 1990). All comparisons
of hydrocephalus groups with their respective comparison group show no sociodemographic
differences.
Sample sizes were varied across groups. Children with SB and no treatment for hydro-
cephalus and children with AS are rare and proved difficult to recruit, particularly in the
narrow age range used for this study. To increase sample size, we accepted additional
children who were too old for the initial assessment, but in the correct age range for the
second yearly follow-up of the initial groups. There were 11 children in Year 1 who did
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not receive Year 2 evaluations, and 11 children who were added in Year 2. An analysis of
the demographic variables in Table 1 for total cohort at Year 2 yielded no statistically
significant differences. No more than three Year 1 subjects were lost per group, but there
was a tendency to lose hydrocephalic subjects with larger discrepancies showing lower
nonverbal scores.
Cognitive Assessments
Each child received the McCarthy Scales of Children’s Abilities (McCarthy, 1972), a
battery of neuropsychological tests, and in Year 2, the WISC-R (Wechsler, 1974). Five
comparisons of discrepant abilities were made. The McCarthy Verbal and Perceptual-
Performance standard scores and the WISC-R VIQ and PIQ represented the first two
comparisons. For the third comparison, neuropsychological tests were used to create
composites of verbal and nonverbal cognitive abilities, reducing the number of dependent
variables for analysis. The verbal composite was created by averaging age-based standard
scores on the Auditory Analysis Test (Rosner & Simon, 1971), Rapid Automatized Nam-
ing (Denckla & Rudel, 1974). Word Fluency (Gaddes & Crockett. 1974), Word Finding
Test (Dennis, Hendrick, Hoffman, & Humphreys, 1987), and the Opposite Analogies,
Fluency, and Vocabulary subtests of the McCarthy. These tests represent a language
construct that is not contaminated with some of the less clearly language-based subtests of
the McCarthy and WISC-R. Similarly. a nonverbal composite was created by averaging
age-based standard scores on the Recognition-Discrimination Test (Saw & Fletcher, 1982).
Beery Visual-Motor Integration (Beery, 1982), and Judgement of Line Orientation Test
(Lindgren & Benton, 1980). The fourth comparison was on the verbal and nonverbal
selective reminding tests (Buschke, 1973; Fletcher, 1985). Finally, many hydrocephalic
children have primary motor handicaps. The fifth comparison addressed the role of motor
demands in tasks assessing nonverbal skills (e.g.. WISC-R PIQ). The nonverbal tasks
were averaged into composites representing motor-free spatial skills (Recognition-Dis-
crimination. Judgement of Line Orientation) and motor-based spatial skills (Beery VMI).
All composites were averages of scores standardized with M = 100 and SD = 15 based on
available normative data.
RESULTS
To provide the largest possible sample size and to address the replicability of the
analyses, results are presented separately for the Year 1 (N= 90) and Year 2 (N=
90)fOllOW-upS.
Tables 2 and 3 present means and standard deviations for Years 1 and 2,
respectively. To address the hypotheses of interest, a multivariate approach to
repeated measures ANOVA was used (O’Brien & Kaiser, 1985). Each compari-
VERBAL-NONVERBAL 599
Table 2. Means and Standard Deviations for Verbal-Nonverbal Variables (M= 100; SD
= 15) by Groups for Year 1 (N = 90).
