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Strokeaha 116 013839
Strokeaha 116 013839
Background and Purpose—The purpose of this systematic review and meta-analysis was to investigate the effects of
exercise training on balance capacity in people in the chronic phase after stroke. Furthermore, we aimed to identify which
training regimen was most effective.
Methods—Electronic databases were searched for randomized controlled trials evaluating the effects of exercise therapy on
balance capacity in the chronic phase after stroke. Studies were included if they were of moderate or high methodological
quality (PEDro score ≥4). Data were pooled if a specific outcome measure was reported in at least 3 randomized controlled
trials. A sensitivity analysis and consequent subgroup analyses were performed for the different types of experimental
training (balance and/or weight-shifting training, gait training, multisensory training, high-intensity aerobic exercise
training, and other training programs).
Results—Forty-three randomized controlled trials out of 369 unique hits were included. A meta-analysis could be conducted
for the Berg Balance Scale (28 studies, n=985), Functional Reach Test (5 studies, n=153), Sensory Organization Test
(4 studies, n=173), and mean postural sway velocity (3 studies, n=89). A significant overall difference in favor of the
intervention group was found for the Berg Balance Scale (mean difference 2.22 points (+3.9%); 95% confidence interval
[CI], 1.26–3.17; P<0.01; I2=52%), Functional Reach Test (mean difference=3.12 cm; 95% CI, 0.90–5.35; P<0.01;
I2=74%), and Sensory Organization Test (mean difference=6.77 (+7%) points; 95% CI, 0.83–12.7; P=0.03; I2=0%).
Subgroup analyses of the studies that included Berg Balance Scale outcomes demonstrated a significant improvement
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after balance and/or weight-shifting training of 3.75 points (+6.7%; 95% CI, 1.71–5.78; P<0.01; I2=52%) and after gait
training of 2.26 points (+4.0%; 95% CI, 0.94–3.58; P<0.01; I2=21, whereas no significant effects were found for other
training regimens.
Conclusions—This systematic review and meta-analysis showed that balance capacities can be improved by well-
targeted exercise therapy programs in the chronic phase after stroke. Specifically, balance and/or weight-shifting
and gait training were identified as successful training regimens. (Stroke. 2016;47:2603-2610. DOI: 10.1161/
STROKEAHA.116.013839.)
Key Words: activities of daily living ◼ exercise therapy ◼ postural balance ◼ stroke
Received April 19, 2016; final revision received July 25, 2016; accepted August 1, 2016.
From the Donders Centre for Neuroscience, Department of Rehabilitation, Radboud University Medical Center, Nijmegen, The Netherlands (H.J.R.v.D.,
A.C.H.G., V.W.); Rehabilitation Medical Centre Groot Klimmendaal, Arnhem, The Netherlands (A.H.); Hogeschool van Arnhem en Nijmegen (HAN),
School of Occupational Therapy, University of Applied Sciences, Nijmegen, The Netherlands (M.A.M.P.); Department of Rehabilitation Medicine, MOVE
Research Institute, VU University Medical Centre, Amsterdam, The Netherlands (J.M.V., G.K.); Neuroscience Campus Amsterdam, VU University,
Amsterdam, The Netherlands (G.K.); Department of Neurorehabilitatioan, Reade Centre of Rehabilitation and Rheumatology, Amsterdam, The Netherlands
(G.K.); Department of Physical Therapy and Human Movement Sciences, Northwestern University, Chicago, IL (G.K.); and Sint Maartenskliniek,
Research, Nijmegen, The Netherlands (A.C.H.G., V.W.).
*Drs Geurts and Weerdesteyn contributed equally.
The online-only Data Supplement is available with this article at http://stroke.ahajournals.org/lookup/suppl/doi:10.1161/STROKEAHA.
116.013839/-/DC1.
