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Neurol Sci (2008) 29:313319

DOI 10.1007/s10072-008-0988-0

O R I G I NA L A RT I C L E

Rehabilitation of sensorimotor integration deficits in balance


impairment of patients with stroke hemiparesis: a before/after
pilot study
Nicola Smania Alessandro Picelli Marialuisa Gandolfi
Antonio Fiaschi Michele Tinazzi

Received: 10 March 2008 / Accepted in revised form: 10 July 2008


Springer-Verlag 2008

Abstract Balance impairment in patients with stroke cate that rehabilitation of sensorimotor integration deficits
hemiparesis is frequently related to deficits of central inte- can improve balance in patients with stroke hemiparesis.
gration of afferent inputs (somatosensory, visual, vestibu-
lar). Our aim was to evaluate whether balance exercises Keywords Balance Posture Rehabilitation Sensory
performed under various sensory input manipulations can integration Stroke
improve postural stability and/or walking ability in
patients with stroke. Seven chronic hemiparetic subjects
were recruited. Patient performance was assessed before,
immediately after and one week after treatment (consist- Introduction
ing of 20 one-hour daily sessions of several balance exer-
cises) by means of the Sensory Organization Balance Test Balance impairment is a very common cause of disability
and the Ten Metre Walking Test. Before treatment, all in patients with stroke [1]. Previous reports have shown
patients showed balance impairment with difficulty inte- that these patients have an increased risk of falls [2], mobil-
grating somatosensory information from the lower ity problems and poor recovery of activities of daily living
extremities and excessive reliance upon visual input in [1]. The specific causes of balance disorders in hemiparet-
standing balance control. After treatment, balance and ic patients after stroke can be manifold. Balance can be
walking speed significantly increased and this improve- affected in various ways which include joint motion limita-
ment was maintained for one week. These findings indi- tion, weakness, altered muscular tone, sensory deficits,
anomalous postural reactions and cognitive problems [3].
A further important cause of balance impairment in
patients with stroke hemiparesis, in the absence of ele-
mentary sensory deficits at clinical evaluation, is a deficit
N. Smania () of the central integration of sensory inputs (somatosenso-
Rehabilitation Unit ry, visual and vestibular) [3, 4]. In normal adult subjects,
G.B. Rossi University Hospital the visual, vestibular and somatosensory systems are all
Via L.A. Scuro, 10 involved in balance control and make up the system of
37134 Verona, Italy
coordinates on which the bodys postural control is based
e-mail: nicola.smania@univr.it
[5]. For instance, in the static standing position, healthy
N. Smania A. Picelli M. Gandolfi A. Fiaschi M. Tinazzi adults normally use somatosensory information which
Department of Neurological and Vision Sciences
Neurorehabilitation Section globally comes from the lower limbs (feet pressure recep-
University of Verona, Italy tors, ankle joint receptors, muscle proprioceptors) in
order to build the main reference coordinates for balance
A. Fiaschi
IRCCS, S. Camillo [6, 7]. When lower limb somatosensory information is
Venice, Italy inadequate (e.g., under a compliant surface support condi-
M. Tinazzi tion), other sensory systems are involved. This central
Neurology Unit, Maggiore Hospital integration of sensory inputs allows potential sensory
Verona, Italy conflicts generated by inadequate afferent information to
314 Neurol Sci (2008) 29:313319

be overcome. For example, vestibular and somatosensory - stability of neurological severity


