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
hemiparesis is frequently related to deficits of central inte-
gration of afferent inputs (somatosensory, visual, vestibu-
lar). Our aim was to evaluate whether balance exercises
performed under various sensory input manipulations can
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-
ing of 20 one-hour daily sessions of several balance exer-
cises) by means of the Sensory Organization Balance Test
and the Ten Metre Walking Test. Before treatment, all
patients showed balance impairment with difficulty inte-
grating somatosensory information from the lower
extremities and excessive reliance upon visual input in
standing balance control. After treatment, balance and
walking speed significantly increased and this improve-
ment was maintained for one week. These findings indi-
N. Smania ()
Rehabilitation Unit
G.B. Rossi University Hospital
Via L.A. Scuro, 10
37134 Verona, Italy
e-mail: nicola.smania@univr.it
N. Smania A. Picelli M. Gandolfi A. Fiaschi M. Tinazzi
Department of Neurological and Vision Sciences
Neurorehabilitation Section
University of Verona, Italy
A. Fiaschi
IRCCS, S. Camillo
Venice, Italy
M. Tinazzi
Neurology Unit, Maggiore Hospital
Verona, Italy
cate that rehabilitation of sensorimotor integration deficits
can improve balance in patients with stroke hemiparesis.
Keywords Balance Posture Rehabilitation Sensory
integration Stroke
Introduction
Balance impairment is a very common cause of disability
in patients with stroke [1]. Previous reports have shown
that these patients have an increased risk of falls [2], mobil-
ity problems and poor recovery of activities of daily living
[1]. The specific causes of balance disorders in hemiparet-
ic patients after stroke can be manifold. Balance can be
affected in various ways which include joint motion limita-
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
of the central integration of sensory inputs (somatosenso-
ry, visual and vestibular) [3, 4]. In normal adult subjects,
the visual, vestibular and somatosensory systems are all
involved in balance control and make up the system of
coordinates on which the bodys postural control is based
[5]. For instance, in the static standing position, healthy
adults normally use somatosensory information which
globally comes from the lower limbs (feet pressure recep-
tors, ankle joint receptors, muscle proprioceptors) in
order to build the main reference coordinates for balance
[6, 7]. When lower limb somatosensory information is
inadequate (e.g., under a compliant surface support condi-
tion), other sensory systems are involved. This central
integration of sensory inputs allows potential sensory
conflicts generated by inadequate afferent information to
314
be overcome. For example, vestibular and somatosensory
information is in conflict with visual information when a
stationary train creates the illusion of movement as anoth-
er train begins to move. Under these very critical condi-
tions, the ability to analyze, compare and select the perti-
nent sensory information is very important in order to
avoid falling. The existence of a general neural process
aimed at resolving sensory conflicts and synthesizing
information from disparate sensory inputs and combining
efferent and afferent information has already been sug-
gested in literature [5]. Several structures of the central
nervous system seem to be involved in sensory integration
such as the visual and vestibular cortex [8, 9], the posteri-
or parietal cortex [10], the dorsolateral prefrontal cortex
[10], the basal ganglia [11], the limbic system [12], the
cerebellum [13] and the reticular system [14].
Recent studies have reported that this process can be
disturbed in patients with stroke. In particular, these
patients present major difficulties during tasks that
require integration of somatosensory information from
the lower extremities (such as during maintenance of
equilibrium under a compliant surface support condition),
and, unlike normal adults, they tend to place dispropor-
tionately greater reliance upon visual input in order to
maintain balance [3, 15].
Although a deficit of sensorimotor integration is now
acknowledged as a major factor in balance disability after
stroke, few studies [3, 16, 17] have been carried out to pro-
pose remediation programs for rehabilitation of the anom-
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-
es performed under different sensory conflict conditions
can lead to an improvement in static and dynamic balance
and walking ability in patients with stroke and whether the
effects of treatment may persist for several days.
Material and methods
Patients
Seven right-handed subjects (5 males and 2 females; mean
age: 63.1 years; range: 5372 years) presenting with hemi-
paresis as a result of chronic stroke (mean time from onset:
14.8 months; range: 1220 months) were recruited from
among 26 patients consecutively admitted to the
Rehabilitation Unit of the G.B. Rossi University Hospital,
Verona, Italy, over the period from January to April 2006.
None of the patients performed any type of rehabilita-
tion treatment in the four months before the start of the
study.
The inclusion criteria were:
- first unilateral brain ischaemic stroke
- at least 1 year from stroke onset
Neurol Sci (2008) 29:313319
- stability of neurological severity
- ability to maintain standing position without aids for at
least 5 minutes
- ability to walk independently for at least 15 metres.
