(Stroke. 1999;30:949-955.)
© 1999 American Heart Association, Inc.
Original Contributions |
From the Division of Stroke Medicine, University of Nottingham (A.S.); Centre for Applied Psychology (M.P.B., S.-M.S.) and Department of Radiology (D.J.W.), University of Leicester; and the Department of Integrated Medicine, Leicester Royal Infirmary (M.E.A.), Leicester, UK.
Correspondence to Dr Alan Sunderland, Division of Stroke Medicine, City Hospital, Hucknall Road, Nottingham NG5 1PB, United Kingdom. E-mail alan.sunderland{at}nottingham.ac.uk
| Abstract |
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MethodsThirty patients within 1 month of an infarct involving the parietal or posterior frontal lobe (15 left and 15 right hemisphere) used the ipsilateral hand in tests that simulated everyday hand functions. Performance was compared with that of healthy age-matched controls using the same hand. Standardized tests were used to assess apraxia, visuospatial ability, and aphasia.
ResultsAll patients were able to complete the dexterity tests, but video analysis showed that performance was slow and clumsy compared with that of controls (P<0.001). Impairment was most severe after left hemisphere damage, and apraxia was a strong correlate of increased dexterity errors (P<0.01), whereas reduced ipsilateral grip strength correlated with slowing (P<0.05). The pattern of performance was different for patients with right hemisphere damage. Here there was no correlation between grip strength and slowing, while dexterity errors appeared to be due to visuospatial problems.
ConclusionsSubtle impairments in dexterity of the ipsilateral hand are common within 1 month of stroke. Ipsilateral sensorimotor losses may contribute to these impairments, but the major factor appears to be the presence of cognitive deficits affecting perception and control of action. The nature of these deficits varies with side of brain damage. The effect of impaired dexterity on functional outcome is not yet known.
Key Words: cognition motor activity rehabilitation
| Introduction |
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One might expect that if a patient does not have normal function on the ipsilateral side to help compensate for hemiparesis, this would be a significant obstacle to rehabilitation, but the clinical implications of these impairments remain unclear for a number of reasons. First, studies have varied greatly in sampling procedures and have seldom focused on well-defined groups of stroke patients at a fixed time after stroke. Second, the assessment procedures have often been far removed from everyday functioning. This has been most marked in studies of apraxia in which the most frequently used assessments are gesture imitation or pantomime of object use,2 and some studies have reported no relationship between such assessments and tests of manual skill.12 13 Finally, there has been inconsistency in dealing with the dependence of manual dexterity on cognitive functioning: some studies of ipsilateral performance have excluded patients who showed clinically obvious apraxia or visuospatial problems,4 10 while others have regarded these cognitive deficits as major causes of ipsilateral impairment.5 8
The current confusion over ipsilateral impairment is also reflected in a lack of integration in attempts to explain it. Some papers have sought an explanation in terms of disruption of ipsilateral motor pathways.4 10 Others have proposed an executive role for the dominant hemisphere in skilled motor control of either hand.8 9 There is also a large body of literature on apraxia,14 15 with theories about disruption of the cognitive representation of actions. Finally, some studies have shown that visuospatial impairments such as visual neglect can prevent accurate reaching with the ipsilateral arm.5 9 Each of these different accounts may have a role to play in understanding the motor performance of different patients with different sites of brain damage, but at present there is no consensus on what types of deficit might commonly lead to clinically significant impairment of ipsilateral hand function.
This article reports an intensive investigation of ipsilateral hand function in a common clinical group for whom, we hypothesized, it might be most severely affected. These were hemiplegic patients within a month of an infarct in the territory of the middle cerebral artery and with a lesion encroaching on the left or right parietal area. These patients might therefore have suffered the combined effects of loss of ipsilateral motor pathways plus deficits in motor performance secondary to apraxia or visuospatial deficits, which are strongly associated with damage to these cortical areas.16 17 The aims of the study were to assess the impact of ipsilateral deficits on simulations of everyday manual tasks and to discover to what extent these deficits were correlated with cognitive impairment.
| Subjects and Methods |
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Stroke Patients
Two hundred fifty-four admissions to an acute stroke unit and a
rehabilitation ward were screened for cases of a first unilateral
cerebrovascular accident (CVA) with parietal lobe involvement.
