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Article history: Background: : Stroke patients experience postural instability that can impede functional improvements in
Received 10 November 2008 their gait. However, the precise functions of the dominant and non-dominant hemispheres in controlling
Received in revised form 2 February 2010 static standing posture and weight-bearing remain unclear.
Accepted 7 February 2010
Objective: : To investigate differences in balancing ability between right-handed patients with right and
Available online 12 March 2010
left hemispheric lesions.
Methods: : Weight shifting was quantitatively evaluated to determine the ability of patients to control
Keywords:
their balance in a static posture and during conscious weight shifting onto the paretic or non-paretic leg.
Instability
Weight shift
Participants were enrolled from a consecutive series of stroke patients attending a rehabilitation program
Stroke (n = 49; 31 male, 18 female; mean age 69.3 ± 9.4 years). Age-matched normal controls were recruited as
Right hemisphere volunteers (n = 12; 4 male, 8 female; mean age 67.9 ± 4.9 years).
Anosognosia Results: : Patients with cortical lesions in the right hemisphere were able to shift less weight onto the non-
paretic leg than patients with cortical lesions in the left hemisphere (p < 0.05). There were no correlations
between the existence of unilateral spatial neglect and the percentage of weight shifted onto the non-
paretic leg, static standing posture (r = 0.27, p = 0.40) or dynamic standing posture (r = −0.37, p = 0.24). In
contrast, there was a significant correlation between the percentage of weight consciously shifted onto
the non-paretic leg and the existence of anosognosia (r = 0.74, p = 0.006), but not between static standing
posture and anosognosia (r = −0.15, p = 0.63).
Conclusion: : Patients with right cortical hemispheric lesions were able to shift less body weight onto
their non-paretic leg. These patients should be encouraged to practice shifting their weight towards their
non-paretic leg to improve their balance.
© 2010 Elsevier B.V. All rights reserved.
0303-8467/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.clineuro.2010.02.006
F. Ishii et al. / Clinical Neurology and Neurosurgery 112 (2010) 406–412 407
2.1. Participants We screened the patients with right hemispheric cortical lesions
(RCI) for the presence of unilateral spatial neglect using a standard-
Japanese patients with clinically and neuroradiologically diag- ized test battery, including line crossing and line bisection, which
nosed stroke were recruited (n = 49; 31 male, 18 female; mean form part of the Behavioral Inattention Test (BIT) [18]. Anosognosia
age 69.3 ± 9.4 years). Participants were medical admission patients was assessed using Bisiach’s scale [19].
from Nagoya City University Medical Center and were registered
as a consecutive series of right-handed stroke patients who were 2.3. Apparatus
attending a rehabilitation program. The inclusion criteria were: (i)
right-handed; (ii) being able to stand alone; (iii) neuroradiologically Weight-bearing was assessed using F-scan Tactile Sensor
verified single vascular lesion in the territory of the middle cere- System computerized force platforms, as described previously
bral artery of one hemisphere, and (iv) within 10–30 days of onset (Tekscan Inc., Boston, MA, United States). Briefly, the sensor was
at the start of the study (Fig. 1). To eliminate potential effects of composed of thin films (0.1 mm) that displayed electrical resistance
varying degrees of neurological dysfunction, including motor, sen- proportional to the physical forces applied. The system consisted of
sory and cerebellar function, all the registered participants were a single platform connected to a personal computer allowing inde-
in Brunnstrom stage 5–6, with no neurological sensory or cerebel- pendent real-time or recorded measurements of the vertical force
lar dysfunction [16]. Patients who were able to bend their knee between the feet and the surface of the platform [20].
joint while maintaining an extended position of the hip joint were
included. Any patients who were unable to understand the study 2.4. Procedures
were excluded. The vibration sense, joint position sense, pain sense,
touch sense and cerebellar ataxia were examined neurologically, Weight-bearing measurements were performed in three differ-
and patients with neurological sensory or cerebellar dysfunctions ent standing positions. In the first series, participants were asked to
were excluded. Patients with contraversive pushing were also stand with a level, shoulder-width stance, with eyes open (Fig. 2a),
excluded on the basis of clinical assessment scale for contraversive and their weight-bearing distribution was recorded and calcu-
pushing [11]. To determine the involvement of the cortical region, lated during a 0.1-ms period at 10, 30 and 60 s after starting the
we separated each hemispheric group by magnetic resonance (MR) static position. In the second series, participants were encour-
408 F. Ishii et al. / Clinical Neurology and Neurosurgery 112 (2010) 406–412
Table 1
Characteristics of the subjects.