The exclusion criteria were:
- posterior circulation stroke
- deficits of somatic sensation involving the paretic
lower limb
- presence of severe hemiplegia (<25 of 42 points on the
7 motor items of the European Stroke Scale) [18, 19]
- vestibular disorders
- paroxysmal vertigo
- presence of other neurological conditions such as neg-
lect, hemianopsia and contraversive pushing syndrome
- presence of orthopaedic diseases involving the lower
limbs.
The demographic and clinical features of each patient
are reported in Table 1.
All patients underwent at least one follow up evalua-
tion by means of the European Stroke Scale (ESS) [18] in
the three months before the study, and comparison of
these data with those collected at the start of the study
showed that patient neurological severity was stable
(Wilcoxon signed rank test: Z = -1.134, p=0.257.
Statistical significance level at p<0.025).
Patients gave their informed consent for participation
in the study. The study was carried out according to the
Declaration of Helsinki and was approved by the Azienda
Ospedaliera di Verona Ethics Committee.
Assessment procedures
Patients underwent a specific training program aimed at
increasing sensory integration and balance ability. Before
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
performed one week after the end of training.
Sensory Organization Balance Test (SOT)
The SOT is a validated [20, 22] timed balance test that eval-
uates somatosensory, visual and vestibular function for
maintenance of upright posture. This test requires that
patients maintain standing balance during a combination of
three visual and two support surface conditions. Tasks were
performed with the eyes open and with the eyes closed; a
visual conflict dome was used to produce inaccurate visual
and vestibular inputs. The support surface conditions
included a hard, flat floor and an 8 cm section of 20.4 kg
firm density foam rubber that reduces the quality of the sur-
face orientation input. During the test, subjects stood bare-
foot in the upright position with their arms alongside the
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-
diately and the number of seconds standing prior to the vio-
lation constituted the trial score. The test was performed
under six conditions: (1) eyes open stable surface; (2)
eyes open compliant surface; (3) eyes closed stable sur-
face; (4) eyes closed compliant surface; (5) visual and
vestibular conflict (wearing visual dome) stable surface;
(6) visual and vestibular conflict (wearing visual dome)
compliant surface. Five trials were carried out for each test
condition. Each trial lasted 30 seconds. Total scores for
each condition were the sums of the scores of each trial
(maximum score for each test condition: 30 x 5 = 150).
Ten Metres Walking Test
This is a validated test [21] used for quantitative analysis of
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.
decreasing the support base amplitude. All these exercis-
es were repeated under different surface and sensory con-
ditions. The specification and sequence of the exercises
were discussed and defined during a staff meeting. In the
first two weeks exercises were performed on a stable sur-
face (floor), in the other two weeks they were performed
on a compliant surface, the section of which was progres-
sively increased from 1.5 to 3, 5 and 8 cm, according to
the patients abilities. During the two training periods
patient vision conditions were progressively changed.
The patient was required to perform the exercises first
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
of a mask (blind condition) and finally wearing a helmet
creating a visual and vestibular conflict (dome condition).
Statistical analysis

Statistical analysis was carried out using the SPSS for

Training procedures
The sensory integration and balance training program
consisted of twenty 50-minute sessions over a 4-week
period. The rehabilitative protocol was based on weight
transfer and balance exercises, performed in the upright
position without any support. Exercises were divided into
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
asking the patient to actively maintain balance control.
According to the patients emergent skills, the therapists
progressively increased the shift width and decreased the
supporting base amplitude. At the second level, patients
performed a single-step simulation shifting their weight
from one foot to the other in a frontal direction. This exer-
cise was performed alternating the front foot. At the third
level the patients, supported by the paretic lower limb,
made rapid movements with the healthy foot in many
directions, progressively increasing weight shifting and
Windows statistical package, version 15.0. Multiple com-
parisons in all the SOT conditions and in the 10 Metres
Walking Test were made on the pre-post treatment and
pre-treatment follow-up data by means of the Wilcoxon
signed rank test. In order to make multiple comparisons,
according to the Bonferroni correction procedure, we set
the statistical significance level at p<0.025.
Results
Sensory Organization Balance Test (SOT)
In the stable surface condition, all patients performed at
ceiling levels in all test sessions (pre-treatment, post-
treatment and follow-up). Thus, no significant variations
in performance were registered in this test. Patients per-
formance in the SOT is shown in Table 2.
Performance in compliant surface sessions showed a sig-
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
Likewise, this could be explained by an improvement in
postural adjustment mechanisms. It is known that walking
performance is strictly related to postural control ability.
Movements of the legs are a source of disturbance of bal-
ance because they are involved in body support, and thus
a displacement of the centre of gravity is observed imme-
diately before and after movement onset. The centre of
gravity shift occurs, for example, during the initiation and
the course of gait [25]. Control of the centre of gravity
shift toward a new position, compatible with equilibrium
during movement, may be related both to anticipatory and
responsive postural adjustments [25]. It is worth noting
that sensory input integration is very important for main-
taining equilibrium, especially during conditions of per-
turbed balance, such as during walking performance.
