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Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen19
Cognitive and motor abilities in preschool hydrocephalics a
b
Nora M. Thompson , Lynn Chapieski , Michael E. Miner c
, Jack M. Fletcher , Susan H. Landry & Juliet Bixby
d
e
a
Southwest Neuropsychiatric Institute ,
b
Blue Bird Clinic, Baylor College of Medicine ,
c
Department of Neurosurgery , Ohio State University ,
f
d
Department of Pediatrics , University of Texas Medical School-Houston , e
Department of Pediatrics , University of Texas Medical Branch-Galveston , f
Department of Pediatrics , Texas Children's Hospital , Published online: 04 Jan 2008.
To cite this article: Nora M. Thompson , Lynn Chapieski , Michael E. Miner , Jack M. Fletcher , Susan H. Landry & Juliet Bixby (1991) Cognitive and motor abilities in preschool hydrocephalics, Journal of Clinical and Experimental Neuropsychology, 13:2, 245-258, DOI: 10.1080/01688639108401041 To link to this article: http://dx.doi.org/10.1080/01688639108401041
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Journal of Clinical and Experimenlal Neuropsychology 1991, V O ~13, . NO. 2, pp. 245-258
0168-8634/9 1/1302-0245$3.00 0 Swets & Zeitlinger
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Cognitive and Motor Abilities in Preschool Hydrocephalics* Nora M. Thompson Southwest Neuropsychiatric Institute
Jack M. Fletcher Department of Pediatrics, University of Texas Medical School-Houston
Lynn Chapieski Blue Bird Clinic, Baylor College of Medicine
Susan H. Landry Department of Pediatrics, University of Texas Medical Branch-Galveston
Michael E. Miner Department of Neurosurgery, Ohio State University
Juliet Bixby Department of Pediatrics, Texas Children’s Hospital
ABSTRACT The neuropsychological performance of three groups of preschool children was evaluated: (a) one with hydrocephalus associated with myelomeningocele; (b) one with hydrocephalus associated with intraventricular hemorrhage and very low birth weight; and (c) a nonhydrocephalic normal comparison group. Multivariate profile analysis revealed lower levels of performance on measures of verbal and nonverbal cognitive skills for both groups of hydrocephalic children relative to normals. Comparison of group profiles on tasks requiring figure copying as opposed to figure matching and analysis of specific gross and fine motor skills revealed that both hydrocephalic groups had impaired visual-motor integration in the presence of average visual perceptual matching. In addition, different patterns of motor ski11 deficits were found for each hydrocephalic group. The results of this study suggest that decreased visual-motor integration and etiology-specific motor deficits are major sequelae of these forms of hydrocephalus in the preschool years.
Hydrocephalus, caused by a variety of congenital and postnatal brain pathologies, results in enlargement of the ventricular system and pressure on surrounding neural tissue (Etheridge, 1983). Myelodysplasia (MDP), or spina bifida, is the
* Preparation of this manuscript was supported in part by NINCDS Grant NS 25368; Neurobehavioral Development of Hydrocephalic Children. Address all correspondence to Nora M. Thompson, Ph.D., Southwest Neuropsychiatric Institute, 8535 Tom Slick Drive, San Antonio, TX 78229, USA. Accepted for publication: June 4, 1990
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most common congenital cause of hydrocephalus in children, occurring in approximately 0.1% of live births in the United States (Liptak et al., 1988). Intraventricular hemorrhage (IVH) as a consequence of prematurity and low birth weight is the most common perinatal etiology of hydrocephalus in children, with an approximate frequency of 2.0% of live births in this country (Volpe, 1981). Yet no study to date has characterized the cognitive sequelae of hydrocephalus in the preschool years drawing a direct comparison between these two common etiologies. Furthermore, there has been a general tendency to study hydrocephalusin MDP children over seven years of age and to study hydrocephalus following IVH in infancy. We compared the performance of preschool-aged hydrocephalic children with either MDP or prematurity/IVHto a normal comparison group on measures of cognitive and motor skills in order to characterize the early consequences of hydrocephalus and to delineate etiology-specific profiles. Hydrocephalic children are at risk for a variety of medical problems that vary with the etiology of the hydrocephalus. For example, the MDP sequence is commonly associated with spina bifida, myelomeningocele, anomalies of the corpus callosum, and the Arnold Chiari malformation. Children with MDP sustain a variety of sensory and motor deficits, the severity of which depends on the spinal level and the degree of cord involvement of the dysraphic lesion (Anderson & Plewis, 1977; Clements & Kaushal, 1970; Grimm, 1976; Woods, 1979). In addition, children with MDP and hydrocephalus may also suffer disturbance of oculomotor function (Clements & Kaushal, 1970; Woods, 1979). In contrast, children with IVH and hydrocephalus are at risk for acute medical complications in infancy. Hydrocephalus in these infants is characteristically associated with a severe (Grade I11 or IV) hemorrhage of the germinal matrix and necrosis of migratory neurons (Dykes et al., 1980). The hemorrhage may resolve into a porencephalic cyst with concomitant neurologic deficits. Specifically, the inflammatory response to the hemorrhage leads to progressive hydrocephalus in some premature children. In addition, perinatal hypoxia, respiratory problems, and feeding difficulties further compromise the infants’ development over the first year of life. Studies of intellectual skills in hydrocephalic children have revealed consistent relationships between intellectual attainments and medical factors. In a study of largely school-aged children with various etiologies of hydrocephalus, Dennis et al., (1981) found that verbal-performance discrepancies varied as a function of the formative pathology of hydrocephalus. They also found that a history of seizures, visual defects, or ambulatory problems were associated with lower IQ scores. However, this study had relatively few children with hydrocephalus secondary to IVH. Investigation into the cognitive characteristicsof MDP hydrocephalic children have documented a tendency for language-based skills to be spared relative to performance-based skills in unselected samples (Badell-Ribera, Shulman, & Paddock, 1966; Spain, 1974; Tew, 1977) as well as in children with IQ scores greater than 70 (Dennis et al., 1981; Shaffer, Friedrich, Shurtleff, & Wolf, 1985).
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Although reports of the “Cocktail Party Syndrome” suggest that language-based skills are not normal in MDP and hydrocephalus (Spain, 1974; Tew, 1979), the “Cocktail Party Syndrome” does not appear to be unique to hydrocephalus (Tew & Laurence, 1979). Regardless, Dennis, Hendrick, Hoffman, and Humphreys (1987) found that MDP hydrocephalics demonstrated impairment of substantive verbal fluency. In contrast to studies suggesting relative sparing of language skills, nonlanguage deficits in MDP hydrocephalics have been documented in visual perception (Miller & Sethi, 1971; Zeiner & Prigatano, 1982), tactile perception (Land, 1977), fine motor speed (Anderson & Plewis, 1577; Prigatano, Zeiner, Pollay, & Kaplan, 1983), and perceptual-motor integration (Land, 1977; McLone, Czyzewski, Raimondi, & Sommers, 1982; Prigatano et al., 1983; Soare & Raimondi. 1977). Although there are many studies of school-aged MDP children (Fletcher & Levin, 1988), only two studies have examined cognitive development in children with MDP and hydrocephalus under the age of 7. Nielsen (1980) evaluated 30 children with hydrocephalus secondary to myelodysplasia at 6, 18, 30, and 72 months of age using different intelligence tests depending on the age of the child. While IQ scores increased over time, it is difficult to determine whether this represents developmental improvement or psychometric differences among the measures used. Spain (1974) studied a large group of 3-year-old children with neural tube defects, including 129 myelodysplasics. Few children showed severe intellectual delays, although shunted patients showed poor eye-hand coordination and ambulatory problems. In contrast to the scarcity of preschool studies of MDP children, investigations describing cognitive abilities in hydrocephalus secondary to IVH have primarily involved infants. This line of research has established that infants who sustain severe hemorrhages have a worse outcome at one and two years than do infants with lesser bleeds (Koons, Sun, Kamtorn, Hagovsky. & Koenigsberger, 1982; Krishnamoorthy, Shannon, DeLong, Todres, & Davis, 1979; Papile, Munsick, Weaver, & Pecha, 1979).Progressive hydrocephalus (Chaplin, Goldstein, Myerberg, Hunt, & Tooley, 1980; Koons et al., 1982; Landry et al., 1984; Teberg et al., 1982) and bronchopulmonary dysplasia (Landry et al., 1984; Landry, Chapieski, Fletcher, Denson, & Francis, 1988) are also associated with poor developmental outcome. Although a discrepancy favoring psychometric intelligence relative to motor skills has been reported (Landry et al., 1984; Landry et al., 1988; Ross & Schechner, 1982), few studies have followed preterm infants past 3 years of age with clear documentation of medical complications. Therefore, it is unclear whether cognitive deficits and/or intellectual-motor discrepancies persist at later ages. The age differences in studies of IVH and MDP children render it difficult to assess the influence of hydrocephalus and related medical complications on cognitive and motor development. Only one study to date has compared the cognitive skills of IVH and congenitally hydrocephalic children (Stellman & Bannister, 1982). These investigators compared 3-year-olds with hydrocephalus due to IVH, aqueductal stenosis, and a contrast group of premature non-
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hydrocephalic children, on the Griffiths Mental Development Scales. The IVH infants scored lower than the other two groups on four of the five Griffiths Scales, with the aqueductal stenosis group also scoring lower than the contrast group on measures of eye-hand coordination and visual-spatial performance. To date, no study has compared IVH hydrocephalic children with MDP hydrocephalic children. Moreover, there has been a general tendency to study hydrocephalus in MDP children over 7 years of age and to study hydrocephalus following IVH in infancy. The present study directly compared hydrocephalic children with either: (1) MDP, or (2) prematurityflVH. to each other and to a normal comparison group. In keeping with the literature on school-aged MDP hydrocephalics, we hypothesized that preschool hydrocephalic children would obtain lower scores o n motor and performance-based tasks, but would not differ from controls on verbal measures.