~
Variable Group
Aqueductal
Spina Bifida Premature Stenosis Normal
Shunt NoShunt Hvd NOH yd Shunt
N 20 13 20 16 8 13
McCarthy
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Verbal
M 85.1 101.6 96.0 99.3 99.8 100.8
SD 12.9 15.8 15.9 11.1 16.6 9.7
Perceptual-
Performance
M 78.1 105.9 89.7 106.2 88.4 106.7
SD 16.8 17.4 24.3 7.6 18.0 11.9
Composites
Verbal
M 82.2 104.4 95.5 99.2 97.5 100.8
SD 14.1 15.1 14.0 12.1 19.7 12.2
Nonverbal
M 71.0 100.6 83.3 97.4 83.7 102.4
SD 19.8 8.7 23.1 7.0 14.6 10.2
Memory*
Verbal
M 90.8 104.3 104.7 98.8 90.2 101.5
SD 8.9 10.8 19.6 14.S 7.6 10.6
Nonverbal
M 83.3 99.1 92.5 99.2 92.1 91.8
SD 12.5 22.9 15.7 19.3 21.6 12.8
Motor
Motor-Free Spatial
M 62.0 100.4 78.9 94.1 81.7 100.0
SD 30.6 9.8 28.2 11.4 16.6 13.3
Motor-Baed Spatial
M 79.9 100.8 87.6 100.7 85.7 104.9
SD 12.2 10.0 19.3 5.0 14.2 9.0
*Sample sizes vary slightly because some children were not able to complete the nonver-
bal memory task.
600 JACK M.FLETCHER ET AL.
Table 3. Means and Standard Deviations for Verbal-Nonverbal Variables (A4= 100. SD
= 15) by Groups for Year 2 (N= 90).
Variable Group
Aqueductal
Spina Bifida Premature Stenosis Normal
Shunt NoShunt Hyd NoHyd Shunt
N 19 13 17 15 8 17
Age (mos.)
M 87.56 88.37 88.57 86.47 88.04 90.57
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effects of hydrocephalus varied across the range of etiologies, and that these
differential effects were not simply the result of including a normal group. In
addition, it was expected that Task differences would interact with Etiology, and
possibly with the Etiology by Hydrocephalus interaction. These interactions would
indicate that the degree of discrepancy in verbal-nonverbal skills was different
for the three etiologies of hydrocephalus. However, if interactions of Task oc-
curred only in relationship to the Hydrocephalus factor, then the presence of
hydrocephalus would be related to skill discrepancies regardless of etiology.
Post hoc comparisons involved tests of simple interaction effects, simple effects,
simple-simple effects, and pairwise comparisons where applicable. The general
strategy followed is outlined in Maxwell and Delaney (1990). To control Type I
error, the Bonfenoni adjustment was employed to maintain alpha at .05 throughout
post hoc analyses for the overall effect being decomposed. Although age differ-
ences were not significant, age varied across etiology groups, so that this variable
was treated as a covariate.
110
105
100
95
W
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U
0
% 90
a5
en
7s
Verbal Perceptual- P e J f ~ m e n ~ e
McCARTHYSCAE
was significant, F(1.78) = 4.49,p c .04.The pattern of results was similar to the
McCarthy, showing larger differences in the AS group. Again, the Hydrocepha-
lus by Etiology interaction was not significant (p < .09).
Verbal-nonverbal composites
The MANOVA for the verbal-nonverbal composites yielded comparable results
to the McCarthy and WISC-R analyses. The 3-way interaction was not significant
at Year 1 or Year 2, F < 1. Again, the Hydrocephalus by Task interaction was
significant for Year 1, F(l,83) = 1 4 . 3 0 , <
~ .0003,and Year 2, F(1, 83) = 5 . 2 6 , p
< .02. There was no evidence of Hydrocephalus by Etiology interactions. As a
group, hydrocephalic children had lower nonverbal than verbal scores.
VERBAL-NONVERBAL 603
Verbal-nonverbal memory
The MANOVA for the memory comparison yielded a significant 3-way interaction
at Year 1. F(2, 75) = 4 . 3 1 , ~< .02. Follow-up of this interaction with the single
degree-of-freedom contrasts yielded no significant effects at the .025 level. In-
spection of means in Table 2 showed a trend for the SB-S, P-Hyd, and normal
groups to have poorer nonverbal than verbal memory scores. However, the lower
scores in the normals made these findings difficult to interpret, particularly in
relationship to the AS group. :n Year 2, there were no significant interactions of
Task with Etiology or Hydrocephalus, F < 1. The main effect of Group was sig-
nificant, F(5, 83) = 23.96, p < .0001, but profiles were similar. Children with
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hydrocephalus obtained lower scores on both measures of memory than did the
comparison groups, with no evidence of discrepancy between verbal and nonver-
bal tasks.