In the literature, a number of studies have been carried
out to evaluate the effectiveness of equilibrium exercise
programs in the treatment of balance disturbances of cen-
tral and peripheral origin [26]. Nonetheless, to the best of
our knowledge, only two very recent randomized con-
trolled trials have evaluated the effectiveness of rehabili-
tation programs aimed at retraining patients with stroke to
regain the ability to rely upon somatosensory inputs for
the maintenance of static and dynamic balance.
In the first of these studies, Bonan et al. [3, 16]
assessed twenty patients with chronic hemiplegia after
stroke (more than 12 months from onset). Patients were
randomized to two groups both of which underwent a 4-
week balance rehabilitation program. Group 1 performed
all the program exercises under vision deprivation while
the same exercises were performed under free vision in
group 2. The results of this study showed that static and
dynamic balance improved more after rehabilitation
under visual deprivation than under free vision. They also
recorded a significant improvement in gait ability after
the training.
317
Fig. 1 Patients performance in the Ten
Metres Walking Test
In the second study, by Bayouk et al. [17], sixteen
patients with chronic hemiplegia after stroke (more than
12 months from onset) were randomized to an experimen-
tal and to a control group. The control group underwent
an 8-week rehabilitation program aimed at improving bal-
ance, gait ability and movement coordination. These exer-
cises were also performed in the experimental group but,
in this case, the program also included exercises executed
while the proprioception of the feet and ankles and/or
vision was manipulated. As a whole, both groups received
the same amount of therapy. As in the study by Bonan et
al [3, 16], a significant improvement in static and dynam-
ic balance was recorded after rehabilitation training. In
contrast, an improvement in walking speed was observed
not only in the experimental but also in the control group.
This aspecific effect of rehabilitation could be ascribed to
the fact that both groups performed walking exercises
according to their training program.
The results of our study extend previous results [3, 16]
showing that a somatosensory integration training pro-
gram can improve balance ability in patients with stroke
and that this improvement is not transient but may persist
for several days.
As regards walking performance, our patients also
showed a remarkable improvement in walking speed after
rehabilitation from a mean value of 0.26 m/s before treat-
ment to 0.45 m/s after treatment, as assessed by the Ten
Metres Walking Test. These changes are very relevant
from a clinical and functional point of view. As Perry et
al. described [27], hemiparetic patients with a mean walk-
ing speed of 0.260.11 m/s can be classified as those who
are able to use walking for all household activities but
unable to enter and leave their homes independently. On
the other hand, patients with a walking speed of 0.40.18
are classified as being capable of entering and leaving
their homes independently, capable of mounting and
318
descending a curb independently, and of being independ-
ently mobile in at least one moderately demanding com-
munity activity (appointments, restaurants).
Although the mechanisms underlying the improve-
ment in gait performance after a somatosensory integra-
tion training program are still subject to debate [17], the
results of the present study suggest that a balance rehabil-
itation program may lead to an improvement in postural
control mechanisms and consequently in gait perform-
ance.
It is interesting to note that the only patient with an ini-
tial low walking speed (<0.1 m/s) was the only one having
no relevant improvement in gait velocity (see Fig. 1). This
could suggest that our sensorimotor rehabilitation training
is not effective in improving gait in patients with a severe
walking impairment. This hypothesis should be examined
by future studies.
The present study has three limits. First: the small
sample size. Future studies with a larger subject popula-
tion are needed to further validate our findings. Second:
the short time of the follow-up. The promising improve-
ments our patients achieved at the end of treatment, and
which were maintained one week after it, show the possi-
ble short-term effectiveness of our rehabilitation program.
Longer follow-up is needed to examine its medium- and
long-term effects. Third: the lack of a control group.
Since this protocol is quite innovative, this is only a pre-
liminary study. A comparison with another convention-
al rehabilitation program is needed in order confirm its
effectiveness.
Conclusions
Postural control is built up by the integration of
somatosensory, visual and vestibular inputs which can be
functionally redundant (as generally happens) or in con-
flict. Afferent and efferent information is combined by a
central integration mechanism [5]. Reliance on visual
input may be defined as a compensatory strategy used by
patients with stroke for by-passing their balance impair-
ment. The visual influence becomes predominant when
other input sources are reduced, and this predominance is
reversible in chronic stroke, as described in our own and
in previous studies [3, 16, 17]. Visual deprivation and sen-
sory conflict probably unmasked an existing but function-
ally inactive recovery. Our results show that a physical
therapy program focusing on balance rehabilitation in
patients with chronic hemiplegia should include exercises
performed in sensory conflict conditions. Further system-
atic randomized controlled trials involving larger series of
patients are warranted to assess the usefulness of this
original procedure in stroke rehabilitation.
Conflict of Interest statement The Authors declare that they have no
conflict of interest related to the publication of this manuscript
Neurol Sci (2008) 29:313319
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