Diagnosis was based on medical notes and routine CT scan report. Thirty
patients (12% of those screened) were recruited to the study. All had
suffered middle cerebral artery stroke (7 hemorrhagic, 23
ischemic). Major reasons for exclusion from the study were
evidence of a previous stroke or neurological disease (47%) or
internal capsule infarcts with no apparent cortical involvement (9%).
The CT scans were later reviewed by an experienced radiologist (D.J.W.)
who was blind to patients' test performances. Table 1
shows the resulting classification of
brain lesions. Seven of the patients were judged to have had posterior
frontal rather than parietal damage, and another 2 had signs of
bilateral damage. These 9 patients were retained in the study but with
attention given to these lesion variables in analysis of
the results.
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Patients were assessed when they were alert enough to cooperate with testing and it was practically possible to arrange a test session. Mean time after left hemisphere stroke (LCVA) was 17.2 days (range, 4 to 29) and after right hemisphere stroke (RCVA) 18.8 days (range, 1 to 31). All of the LCVA group were said to have been right-handed before their stroke. Two of the RCVA group had been left-handed. All patients used the hand ipsilateral to their lesion for the dexterity tests.
Two measures of functional impairment were the Barthel Index of
dependence in self-care18 and the Extended Motricity Index
of range and strength of movement in the contralateral
arm.19 The LCVA and RCVA groups were similar on these
measures (Barthel: LCVA mean=11.4, SD=5.0, range 4 to 20; RCVA
mean=10.8, SD=4.9, range=5 to 20. EMI: LCVA mean=39.5, SD=36.9, range=0
to 93; RCVA mean=24.7, SD=34.0, range 0 to 92). Mann-Whitney
U tests comparing the groups on these measures confirmed no
significant effects (P>0.2). Table 2
shows that the 2 groups were similar in
sex ratio and years of education, but the average age for the LCVA
group was higher than for the RCVA group (means of 67 versus 58 years;
Mann-Whitney U test, P<0.05).
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Control Subjects
Healthy volunteers were drawn from a number of community groups.
Inclusion criteria were no history of stroke or other neurological
disease and no significant problems with hand movement due to
arthritis, etc. They were similar to the stroke patients in age and
years of education (see Table 2
). All of them were right-handed,
but equal numbers were assessed using their right hand (right-handed
controls, RC) or the left hand (left-handed controls, LC). Groups were
allocated alternately as healthy volunteers were recruited.
Procedure
The subject sat in a chair/wheelchair at a standard height
dining table. The stroke patients used the hand ipsilateral to lesion
site throughout, while the healthy volunteers used either their left or
right hand, depending on control group.
Dexterity in Simulations of Everyday Tasks
These tests were performed on a rectangular baseboard measuring
75x31 cm, located on the tabletop and centered at body midline. A
video camera was positioned above the baseboard and pointing downward
to provide a record of task performance for later
analysis. Instructions were given verbally and by
demonstration. Subjects were asked to do the tasks "as quickly as you
can," and the subtests were always given in the following
sequence.
Jebsen Hand Function Test
This was designed to simulate common everyday manual
skills.20 Subtests from this battery were given with
slight modifications to the original published procedure in an attempt
to increase reliability. These modifications were that all subtests
began with the subject's hand resting on the table at midline and each
subtest was repeated 3 times. The subtests were the following. (1)
Card Turning. The subject turned over each of 5 index cards
(7.5 cmx12.5 cm) positioned evenly along the baseboard. (2)
Picking Up Small Common Objects. Two paper clips, 2 bottle
tops, and 2 coins were spaced along the baseboard with a tin can (13 cm
high with a diameter of 9 cm) at the far end. The subject had to make
cross-body movements to pick up each object in turn and drop it into
the can.
A wooden board 2 cm thick was positioned at the back of the baseboard to provide the ledge used in the last 2 subtests. (3) Simulated Feeding (Bean Spooning). A teaspoon was used to spoon 5 kidney beans spaced along the back of the ledge into a can at the body midline. (4) Stacking Checkers. Four red wooden checkers spaced against the front of the ledge were stacked on top of the ledge.
