relation of cerebral blood flow to motor and

309

Relation of Cerebral Blood Flow to Motor andCognitive Functions in Chronic Stroke Patients

Sakan Mori, MD; Seizo Sadoshima, MD; Setsuro Ibayashi, MD;Kozo lino, MD; Masatoshi Fujishima, MD

Background and Purpose The aim of this study was toexamine the levels of cerebral blood flow in relation to motorand cognitive functions in 300 chronic unilateral stroke pa-tients (age, 6412 years; meanSD).

Methods Cerebral blood flow was measured by the 133Xeinhalation method, adjusted for age, sex, and Pco2 level. Motorfunction was scored according to Brunnstrom hemiplegicstaging and cognitive function according to the Hasegawadementia rating scale tested in Japanese.

Results Asymmetries of blood flow between affected andnonaffected hemispheres increased with lesion size and werehighest in 11 embolic strokes (209%) and higher in 80nonembolic cortical infarctions (11 11%) and 76 hemor-rhages (9 7%) than in the group of 133 subcortical infarctions(26%) or 16 control subjects (12%). Severity of hemipare-sis con-elated with decreased cerebral blood flow in theaffected hemisphere (P

310 Stroke Vol 25, No 2 February 1994

lisms were cardiogenic. Among 80 nonembolic cortical infarc-tions, 71 were thrombotic and 9 were undetermined. Embolicstroke was not observed among subcortical infarctions. Therewere 76 patients with lacunae among 133 patients with sub-cortical infarctions. All hemorrhages were located in subcor-tical regions. Control subjects had no brain lesions by CTstudies. Follow-up studies of CT were performed at themeasurements of CBF to confirm that edema or hematomahad disappeared and that there was no recurrence of stroke.The size of the hematoma was estimated as an oval shape by[3.14 x (length/2) x (width/2)] of the hyperdense lesion in theslice showing the maximum area at the acute stage. The size ofthe infarcted lesion was estimated as an oval or a rectangle bymultiplying the maximum length times width of the hypodenselesion in the slice showing the largest area at the chronic stage.

Regional CBF was measured by the 133Xe inhalation techniqueusing a 22-probe (11 over each hemisphere) Novo-Cerebrographwith the patient in the resting condition with eyes closed, asdescribed previously.19-20 The 133Xe gas mixture with air (3mCi/L) was administered by means of a close-fitting face maskfor 1 minute, and 1MXe clearance curves were examined for 10minutes. The clearance curves were subjected to two-compart-ment analysis,21 and the initial slope index22 was used, since thisis one of the most reliable flow parameters, relatively unaffectedby compartmental instability (slippage) that may occur in thetwo-compartment analysis.21-22 The values from each detectorwere calculated and averaged to determine mean hemisphericCBF. Levels of blood pressure, expired end-tidal PCO2 (Pecc^),hematocrit, and hemoglobin concentrations were simultaneouslyrecorded. All CBF values were corrected to the Peco? level of36.5 mm Hg, according to Maximilian et al23:

CBF-0.75x(PeCO2-36.5)Mean Peco2 (SD) for the entire sample was 34.63.7.Decrease in CBF was counted as significant when the valueswere under - 2 SD from those of control subjects (35.1milliliters per 100 grams per minute for the affected hemi-sphere and 34.8 milliliters per 100 grams per minute for thenonaffected hemisphere). The differences in CBF in affectedand nonaffected hemispheres were expressed as percent asym-metries according to Mosmans et al14:

% Asymmetry=-

JCBF in nonaffectedllcBF in affectedl[ hemisphere J [ hemisphere J

mean CBF of both hemispheres -X100

All CBF measurements were made at least 1 month afterstroke. The CBF measurements were done at 192 300 days(median, 64) after the onset of stroke. Raw scores for CBFdecreased with advancing age in the affected (-0.19 millilitersper 100 grams per minute per year, P

Mori et al Motor and Cognitive Functions and CBF 311

TABLE 1. Characteristics of 300 Patients and 16 Control Subjects

Age, yMale: femaleSystolic blood pressure, mm HgDlastollc blood pressure, mm HgHematocrtt, %Size of lesion, cm2