METHOD Subjects The sample (N = 65) consisted of three groups of children between four years, three months and seven years, three months of age. Two of the groups were characterized by hydrocephalus, in conjunction with either MDP or IVH. while a third contrast group was free of developmental abnormalities. Table 1 presents the means and standard deviations for age as well as the frequencies and percentages for gender, race, and socioeconomic status as measured by the Hollingshead-Redlich Two Factor Index of Social Position (Hollingshead & Redlich, 1958). The three groups did not differ in age, F (2, 62)= 1.5. p > .lo, gender, x2 (2, N = 65) = .45,p > .50, or socioeconomicstatus, ~ ~ (N4=,65)= 3.11, p > 50. The groups differed in race, ~ ~ (N4=, 65)= 10.39.p < .05. reflecting the absence of Black children in the MDP group and of Hispanic children in the IVH group. These findings parallel the epidemiology of these disorders in the population (Ericson, 1976; Keller, 1981). The MDP group consisted of subjects recruited by letter and telephone call from a large spina bifida clinic, two pediatric neurosurgeons, and the local Spina Bifida Association. Inclusion criteria consisted of (1) primary diagnosis of myelodysplasia at birth without additional birth defects, (2) history of hydrocephalus related to myelodysplasia diagnosed at birth or occurring within the first month of life, and (3) medically stable at the time of testing. Exclusion criteria were (1) primary sensory loss, (2) psychiatric disturbance, (3) McCarthy GCI below 70, or (4)acute hydrocephalic condition. Of the 45 children with myelodysplasiain the age range of this study. 17 were excluded due to profound retardation, 2 had primary sensory loss, 1 was not a native English speaker, 4 lived at too great a distance from the clinic, and 1 family refused participation. The characteristics of the resultant MDP group ( n = 20) were obtained by parental consent from medical records.' The IVH group consisted of 20 children with hydrocephalus secondary to bleeding into the ventricles as a complication of premature birth and very low birth weight. The intellectual, motor, and attentional development of the cohort from which these subjects were selected has been described up to three years of age (Landry et al., 1988). These children had birth weights below 1800 grams, were at least six weeks premature, and obtained a GCI above 70 on the McCarthy Scales of Children's Abilities. Hydrocephalus
-
'
The medical characteristicsof the MDP group can be provided to interested readers upon request.
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Table 1. Demographic Characteristics of the Sample. Myelodysplasia n
Intraventricular Hemorrhage
Contrast
20
20
25
64.9 9.3
67.7 9.8
62.5 10.5
6 (30%) 5 (25%) 9 (45%)
6 (30%) 8 (40%) 6 (30%)
1 1 (44%)
14 (70%) 0 (00%) 6 (30%)
16 (80%) 4 (20%) 0 (00%)
19 (76%) 2 (08%) 4 (16%)
8 (40%) 12 (60%)
10 (50%) 10 (50%)
12 (48%) 13 (52%)
Age (months)
M
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SD
Socioeconomic StatusaVb 1-2 3 4-5 Raceb Caucasian Black Hispanic Genderb Male Female a
8 (32%) 6 (24%)
Socioeconomic Status based on the Hollingshead Two-Factor Index. Levels 1 and 2 combined, as well as levels 4 and 5. Socioeconomic Status, Race, and Gender expressed in frequencies and percentages within each group.
was treated with diuretics and lumbar puncture in 17 children and 3 were shunted. None of the children had primary sensory loss, psychiatric disturbance, or an acute hydrocephalic condition. Although perinatal respiratory problems in this group ranged from mild to severe, none of these children had persisting difficulties attributable to bronchopulmonary dysplasia. Five children had been excluded with a McCarthy GCI of 70 or less. Two of these five excluded children presented with severe spasticity sufficient to preclude manipulation of the test materials. Presence of hydrocephalus was verified by CT scan and ultrasonography ,with all children demonstrating progressive hydrocephalus secondary to Grade III or IV hemorrhage. A comparison group of 25 children was recruited through the University of Texas Medical School Pediatric Clinic and among siblings and relatives of the hydrocephalic children. The children constituting the comparison group were the products of normal full-term gestation, weighed more than 3000 grams at birth, and were discharged from the hospital within three days of birth. All of these children were free of neurologic, psychiatric, or developmental abnormality.
Procedures The McCarthy Scales of Children’s Abilities (MSCA; McCarthy, 1972) were employed in order to obtain an overall estimate of cognitive ability, the General Cognitive Index (GCI), and to evaluate cognitive strengths and weaknesses, The McCarthy provides three unique scales (Verbal, Perceptual-Performance, and Quantitative) which are combined to form the GCI, as well as two scales (Memory and Motor) which overlap with the first three scales.
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Fine motor skills were evaluated using the Purdue Pegboard for younger children (Wilson, Iacoviello. Wilson, & Riscucci, 1982). The m a n number of pegs placed in three consecutive 10-s trials was obtained for each hand separately. The index of fine motor dexterity was computed by taking the mean of the score for both hands. In order to assess visual-spatial skills with and without a motor component, the Beery Test of Visual-Motor Integration (VML; Beery, 1982) and the Recognition-Discrimination Test (RD; Satz & Fletcher, 1982) were administered. The VMI requires the child to drawto-copy a series of geometric line drawings of increasing complexity. RD is a motor-free measure of visual-perceptual matching in which the child chooses an exact duplicate of increasingly complex geometric line drawings from a multiple choice format.
Statistical Analyses Standard scores with a mean of 100 and a standard deviation of 15 were computed for each measure using age-based norms to ensure the scaling equivalence required for comparison of scores across measures. Three profile analyses (PA) were performed on (a) the Verbal and Perceptual-Performance Scales of the McCarthy in order to compare languagebased and performance-based cognitive abilities, @) the VMI and RD in order to compare a motor-based and a motor-free test of visual-spatial skills, and (c) McCarthy Subtest 9, Subtest 10, and the Purdue Pegboard in order to compare gross motor coordination in the lower and upper extremities and fine motor coordination. Profile analysis, a well-established application of MANOVA techniques, is a multivariate procedure which provides a comparison of two or more groups on a set of measured variables (Harris,1985). This procedure provides a method for assessing group differences in profile shape and elevation, and is ideal for testing differential performance both within and between groups. The Quantitative, Memory, and Motor Scales of the McCarthy were each analyzed for group differences using ANOVA. The Memory and Motor Scales were not included in the PA because of content overlap with the Verbal and Perceptual-PerformanceScales. Because factor analytic support for the Quantitative Scale has been inconsistent across the age span included in this study for both normal and delayed populations (Kaufman &I Kaufman, 1977; Keith & Bolen. 1980), the Quantitative Scale was not included in the PA. In order to follow-up the results of each profile analysis, ANOVAs. between-group t tests, and paired-comparison t tests were performed. In order to control experiment-wise error rate, alpha was conservatively adjusted to .025 for PA involving two dependent variables and to .017 for the PA with three dependent variables. The LSD method was used to follow-up significant ANOVAs since it controls alpha at .05 when the number of contrasts equals three.
