(Stroke. 2000;31:1365.)
© 2000 American Heart Association, Inc.
Original Contributions |
Improved Functional Outcome in Patients With Hemorrhagic Stroke in Putamen and Thalamus Compared With Those With Stroke Restricted to the Putamen or Thalamus
From the Department of Neurology (I.M., J.K.), Toneyama National Hospital, Osaka, Japan; Bobath Memorial Hospital (T.S.), Osaka, Japan; and Department of Neurology and Neuroscience (B.T.V.), Cornell University Medical College, The Burke Medical Research Institute, White Plains, NY.
Correspondence to Ichiro Miyai, MD, PhD, Department of Neurology, Toneyama National Hospital, 5-1-1, Toneyama, Toyonaka City, Osaka, 560-8552, Japan. E-mail webeo{at}ga2.so-net.ne.jp
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Abstract |
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Background and Purpose—We analyzed the effect of late intensive inpatient rehabilitation on the functional outcome of patients with subcortical hemorrhagic stroke.
Methods—Patients who were nonambulatory with hemorrhagic stroke in the internal capsule and putamen (n=55), the thalamus (n=24), or all 3 regions (n=15) underwent intensive inpatient rehabilitation. Patients with surgical intervention or an episode of ventricular hemorrhage were excluded. Lesion location was evaluated by MRI 4 months after the ictus.
Results—Demographic data, initial disability, and impairment measures were comparable in the 3 groups. Functional outcome demonstrated significant differences in mobility subscores (P<0.05) of the Functional Independence Measure such that patients with injury in the 3 regions were more likely to ambulate independently than were patients in the other groups. Lesion location data demonstrated that the ventral anterior nucleus of the thalamus was always spared; the ventral posterior (lateral and medial) nucleus was always damaged, and the ventral lateral nucleus was frequently damaged. Putaminal damage always included the postcommissural area. In addition, the entire posterior half limb of the internal capsule was always damaged.
Conclusions—Subcortical lesions to multiple structures in the basal ganglia–thalamocortical motor circuits permitted enhanced motor recovery. Lesion location predicted the level of independent ambulation and the rate of recovery in patients with stroke who were nonambulatory before neurorehabilitation therapy.
Key Words: cerebral hemorrhage • putamen • rehabilitation • thalamus
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Introduction |
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Outcome and functional imaging studies have demonstrated that recovery mechanisms proceed at different rates1 2 3 4 and as a function of lesion size and location.5 6 7 Furthermore, they have enhanced an understanding of the pathogenesis of the late consequences of stroke by suggesting candidate brain regions that may underlie recovery. For example, recent studies have demonstrated that middle cerebral artery stroke in which damage extends to the premotor cortex (PMC) has been associated with poor functional outcome.8 9 Clearly, damage that includes the parallel outputs from the primary motor area, PMC, and supplementary motor area (SMA) magnifies the functional disability and diminishes the response to rehabilitation efforts.10 11 12 These structure-function relationships prompted us to test whether location of damage restricted to the subcortical structures (putamen [Pt] and thalamus [Th]) differentially affected functional outcome. Neuroimaging information was obtained during a chronic stable phase after hematoma and edema resolution.
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Subjects and Methods |
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We screened 132 consecutive patients with subcortical hemorrhage and without a previous history of cerebrovascular disease. The conventional treatment required patients to remain in the local acute care hospitals and receive some physical therapy for 2 to 3 months. Patients who remained persistently dependent and nonambulatory were transferred to the Bobath Memorial Hospital for inpatient rehabilitation. On average, 106 days (±6 SEM) after the acute stroke, the patients who were persistently nonambulatory began this study and their rehabilitation.13 Patients with severe medical complications (n=17) participated in abbreviated programs, but they were excluded because they were not available for weekly assessments. Patients with isolated motor or visual deficits (n=14) were excluded in favor of patients with more severe deficits in motor, vision, and sensory processing.14 Patients who required surgical intervention (n=20) or who sustained ventricular hemorrhage (n=12) were excluded. With these criteria, 94 patients with subcortical hemorrhage with motor, vision, and sensory deficits were identified for further study.