Cerebral blood flow (ISI), mL/100 gper min

Affected hemisphereNonaffected hemisphereHemispheric asymmetry, %

Scores for Brunnstrom stage (median)FingerArmLeg

Hasegawa dementia rating scaleRisk factors, No. of cases

Hypertension**Diabetes mellitusHypercholesterolemlaAtrial fibrillation**Smoking

Cortical Infarction

Embolicn=11

64137:4

1262079113942615tl|#

308t||368*209t||#t

2.41.7(2)t1|W2.91.9(2)t||*3.31.8(3)t||W

19.98.0t|t*

3 (27%)4(36%)3(27%)5 (45%)3 (27%)

Nonembollcn=80

6612#54:26

1392081 14406198t||#

358fl|387*1111t|

4.11.9(5)t4.31.6(5)t4.61.3(5)t

27.1 6.5

45 (56%)24(30%)17(21%)6(8%)

40 (50%)

SubcortlcalInfarction

n=1336510#82:51

13922821339532

40741 6

26

4.7+1.5(5)4.81.4(5)5.01.1 (5)

28.76.2

97 (73%)53(40%)29(22%)3(2%)

59 (44%)

Hemorrhagen=76

581240:36

138208512405125t||

36 + 6fj|39 6*97fl|

4.01.7(4.5)t4.11.4(4)t4.51.2(5)t

27.85.3

55(72%)15(20%)15(20%)1 (1%)

23(30%)

StrokePatients(Total)n=300

6412183:117138218213395t109t

378t396t79t

4.31.8(5)t4.4+1.5 (5)t4.71.3(5)t

27.76.3*

200 (67%)96 (32%)64(21%)15(5%)

125(42%)

Controln=16

63710:6

14320801543500

444445

12

6.00.0 (6)6.00.0 (6)6.00.0 (6)

31.1 0.9

11 (69%)4 (25%)1 (6%)1 (6%)

4 (25%)ISI Indicates Initial slope Index.Values are meanSD. *P


TABLE 2. Reductions In Cerebral Blood Flow Within Bilateral or Unilateral Hemisphere In 300 Chronic Stroke Patients

Age, yMale: femaleSystolic blood pressure, mm HgDlastolic blood pressure, mm HgHematocrlt, %Size of lesion, cm2

Cerebral blood flow (Initial slope Index)Affected hemisphere, ml_/100 g per minNonaffected hemisphere, ml_/100 g per minHemispheric asymmetry, %

Brunnstrom stage (median)FingerAimLeg

Hasegawa dementia rating scale

BilateralReduction

n=67641242:25

1352182134051311t

284t31 3t1111t*

3.51.9(3)t3.71.6(3)t4.01.3(4)f258t

Hemispheric Cerebral Blood Row

UnilateralReduction

n=52621034:18

1342081 143941510t

322t382t168t

3.41.8(3)t3.71.6(3)t4.21.4(4)t27 6*

MinimalReduction

n=1816412

107:7414121

831339588

425

43535

4.81.5(5)4.9+1.3(5)5.1 1.0 (5)295

Values are meanSD.*P


D)2EoU)ccIJm

p


Affected Hemisphere

60-sI 50E 40-

5 30-

20-O X

Nonaffected Hemisphere

e

60

50

40"

30

20

10 15 20 25 30 0 5 10Hasegawa Dementia Rating Scale

15 20 25 30

FIG 2. Scatterplots showing relation between scores on Hasegawa dementia rating scale and cerebral blood flow (initial slope index)in the affected (left panel) and nonaffected hemispheres (right panel) in 300 patients with chronic stroke. Lines represent linearregression fits to the data points (P


tendency of CBF behavior in the same group of pa-tients. The major findings in the present study may besummarized as follows: (1) the severity of hemiparesiscorrelated directly with the severity of decreased CBFin the affected hemisphere and with increased asymme-tries of CBF between affected and nonaffected hemi-spheres, and (2) declines in cognitive function wereclosely related to decreased CBF in the nonaffectedhemisphere (or bilateral CBF reductions), left hemi-spheric lesions, and embolic strokes.