Williams Doors
This test assesses dexterity in opening and closing small doors
and has been shown to be a correlate of dependency in the
elderly.21 Modifications to the original procedure were
that only 1 door (15x23cm) was used, fastened with a small bolt. The
door was angled at 45° so that a clear view of manipulation of the
bolt could be recorded by the overhead video camera. The opening
edge of the door was at body midline, and it opened toward the
ipsilateral side. The subject began with the hand on the baseboard at
body midline and then had to unfasten the bolt and pull the door open
until it reached 90°. The hand was then returned to the resting
position before the subject reached up again to close the door. This
procedure was repeated for 3 trials.
The videotapes of these dexterity tests were analyzed to obtain
measures of speed and accuracy. Speed was measured by adding a
1/100-second timebase to the tape and reviewing it, frame by frame, to
time the period from when the hand first moved from the rest
position until completion of the trial. Accuracy was independently
assessed by 2 raters (A.S. and M.B.), and 1 error was scored whenever
there was not smooth, uncorrected execution of the component actions in
each task. Thus, the maximum number of possible errors on each trial
was 5 for card turning (1 for each card), 6 for picking up objects (1
for each object), 5 for spooning beans (1 for each bean), 4 for
checkers (1 for each checker), and 2 for the Williams doors (1
for opening and 1 for closing). For the Jebsen subtests, the
statistic22 for interrater agreement on errors ranged
between "good" and "poor" (.64 to .33, P<0.001;
extremes of 95% CI, .82 to .19), but on the Williams test it was below
significance at .13 (95% CI, 0 to .28). However, total error scores
calculated by averaging percentage error rates across all 5 dexterity
tests showed high interrater reliability (r=0.81,
P<0.001). A total error score was therefore used in the
analysis. This was the average score for the 2 raters except
where there was a disparity of >1 point on any trial when consensus
was reached by joint viewing of the video.
Cognitive Performance
Apraxia Assessment23
The subject was asked to produce each of 9 actions. The
instructions were "Show me how you would use
a ... cup ... key ...ball ... pencil ... toothbrush ... hammer,"
and "Show me how you ... salute ... threaten with a
fist ... wave goodbye." If performance was not perfect,
the action was then demonstrated for the subject to imitate. Each item
was scored by the examiner on 3-point scales: 0=unable/gross errors,
1=possible errors, and 2=correct.
Line Cancellation24
A test for visual neglect in which the subject has to put a
pencil mark through each 40 oblique lines scattered across an A4-size
page.
Judgment of Line Orientation (Benton Lines Test)25
A test of visuospatial perception in which the subject has
to identify short oblique lines that are at matching angles to the
horizontal. The score is the number of correct matches with a
correction for sex and age.
Token Test Parts I and V26
A measure of receptive dysphasia in which the subject has to
follow verbal commands by moving colored tokens.
Grip Strength
A Jamar dynamometer (model 0030J4) was used to measure grip
strength over 3 trials (alternating with trials using the contralateral
hand). The dynamometer was held in front of the subject so that a
comfortable power grip was possible with the elbow slightly flexed.
Statistical Analysis27
Means were compared by using analysis of
covariance. The factors were stroke (stroke or control group)
and side (left hand or right hand used), with age in years removed as
the covariate. Interactions were explored by using t tests
for simple effects. Hypotheses regarding correlations between
variables were tested using controlled stepwise multiple regression
to assess the effect of a selected variable(s) once others were
partialed out.
| Results |
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The mean percentage error rate (see "Subjects and Methods")
provided a summary measure for all types of error across the 5 tasks
(the 4 subtests of the Jebsen plus the Williams test). Figure 1
shows the resulting scores.
Analysis of covariance (with age as the covariate)
showed a large main effect of stroke
(F(1,59)=16.3, P<0.001) but no
significant stroke xside interaction
(F(1,59)=0.8, NS). The trend toward poorer
performance with the left hand failed to reach significance
(main effect of side, F(1,59)=2.3, NS), and
removing the 2 left-handed RCVA patients did not affect this
result.