RESULTS Group means and standard deviations for the McCarthy Scales and the neuropsychological measures are presented in Tables 2 and 3. The P A of the McCarthy Verbal and Perceptual-Performance Scales revealed n o significant effect for the test of parallelism, F < 1.0, indicating that the profiles were similar in shape across groups. A significant levels effect was found, F ( 2 , 6 2 ) = 8.1, p < .001, indicating the presence of between-group differences in overall level. Follow-up comparisons revealed that the performance of the contrast group was significantly higher than performance of both the MDP and the IVH groups at p c .01, who did not differ. The flatness hypothesis was not rejected, F c 1.O, indicating n o significant differences between the Verbal and Perceptual-
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Tabel 2. Group Means and Standard Deviations for McCarthy Scales. Myelodysplasia Scale
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General Cognitive Index Verbal PerceptualPerformance Quantitative Memory Motor
Intraventricular Hemorrhage
Contrast
M
SD
M
SD
M
SD
95.0
11.8
92.1
15.9
107.2
11.2
98.4
13.3
95.1
13.1
106.4
11.7
98.0 91.2 92.8 69.6
14.8 14.0 15.5 15.8
91.2 94.5 97.9 84.9
16.3 13.6 13.3 17.3
106.2 103.4 107.3 103.5
9.9 10.8 11.7 9.0
Note. All scores were standardized with a mean of 100 and a standard deviation of 15.
Performance Scales. Inspection of Table 2 reveals the differences in overall level of performance, with the contrast group scoring higher than either the MDP or IVH groups. However, comparable scores were obtained on the Verbal and Perceptual-Performance Scales for all groups. Group profiles on the VMI and RD were analyzed next. In this analysis. the parallelism hypothesis was rejected, F ( 2 , 6 2 ) = 9.0, p c .001, indicating significant differences in profile shape among the three groups. Follow-up ANOVAs revealed that the MDP and IVH groups did not differ from each other in shape, F < 1.O, but that both hydrocephalic groups differed from the contrast group, p < .001. Since the profiles of the MDP and IVH groups did not differ in shape, these two groups were compared for levels and flatness effects. Although no significant levels effect was found, F < 1.O, the flatness hypothesis was rejected, F(1,38)= 7.8, p c .001. These findings indicate that not only were the MDP and IVH groups similar in profile shape and level, but also that both groups displayed a discrepancy between the VMI and the RD. Inspection of group means shows average performance levels on RD and lower scores on the VMI for both groups (see Table 3). The third PA provided a more specific comparison of motor skills among the groups. The profiles differed significantly in shape, F(4,114) = 10.9,p < .001. The groups were compared to each other using MANOVA to determine which groups were dissimilar in profile shape. Results indicated that the MDP profile differed from both the contrast group, F ( 2 , 5 7 ) = 25.4, p < .001, and from the IVH group, F ( 2 , 57) = 8.3, p < .001.The contrast group and the IVH group did not differ in profile shape, F(2, 57) = 3.9, p > .017. This means that the IVH and contrast groups displayed similar motor performance patterns, although the contrast group scored at a higher overall level. However, the MDP group showed a much different
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Table 3.Group Means and Standard Deviations for Neuropsychological Tests. Myelodysplasia
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Test
M
SD
Recognition Discrimination 102.9 12.1 Beery VisualMotor Integration 75.5 26.6 McCarthy Subtest 9 Gross Motor Legs 57.6 11.8 McCarthy Subtest 10 Gross Motor Arms 81.3 18.7 Purdue Pegboard Fine Motor 72.3 15.6
Intraventricular Hemorrhage
Contrast
M
SD
M
SD
101.5
10.5
107.7
8.8
72.0 21.2
102.0 21.6
81.6 17.8
107.1
88.1
16.9
77.7 12.2
6.9
99.8 11.3 94.6
12.3
Nore. All scores were standardized with a mean of 100 and a standard deviation of 15.
pattern of motor performance. In order to interpret these findings, the levels and flatness hypotheses were evaluated for the IVH and contrast groups. Results of the PA of motor skills for the IVH and contrast groups indicated that both the levels and flatness hypotheses were rejected [ F(1,40)= 3 5 . 5 , ~< .001; and F(2, 39) = 7.4, p < .01, respectively 1. These findings indicate that the contrast group performed at higher levels than the IVH group and that their profiles were not flat. In order to compare performance of the three groups on each of the three motor tasks, separate ANOVAs were performed along with follow-up LSD comparisons. The groups differed on the measure of gross arm coordination, F(2,62) = 7.7, p < .001. The two hydrocephalic groups did not differ from each other, but they both scored significantly lower than the contrast group. Significant differences were also found for gross leg coordination, F(2, 6 2 ) = 83.9, p < .OOOl,with the MDP group scoring lower than the IVH group and the IVH group scoring lower than the contrast group. Significant differences were also found on the fine motor task, F(2, 6 2 ) = 17.8, p < .001.The contrast group scored higher than both the IVH and the MDP groups on fine motor coordination, although the hydrocephalic groups did not differ from one another. These results demonstrate similar degrees of impairment on both fine motor and gross arm coordination in the hydrocephalic groups. In addition, gross leg coordination, while discrepant from the contrast group in both hydrocephalic groups, was most severely affected in the MDP group. To amplify specific McCarthy results, separate ANOVAs were performed on the Quantitative, Memory, and Motor Scales. Significant group differences on the Quantitative Scale, F (2, 64) = 5.6, p < .01, reflected the lower scores ob-
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tained by both hydrocephalic groups as compared to contrast group. The same pattern of group differences was found on the Memory Scale, F (2,64) = 6.7, p c .01. The two hydrocephalic groups scored significantly lower than the contrast group, but did not differ from each other. Group differences were most striking on the Motor Scale, F(2, 64) = 32.2, p < ,001. Follow-up LSD analysis revealed that the contrast group scored significantly higher than both hydrocephalic groups. In addition, the IVH group obtained significantly higher scores than the MDP group. Since these groups did not differ on the VMI or Perceptual-Performance Scale, it is likely that performance on subtests 9 and 10 account for the differences on the Motor Scale.
DISCUSSION Few studies have compared the cognitive and motor abilities of young hydrocephalic children. In addition, no published study has directly compared children with hydrocephalus secondary to IVH with MDP on psychometric tests. In the present study, both MDP and IVH groups obtained similar patterns of verbal and nonverbal intelligence scores. Although the difference in overall level of intelligence between both hydrocephalic groups and the comparison group reached statistical significance, this result is of little clinical significance since the group means for the hydrocephalic groups were well within the average range of intelligence. Both hydrocephalic groups had impaired visual-motor integration in the presence of average visual perceptual matching. However, different patterns of motor skill deficits were found for each hydrocephalic group. The pattern of Verbal and Perceptual- Performance Scale scores did not differ across groups. While these findings are consistent with descriptions of uniformly lower mental scores in three-year-olds with IVH (Landry et al., 1984; Landry et al., 1988; Ross & Schechner, 1982), they depart from previous studies describing inferior nonverbal abilities in congenital hydrocephalics. Lower performance scores have been described for MDP children age seven years and older (Dennis et al., 1981; Shaffer et al., 1985), but have not been addressed in studies of younger congenital hydrocephalics. Therefore, one explanation of our findings is that the nonverbal deficit is not manifest in the preschool years. On the other hand, the absence of a significant verbal-performance discrepancy in our study may be due to the interplay of specific motor defects (reduced manual speedkoordination and defective visual-motor integration) with measurement characteristics of the McCarthy Scales. Previous studies of IQ in MDP have generally utilized the Wechsler Scales of Intelligence for Children which requires timed motoric responses for the Performance Scale. In contrast, the Perceptual-Performance Scale of the MSCA does not emphasize quick responding to the same degree. It is possible that hydrocephalic children do not have performance-based difficulties in the absence of time constraints, particularly given the average levels of ability demonstrated on our figure-matching test