In chronic stroke patients, the degree of CBF reduc-tions in the affected hemisphere (or CBF asymmetries)correlated with the severity of the stroke and the extentof the lesions.19 As previously reported in patients withchronic putaminal hemorrhage,36 CBF reductions in theaffected hemisphere correlated with the maximum he-matoma volume in the acute stages, which may directlyreflect the extent of the lesion. In patients with deep-seated lesions, CBF reductions ipsilateral to the lesionmay be predominantly remote effects37 called transneu-ronal depression. Asymmetries of CBF were greater inpatients with cortical infarctions and hemorrhages thanin those with subcortical infarctions. The larger extentof lesions in the cortex or subcortex may be reflected bythe greater asymmetries, as shown in our data.

Bilateral CBF reductions were observed in 22% of allthe patients, but the mechanisms are not fully known.Five possible explanations were considered: (1) trans-hemispheric diaschisis,416-18 (2) systemic circulatory dis-turbances,13 (3) underlying cerebral arterial changesassociated with risk factors,15 (4) interhemisphericsteal,38-39 and (5) decrease in global neuronal activitiesafter stroke.16 First, a number of studies of CBF1618 andmetabolism4'40'41 have emphasized the evidence of trans-hemispheric diaschisis. Second, there was no heartfailure, orthostatic hypotension, or other severe sys-temic circulatory disturbances present in our patients.Third, hypertension42 and other risk factors such assmoking43 and hyperlipidemia44 may play an importantpart in diffuse reductions of CBF. From our data,however, this is an unlikely explanation because thefrequency and presence of such risk factors were similarbetween patients with bilateral and unilateral CBFreductions. Therefore, incidence of cerebrovascularchanges associated with risk factors may be similarbetween two groups except for the embolic patients. It isnot known whether CBF was already reduced before thestroke in patients showing bilateral CBF reductions;however, after the stroke, decreased CBF in the contra-lateral hemisphere appeared to correlate with globaldecreases in cognitive function. We assume that amongpatients suffering from declines in physical, mental,daily living, and social activities after stroke,45 globalneuronal activities become decreased and CBF also maydecrease in the contralateral hemisphere, coupling withdecreased metabolic demands. Unilateral lesions weredetermined by clinical examinations and brain CT find-ings; more strict criteria using magnetic resonance im-aging, cervical and transcranial Doppler ultrasonogra-phy, and cerebral angiography would be required toavoid the coexistence of asymptomatic cerebrovascularchanges and to reveal the mechanism of bilateral CBFreductions.

Even during rehabilitation, 73% of our patients stillsuffered motor deficit after recovery from stroke. The

severity of hemiparesis correlated well with the degTeeof decreased CBF in the affected hemisphere andincreased CBF asymmetries. The present results are inaccord with previous reports that higher asymmetriesare associated with neurological disability scores1314and angiographic findings,14 which primarily reflect se-verity of brain damage. Declines in motor functionmainly are due to neuronal damage of the motorpathways, including the motor cortex, internal capsule,and basal ganglia. A larger size of lesion is primarilyresponsible for more severe motor impairment. How-ever, anatomic localization for motor functions based onCT findings are reported to be different for eachpatient.46 A decrease in cortical blood flow (includingmotor cortex) ipsilateral to the lesion that is due directlyto the cortical lesion, indirectly to transneuronal depres-sion of the ipsilateral cortex from a subcortical le-sion, 17.37,40,41

o r ( j u e t o ipsilateral cerebrovascularchanges appears to be one possible explanation forsevere motor impairment. We speculate that even insome cases with small-sized, deep lesions, decrease incortical neuronal activities, which may be coupled withdecreased CBF, on the same side of the lesion may be inpart associated with more severe motor deficits, result-ing in increased asymmetries of CBF. We confirmedthat asymmetry of CBF may be useful for evaluatingmotor impairments even after full recovery from stroke.