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Across the 5 tasks, the mean time for completion was 12.3 seconds for
the LCVA group, 8.3 seconds for the LC group, 9.2 seconds for RCVA, and
8.1 seconds for RC. To obtain a better measure of speed, which gave
equal weighting to each task, the performance of control
subjects was used to construct standard scales for each task (mean of 0
and SD of 1). The mean for times expressed as standard scores are shown
in Figure 1
. Analysis of covariance (with age as
the covariate) showed a significant interaction between stroke groups
and controls (F(1,59)=7.12,
P=0.01).This interaction remained if the 2 LCVA cases with
bilateral damage were removed (F(1,57)=4.2,
P<0.05). Figure 1
shows that this interaction arises
because the LCVA patients were very much slower than their control
group (t(31)=4.03, P<0.001), whereas
those in the RCVA group were only slightly slower
(t(29)=2.41, P<0.05).
Cognitive Performance
Dysphasia
Table 3
shows that, as expected,
only the LCVA group was impaired compared with controls on the Token
Test (strokexside interaction, F(1,59)=26.0,
P<0.001)). Eight LCVA patients scored less than 20 of 32
and were definitely dysphasic. A direct contrast of LCVA and RCVA
groups confirmed significantly poorer performance for the
former (t(28)=5.33, P<0.001), whereas
the LC and RC groups showed no significant difference
(t(32)=.45, NS).
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Apraxia
Table 3
shows that the LCVA group was impaired on both
action to verbal command and on action imitation. On imitation, 10 of
the 15 patients were poorer than any control. Two RCVA patients scored
15 of 18 on action imitation, but otherwise patients in this group were
unimpaired, and the strokexside interaction was highly significant
(F(1,59)=14.8, P<0.001). A direct
contrast of LCVA and RCVA groups confirmed significantly poorer
performance for former (t(28)=3.88,
P=0.001), whereas the LC and RC groups showed no significant
difference (t(32)=.08, NS)
Visuospatial Deficits
Members of the RCVA group were impaired on line cancellation. No
control subject or LCVA patient omitted any lines, whereas 4 RCVA
patients made omissions. There were no cases of severe visual neglect,
with the maximum number of omissions to the left being 2. On the Benton
Lines test, 3 aphasic patients were unable to comprehend the test and
were unassessable. Table 3
shows that for the remaining subjects
there was a large main effect of stroke
(F(1,56)=12.9, P=0.001), with the LCVA
and RCVA groups showing a similar level of impairment.
Grip Strength
Table 3
shows that there was a wide range of grip strength
within both stroke and control groups, probably reflecting normal
variation with age and sex. Analysis of covariance
confirmed that these variables were significant covariates of grip
strength (P<0.001 for both). Mean scores corrected for age
and sex were LCVA=19 kg, LC=34 kg, RCVA=22 kg, and RC =28 kg. The
effect of stroke was highly significant
(F(1,58)=17.6, P<0.001), but the
trend toward differential impairment of the LCVA group did not reach
significance (strokexside interaction,
F(1,58)=3.2, P=0.07).
Correlates of Impaired Everyday Dexterity
The relationship between impairment on the dexterity simulation
tests and performance on other measures was analyzed
both in terms of group regression analyses and individual case
profiles.
Multiple Regression
For each of the stroke groups, multiple regression was used to
investigate the extent to which the summary measures for speed and
accuracy of dexterity could be predicted from variables of
increasing complexity. The starting point was to look at the predictive
value of age and sex alone and then to include in the equation simple
motor function (grip strength). The cognitive measures of aphasia,
apraxia, and visuospatial deficit were then compared as final additions
to the regression equation. The results are illustrated in Figure 2
, which shows the changes in
R2 as variables are entered into
the equation with adjustment for the number of variables in the
equation at any point.27
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Figure 2
shows that for the RCVA group, visuospatial scores
significantly predicted dexterity errors, whereas none of the other
variables approached significance. There were no significant
predictors of dexterity speed for this group. For the LCVA group, there
was a different pattern of results for dexterity errors and speed.