Correspondence to Hanneke J.R. van Duijnhoven, MD, MSc, Donders Centre for Neuroscience, Department of Rehabilitation, Radboud University
Medical Center, Nijmegen, The Netherlands. E-mail hanneke.vanduijnhoven@radboudumc.nl
© 2016 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.116.013839
2603
2604 Stroke October 2016
goal of rehabilitation treatment is to improve balance capacity, any of these aspects and should be validated and found reliable for
for which various types of exercise therapy are being used.7 individuals with stroke. Balance outcomes should measure at the ICF
(International Classification of Functioning, Disability and Health)
Previous meta-analyses of the effects of exercise therapy on
level of body functions and structures (such as posturography) or
improving balance capacity have been inconclusive.8–11 There capacities/activities (such as the Berg Balance Scale [BBS]).
seemed to be an effect of biofeedback training on postural
sway and of repetitive task training on sit-to-stand activities,8 Study Identification
but both types of training did not result in better performance We searched PubMed, Excerpta Medica Databank (EMBASE), and
on clinical tests of balance capacity.9 In addition, it remained the Physiotherapy Evidence Database (PEDro) from 2000 to January
unclear which type of training regimen would be most effective. 2015. Indexing terms and free-text words of the following key words
Furthermore, previous meta-analyses did not address whether were used: “postural balance” or “balance” and “chronic stroke” or
training effects differed between poststroke stages. One system- “stroke” or “cerebrovascular accident” and “training” or “balance
training” or “physical activity” or “physical therapy” or “rehabilita-
atic review reported that favorable effects of balance exercises tion” and “randomized controlled trial” or “RCT” or “randomized
were restricted to the chronic phase (≥6 months post onset), but clinical trial” (Table I in the online-only Data Supplement). Studies
a meta-analysis was not included to substantiate this statement.12 were included if (1) the study population included adults (≥18 years
Nevertheless, several studies that have been published since sug- of age), with a minimal time since stroke of 6 months for all included
gest that exercise therapy may yield significant improvements in participants; (2) the design was an RCT; (3) the intervention studied
was a form of exercise therapy; (4) at least one of the study outcomes
balance capacity in individuals in the chronic phase of stroke.13,14 evaluated balance capacity; (5) the study showed at least moderate-to-
Evaluating the effects of exercise therapy in the chronic high methodological quality based on the PEDro score (see Quality
phase of stroke is of particular interest because the results are appraisal); and (6) the study was published in the English language.
unlikely to be influenced by spontaneous neurological recov- Bibliographies of selected studies were searched manually for addi-
tional relevant studies. The protocol of this review was not previously
ery. Spontaneous recovery generally is apparent in the first 2
published. We adhered to the PRISMA guidelines.21
to 3 months after stroke3,15 and may demonstrate large hetero-
geneity across individuals.8 However, on average, little if any
further recovery is expected beyond 6 months after stroke.16 Quality Appraisal
The Physiotherapy Evidence Database (PEDro) Scale22 23 (range,
Therefore, the purpose of the present systematic review was 0–10) was used to assess methodological quality of the included
to investigate the effects of exercise therapy on balance capac- studies. When a PEDro score was not available from the database,
ity in the chronic phase after stroke. We included articles on the study was scored by 2 reviewers independently (H.D. and M.P.
all types of training regimens that reported measures of bal- or A.H.). In the case of disagreement, an additional assessment was
ance capacity to evaluate training effects. Because we were done by a third reviewer (A.H. or M.P.). Studies were considered to
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Figure 1. PRISMA flow diagram. BBS indicates Berg Balance Scale; COP, center of pressure; EMBASE, Excerpta Medica Database;
PEDro Pysiotherapy evidence database; and RCTs, randomized controlled trials. *Note that some studies report more than one outcome
measure.