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(RD). The extent to which verbal-performance discrepancies are specific to older hydrocephalic children as opposed to reflecting the interaction of motor slowing with performance requirements on intelligence tests requires further clarification. The data on visual perceptual skills with and without a motor component suggest that nonverbal, visual-spatial processes may be intact when assessed by untimed matching-to-sample procedures. Although this seems contrary to previous studies identifying visual perception deficits (Zeiner & Prigatano, 1982;Miller & Sethi, 1971),a closer examination of the tasks reveals important differences. In both of the latter studies, serial tachistoscopic presentation of the stimuli was used; this imposes a time limit for viewing the stimuli and adds a memory component to the task. This raises the interesting possibility that hydrocephalics may have difficulty meeting the perceptual constraints of the tachistoscopic paradigm. Certainly, visual perception is not unaffected in hydrocephalus and perceptual deficits have been reported in higher-order aspects of visual perception such as figure-ground discrimination (Miller & Sethi, 1971). The results of our study utilizing an untimed matching-to-sample presentation of stimuli suggest that simple visual discrimination skills may be intact in preschool hydrocephalics and highlight the importance of considering both accuracy and latency measures. Accurate yet slow performance has been reported for subgroups of hydrocephalic children on language measures (Dennis et al. 1987).We are currently investigating response latencies of hydrocephalic children on simple visual discrimination tasks. In contrast with average levels of performance on RD, performance on the visual-motor integration task was impaired for both groups of hydrocephalics, providing further support for previous reports (Land, 1977;McLone et al., 1982; Prigatano et al., 1983; Soare & Raimondi, 1977)and extending these findings to the preschool years. This finding is especially important since visual-motor integration is a key factor in the development of handwriting ability (Sovik, 1975). The extent to which visual-motor deficit predicts subsequent academic problems for children with hydrocephalus awaits further study. It is interesting to note that both hydrocephalic groups scored below average on the VMI and exhibited average scores on the Perceptual-Performance Scale of the McCarthy. One of the subtests making up the Perceptual-Performance Scale (Draw-a-Design) has a format which is almost identical to the VMI (i.e. drawing geometric line drawings of increasing complexity). In our sample, scores on the Draw-a-Design subtest were significantly higher than scores on the VIvlI for both hydrocephalic groups, but did not differ from the VMI in the contrast group. The low correlation of the VMI with Draw-a-Design ( r = .47)in our sample suggests important differences between the tests. Whether such differences can be explained by the normative samples, item scaling, or other factors is not clear and requires further study. Nonetheless, these findings suggest that the VMI is more sensitive to the visual-motor integration deficit in preschool hydrocephalics. The summary measure of motor skills (The McCarthy Motor Scale) revealed that the MDP group obtained the lowest scores. The IVH group achieved inter-
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mediate scores and the contrast group performed at average levels. More specifically, it is noteworthy that both hydrocephalic groups demonstrated a similar degree of impairment on a timed measure of fine motor coordination. This is consistent with previous reports for MDP children (Anderson & Plewis, 1977; Prigatano et al., 1983) and has not been reported for IVH hydrocephalics. Our study demonstrates that fine motor deficits are apparent in preschool children with either MDP or IVH hydrocephalus. This is interesting because, in comparison, a lesser degree of impairment was found for gross arm coordination. Both the fine motor and the gross arm coordination tasks have visual-motor task requirements. However, it may be that the hydrocephalic children have greater difficulty with the speed requirements on the fine motor task. In contrast, the patterns of gross motor coordination in the legs highlights deficits specific to each etiology of hydrocephalus. In MDP the level of the dysraphic spinal lesion is directly related to the degree of sensory-motorimpairment. In contrast, the impairment of lower limb coordination in IVH and prematurity is more subtle, probably due to balance problems, the origin of which is unknown. The differences in degree and quality of lower limb coordination demonstrates that children with hydrocephalus present with deficits secondary to the etiology, as well as those cognitive deficits attributable to the hydrocephalic process per se . In most respects, the results of this study are generalizable to independent samples of hydrocephalic preschool children. However, the treatment characteristics of our sample must be addressed with regard to external validity. In the present sample, 16 of the 20 MDP hydrocephalics received ventriculo-peritonea1 (V-P) shunts, while the other 4 were successfully controlled with diuretics. In contrast, only 3 of the 20 IVH hydrocephalics were shunted, while the remainder were treated with lumbar puncture and/or diuretics. Because of this, the MDP group contains a greater number of children with a V-P shunt and the lesion occasioned by the shunt placement. The lower proportion of shunted IVH hydrocephalic children relative to the shunted MDP hydrocephalicsreflects many factors, including the progression of the hydrocephalic process, the medical stability of the infant when surgery is contemplated, and how these factors influenced the treatment decisions of our surgeons. The treatment characteristics of our sample may differ from samples drawn from other hospitals or born prior to 1980, as a function of the decision process involved in treating hydrocephalus. In spite of these treatment differences, all the hydrocephalic children in this study had enlarged ventricles documented by CT scan. Nonetheless, the potential influence of differential treatment effects on the cognitive outcome in hydrocephalus cannot be overlooked and requires further study. It will be important in future studies to determine whether the similarities and differences between the two hydrocephalic groups persist in later childhood. In addition, it will be important to evaluate whether additional deficits (e.g. visual discrimination) emerge at later ages. The extent to which cognitive and motor deficits are related to specific aspects of academic progress must also be explored.
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Future research should expand this study with more detailed examination of treatment variables and inclusion of a broader range of hydrocephalic etiologies.
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REFERENCES Anderson, E.M., & Plewis, I. (1977). Impairment of a motor skill in children with spina bifida cystica and hydrocephalus: An exploratory study. British Journal of Psychology, 680,61-70. Badell-Ribera, A., Shulman, K., & Paddock. N. (1966). The relationship of non-progressive hydrocephalus to intellectual functioning in children with spina bifida cystica. Pediarrics, 37, 787-793. Beery, K. (1982). Developmental test of visual-motor integration. Chicago: Follett. Chaplin, E.R.. Goldstein, G.W., Myerberg, D.Z., Hunt, J.V., & Tooley, W.H. (1 980). Post hemorrhagic hydrocephalus in the preterm infant. Pediatrics, 65,901 -909. Clements. D.B., Bt Kaushal, K. (1970). A study of the ocular complicationsof hydrocephalus and meningomyelocele. Transactions of the Ophthalmology Society, 90,383-390. Dennis, M. Fitz, C.R., Netley, C.T., Sugar, J., Harwood-Nash, D.C.F..Hendrick, E.B., Hoffman, H.J., & Humphreys, R.P. (1981). The intelligence of hydrocephalic children. Archives of Neurology, 38,607-615. Dennis, M.. Hendrick, E.B., Hoffman, H.J.. & Humphreys, R.P. (1987). Language of hydrocephalic children and adolescents. Journal of Clinical and Experimental Neuropsychology. 9,593-621. Dykes, F.D.. Lazzara, A.. Ahmann, P., Blumenstein, B., Schwartz. J., & Brann, A.W. (1980). Intraventricular hemorrhage: A prospective evaluation of etiopathogenesis. Pediatrics, 66,42-49. Ericson, J.D. (1 976). Racial variation in the incidence of congenital malformations. Annals of Human Genetics, 39, 315-322. Etheridge, J.E. (1983). Birth defects and developmental disorders. In T.W. Farmer (Ed.), Pediatric Neurology (pp.67-92). Philadelphia: Harper & Row. Fletcher, J.M., & Levin, H.S. (1988). Neurobehavioral effects of brain injury in children. In D. Routh (Ed.), Hana3ookofpediawicpsychobgy (pp. 258-298). New York: Guilfod. Grimm, R.A. (1976). Hand function and tactile perception in a sample of children with myelomeningocele. The American Journal of Occupational Therapy, 30.234-240. Harris. R.J. (1985). A primer of multivariate statistics. Orlando, FL: Academic. Hollingshead, A.B.. & Redlich, F.C. (1958). Two-factor indexof social class. New York: John Wiley. Kaufman, A.S., & Kaufman, N.L. (1977). Clinical evaluation of young children with the McCarthy Scales. New York: Grune & Stratton. Keith, T.Z., & Bolen, L.M. (1980). Factor structure of the McCarthy Scales for children experiencing problems in school. Psychology in the Schools, 17,320-326. Keller, C. (1981). Epidemiological characteristics of preterm birth. In S.Friedman & M. Sigman (Eds.), Preterm birth and psychological development (pp. 3-16). New York: Academic. Koons, A., Sun. S.. Kamtom, V., Hagovsky, M., & Koenigsberger, R. (1982). Neurodevelopmental outcome related to intraventricular hemorrhage and perinatal events. Paper presented at the Prenatal Intracranial Hemorrhage Conference, Washington, D.C. Krishnamoorthy,K.S.,Shannon, D., DeLong, G., Todres, I.. & Davis, K. (1979). Neurologic sequelae in the survivors of neonatal intraventricular hemorrhage. Pediatrics, 64.233237. Land, L.C. (1977). A study of the sensory integration of children with myelomeningocele. In R.L. McLawrin (Ed.), Myelomeningocele (pp. 115-140).New York:Grune & Stratton.