Cognitive scores correlated well with CBF in bothhemispheres. In contrast to motor function, individualside-to-side asymmetries may have little significance oncognitive function, mainly because of bilateral CBFreductions.41 Decrease in cortical blood flow contralat-eral to the lesion resulting in bilateral CBF reduction bydecreased neuronal activities caused by transhemi-spheric diaschisis18'40'41 and declines in physical, mental,daily living and social activities45 may partially contrib-ute to severe cognitive impairment. Our study suggestedthat left hemispheric lesions among patients havingbilateral CBF reductions are important contributors todeclines in cognitive functions despite higher globalCBF than patients with right hemispheric lesions. Itappears, therefore, that left hemispheric lesions aremore responsible for cognitive impairments than thoseaffecting the right hemisphere. Impaired accuracy ofresponses47 and slower response time48 to multiple-choice paradigms have been reported among patientswith left hemispheric brain damage compared with righthemispheric damage. Robinson et al49 reported post-stroke depression to be associated with global intellec-tual impairments, especially with left anterior lesions.Thus, impaired processes for cognition, and possiblymood changes, may be responsible for global cognitivedecline in patients with left hemispheric lesions.

Patients with embolic stroke that was correlated withcognitive impairment (Table 3) showed the largest sizeof lesion (Table 1). Although lesion size failed to becorrelated with functional scores by multiple regressionanalysis, we cannot deny the primary importance oflesion size, which was closely correlated with individualfunctional impairment by simple regression analysis. Wedoubt that the lesion size is very important for func-tional outcome.50-51 In patients with multiple infarcts,intellectual impairment was correlated with infarct vol-ume.52 The main reason for our failure may be that wecould not detect the precise size of the irregular shape

by guest on April 4, 2015http://stroke.ahajournals.org/Downloaded from


of lesion by two-dimensional analysis. More accuratemorphological estimation of lesion volume by three-dimensional analysis would be required.

HDS scores correlated well with CBF reductions andwith other intelligence tests, as previously reported.911-12In chronic stroke patients with dementia, the mean valuesfor CBF are reduced bilaterally, which is a characteristicdifference from that of patients without dementia.10 Fur-thermore, CBF reductions in frontal and temporal cortex(bilaterally) and thalamus have been reported to correlatewith severity of cognitive impairment in patients withmulti-infarct dementia.12 The technique of 133Xe CBFmeasurement is greatly biased toward cortical lesions, andwe cannot detect CBF in deep structures by this technicallimitation. We have recently shown that CBF reductions inthe deep white matter measured by positron emissiontomography (PET) are associated with declines in oxygenmetabolism in demented patients.53 Although the associ-ation of cognitive dysfunction and bilateral reduction inCBF may be complex and multifactorial, further examina-tions concerning cerebral metabolic changes by PET stud-ies could reveal direct metabolic functional relations.

The brain is a complex organ having many structuraland functional components that not only operate sepa-rately but also cooperate with each other through neu-ronal pathways to maintain integrated function. Clinicalimplications of these complex and multifactorial phenom-ena should be done carefully. We preliminarily assessedthe relation between CBF and brain functions in 300unilateral stroke patients after full recovery from stroke.Despite limitations on methods and interpretations, ourfindings may give information about different tendenciesof CBF behavior associated with the functional impair-ments among the same group of patients. We confirmedthat severity of hemiparesis correlates with the degree ofCBF asymmetries between affected and nonaffectedhemispheres and thus reflects the extent and location ofthe lesion in the affected hemisphere. In contrast, bilateralreductions in CBF resulting from a left hemispheric lesioncontribute to declines of cognitive function. The precisemechanism of this phenomenon is not yet known. It wouldbe interesting to further analyze the possible relationsamong the lesion size, cerebral metabolism, vascularchanges, and brain-specific functions. Follow-up study ofCBF may also be useful to interpret clinical consequences.

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S Mori, S Sadoshima, S Ibayashi, K Lino and M FujishimaRelation of cerebral blood flow to motor and cognitive functions in chronic stroke patients.

Print ISSN: 0039-2499. Online ISSN: 1524-4628 Copyright 1994 American Heart Association, Inc. All rights reserved.

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