Brunnstrom stage
V 5 5 3 12 p = 0.994
VI 7 5 2 10
One-way analysis of variance (ANOVA) and the Turkey were used to compare means of both age and duration of illness among five groups.
After analyzing the equalities of variance using an F-test, the sampling distributions of Brunnstrom stage in the two groups, RI and LI, were analyzed using Pearson’s chi-
squared tests.
RI = right hemispheric infarction; LI = light hemispheric infarction; RCI = right hemispheric infarction in territory of middle cerebral cortical artery; RPI = right hemispheric
infarction in territory of middle cerebral perforating artery; LCI = light hemispheric infarction in territory of middle cerebral cortical artery; LPI = light hemispheric infarction
in territory of middle cerebral perforating artery.
aged to shift as much weight as possible onto the non-paretic leg, 3. Results
while the paretic leg remained on the platform. The percentage of
forced weight was measured as for the static standing measure- All participants with stroke demonstrated asymmetrical
ment (Fig. 2b). In the third series, participants were encouraged to weight-bearing during static posture. Participants with LI bore
bear maximal weight on the paretic leg and maintain this forced >50% of their weight on the non-paretic leg in static standing pos-
position, and the percentage of weight-bearing was calculated as ture (Table 2a), while participants with RI bore most of their weight
described above (Fig. 2c). Rest periods of 2–3 min were allowed on the paretic leg (Table 2a). The percentage of weight borne on
between each position. Testing in the three positions was repeated the non-paretic leg during static standing was significantly differ-
three times on the same day, and the mean results of the three ent between patients with LI and those with RI (LI; 10 s 53.7 ± 3.5,
measurements in each position were analyzed statistically. 30 s 52.8 ± 4.5, 60 s 53.1 ± 4.9, RI; 10 s 48.8 ± 5.4, 30 s 49.6 ± 3.1, 60 s
48.4 ± 5.0) (unpaired samples Tukey’s post-hoc test: p < 0.05). Age-
2.5. Statistical analysis matched control participants divided their weight equally between
each leg in the static position (NR; 10 s 50.1 ± 1.9, 30 s 50.8 ± 3.2,
After analyzing the equalities of variance using an F-test, the 60 s 50.4 ± 3.8, NL; 10 s 49.9 ± 1.9, 30 s 49.2 ± 3.2, 60 s 49.6 ± 3.8)
sampling distributions of Brunnstrom stage between the two (Table 2a).
groups, RI and LI, were analyzed using Pearson’s chi-squared tests. We also examined the maximum percentage of weight volun-
Data were analyzed by one-way ANOVA to identify any significant tarily shifted between the paretic and non-paretic legs. Patients
differences in characteristics of patients, age and duration of illness, with LI were able to transfer significantly more of their body weight
and percentage of weight shifting through the paretic or non- to the non-paretic leg than those with RI (LI; 10 s 81.5 ± 8.6, 30 s
paretic leg among the groups. Parametric comparisons between 79.7 ± 10.2, 60 s 76.7 ± 13.3, RI; 10 s 70.4 ± 10.6, 30 s 68.7 ± 11.0,
the groups were carried out using Tukey’s post-hoc tests. To evalu- 60 s 64.9 ± 13.8) (unpaired samples Tukey’s post-hoc test: p < 0.05)
ate the significance of neuropsychological impairment, Spearman’s (Table 2b). However, there was no significant difference in the abil-
rank correlation was calculated to analyze the relationship between ity to shift weight to the paretic leg between the two groups (LI;
unilateral spatial neglect or anosognosia, and the average percent- 10 s 81.8 ± 7.8, 30 s 81.8 ± 7.7, 60 s 80.4 ± 9.4, RI; 10 s 78.8 ± 10.9,
age of weight shifted onto each leg in nine measurement times. 30 s 77.4 ± 11.2, 60 s 77.7 ± 10.5) (Table 2b). Control participants
Statistical significance was set at p < 0.05. were able to shift >80% of their weight onto either leg (NR; 10 s
Fig. 2. Schematic presentation of static posture and maximum voluntary weight shift.