Motor-free-motor-based
The final analysis addressed the role of the motor demands of the nonverbal
tasks, comparing a composite of spatial skills with no copying component and a
visual-motor component. There was no significant :3-way interaction, F(2, 83) =
2.65, p < .08.Moreover, as Table 2 shows, the SB-S and P-Hyd groups scored
lower on the motor-free tasks. Hence, the discrepancy in nonverbal processing
cannot be attributed to motor demands of the tasks. In Year 2, there were no
interactions involving Task with Hydrocephalus or Etiology, F < 1. In general,
children with hydrocephalus in this study had lower scores on both nonverbal
measures, so demands for motoric functioning (copying) did not explain the
observed discrepancies in verbal and nonverbal skills.
Treatment effects
Since treatment was confounded in the SB-S, SB-nos, and P-Hyd groups, addi-
tional analyses were conducted to examine relationships of etiology and treatment
(shunt, medication). For these analyses, hypotheses concerning interactions of
Etiology (SB, prematurity), Treatment (shunt, no shunt) and Task (Verbal,
Nonverbal) were evaluated on tasks showing discrepancies in hydrocephalic
cases.
Table 4 presents means and standard deviations for these analyses. For the
McCarthy, significant Task by Treatment interactions were apparent for Year 1,
F(1, 39) = 12.74, p < .001, and Year 2, F(1, 34) = 5.81, p < .03. Relative to
hydrocephalic children treated only with medication, inspection of means and
standard deviations in Table 4 shows that the shunted cases (collapsed across
etiology) had lower Perceptual-Performance scores than Verbal scores. Similar
findings were apparent for the Year 2 WISC-R scores, F ( 1 , 33) = 4.31, p < .05.
For composite scores, interactions of Task and Treatment were also found at
Year 1, F(1, 39) = 8.82, p < .006, and Year 2, F(1, 34) = 3.90, p c .06. As Table
4 shows, shunted children in both etiologies had larger discrepancies. To evalu-
ate if the results in Table 4 were explainable by the tendency to shunt children in
604 JACK M.FLETCHER ET AL.
Table 4. Means and Standard Deviations for Verbal-Nonverbal variables (M= 100; SD =
15).
Group
N 20 19 4 3 8 6 12 11
McCarthy
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Verbal
M 85.1 84.7 97.7 95.5 89.3 88.0 100.4 98.0
SD 12.9 14.4 25.3 30.0 12.3 11.5 17.0 19.5
Perceptual-
Performance
M 78.1 82.5 106.0 98.5 69.4 76.0 103.2 106.1
SD 16.8 14.8 22.8 22.7 10.8 16.9 21.2 16.1
WISC-R
Verbal
M - 88.2 - 108.0 - 95.2 - 99.6
SD - 15.1 - 29.5 - 22.3 - 16.4
Performance
M - 82.6 - 105.3 - 78.3 - 108.5
SD - 19.2 - 6.7 - 18.4 - 14.5
Composites
Verbal
M 82.2 83.5 99.1 84.7 87.2 85.7 99.1 97.7
SD 14.1 16.1 21.2 35.5 13.7 6.3 99.1 13.2
Nonverbal
M 71.0 80.2 98.4 93.8 63.0 74.4 98.4 98.5
SD 19.8 10.4 22.7 17.8 17.5 14.4 8.7 11.6
DISCUSSION
tion of means (Tables 2 and 3) revealed larger discrepancies in verbal and nonverbal
skills in the AS group, with smaller discrepancies in children with etiologies
reflecting SB and prematurity. This is especially apparent in Year 2, when the
children were more comparable (on average) in age to Dennis et al. (1981). There
were major differences in the design of Dennis et al. (1981) and the present
study. The present study was prospectively conducted in a narrower age range.