Dexterity errors were predicted only by action imitation scores. Grip
strength showed a nonsignificant trend (P=0.08). In
contrast, dexterity speed was not predicted by action imitation, but
sex and age had a significant effect, with a further significant
increase in R2 when ipsilateral grip
strength was added into the equation. There was no further significant
increase in R2 when any of the
cognitive variables was entered.
Single Case Associations and Dissociations
These multiple regression analyses therefore indicated
that 3 experimental variables predicted dexterity: action imitation
score, visuospatial score, or grip strength. The strength of these
predictors was explored at the single case level by categorizing scores
as "abnormal" (beyond the range for normal controls), "poor"
(within the range of control scores but below the 10th percentile), or
"normal" (at or above the 10th centile for controls).
Table 4
shows that all LCVA patients who
had abnormally high error rates on the dexterity tests were also
apraxic on action imitation. However, 1 apraxic patient had normal
error rate and speed on the dexterity tests. For the RCVA group, the
relationship between high dexterity error rates and visuospatial
problems was also imperfect: 1 patient was normal on dexterity but made
an error on the cancellation test, and 1 patient had a high dexterity
error rate but was normal on visuospatial tests.
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All LCVA patients who had abnormally weak ipsilateral grip were slow on the dexterity tests, and in 2 of these cases this was an isolated deficit with normal error rates for the dexterity tests. No such relationship was apparent for the RCVA group, despite 5 patients whose grip strength fell below the normal range.
Additional Neurological Variables
Degree of paresis of the contralateral arm as measured by the
Extended Motricity Index was not a correlate of ipsilateral dexterity
speed or accuracy for the LCVA or RCVA group (r<.3, NS, for
all). A comparison of the 7 patients judged to have posterior frontal
and no parietal damage with the remainder showed no significant
differences for dexterity speed or errors (Mann Whitney U
tests, P>0.1 for all).
| Discussion |
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Our results indicate that these dexterity problems are probably due to cognitive deficits affecting perception and control of action. Others4 10 have suggested that ipsilateral sensorimotor losses might be important for hand function. We found that ipsilateral grip strength was reduced, but this coexisted with normal dexterity for patients with right hemisphere damage, indicating that this mild weakness was not a sufficient cause for dexterity problems. We did not measure strength in ipsilateral proximal muscles that might be more impaired,28 nor did we assess sensation. We cannot, therefore, exclude the possibility that these unassessed aspects of sensorimotor function were important for dexterity. However, our analyses of errors on the dexterity tasks and of correlations with performance on cognitive tests showed varying patterns of impairment of dexterity that appeared characteristic of the cognitive deficits seen after right or left hemisphere damage.
Impaired ipsilateral function has been reported in studies that have excluded patients with obvious cognitive impairment,4 10 but our results indicate that mild deficits in cognition are sufficient to impair dexterity. The presence of milder cognitive deficits could therefore account for the findings in those studies, particularly as the impairment they reported was most apparent on more complex tasks demanding precise visuomotor control, such as tracking moving targets.4 In summary, we believe that while unilateral hemisphere stroke does lead to some slight ipsilateral sensorimotor impairments, particularly early after stroke, it is impairment at a higher, cognitive level which has implications for everyday dexterity. The nature of these cognitive deficits will now be considered.
Ideomotor Apraxia
This study confirmed previous research2 in showing a
high incidence of inability to imitate actions among patients with left
hemisphere damage. This is widely accepted as a defining feature of
ideomotor apraxia, which is thought to be a problem in the mental
representation of action or posture.14 15
Consistent with this theory, the multiple regression
analysis showed that severity of impairment of action imitation
after left hemisphere damage was predictive of the error rate on
dexterity tasks. Also, the problems in orienting the spoon that were
observed in the bean-spooning task strongly suggested an inability to
remember or perceive the correct action. On the other hand, the
association between impaired action imitation and frequent dexterity
errors was not perfect. In particular, 1 patient who was severely
impaired on action imitation was at the normal level on all dexterity
tasks. On balance, we feel that the multiple regression results plus
the video error analysis argue strongly for the validity of the
concept of ideomotor apraxia as a major cause of dexterity problems
after left hemisphere damage, and that dissociations with action
imitation performance in some cases may arise from patient
variability over time or the limitations of our methods of
assessment.