Subjects maintained the basic position during rest. They then shifted their weight maximally onto the non-paretic leg, and then changed the weight shift to the paretic leg.
The pressure measured through each leg was shown as a percentage of the total weight, measured by the foot scan computerized force platform system.
(a) Static position, (b) maximum voluntary weight shifting onto left leg, (c) maximum voluntary weight shifting onto right leg.
Table 2a
Percentage of weight sustained in static position in RI, LI, NR and NL groups (Tukey’s post-hoc test; p values).
10 s RI LI NR NL 30 s RI LI NR NL 60 s RI LI NR NL
RI (n = 22) 48.8 ± 5.4 – 0.001 0.858 0.800 RI 49.6 ± 3.1 – 0.026 0.986 0.810 RI 48.4 ± 5.0 – 0.005 0.629 0.894
LI (n = 28) 53.7 ± 3.5 – 0.024 0.033 LI 52.8 ± 4.5 – 0.037 0.461 LI 53.1 ± 4.9 – 0.360 0.146
NR (n = 12) 50.1 ± 1.9 – 1.000 NR 50.8 ± 3.2 – 0.698 NR 50.4 ± 3.8 – 0.973
Table 2b
Maximum voluntary percentage of weight sustained in RI, LI, NR and NL groups (Tukey’s post-hoc test; p values).
10 s RI LI NR NL 30 s RI LI NR NL 60 s RI LI NR NL
409
410 F. Ishii et al. / Clinical Neurology and Neurosurgery 112 (2010) 406–412
0.675
0.985
0.956
0.997
0.007
84.6 ± 7.8, 60 s 84.4 ± 7.6) (Table 2b).
NL
–
To determine the involvement of the cortical region, we com-
pared weight-bearing in relation to the infarct-related artery. We
0.909
0.739
1.000
0.002
NR
separated each group into patients with infarction in the territory
–
of the cortical artery and those with infarction in the territory of
0.126
0.636
0.019
the perforating artery. Patients with a left hemispheric infarction
LPI
–
in the territory of middle cerebral cortical artery (LCI) put >50% of
their body weight on the non-paretic leg when standing still, while
0.001
0.002
LCI
patients with a right hemispheric infarction in the territory on mid-
–
dle cerebral cortical artery (RCI) put <50% of their weight on the
0.974
0.965
0.861
1.000
0.038
(Table 3a).
NL
0.294
0.003
with RCI were able to shift less weight onto their non-paretic leg,
NR
compared with those with LCI (LCI; 10 s 81.8 ± 7.7, 30 s 81.8 ± 9.0,
0.125
0.976
0.094
(unpaired samples Tukey’s post-hoc test: p < 0.05) (Table 3b). There
was no significant difference in maximum voluntary weight shift-
0.051
0.001
LCI
ing onto the non-paretic leg between the LPI and RPI groups
–
Percentage of weight sustained in static position in RCI, RPI, LCI, LPI, NR and NL groups (Tukey’s post-hoc test; p values).
tary weight shifting onto the paretic leg (LCI; 10 s 81.0 ± 7.6,
30 s 77.8 ± 10.1, 60 s 72.0 ± 16.4, RCI; 10 s 78.9 ± 10.4, 30 s
RCI
(Table 3b).
We performed neuropsychological tests in 12 patients with
RCI to clarify the role of unilateral spatial neglect or anosognosia.
30 s
These included line bisection and line crossing, which form part
of the BIT battery, and Bisiach’s anosognosia scale. The results in
seven of the 12 were indicative of unilateral spatial neglect, with
0.241
0.500
1.000
1.000
0.004
NL
cut-off points below seven for the line bisection score and 34 for
–
the line crossing score in the BIT Japanese Version. There was
0.999
0.570
0.190
0.003
10 s
showed even significant difference compared with LCI, RPI and LPI
(data not shown).