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Landry, S.H., Chapieski. L., Fletcher, J.M., Denson. S.. & Francis, D. (1988). Three-year outcome for low birthweight infants: Differential effects of early medical complications. Journal of Pediatric Psychology, 13, 317-327. Landry, S.H., Fletcher, J.M., Zarling, C.L., Chapieski, L., Francis, D.J..& Denson, S. (1984). Differential outcomes associated with early complications in premature infants. Journal of Pediatric Psychology, 9, 385-401. Liptak, G.S., Bloss, J.W., Briskin, H.. Campbell, J.E., Hebert, E.B., & Revell, G.M. (1988). The management of children with spinal dysraphism. Journal of Child Neurology, 3,3-20. McCarthy, D. (1972). The McCarthy Scales of Children’s Abilities. New York: Psychological Corporation. McLone, D.G., Czyzewski, D., Raimondi, A., & Sommers, R. (1982). Central nervous system infections as a limiting factor in intelligence of children with myelomeningocele. Pediatrics, 70, 338-342. Miller, E., & Sethi, L. (1971). The effects of hydrocephalus on perception. Developmental Medicine and Child Neurology, 13. (Suppl. 2.5). 77-81. Nielsen, H.H. (1980). A longitudinalstudy of the psychologicalaspects of myelomeningocele. Scandinavian Journal of Psychology, 21,45-54. Papile, L.A., Munsick, G., Weaver, N., & Pecha, S. (1979). Cerebral intraventricular hemorrhage in infants (CVH) 1500 grams: Developmental follow-up at one year. Pediatric Research, 13, 528. Prigatano, G., Zeiner, H., Pollay, M., & Kaplan, R. (1983). Neuropsychological functioning in children with shunted, uncomplicated hydrocephalus. Child‘s Brain, 10, 1 12-120. Ross, G., & Schechner, S. (1982). Peritintraventricular hemorrhage as a risk factor in the development of premature infants. Paper presented at the International Conference on Infancy, Austin, TX. Satz, P., & Fletcher, J.M. (1982). Florida Kindergarten Screening Battery. Florida: Psychological Assessment Resources. Shaffer, J., Friedrich, W.N., Shurtleff, D.B., & Wolf, L. (1985). Cognitive and achievement status of children with myelomeningocele. Journal of Pediatric Psychology, 10, 325336. Soare, P., & Raimondi, A. (1977). Intellectual and perceptual-motor characteristics of treated myelomeningocelechildren. American Journal of Diseases in Children, 131,199204. Sovik, N. (1975). Developmental cybernetics of handwriting and graphic behavior. Oslo: Universitetsforglaget. Spain, B. (1974). Verbal and performance ability in pre-school children with spina bifida. Developmental Medicine and Child Neurology, 16, 773-780. Stellman, G.R.. & Bannister, C.M. (1982). The first three years: A comparative study of the developmental assessment of premature and full-term hydrocephalic children. Spina S i f d a Therapy, 4,91-101. Teberg, A.J.. Wu. P.Y., Hodgman, J., Mich, C., Garfinkle, J., Azen, S., & Wingert, W. (1982) Infants with birth weight under 1500 grams: Physical, neurological and developmental outcomes. Critical Care Medicine, 10, 10- 14. Tew, B. (1977). Spina bifida children’s scores on the Wechsler Intelligence Scale for Children. Perceptual and Motor Skills, 44, 381-382. Tew, B. (1979). The “Cocktail Party Syndrome”in children with hydrocephalus and spina bifida. British Journal of Disorders of Communication, 14, 89-101. Tew, B., & Laurence, K. (1979). The clinical and psychological characteristics of children with the “cocktail party” syndrome. Zeitschrift fur Kinderchirurgie und Grezebiete, 28, 360-367. Volpe, J.J (1981). Neonatal intraventricular hemorrhage. New England Journal of Medicine, 304, 886-89 1.
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Wilson. B.C.. Iacoviello, J.M.. Wilson, J.J., & Riscucci, D. (1982). &due pegboard performance of normal preschool children. Journal of Clinical Neuropsychology, 4,1926. Woods, G.E.(1979). Visual problems in the handicapped child. Child: Care, health, and development, 5,303-322. Zeiner, H.K., & Prigatano, G.P. (1982). Information processing deficits in hydrocephalic and letter reversal children. Neuropsychologia, 20,483492.
Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen19
Cognitive and motor abilities in preschool hydrocephalics a
b
Nora M. Thompson , Lynn Chapieski , Michael E. Miner c
, Jack M. Fletcher , Susan H. Landry & Juliet Bixby
d
e
a
Southwest Neuropsychiatric Institute ,
b
Blue Bird Clinic, Baylor College of Medicine ,
c
Department of Neurosurgery , Ohio State University ,
f
d
Department of Pediatrics , University of Texas Medical School-Houston , e
Department of Pediatrics , University of Texas Medical Branch-Galveston , f
Department of Pediatrics , Texas Children's Hospital , Published online: 04 Jan 2008.
To cite this article: Nora M. Thompson , Lynn Chapieski , Michael E. Miner , Jack M. Fletcher , Susan H. Landry & Juliet Bixby (1991) Cognitive and motor abilities in preschool hydrocephalics, Journal of Clinical and Experimental Neuropsychology, 13:2, 245-258, DOI: 10.1080/01688639108401041 To link to this article: http://dx.doi.org/10.1080/01688639108401041
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Journal of Clinical and Experimenlal Neuropsychology 1991, V O ~13, . NO. 2, pp. 245-258
0168-8634/9 1/1302-0245$3.00 0 Swets & Zeitlinger
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Cognitive and Motor Abilities in Preschool Hydrocephalics* Nora M. Thompson Southwest Neuropsychiatric Institute
Jack M. Fletcher Department of Pediatrics, University of Texas Medical School-Houston
Lynn Chapieski Blue Bird Clinic, Baylor College of Medicine
Susan H. Landry Department of Pediatrics, University of Texas Medical Branch-Galveston
Michael E. Miner Department of Neurosurgery, Ohio State University
Juliet Bixby Department of Pediatrics, Texas Children’s Hospital
ABSTRACT The neuropsychological performance of three groups of preschool children was evaluated: (a) one with hydrocephalus associated with myelomeningocele; (b) one with hydrocephalus associated with intraventricular hemorrhage and very low birth weight; and (c) a nonhydrocephalic normal comparison group. Multivariate profile analysis revealed lower levels of performance on measures of verbal and nonverbal cognitive skills for both groups of hydrocephalic children relative to normals. Comparison of group profiles on tasks requiring figure copying as opposed to figure matching and analysis of specific gross and fine motor skills revealed that both hydrocephalic groups had impaired visual-motor integration in the presence of average visual perceptual matching. In addition, different patterns of motor ski11 deficits were found for each hydrocephalic group. The results of this study suggest that decreased visual-motor integration and etiology-specific motor deficits are major sequelae of these forms of hydrocephalus in the preschool years.
Hydrocephalus, caused by a variety of congenital and postnatal brain pathologies, results in enlargement of the ventricular system and pressure on surrounding neural tissue (Etheridge, 1983). Myelodysplasia (MDP), or spina bifida, is the
* Preparation of this manuscript was supported in part by NINCDS Grant NS 25368; Neurobehavioral Development of Hydrocephalic Children. Address all correspondence to Nora M. Thompson, Ph.D., Southwest Neuropsychiatric Institute, 8535 Tom Slick Drive, San Antonio, TX 78229, USA. Accepted for publication: June 4, 1990
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most common congenital cause of hydrocephalus in children, occurring in approximately 0.1% of live births in the United States (Liptak et al., 1988). Intraventricular hemorrhage (IVH) as a consequence of prematurity and low birth weight is the most common perinatal etiology of hydrocephalus in children, with an approximate frequency of 2.0% of live births in this country (Volpe, 1981). Yet no study to date has characterized the cognitive sequelae of hydrocephalus in the preschool years drawing a direct comparison between these two common etiologies. Furthermore, there has been a general tendency to study hydrocephalusin MDP children over seven years of age and to study hydrocephalus following IVH in infancy. We compared the performance of preschool-aged hydrocephalic children with either MDP or prematurity/IVHto a normal comparison group on measures of cognitive and motor skills in order to characterize the early consequences of hydrocephalus and to delineate etiology-specific profiles. Hydrocephalic children are at risk for a variety of medical problems that vary with the etiology of the hydrocephalus. For example, the MDP sequence is commonly associated with spina bifida, myelomeningocele, anomalies of the corpus callosum, and the Arnold Chiari malformation. Children with MDP sustain a variety of sensory and motor deficits, the severity of which depends on the spinal level and the degree of cord involvement of the dysraphic lesion (Anderson & Plewis, 1977; Clements & Kaushal, 1970; Grimm, 1976; Woods, 1979). In addition, children with MDP and hydrocephalus may also suffer disturbance of oculomotor function (Clements & Kaushal, 1970; Woods, 1979). In contrast, children with IVH and hydrocephalus are at risk for acute medical complications in infancy. Hydrocephalus in these infants is characteristically associated with a severe (Grade I11 or IV) hemorrhage of the germinal matrix and necrosis of migratory neurons (Dykes et al., 1980). The hemorrhage may resolve into a porencephalic cyst with concomitant neurologic deficits. Specifically, the inflammatory response to the hemorrhage leads to progressive hydrocephalus in some premature children. In addition, perinatal hypoxia, respiratory problems, and feeding difficulties further compromise the infants’ development over the first year of life. Studies of intellectual skills in hydrocephalic children have revealed consistent relationships between intellectual attainments and medical factors. In a study of largely school-aged children with various etiologies of hydrocephalus, Dennis et al., (1981) found that verbal-performance discrepancies varied as a function of the formative pathology of hydrocephalus. They also found that a history of seizures, visual defects, or ambulatory problems were associated with lower IQ scores. However, this study had relatively few children with hydrocephalus secondary to IVH. Investigation into the cognitive characteristicsof MDP hydrocephalic children have documented a tendency for language-based skills to be spared relative to performance-based skills in unselected samples (Badell-Ribera, Shulman, & Paddock, 1966; Spain, 1974; Tew, 1977) as well as in children with IQ scores greater than 70 (Dennis et al., 1981; Shaffer, Friedrich, Shurtleff, & Wolf, 1985).