The location and distribution of the lesion were specified with MRI (1.0-T superconductive; Shimadzu, MAGNEX Epios10, 8.5 mm, slice thickness) that included T2-weighted (repetition time 3630 ms, echo time 110 ms) axial spin echo images and T1-weighted (repetition time 500 ms, echo time 15 ms) axial spin echo images. MRIs were taken an average of 4 months after the ictus. The rationale for this timing is delineated later. On the basis of image anatomic information, patients were divided into 3 groups: those with damage to the Pt (n=55), Th (n=24), and Pt and Th (P+T; n=15). Lesion volume was calculated with NIH Image Version 1.60.9
There is information about the change in hemorrhage size over time with CT images15 ; less information is available for MRIs, so in 7 patients, we evaluated the change in the size of the hematoma with serial T1- and T2-weighted images taken on admission and repeated every 2 months. Lesion density maps for each patient were made with the use of standardized horizontal templates16 and NIH Image 1.60.
At Bobath Memorial Hospital, all patients participated in
rehabilitation according to the standards of the neurodevelopmental
technique, which includes one 45-minute session of physical therapy and
one 45-minute session of occupational therapy, 5 days a
week.13 17 On admission and discharge, functional outcome
was evaluated with the use of standardized measures of documented
reliability: the Functional Independence Measure (FIM) for
disability18 and the Stroke Impairment Assessment Set
(SIAS) for neurological impairment.19 20 We also
analyzed motor and cognition subscores of FIM. Motor subscores
of SIAS (0 to 25) consist of 2 tests for the upper extremity (0 to 10)
and 3 tests for the lower extremity (0 to 15). Sensory subscores of
SIAS (0 to 12) evaluate superficial sensation and deep sensation of the
affected upper (0 to 6) and lower (0 to 6) extremities. The sitting
balance subscore of SIAS ranges from 0 (cannot sit without support) to
3 (normal sitting balance). Trained nurses rated the FIM, and
physicians, who were blinded to lesion location, rated the SIAS. FIM
evaluation was performed every 2 to 3 weeks, and when FIM score reached
a plateau, the patient was discharged. Interrater reliability for
individual items of SIAS and FIM was estimated with the use of a
weighted 
statistic (n=16).,21 and the correlation
among raters was good to very good (=0.62 to 0.93). Spearman
correlation coefficients across the raters were significant for total
SIAS score (0.944, P<0.0005) and total FIM score (0.973,
P<0.005). These reliability measures have been used and
tested previously.9
Because of the interval impairment and disability outcome measures, the
statistical analysis was performed with the Kruskal-Wallis
test. Demographic data were analyzed with ANOVA and
2 test. Changes in lesion volume was
analyzed with a repeated measures ANOVA followed by a post hoc
test (Fisher’s least significant difference test). The level of
significance was accepted at P<0.05. All statistical
analyses were performed with the use of SPSS for Microsoft
Windows, version 8.0J.
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Results |
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Lesion volume shrank significantly between 2 and 4 months on the T1- and T2-weighted images, but lesion volume was unchanged between 4 and 6 months on both the T1- and T2-weighted images (Figure 1
and Table 1). We used the T2-weighted image
of MRI taken 4 months after hemorrhage to evaluate the site and
volume of lesions, because the border of the lesions was easier to
delineate on T2- than on T1-weighted images. As expected, lesion volume
on T2-weighted image at 4 months after the onset was larger
(P<0.05) in P+T (8.48 cm3) than in Pt
(6.42 cm3) or Th (6.25 cm3)
groups. The incidence of the wallerian degeneration as detected with
MRI22 was comparable in the groups (Table 2). Periventricular
high-intensity areas on T2-weighted images were completely absent.
Lesion location data demonstrated that all groups had an intact
anterior ventral nucleus and damage in the posterior half of the
internal capsule. The Th and P+T groups always had lesions in the
posterolateral ventral nucleus and posteromedial ventral nucleus. The
lateral ventral nucleus was damaged in 18 of 24 patients in the Th
group (75%) and 12 of 15 patients in the P+T group (80%). The Pt and
P+T groups always had damage in the postcommissural area of the Pt
(Figure 2).
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Demographic data are shown in Table 2
. Mean age, days after
stroke, length of stay, Mini-Mental State Examination, sex, and
location of lesion were comparable in the 3 groups. All patients had
hemiparesis and hemisensory deficits (as scored on the
sensory subscale of SIAS). All patients in the Th and P+T groups and
most of the patients in the Pt group had spastic hemiparesis. Six of 55
patients in the Pt group had flaccid hemiparesis.