F. Ishii et al. / Clinical Neurology and Neurosurgery 112 (2010) 406–412 411
4. Discussion
0.384
0.978
0.271
0.946
0.967
0.100
0.850
0.073
1.000
0.001
NL
–
In this study, we found that all stroke patients adopted
0.985
0.075
0.394
0.471
0.001
0.017
0.047
0.014
asymmetrical weight-bearing when standing still with their feet
NR
shoulder-width and eyes open. However, the percentage of body
–
weight shifted to the non-paretic leg differed significantly, depend-
0.862
0.790
0.628
0.997
0.193
0.001
ing on the side of the lesion. Patients with LI put >50% of their weight
LPI
–
on their non-paretic leg, while those with RI put <50% of their
0.376
0.869
0.479
0.001
weight on their non-paretic leg. There was also a significant dif-
LCI
–
ference in the maximum percentage of weight voluntarily shifted
onto the non-paretic leg between patients with LI and those with
0.948
0.025
RPI
RI. Patients with RCI were less able to consciously shift weight onto
–
–
their non-paretic leg, compared with those with LCI. This indicates
the importance of right cortical function in controlling stability
RCI
–
during standing, and in consciously shifting weight to the non-
paretic leg. This instability could be associated with the presence
RCI 76.1 ± 10.7
RPI 72.6 ± 10.0
NR 87.5 ± 5.7
NL 84.4 ± 7.6
NL 84.4 ± 7.6
The ability to maintain balance while standing still is controlled
by interplay between the motor, sensory and cognitive systems
60 s
0.275
0.594
0.992
0.703
0.970
1.000
0.001
0.034
0.267
0.082
0.420
0.701
Our results also showed that patients with RCI bore more weight
0.249
0.911
0.559
0.922
0.890
0.001
on their paretic leg when standing still, compared with those with
LPI
LCI. In contrast, patients with RPI and LPI showed similar dis-
0.153
1.000
1.000
0.001
0.998
RPI
NR 86.8 ± 5.2
NL 84.6 ± 7.8
NL 84.6 ± 7.8
0.148
0.110
0.695
0.200
1.000
1.000
0.001
0.002
and claim that their paralyzed limbs can still move, despite obvi-
ous motor impairment. It has been suggested that this symptom
0.959
0.116
0.309
0.156
0.211
0.706
0.001
0.002
NR
systems, and that the causal lesion involves the frontal cortex,
0.123
0.987
0.990
0.992
1.000
0.001
0.994
0.995
0.205 0.001
–
Percentage sustained through non-paretic leg
out of 12 of our participants with RCI had lesions in the frontal lobe,
Percentage sustained through paretic leg
–
were able to transfer less weight to their non-paretic leg than aged-
RCI (n = 12) 66.9 ± 9.5
10 s
Table 4
Characteristics of the subjects with right hemispheric infarction in the territory of the cortical artery.
Case Age, years USN Anosognosia Static (%) non-paretic leg Shift non-paretic leg (%) Infarction region
The numbers in either static or shift onto non-paretic leg show the average percentage in nine measurement times as representative value.
USN: unilateral spatial neglect (cut-off point: line bisection 7 and line crossing 34, respectively).
the paretic leg. This could improve balance during standing and [10] Karnath HO, Ferber S, Dichgans J. The neural representation of postural control
walking in patients with cortical damage to the non-dominant in humans. Proc Natl Acad Sci USA 2000;97(25):13931–6.
[11] Karnath HO, Ferber S, Dichgans J. The origin of contraversive pushing: evidence
hemisphere. Further studies, including functional image, will be for a second graviceptive system in humans. Neurology 2000;55(9):1298–304.
needed to clarify the mechanism of instability, why patients with [12] Lafosse C, Kerckhofs E, Vereeck L, Troch M, Van Hoydonck G, Moeremans M,
anosognosia could not well shift onto non-paretic leg, and to et al. Postural abnormalities and contraversive pushing following right hemi-
sphere brain damage. Neuropsychol Rehabil 2007;17(3):374–96.
improve rehabilitation method for patients with instability. [13] Karnath HO, Johannsen L, Broetz D, Ferber S, Dichgans J. Prognosis of contraver-
sive pushing. J Neurol 2002;249(9):1250–3.
5. Conclusions [14] Pedersen PM, Wandel A, Jorgensen HS, Nakayama H, Raaschou HO, Olsen TS.
Ipsilateral pushing in stroke: incidence, relation to neuropsychological symp-
toms, and impact on rehabilitation. The Copenhagen stroke study. Arch Phys
We determined that patients with RCI were able to shift less Med Rehabil 1996;77(1):25–8.
weight onto their non-paretic leg, compared with those with LCI, [15] Spinazzola L, Cubelli R, Della Sala S. Impairments of trunk movements follow-
ing left or right hemisphere lesions: dissociation between apraxic errors and
while there was no significant difference in terms of their abilities postural instability. Brain 2003;126(Pt 12):2656–66.
to shift weight onto their non-paretic leg between patients with RPI [16] Brunnstrom S. Motor testing procedures in hemiplegia: based on sequential
and those with LPI. We also revealed that the presence of anosog- recovery stages. Phys Ther 1966;46(4):357–75.