information is in conflict with visual information when a - ability to maintain standing position without aids for at
stationary train creates the illusion of movement as anoth- least 5 minutes
er train begins to move. Under these very critical condi- - ability to walk independently for at least 15 metres.
tions, the ability to analyze, compare and select the perti- The exclusion criteria were:
nent sensory information is very important in order to - posterior circulation stroke
avoid falling. The existence of a general neural process - deficits of somatic sensation involving the paretic
aimed at resolving sensory conflicts and synthesizing lower limb
information from disparate sensory inputs and combining - presence of severe hemiplegia (<25 of 42 points on the
efferent and afferent information has already been sug- 7 motor items of the European Stroke Scale) [18, 19]
gested in literature [5]. Several structures of the central - vestibular disorders
nervous system seem to be involved in sensory integration - paroxysmal vertigo
such as the visual and vestibular cortex [8, 9], the posteri- - presence of other neurological conditions such as neg-
or parietal cortex [10], the dorsolateral prefrontal cortex lect, hemianopsia and contraversive pushing syndrome
[10], the basal ganglia [11], the limbic system [12], the - presence of orthopaedic diseases involving the lower
cerebellum [13] and the reticular system [14]. limbs.
Recent studies have reported that this process can be The demographic and clinical features of each patient
disturbed in patients with stroke. In particular, these are reported in Table 1.
patients present major difficulties during tasks that All patients underwent at least one follow up evalua-
require integration of somatosensory information from tion by means of the European Stroke Scale (ESS) [18] in
the lower extremities (such as during maintenance of the three months before the study, and comparison of
equilibrium under a compliant surface support condition), these data with those collected at the start of the study
and, unlike normal adults, they tend to place dispropor- showed that patient neurological severity was stable
tionately greater reliance upon visual input in order to (Wilcoxon signed rank test: Z = -1.134, p=0.257.
maintain balance [3, 15]. Statistical significance level at p<0.025).
Although a deficit of sensorimotor integration is now Patients gave their informed consent for participation
acknowledged as a major factor in balance disability after in the study. The study was carried out according to the
stroke, few studies [3, 16, 17] have been carried out to pro- Declaration of Helsinki and was approved by the Azienda
pose remediation programs for rehabilitation of the anom- Ospedaliera di Verona Ethics Committee.
alous processing of afferent sensory inputs in hemiplegic
patients. The main objective of the present study was to
evaluate whether a training program consisting of exercis- Assessment procedures
es performed under different sensory conflict conditions
can lead to an improvement in static and dynamic balance Patients underwent a specific training program aimed at
and walking ability in patients with stroke and whether the increasing sensory integration and balance ability. Before
effects of treatment may persist for several days. and after training, patients were submitted to the Sensory
Organization Balance Test (SOT) [20] and the Ten Metres
Walking Test [21]. A further follow-up evaluation was
Material and methods performed one week after the end of training.

Patients
Sensory Organization Balance Test (SOT)
Seven right-handed subjects (5 males and 2 females; mean The SOT is a validated [20, 22] timed balance test that eval-
age: 63.1 years; range: 5372 years) presenting with hemi- uates somatosensory, visual and vestibular function for
paresis as a result of chronic stroke (mean time from onset: maintenance of upright posture. This test requires that
14.8 months; range: 1220 months) were recruited from patients maintain standing balance during a combination of
among 26 patients consecutively admitted to the three visual and two support surface conditions. Tasks were
Rehabilitation Unit of the G.B. Rossi University Hospital, performed with the eyes open and with the eyes closed; a
Verona, Italy, over the period from January to April 2006. visual conflict dome was used to produce inaccurate visual
None of the patients performed any type of rehabilita- and vestibular inputs. The support surface conditions
tion treatment in the four months before the start of the included a hard, flat floor and an 8 cm section of 20.4 kg
study. firm density foam rubber that reduces the quality of the sur-
The inclusion criteria were: face orientation input. During the test, subjects stood bare-
- first unilateral brain ischaemic stroke foot in the upright position with their arms alongside the
- at least 1 year from stroke onset body and their feet on the predesignated site. If the subject
Neurol Sci (2008) 29:313319 315

Table 1 Demographic and clinical features of patients

Patients Age (yrs) Sex Handedness Time from Neurological Type of Lesion
stroke (mo) severity (ESS) lesion localization

1 65 M Right 13 68 Ischaemic Right F-ins


2 72 M Right 12 72 Ischaemic Left F-P-T
3 58 M Right 12 72 Ischaemic Left T-O-ins
4 60 M Right 14 74 Ischaemic Right T-P-ins
5 68 F Right 15 80 Ischaemic Left T-P
6 53 F Right 18 86 Ischaemic Left F-P
7 66 M Right 20 86 Ischaemic Right F-P-T-ins
Mean 63.1 14.9 76.9
S.D. 6.5 3.08 7.2

F, frontal; P, parietal; T, temporal; O, occipital; ins, insular; ESS, European Stroke Scale; M, male; F, female; mo, months; yrs, years

activated any postural reaction, the test was stopped imme- decreasing the support base amplitude. All these exercis-
diately and the number of seconds standing prior to the vio- es were repeated under different surface and sensory con-
lation constituted the trial score. The test was performed ditions. The specification and sequence of the exercises
under six conditions: (1) eyes open stable surface; (2) were discussed and defined during a staff meeting. In the
eyes open compliant surface; (3) eyes closed stable sur- first two weeks exercises were performed on a stable sur-
face; (4) eyes closed compliant surface; (5) visual and face (floor), in the other two weeks they were performed
vestibular conflict (wearing visual dome) stable surface; on a compliant surface, the section of which was progres-
(6) visual and vestibular conflict (wearing visual dome) sively increased from 1.5 to 3, 5 and 8 cm, according to
compliant surface. Five trials were carried out for each test the patients abilities. During the two training periods
condition. Each trial lasted 30 seconds. Total scores for patient vision conditions were progressively changed.
each condition were the sums of the scores of each trial The patient was required to perform the exercises first
(maximum score for each test condition: 30 x 5 = 150). with their eyes open (free-vision condition), then wearing
a panel held horizontally on thei chest to mask vision of
the feet (foot-masking condition), then blinded by means
Ten Metres Walking Test of a mask (blind condition) and finally wearing a helmet
This is a validated test [21] used for quantitative analysis of creating a visual and vestibular conflict (dome condition).
gait. Patients were required to walk on a flat hard floor at
their most comfortable pace for 10 metres using their usual
assistive device and orthoses. Scoring was walking speed. Statistical analysis