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Although reports of the “Cocktail Party Syndrome” suggest that language-based skills are not normal in MDP and hydrocephalus (Spain, 1974; Tew, 1979), the “Cocktail Party Syndrome” does not appear to be unique to hydrocephalus (Tew & Laurence, 1979). Regardless, Dennis, Hendrick, Hoffman, and Humphreys (1987) found that MDP hydrocephalics demonstrated impairment of substantive verbal fluency. In contrast to studies suggesting relative sparing of language skills, nonlanguage deficits in MDP hydrocephalics have been documented in visual perception (Miller & Sethi, 1971; Zeiner & Prigatano, 1982), tactile perception (Land, 1977), fine motor speed (Anderson & Plewis, 1577; Prigatano, Zeiner, Pollay, & Kaplan, 1983), and perceptual-motor integration (Land, 1977; McLone, Czyzewski, Raimondi, & Sommers, 1982; Prigatano et al., 1983; Soare & Raimondi. 1977). Although there are many studies of school-aged MDP children (Fletcher & Levin, 1988), only two studies have examined cognitive development in children with MDP and hydrocephalus under the age of 7. Nielsen (1980) evaluated 30 children with hydrocephalus secondary to myelodysplasia at 6, 18, 30, and 72 months of age using different intelligence tests depending on the age of the child. While IQ scores increased over time, it is difficult to determine whether this represents developmental improvement or psychometric differences among the measures used. Spain (1974) studied a large group of 3-year-old children with neural tube defects, including 129 myelodysplasics. Few children showed severe intellectual delays, although shunted patients showed poor eye-hand coordination and ambulatory problems. In contrast to the scarcity of preschool studies of MDP children, investigations describing cognitive abilities in hydrocephalus secondary to IVH have primarily involved infants. This line of research has established that infants who sustain severe hemorrhages have a worse outcome at one and two years than do infants with lesser bleeds (Koons, Sun, Kamtorn, Hagovsky. & Koenigsberger, 1982; Krishnamoorthy, Shannon, DeLong, Todres, & Davis, 1979; Papile, Munsick, Weaver, & Pecha, 1979).Progressive hydrocephalus (Chaplin, Goldstein, Myerberg, Hunt, & Tooley, 1980; Koons et al., 1982; Landry et al., 1984; Teberg et al., 1982) and bronchopulmonary dysplasia (Landry et al., 1984; Landry, Chapieski, Fletcher, Denson, & Francis, 1988) are also associated with poor developmental outcome. Although a discrepancy favoring psychometric intelligence relative to motor skills has been reported (Landry et al., 1984; Landry et al., 1988; Ross & Schechner, 1982), few studies have followed preterm infants past 3 years of age with clear documentation of medical complications. Therefore, it is unclear whether cognitive deficits and/or intellectual-motor discrepancies persist at later ages. The age differences in studies of IVH and MDP children render it difficult to assess the influence of hydrocephalus and related medical complications on cognitive and motor development. Only one study to date has compared the cognitive skills of IVH and congenitally hydrocephalic children (Stellman & Bannister, 1982). These investigators compared 3-year-olds with hydrocephalus due to IVH, aqueductal stenosis, and a contrast group of premature non-
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hydrocephalic children, on the Griffiths Mental Development Scales. The IVH infants scored lower than the other two groups on four of the five Griffiths Scales, with the aqueductal stenosis group also scoring lower than the contrast group on measures of eye-hand coordination and visual-spatial performance. To date, no study has compared IVH hydrocephalic children with MDP hydrocephalic children. Moreover, there has been a general tendency to study hydrocephalus in MDP children over 7 years of age and to study hydrocephalus following IVH in infancy. The present study directly compared hydrocephalic children with either: (1) MDP, or (2) prematurityflVH. to each other and to a normal comparison group. In keeping with the literature on school-aged MDP hydrocephalics, we hypothesized that preschool hydrocephalic children would obtain lower scores o n motor and performance-based tasks, but would not differ from controls on verbal measures.
METHOD Subjects The sample (N = 65) consisted of three groups of children between four years, three months and seven years, three months of age. Two of the groups were characterized by hydrocephalus, in conjunction with either MDP or IVH. while a third contrast group was free of developmental abnormalities. Table 1 presents the means and standard deviations for age as well as the frequencies and percentages for gender, race, and socioeconomic status as measured by the Hollingshead-Redlich Two Factor Index of Social Position (Hollingshead & Redlich, 1958). The three groups did not differ in age, F (2, 62)= 1.5. p > .lo, gender, x2 (2, N = 65) = .45,p > .50, or socioeconomicstatus, ~ ~ (N4=,65)= 3.11, p > 50. The groups differed in race, ~ ~ (N4=, 65)= 10.39.p < .05. reflecting the absence of Black children in the MDP group and of Hispanic children in the IVH group. These findings parallel the epidemiology of these disorders in the population (Ericson, 1976; Keller, 1981). The MDP group consisted of subjects recruited by letter and telephone call from a large spina bifida clinic, two pediatric neurosurgeons, and the local Spina Bifida Association. Inclusion criteria consisted of (1) primary diagnosis of myelodysplasia at birth without additional birth defects, (2) history of hydrocephalus related to myelodysplasia diagnosed at birth or occurring within the first month of life, and (3) medically stable at the time of testing. Exclusion criteria were (1) primary sensory loss, (2) psychiatric disturbance, (3) McCarthy GCI below 70, or (4)acute hydrocephalic condition. Of the 45 children with myelodysplasiain the age range of this study. 17 were excluded due to profound retardation, 2 had primary sensory loss, 1 was not a native English speaker, 4 lived at too great a distance from the clinic, and 1 family refused participation. The characteristics of the resultant MDP group ( n = 20) were obtained by parental consent from medical records.' The IVH group consisted of 20 children with hydrocephalus secondary to bleeding into the ventricles as a complication of premature birth and very low birth weight. The intellectual, motor, and attentional development of the cohort from which these subjects were selected has been described up to three years of age (Landry et al., 1988). These children had birth weights below 1800 grams, were at least six weeks premature, and obtained a GCI above 70 on the McCarthy Scales of Children's Abilities. Hydrocephalus
-
'
The medical characteristicsof the MDP group can be provided to interested readers upon request.