Sample sizes were larger for most groups, and comparison groups untreated for
hydrocephalus were also included. Dennis et al. (1981) did not find differences
due to etiology on absolute measures of verbal and nonverbal cognitive skills.
Differences were apparent only on a within-group difference score, which was
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directly addressed in our study by testing interactions involving Task. This in-
teraction was not directly tested in Dennis et al. (1981), probably because of
sample size limitations. However, our statistical approach may not have had
sufficient power to detect interactions with etiology, reflecting the small size of
the AS group (n=8). This analysis warrants replication with a larger sample of
AS patients.
Unlike our first study (Thompson et al., 198l), we found interactions of
hydrocephalus per se with verbal and nonverbal discrepancies. In addition, these
discrepancies did not reflect motor demands of the nonverbal tasks. This latter
finding can be attributable to the more sophisticated measurement of spatial
skills in the current study. Thompson et al. (1991) only employed the Recognition-
Discrimination Test (RD). This task, which involves simple matching of geometric
designs, may not be sensitive to the spatial processing problems of hydrocephalic
children. In contrast, the Judgement of Line Orientation Test (JLO) used in the
curren. study may be more sensitive than RD to spatial processing deficits.
Studies in adults using evoked potential and regional cerebral blood flow meth-
odologies have shown that performance on the JLO is primarily mediated by the
right hemisphere (Deutsch, Bourbon, Papanicolaou, Br Eisenberg, 1988). Similarly,
Papanicolaou, DiScenna, Gillespie, and Aram (1990) found that the K O consistently
produced lower amplitudes in evoked potentials fiom the right hemisphere in
children with unilateral cerebral insults. Hence, the JLO, which is a more complex
visual-spatial task than RD, may be more sensitive to spatial processing deficits
in adults and children with brain impairment.
The interactions of hydrocephalus and verbal-nonverbal performance in this
study are not necessarily inconsistent with Thompson et al. (1991), who only
addressed etiology differences, not average effects of hydrocephalus. Since AS
subjects show larger verbal-nonverbal discrepancies, adding the AS group may
have been sufficient to detect an interaction in this study. There are also signifi-
cant sampling differences reflected by the lower Year 2 McCarthy GCI of the
SB-S group in the current study (M = 78.6, SD = 20.10) versus Thompson et d.(A4
= 95, SD = 11.8). Thompson et al. (1991) included 4 unshunted children in the
SB group, which should increase intellectual levels in the SB group relative to
those in the current SB-S group, all of whom were shunted. The children in
Thompson et al. (1991) were also comparable in age to subjects during Year 2 of
606 JACK M.FLETCHER ET AL.
the present study, where discrepancies on the McCarthy Scales were less appar-
ent in the current study (see Table 3). Again, investigation of etiology differences
in larger samples is clearly needed. Of particular interest is the possibility of
differential growth effects: this will be addressed in the longitudinal study when
collection of a third follow-up has been completed.
The basis for verbal-nonverbal discrepancies undoubtedly extends beyond
the etiology of the hydrocephalus. The reductions in verbal skills in the SB-Sand
P-Hyd groups may reflect the higher frequency of other brain anomalies in these
groups. In the SB-S group, the Arnold-Chiari malformation and oculomotor
defects may be relevant ponders et al., 1990);in the P-Hyd group, the significant
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with more general reductions in higher-order skills such as memory and prob-
lem-solving. Severely head-injured children do not show discrepancies in per-
formance on the Verbal and Nonverbal Selective Reminding tests (Gilliam, Fletcher,
Levin, & Ewing-Cobbs, 1988). However, children with post-CNS irradiation for
leukemia do show poorer nonverbal memory performance (Copeland et al., 1985).
Both of these latter disorders principally (but not exclusively) involve multi-
focal lesions of the cerebral white matter and show other evidence for poorer
development of nonverbal processing skills (Fletcher & Copeland, 1988). Additional
research in larger samples is needed to address the basis for these findings.
A final comment concerns the confounding of hydrocephalus and its treatment
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