A puzzle for researchers in this area has been anecdotal evidence that apraxic patients behave normally in everyday settings. So, De Renzi et al2 comment, "The most striking dissociation found in apraxic patients is their inability to perform on command an action which is perfectly executed when roused by a congruent situation: eg, waving goodbye when the doctor is leaving." Furthermore, some studies have found no correlation between scores on action imitation tests and performance on tests of motor skill, such as pegboard performance,7 repetitive motor sequence learning,8 or reaction time.13 The present study offers a resolution to these problems. First, a general observation was that all our patients were finally successful in completing the dexterity tasks and that their clumsiness was often only evident from detailed video analysis. The apparent normality of apraxic patients in everyday settings may therefore simply reflect the subtle nature of their deficit, which becomes clinically obvious only under the controlled conditions of an action imitation test. Second, the failure of some studies to find correlations with tests of motor skill can be explained by the reliance of those studies on measures of speed rather than error. An important finding in the present study was that apraxia appeared to have a consistent effect on error rate but not speed. This is in agreement with other studies7 8 which have found that apraxic patients have increased error rates on motor tasks and that apraxic movement is characterized by spatial disturbance rather than by abnormalities in the timing of movements.15
Slowing After Left Hemisphere Damage
Patients with left hemisphere damage were often slow in their
performance of the dexterity tasks. This is consistent
with a body of research showing that left hemisphere damage causes
greater problems than right-sided damage on tasks which require rapid
or accurately timed responses5 8 and has led to the
hypothesis that the left hemisphere is dominant for the control of
preprogrammed, ballistic movements.9 A new finding from
this study was the correlation between slowing and weakness of
ipsilateral grip. The absence of any such correlation for the RCVA
group suggested that weakness was not in itself the cause of slowing.
Perhaps the correlation for the LCVA group was due to the anatomic
proximity in the left hemisphere of areas that are the origin of
ipsilateral corticospinal pathways and areas that may be important for
ballistic control. The anatomic data in this study was not detailed
enough to test this hypothesis. What is certain from this and previous
studies is that the slowing seen after left hemisphere damage cannot be
attributed to apraxia and, therefore, that there is a separate
underlying deficit which affects dexterity in this group.
Visuospatial Deficits
The multiple regression analysis showed that visuospatial
deficits (omissions on line cancellation or problems in judgment of
spatial orientation) were predictive of dexterity error rates for the
RCVA group. Also, the errors observed on the dexterity tasks suggested
problems of visual attention or spatial judgment. There was no such
association in the LCVA group despite equivalent performance on
the Benton Lines test. However, dysphasia or dyslexia can impair
comprehension of this task. Benton et al25 suggest that
performance may not reflect visuospatial ability when patients
are "aphasic and confused," and there was no evidence of
visuospatial problems within the LCVA group on the line cancellation
test, which all patients could readily comprehend. In summary, although
these results are not completely clear cut, they are consistent
with the proposal that visuospatial deficits were the major cause of
dexterity errors after right but not left hemisphere damage. This is in
agreement with previous research indicating reduction in the accuracy
of rapid reaching for targets due to mild visual neglect or spatial
disorientation after right hemisphere damage.5 9
Clinical Implications
The presence of subtle losses in dexterity particularly after left
hemisphere stroke has clinical implications. There has been an
understandable tendency to ascribe clumsiness in use of the ipsilateral
hand to normal difficulty in learning to use the nondominant hand for
most tasks, whereas this study makes it clear that these patients are
also struggling against high-level deficits in skilled motor control.
This may have an impact at 2 levels: first, it may slow or reduce the
acquisition of left hand skills to compensate for hemiplegia, and
second, these deficits may impair relearning of control of a
hemiparetic arm. A follow-up study of patients at 6 months after stroke
will attempt to describe the impact of these obstacles to recovery and
the potential for therapeutic intervention.
| Acknowledgments |
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Received October 5, 1998; revision received February 9, 1999; accepted February 9, 1999.
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