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Table 1. Demographic Characteristics of the Sample. Myelodysplasia n
Intraventricular Hemorrhage
Contrast
20
20
25
64.9 9.3
67.7 9.8
62.5 10.5
6 (30%) 5 (25%) 9 (45%)
6 (30%) 8 (40%) 6 (30%)
1 1 (44%)
14 (70%) 0 (00%) 6 (30%)
16 (80%) 4 (20%) 0 (00%)
19 (76%) 2 (08%) 4 (16%)
8 (40%) 12 (60%)
10 (50%) 10 (50%)
12 (48%) 13 (52%)
Age (months)
M
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SD
Socioeconomic StatusaVb 1-2 3 4-5 Raceb Caucasian Black Hispanic Genderb Male Female a
8 (32%) 6 (24%)
Socioeconomic Status based on the Hollingshead Two-Factor Index. Levels 1 and 2 combined, as well as levels 4 and 5. Socioeconomic Status, Race, and Gender expressed in frequencies and percentages within each group.
was treated with diuretics and lumbar puncture in 17 children and 3 were shunted. None of the children had primary sensory loss, psychiatric disturbance, or an acute hydrocephalic condition. Although perinatal respiratory problems in this group ranged from mild to severe, none of these children had persisting difficulties attributable to bronchopulmonary dysplasia. Five children had been excluded with a McCarthy GCI of 70 or less. Two of these five excluded children presented with severe spasticity sufficient to preclude manipulation of the test materials. Presence of hydrocephalus was verified by CT scan and ultrasonography ,with all children demonstrating progressive hydrocephalus secondary to Grade III or IV hemorrhage. A comparison group of 25 children was recruited through the University of Texas Medical School Pediatric Clinic and among siblings and relatives of the hydrocephalic children. The children constituting the comparison group were the products of normal full-term gestation, weighed more than 3000 grams at birth, and were discharged from the hospital within three days of birth. All of these children were free of neurologic, psychiatric, or developmental abnormality.
Procedures The McCarthy Scales of Children’s Abilities (MSCA; McCarthy, 1972) were employed in order to obtain an overall estimate of cognitive ability, the General Cognitive Index (GCI), and to evaluate cognitive strengths and weaknesses, The McCarthy provides three unique scales (Verbal, Perceptual-Performance, and Quantitative) which are combined to form the GCI, as well as two scales (Memory and Motor) which overlap with the first three scales.
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Fine motor skills were evaluated using the Purdue Pegboard for younger children (Wilson, Iacoviello. Wilson, & Riscucci, 1982). The m a n number of pegs placed in three consecutive 10-s trials was obtained for each hand separately. The index of fine motor dexterity was computed by taking the mean of the score for both hands. In order to assess visual-spatial skills with and without a motor component, the Beery Test of Visual-Motor Integration (VML; Beery, 1982) and the Recognition-Discrimination Test (RD; Satz & Fletcher, 1982) were administered. The VMI requires the child to drawto-copy a series of geometric line drawings of increasing complexity. RD is a motor-free measure of visual-perceptual matching in which the child chooses an exact duplicate of increasingly complex geometric line drawings from a multiple choice format.
Statistical Analyses Standard scores with a mean of 100 and a standard deviation of 15 were computed for each measure using age-based norms to ensure the scaling equivalence required for comparison of scores across measures. Three profile analyses (PA) were performed on (a) the Verbal and Perceptual-Performance Scales of the McCarthy in order to compare languagebased and performance-based cognitive abilities, @) the VMI and RD in order to compare a motor-based and a motor-free test of visual-spatial skills, and (c) McCarthy Subtest 9, Subtest 10, and the Purdue Pegboard in order to compare gross motor coordination in the lower and upper extremities and fine motor coordination. Profile analysis, a well-established application of MANOVA techniques, is a multivariate procedure which provides a comparison of two or more groups on a set of measured variables (Harris,1985). This procedure provides a method for assessing group differences in profile shape and elevation, and is ideal for testing differential performance both within and between groups. The Quantitative, Memory, and Motor Scales of the McCarthy were each analyzed for group differences using ANOVA. The Memory and Motor Scales were not included in the PA because of content overlap with the Verbal and Perceptual-PerformanceScales. Because factor analytic support for the Quantitative Scale has been inconsistent across the age span included in this study for both normal and delayed populations (Kaufman &I Kaufman, 1977; Keith & Bolen. 1980), the Quantitative Scale was not included in the PA. In order to follow-up the results of each profile analysis, ANOVAs. between-group t tests, and paired-comparison t tests were performed. In order to control experiment-wise error rate, alpha was conservatively adjusted to .025 for PA involving two dependent variables and to .017 for the PA with three dependent variables. The LSD method was used to follow-up significant ANOVAs since it controls alpha at .05 when the number of contrasts equals three.
RESULTS Group means and standard deviations for the McCarthy Scales and the neuropsychological measures are presented in Tables 2 and 3. The P A of the McCarthy Verbal and Perceptual-Performance Scales revealed n o significant effect for the test of parallelism, F < 1.0, indicating that the profiles were similar in shape across groups. A significant levels effect was found, F ( 2 , 6 2 ) = 8.1, p < .001, indicating the presence of between-group differences in overall level. Follow-up comparisons revealed that the performance of the contrast group was significantly higher than performance of both the MDP and the IVH groups at p c .01, who did not differ. The flatness hypothesis was not rejected, F c 1.O, indicating n o significant differences between the Verbal and Perceptual-
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Tabel 2. Group Means and Standard Deviations for McCarthy Scales. Myelodysplasia Scale
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General Cognitive Index Verbal PerceptualPerformance Quantitative Memory Motor
Intraventricular Hemorrhage
Contrast
M
SD
M
SD
M
SD
95.0
11.8
92.1
15.9
107.2
11.2
98.4
13.3
95.1
13.1
106.4
11.7
98.0 91.2 92.8 69.6
14.8 14.0 15.5 15.8
91.2 94.5 97.9 84.9
16.3 13.6 13.3 17.3
106.2 103.4 107.3 103.5
9.9 10.8 11.7 9.0
Note. All scores were standardized with a mean of 100 and a standard deviation of 15.
Performance Scales. Inspection of Table 2 reveals the differences in overall level of performance, with the contrast group scoring higher than either the MDP or IVH groups. However, comparable scores were obtained on the Verbal and Perceptual-Performance Scales for all groups. Group profiles on the VMI and RD were analyzed next. In this analysis. the parallelism hypothesis was rejected, F ( 2 , 6 2 ) = 9.0, p c .001, indicating significant differences in profile shape among the three groups. Follow-up ANOVAs revealed that the MDP and IVH groups did not differ from each other in shape, F < 1.O, but that both hydrocephalic groups differed from the contrast group, p < .001. Since the profiles of the MDP and IVH groups did not differ in shape, these two groups were compared for levels and flatness effects. Although no significant levels effect was found, F < 1.O, the flatness hypothesis was rejected, F(1,38)= 7.8, p c .001. These findings indicate that not only were the MDP and IVH groups similar in profile shape and level, but also that both groups displayed a discrepancy between the VMI and the RD. Inspection of group means shows average performance levels on RD and lower scores on the VMI for both groups (see Table 3). The third PA provided a more specific comparison of motor skills among the groups. The profiles differed significantly in shape, F(4,114) = 10.9,p < .001. The groups were compared to each other using MANOVA to determine which groups were dissimilar in profile shape. Results indicated that the MDP profile differed from both the contrast group, F ( 2 , 5 7 ) = 25.4, p < .001, and from the IVH group, F ( 2 , 57) = 8.3, p < .001.The contrast group and the IVH group did not differ in profile shape, F(2, 57) = 3.9, p > .017. This means that the IVH and contrast groups displayed similar motor performance patterns, although the contrast group scored at a higher overall level. However, the MDP group showed a much different
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Table 3.Group Means and Standard Deviations for Neuropsychological Tests. Myelodysplasia
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Test
M
SD
Recognition Discrimination 102.9 12.1 Beery VisualMotor Integration 75.5 26.6 McCarthy Subtest 9 Gross Motor Legs 57.6 11.8 McCarthy Subtest 10 Gross Motor Arms 81.3 18.7 Purdue Pegboard Fine Motor 72.3 15.6
Intraventricular Hemorrhage
Contrast
M
SD
M
SD
101.5
10.5
107.7
8.8
72.0 21.2
102.0 21.6
81.6 17.8
107.1
88.1
16.9
77.7 12.2
6.9
99.8 11.3 94.6
12.3
Nore. All scores were standardized with a mean of 100 and a standard deviation of 15.