Baseline scores of FIM and SIAS on admission and gain after inpatient
rehabilitation are shown in Table 3. The
Kruskal-Wallis test demonstrated that the groups were comparable on
admission impairment and disability scales. By discharge, the
analysis revealed significant differences among the groups on
disability measures but not impairment measures. Specifically, there
was a significant difference in the gain of mobility subscore of FIM,
and there were no significant differences in the gain of total FIM
scores, ADL subscores, cognition subscores, motor scores of SIAS, SIAS
for sensation, and SIAS for sitting balance. Subsequent Mann-Whitney
test showed that the gain in mobility subscore of FIM was significantly
higher in the P+T group than in the Th group (P<0.05).
There was a trend indicating the P+T group also gained more on the
mobility subscore than the Pt group (P=0.058).
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These statistical changes have clinical relevance in that 53.3% (8 of
15) of the P+T group were independent in ADL and mobility on discharge,
whereas these levels of functional independence were attained by only
41.8% in the P group and 33.3% in the T group. Because ambulation was
crucial for a discharge to home instead of a long-term care facility,
we performed an additional analysis on the probability that the
lesion site predicted independent ambulation. The probability of
ambulation without physical assistance was 60% (33 of 55) in the Pt
group, 62.5% (15 of 24) in the Th group, and 93.3% (14 of 15) in the
P+T group (2, P<0.05).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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These data demonstrate that patients with stroke who experienced intensive multidisciplinary rehabilitation 3 months later continued to improve their functional outcome, particularly with regard to independent ambulation. The results suggest that patients with sensorimotor deficits after hemorrhagic injury of both the Pt and Th have better functional outcome than those with less extensive hemorrhagic injury limited to either the Pt or Th alone. Significant changes in disability or functional outcome occurred in the context of comparable improvement in impairment among all groups. Because the treatment for each group was similar, the different outcomes may depend on the characteristics of the injury. Indeed, our patients form a special subgroup of those with subcortical hemorrhage; namely, they survived a subcortical hemorrhagic stroke without surgical intervention, and they were evaluated during the initial 4 months after the ictus. Several studies have demonstrated that patients with acute thalamic hemorrhage, particularly with extension to the ventricles, often require surgical intervention and have a poor prognosis.23 24 25
Although the present data cannot specify the mechanism by which combined damage to the Pt and Th (the P+T group) leads to enhanced functional outcome, there are a number of candidate regions crucial for reorganization that were not damaged. In the study patients, the areas that were commonly intact include the PMC, SMA, caudate, globus pallidus, the nucleus ventralis anterior of the Th, and the anterior limb of the internal capsule. Functional imaging information1 2 3 4 and neurophysiological studies of dystonia26 demonstrate that damage in the basal ganglia and Th caused reorganization of cortical function, especially in the PMC and SMA. To these intact anterior motor pathways, there also are intact ipsilateral pathways in the unaffected hemisphere. Recent functional MRI studies of motor recovery demonstrated that 65% to 75% of patients with volumetrically larger lesions had ipsilateral hemisphere activation.6 7 Indeed, the study of motor recovery after stroke with the use of transcranial magnetic stimulation studies has also demonstrated the activation of both contralateral and ipsilateral connections.27 Because the regions of potential reorganization (cortical, subcortical, and anterior limbs of the internal capsule) were common to all 3 groups, it may be that the greater volume of subcortical damage acts to stimulate more effective reorganization. There are emerging precedents for this possibility.10 11 28
Disability measures, FIM mobility scores, and ambulation demonstrated greater improvement in P+T than in Pt or Th, but there were no significant differences in the change in impairment scores. Our previous report demonstrated that disability recovery might occur without a change in impairment.12 In fact, there are several precedents for significant reduction in disability without change in impairment score.29 30 In general, rehabilitation efforts have been concerned with compensation for function rather than amelioration of neurological deficit. As our understanding of the pathogenesis of disability grows, it may be possible to focus on changing the level of impairment, too.31 32 33
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Acknowledgments |
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This work was supported by funds for the comprehensive research on aging and health in Japan. We thank Naomi Hoshina for assistance with data collection.
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Footnotes |
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A preliminary version of this study was presented at the 2nd World Congress in Neurological Rehabilitation, Toronto, Canada, 1999.
Received August 9, 1999; revision received March 6, 2000; accepted March 6, 2000.
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