Statistical analysis was carried out using the SPSS for


Training procedures Windows statistical package, version 15.0. Multiple com-
parisons in all the SOT conditions and in the 10 Metres
The sensory integration and balance training program Walking Test were made on the pre-post treatment and
consisted of twenty 50-minute sessions over a 4-week pre-treatment follow-up data by means of the Wilcoxon
period. The rehabilitative protocol was based on weight signed rank test. In order to make multiple comparisons,
transfer and balance exercises, performed in the upright according to the Bonferroni correction procedure, we set
position without any support. Exercises were divided into the statistical significance level at p<0.025.
three levels: first, starting from the patients most stable
and comfortable standing position, trained physiothera-
pists shifted the pelvis in a frontal and a sagittal direction Results
asking the patient to actively maintain balance control.
According to the patients emergent skills, the therapists Sensory Organization Balance Test (SOT)
progressively increased the shift width and decreased the
supporting base amplitude. At the second level, patients In the stable surface condition, all patients performed at
performed a single-step simulation shifting their weight ceiling levels in all test sessions (pre-treatment, post-
from one foot to the other in a frontal direction. This exer- treatment and follow-up). Thus, no significant variations
cise was performed alternating the front foot. At the third in performance were registered in this test. Patients per-
level the patients, supported by the paretic lower limb, formance in the SOT is shown in Table 2.
made rapid movements with the healthy foot in many Performance in compliant surface sessions showed a sig-
directions, progressively increasing weight shifting and nificant improvement after treatment: eyes open (Z = - 2.366,
316 Neurol Sci (2008) 29:313319

p=0.018); eyes closed (Z = -2.371, p=0.018); visual dome

follow-up
(Z = -2.375, p=0.018). This improvement was confirmed
1 week

141.71
at the one-week follow-up evaluation: eyes open (Z = -

5.25
144
136
148
139
149
138
138
2.366, p=0.018); eyes closed (Z = -2.366, p=0.018); visu-
al dome (Z = -2.384, p=0.017).

149.43
After

0.98
150
150
148
148
150
150
150
Ten Metres Walking Test
Before
Dome

11.57
5.74
20
15
10

15
12
Walking speed showed a significant improvement after
5

4
treatment: (Z = -2.371, p=018). This improvement was con-
follow-up
1 week

148.57
firmed at the one-week follow-up evaluation (Z =-2.371,

1.99
150
150
147
150
148
145
150 p=0.018). Each patients pre-treatment, post-treatment
149.43 and follow up performance in the Ten Metres Walking
Test is shown in Figure 1.
After

0.98
150
150
148
148
150
150
150
Before

Discussion
32.86
12.20
Blind

50
45
20
20
25
30
40

Restoring balance and mobility is an important goal of


follow-up
1 week

145.29

stroke rehabilitation, and prospects of improving balance


4.72
150
146
150
140
138
145
148

and gait even in chronic patients have been shown after


specific rehabilitation programs [23, 24]. The present
149.57

study shows that, following a specific training program


After

0.79
150
150
149
148
150
150
150

based on weight transfer and balance exercises performed


Free vision

under different conditions of manipulation of sensory


inputs, patients achieved a significant improvement in
Before

80.86
23.53
Table 2 Patients performance in the SOT before treatment, after treatment and at the one week follow-up evaluation

110
100

105

their ability to maintain balance control. Gait ability,


60
56
60
75

measured as walking speed, also showed a statistically


follow-up

significant improvement. These changes could not be


1 week

149.14
1.21
150
148
150
150
149
147
150

ascribed to spontaneous recovery, because all the patients


included in this study were at a chronic stage of illness
(more than one year from stroke onset and no significant
149.80
After

0.38
150
150
149
150
150
150
150

difference between the ESS data collected in the three


months before and at the start of the study).
We argue that the improvement seen in our patients
148.80
1 week Before
Dome