pattern of motor performance. In order to interpret these findings, the levels and flatness hypotheses were evaluated for the IVH and contrast groups. Results of the PA of motor skills for the IVH and contrast groups indicated that both the levels and flatness hypotheses were rejected [ F(1,40)= 3 5 . 5 , ~< .001; and F(2, 39) = 7.4, p < .01, respectively 1. These findings indicate that the contrast group performed at higher levels than the IVH group and that their profiles were not flat. In order to compare performance of the three groups on each of the three motor tasks, separate ANOVAs were performed along with follow-up LSD comparisons. The groups differed on the measure of gross arm coordination, F(2,62) = 7.7, p < .001. The two hydrocephalic groups did not differ from each other, but they both scored significantly lower than the contrast group. Significant differences were also found for gross leg coordination, F(2, 6 2 ) = 83.9, p < .OOOl,with the MDP group scoring lower than the IVH group and the IVH group scoring lower than the contrast group. Significant differences were also found on the fine motor task, F(2, 6 2 ) = 17.8, p < .001.The contrast group scored higher than both the IVH and the MDP groups on fine motor coordination, although the hydrocephalic groups did not differ from one another. These results demonstrate similar degrees of impairment on both fine motor and gross arm coordination in the hydrocephalic groups. In addition, gross leg coordination, while discrepant from the contrast group in both hydrocephalic groups, was most severely affected in the MDP group. To amplify specific McCarthy results, separate ANOVAs were performed on the Quantitative, Memory, and Motor Scales. Significant group differences on the Quantitative Scale, F (2, 64) = 5.6, p < .01, reflected the lower scores ob-
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tained by both hydrocephalic groups as compared to contrast group. The same pattern of group differences was found on the Memory Scale, F (2,64) = 6.7, p c .01. The two hydrocephalic groups scored significantly lower than the contrast group, but did not differ from each other. Group differences were most striking on the Motor Scale, F(2, 64) = 32.2, p < ,001. Follow-up LSD analysis revealed that the contrast group scored significantly higher than both hydrocephalic groups. In addition, the IVH group obtained significantly higher scores than the MDP group. Since these groups did not differ on the VMI or Perceptual-Performance Scale, it is likely that performance on subtests 9 and 10 account for the differences on the Motor Scale.
DISCUSSION Few studies have compared the cognitive and motor abilities of young hydrocephalic children. In addition, no published study has directly compared children with hydrocephalus secondary to IVH with MDP on psychometric tests. In the present study, both MDP and IVH groups obtained similar patterns of verbal and nonverbal intelligence scores. Although the difference in overall level of intelligence between both hydrocephalic groups and the comparison group reached statistical significance, this result is of little clinical significance since the group means for the hydrocephalic groups were well within the average range of intelligence. Both hydrocephalic groups had impaired visual-motor integration in the presence of average visual perceptual matching. However, different patterns of motor skill deficits were found for each hydrocephalic group. The pattern of Verbal and Perceptual- Performance Scale scores did not differ across groups. While these findings are consistent with descriptions of uniformly lower mental scores in three-year-olds with IVH (Landry et al., 1984; Landry et al., 1988; Ross & Schechner, 1982), they depart from previous studies describing inferior nonverbal abilities in congenital hydrocephalics. Lower performance scores have been described for MDP children age seven years and older (Dennis et al., 1981; Shaffer et al., 1985), but have not been addressed in studies of younger congenital hydrocephalics. Therefore, one explanation of our findings is that the nonverbal deficit is not manifest in the preschool years. On the other hand, the absence of a significant verbal-performance discrepancy in our study may be due to the interplay of specific motor defects (reduced manual speedkoordination and defective visual-motor integration) with measurement characteristics of the McCarthy Scales. Previous studies of IQ in MDP have generally utilized the Wechsler Scales of Intelligence for Children which requires timed motoric responses for the Performance Scale. In contrast, the Perceptual-Performance Scale of the MSCA does not emphasize quick responding to the same degree. It is possible that hydrocephalic children do not have performance-based difficulties in the absence of time constraints, particularly given the average levels of ability demonstrated on our figure-matching test
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(RD). The extent to which verbal-performance discrepancies are specific to older hydrocephalic children as opposed to reflecting the interaction of motor slowing with performance requirements on intelligence tests requires further clarification. The data on visual perceptual skills with and without a motor component suggest that nonverbal, visual-spatial processes may be intact when assessed by untimed matching-to-sample procedures. Although this seems contrary to previous studies identifying visual perception deficits (Zeiner & Prigatano, 1982;Miller & Sethi, 1971),a closer examination of the tasks reveals important differences. In both of the latter studies, serial tachistoscopic presentation of the stimuli was used; this imposes a time limit for viewing the stimuli and adds a memory component to the task. This raises the interesting possibility that hydrocephalics may have difficulty meeting the perceptual constraints of the tachistoscopic paradigm. Certainly, visual perception is not unaffected in hydrocephalus and perceptual deficits have been reported in higher-order aspects of visual perception such as figure-ground discrimination (Miller & Sethi, 1971). The results of our study utilizing an untimed matching-to-sample presentation of stimuli suggest that simple visual discrimination skills may be intact in preschool hydrocephalics and highlight the importance of considering both accuracy and latency measures. Accurate yet slow performance has been reported for subgroups of hydrocephalic children on language measures (Dennis et al. 1987).We are currently investigating response latencies of hydrocephalic children on simple visual discrimination tasks. In contrast with average levels of performance on RD, performance on the visual-motor integration task was impaired for both groups of hydrocephalics, providing further support for previous reports (Land, 1977;McLone et al., 1982; Prigatano et al., 1983; Soare & Raimondi, 1977)and extending these findings to the preschool years. This finding is especially important since visual-motor integration is a key factor in the development of handwriting ability (Sovik, 1975). The extent to which visual-motor deficit predicts subsequent academic problems for children with hydrocephalus awaits further study. It is interesting to note that both hydrocephalic groups scored below average on the VMI and exhibited average scores on the Perceptual-Performance Scale of the McCarthy. One of the subtests making up the Perceptual-Performance Scale (Draw-a-Design) has a format which is almost identical to the VMI (i.e. drawing geometric line drawings of increasing complexity). In our sample, scores on the Draw-a-Design subtest were significantly higher than scores on the VIvlI for both hydrocephalic groups, but did not differ from the VMI in the contrast group. The low correlation of the VMI with Draw-a-Design ( r = .47)in our sample suggests important differences between the tests. Whether such differences can be explained by the normative samples, item scaling, or other factors is not clear and requires further study. Nonetheless, these findings suggest that the VMI is more sensitive to the visual-motor integration deficit in preschool hydrocephalics. The summary measure of motor skills (The McCarthy Motor Scale) revealed that the MDP group obtained the lowest scores. The IVH group achieved inter-
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mediate scores and the contrast group performed at average levels. More specifically, it is noteworthy that both hydrocephalic groups demonstrated a similar degree of impairment on a timed measure of fine motor coordination. This is consistent with previous reports for MDP children (Anderson & Plewis, 1977; Prigatano et al., 1983) and has not been reported for IVH hydrocephalics. Our study demonstrates that fine motor deficits are apparent in preschool children with either MDP or IVH hydrocephalus. This is interesting because, in comparison, a lesser degree of impairment was found for gross arm coordination. Both the fine motor and the gross arm coordination tasks have visual-motor task requirements. However, it may be that the hydrocephalic children have greater difficulty with the speed requirements on the fine motor task. In contrast, the patterns of gross motor coordination in the legs highlights deficits specific to each etiology of hydrocephalus. In MDP the level of the dysraphic spinal lesion is directly related to the degree of sensory-motorimpairment. In contrast, the impairment of lower limb coordination in IVH and prematurity is more subtle, probably due to balance problems, the origin of which is unknown. The differences in degree and quality of lower limb coordination demonstrates that children with hydrocephalus present with deficits secondary to the etiology, as well as those cognitive deficits attributable to the hydrocephalic process per se . In most respects, the results of this study are generalizable to independent samples of hydrocephalic preschool children. However, the treatment characteristics of our sample must be addressed with regard to external validity. In the present sample, 16 of the 20 MDP hydrocephalics received ventriculo-peritonea1 (V-P) shunts, while the other 4 were successfully controlled with diuretics. In contrast, only 3 of the 20 IVH hydrocephalics were shunted, while the remainder were treated with lumbar puncture and/or diuretics. Because of this, the MDP group contains a greater number of children with a V-P shunt and the lesion occasioned by the shunt placement. The lower proportion of shunted IVH hydrocephalic children relative to the shunted MDP hydrocephalicsreflects many factors, including the progression of the hydrocephalic process, the medical stability of the infant when surgery is contemplated, and how these factors influenced the treatment decisions of our surgeons. The treatment characteristics of our sample may differ from samples drawn from other hospitals or born prior to 1980, as a function of the decision process involved in treating hydrocephalus. In spite of these treatment differences, all the hydrocephalic children in this study had enlarged ventricles documented by CT scan. Nonetheless, the potential influence of differential treatment effects on the cognitive outcome in hydrocephalus cannot be overlooked and requires further study. It will be important in future studies to determine whether the similarities and differences between the two hydrocephalic groups persist in later childhood. In addition, it will be important to evaluate whether additional deficits (e.g. visual discrimination) emerge at later ages. The extent to which cognitive and motor deficits are related to specific aspects of academic progress must also be explored.
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Future research should expand this study with more detailed examination of treatment variables and inclusion of a broader range of hydrocephalic etiologies.
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