[17] Shewan CM, Kertesz A. Reliability and validity characteristics of the Western
nosia, but not unilateral spatial neglect, was correlated with the
Aphasia Battery (WAB). J Speech Hear Disord 1980;45(3):308–24.
percentage of weight shifted onto the non-paretic leg in patients [18] Hartman-Maeir A, Katz N. Validity of the behavioral inattention test (BIT):
with RCI. relationships with functional tasks. Am J Occup Ther 1995;49(6):507–16.
[19] Bisiach E, Vallar G, Perani D, Papagno C, Berti A. Unawareness of disease
following lesions of the right hemisphere: anosognosia for hemiplegia and
References anosognosia for hemianopia. Neuropsychologia 1986;24(4):471–82.
[20] Randolph AL, Nelson M, Akkapeddi S, Levin A, Alexandrescu R. Reliability of
[1] Goldstein LB. Acute ischemic stroke treatment in 2007. Circulation measurements of pressures applied on the foot during walking by a comput-
2007;116(13):1504–14. erized insole sensor system. Arch Phys Med Rehabil 2000;81(5):573–8.
[2] Indredavik B, Bakke F, Slordahl SA, Rokseth R, Haheim LL. Stroke unit treat- [21] Jacobs JV, Horak FB. Cortical control of postural responses. J Neural Transm
ment improves long-term quality of life: a randomized controlled trial. Stroke 2007;114(10):1339–48.
1998;29(5):895–9. [22] Dickstein R, Abulaffio N. Postural sway of the affected and nonaffected
[3] Ones K, Yilmaz E, Cetinkaya B, Caglar N. Quality of life for patients poststroke pelvis and leg in stance of hemiparetic patients. Arch Phys Med Rehabil
and the factors affecting it. J Stroke Cerebrovasc Dis 2005;14(6):261–6. 2000;81(3):364–7.
[4] Aruin AS, Hanke T, Chaudhuri G, Harvey R, Rao N. Compelled weightbearing [23] Rode G, Tiliket C, Charlopain P, Boisson D. Postural asymmetry reduction by
in persons with hemiparesis following stroke: the effect of a lift insert and vestibular caloric stimulation in left hemiparetic patients. Scand J Rehabil Med
goal-directed balance exercise. J Rehabil Res Dev 2000;37(1):65–72. 1998;30(1):9–14.
[5] Garland SJ, Willems DA, Ivanova TD, Miller KJ. Recovery of standing balance and [24] Laufer Y, Sivan D, Schwarzmann R, Sprecher E. Standing balance and func-
functional mobility after stroke. Arch Phys Med Rehabil 2003;84(12):1753–9. tional recovery of patients with right and left hemiparesis in the early stages
[6] Nyberg L, Gustafson Y. Patient falls in stroke rehabilitation. A challenge to of rehabilitation. Neurorehabil Neural Repair 2003;17(4):207–13.
rehabilitation strategies. Stroke 1995;26(5):838–42. [25] Berti A, Bottini G, Gandola M, Pia L, Smania N, Stracciari A, et al.
[7] Bohannon RW, Smith MB, Larkin PA. Relationship between independent sitting Shared cortical anatomy for motor awareness and motor control. Science
balance and side of hemiparesis. Phys Ther 1986;66(6):944–5. 2005;309(5733):488–91.
[8] Dettmann MA, Linder MT, Sepic SB. Relationships among walking performance, [26] Hartman-Maeir A, Soroker N, Katz N. Anosognosia for hemiplegia in stroke
postural stability, and functional assessments of the hemiplegic patient. Am J rehabilitation. Neurorehabil Neural Repair 2001;15(3):213–22.
Phys Med 1987;66(2):77–90. [27] Goldie PA, Matyas TA, Evans OM, Galea M, Bach TM. Maximum voluntary
[9] Davies PM. Steps to follow: a guide to the treatment of adult hemiplegia. New weight-bearing by the affected and unaffected legs in standing following stroke.
York, NY: Sprinder; 1985. Clin Biomech (Bristol, Avon) 1996;11(6):333–42.