1.07

could be mainly ascribed to a change in sensory strate-


150
148
148
148
148
150
150

gies used by patients in controlling their standing pos-


follow-up

ture. As recently reported by Di Fabio and Badke [15],


149.57
0.79
150
150
150
148
150
150
149

unlike normal subjects, patients with stroke tend to rely


upon visual rather than somatosensory inputs in order to
After

maintain the standing position. This observation was


150
150
150
150
150
150
150
150
0

confirmed by our pre-treatment SOT data which showed


Compliant surface

that postural stability was markedly decreased in all the


1 week Before
Blind

150
150
148
148
148
149
150
149

somatosensory conflict (compliant surface) conditions,


1

and in particular during the blind and dome conditions


follow-up

(see Table 2). After treatment, all patients exhibited near-


150
150
150
150
150
150
150
150

normal performance in all the SOT compliant surface


0

conditions. Thus, following exercise training aimed at


After

progressively inducing the patient to use lower limb


150
150
150
150
150
150
150
150
Stable surface

0
Free vision

somatosensory inputs for controlling standing stability,


Before

patients are able to improve their ability to stand even in


150
150
150
150
150
150
150
150

conditions in which somatosensory input has been


0

altered in several ways.


Patients

It is very relevant from a functional point of view that


Mean
S.D.

similar improvement was also seen in walking speed.


1
2
3
4
5
6
7
Neurol Sci (2008) 29:313319 317

Fig. 1 Patients performance in the Ten


Metres Walking Test

Likewise, this could be explained by an improvement in In the second study, by Bayouk et al. [17], sixteen
postural adjustment mechanisms. It is known that walking patients with chronic hemiplegia after stroke (more than
performance is strictly related to postural control ability. 12 months from onset) were randomized to an experimen-
Movements of the legs are a source of disturbance of bal- tal and to a control group. The control group underwent
ance because they are involved in body support, and thus an 8-week rehabilitation program aimed at improving bal-
a displacement of the centre of gravity is observed imme- ance, gait ability and movement coordination. These exer-
diately before and after movement onset. The centre of cises were also performed in the experimental group but,
gravity shift occurs, for example, during the initiation and in this case, the program also included exercises executed
the course of gait [25]. Control of the centre of gravity while the proprioception of the feet and ankles and/or
shift toward a new position, compatible with equilibrium vision was manipulated. As a whole, both groups received
during movement, may be related both to anticipatory and the same amount of therapy. As in the study by Bonan et
responsive postural adjustments [25]. It is worth noting al [3, 16], a significant improvement in static and dynam-
that sensory input integration is very important for main- ic balance was recorded after rehabilitation training. In
taining equilibrium, especially during conditions of per- contrast, an improvement in walking speed was observed
turbed balance, such as during walking performance. not only in the experimental but also in the control group.
In the literature, a number of studies have been carried This aspecific effect of rehabilitation could be ascribed to
out to evaluate the effectiveness of equilibrium exercise the fact that both groups performed walking exercises
programs in the treatment of balance disturbances of cen- according to their training program.
tral and peripheral origin [26]. Nonetheless, to the best of The results of our study extend previous results [3, 16]
our knowledge, only two very recent randomized con- showing that a somatosensory integration training pro-
trolled trials have evaluated the effectiveness of rehabili- gram can improve balance ability in patients with stroke
tation programs aimed at retraining patients with stroke to and that this improvement is not transient but may persist
regain the ability to rely upon somatosensory inputs for for several days.
the maintenance of static and dynamic balance. As regards walking performance, our patients also
In the first of these studies, Bonan et al. [3, 16] showed a remarkable improvement in walking speed after
assessed twenty patients with chronic hemiplegia after rehabilitation from a mean value of 0.26 m/s before treat-
stroke (more than 12 months from onset). Patients were ment to 0.45 m/s after treatment, as assessed by the Ten
randomized to two groups both of which underwent a 4- Metres Walking Test. These changes are very relevant
week balance rehabilitation program. Group 1 performed from a clinical and functional point of view. As Perry et
all the program exercises under vision deprivation while al. described [27], hemiparetic patients with a mean walk-
the same exercises were performed under free vision in ing speed of 0.260.11 m/s can be classified as those who
group 2. The results of this study showed that static and are able to use walking for all household activities but
dynamic balance improved more after rehabilitation unable to enter and leave their homes independently. On
under visual deprivation than under free vision. They also the other hand, patients with a walking speed of 0.40.18
recorded a significant improvement in gait ability after are classified as being capable of entering and leaving
the training. their homes independently, capable of mounting and
318 Neurol Sci (2008) 29:313319

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