2606 Stroke October 2016
groups, ranging from 4.5 to 61.7 hours. In 5 other studies, the found for multisensory training (4 studies; MD=0.38 points
control group did not receive any intervention. Twenty-two [random]; 95% CI, −1.32 to 2.08; P=0.66; I2=22%) and high-
out of the 43 selected studies showed a significant between- intensity aerobic training (4 studies; MD=0.32 points [fixed];
group difference for at least one of the outcome measures 95% CI, −0.69 to 1.34; P=0.53; I2=0%). The induced gains in
reported. This was the case for 11 out of 12 balance and/or BBS scores were not modified by between-group differences
functional weight-shifting training studies, 7 out of 14 gait in intensity of training (P=0.18). The overall postintervention
training studies, 2 out of 7 multisensory training studies, none effects were modified by small studies, but the SES remained
of the high-intensity aerobic exercise training studies, and 3 significant (MD=1.04 points [random]; 95% CI, 0.03–2.06;
out of 6 of the studies with other training regimens. after imputation of 9 studies, Eggert regression intercept
P<0.01; Figure IV in the online-only Data Supplement). Meta
Quality Appraisal regression of PEDro score on immediate postintervention dif-
Three studies were excluded from further analysis because of ferences in means for the BBS studies did not show any modi-
a PEDro score <4 (high risk of bias). PEDro scores of the fying effects (28 studies; slope=0.03 [fixed]; 95% CI, −0.27 to
included studies varied from 4 to 9 (Table II in the online-only 0.32; P=0.85; Figure V in the online-only Data Supplement).
Data Supplement). Of all included studies, 34 studies showed
high quality and 9 moderate quality. Discussion
This systematic review included 43 trials to assess the
Meta-Analysis effects of exercise therapy on balance capacity in people
A total of 21 different outcome measures were used (Figure 1). in the chronic phase after stroke. Meta-analyses showed an
Pooling of results was possible for the BBS (n=28), Functional overall improvement on several clinical balance tests (BBS,
Reach Test (n=5), Sensory Organization Test (SOT) (n=4), and Functional Reach Test, and SOT) after exercise therapy. The
postural sway velocities while standing with eyes open (n=3). sensitivity analysis with subsequent subgroup analyses of the
One of the studies reporting BBS scores did not include an BBS data, however, showed that significant improvements
immediate postintervention measurement but merely reported were restricted to balance and/or functional weight-shifting
follow-up scores.27 This study could therefore only be used training and gait training. Importantly, the induced gains in
in the follow-up analysis. One study did not report postinter- BBS scores were not influenced by differences in the intensity
vention scores but merely prepost intervention differences.28 of training applied between experimental and control arm of
Unfortunately, we could not get in contact with the authors included trials. By specifically focusing on studies conducted
of this study. Therefore, the postintervention outcomes were in the chronic phase after stroke, the present meta-analysis
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calculated by using the mean preintervention scores and the convincingly demonstrates that exercise therapy may induce
pre- to postintervention difference. gains in balance capacity.
Pooling of studies for the immediate postintervention The present meta-analysis showed ambiguous results for
effects showed a significant SES in favor of the intervention outcomes on the level of body functions and structures (SOT;
group for the BBS (28 studies; n=985; MD=2.22 points [ran- posturography measures), but yielded significant improve-
dom]; 95% CI, 1.26–3.17; P<0.01; I2=52%; Figure 2; Table ments after exercise therapy in outcome measures on the ICF
III in the online-only Data Supplement), the Functional Reach level of activities (BBS; Functional Reach Test). This finding
Test (5 studies; n=153; MD=3.12 cm [random]; 95% CI, suggests that the observed improvements in balance capacity
0.90–5.35; P<0.01; I2=74%; Figure 2), and the SOT (4 stud- are most likely because of optimization of compensatory bal-
ies; n=173; MD=6.77% [random]; 95% CI, 0.83–12.7; P=0.03; ance control strategies, such as strengthening of ankle and hip
I2=0%; Figure 2). Nonsignificant SES were found for postural strategies on the nonparetic side, improvement of trunk con-
sway velocities (3 studies; n=89; anterior–posterior direction trol, optimization of stepping strategies, and a more general
MD=0.57 mm/s [random]; 95% CI, −1.18 to 2.31; P=0.52; adjustment of motor responses to altered sensory input and
I2=74%; mediolateral direction MD=0.82 mm/s [random]; 95% body dynamics.7 Yet, it has to be noted that the meta-analyses
CI, −2.55 to 4.20; P=0.63; I2=91%; Figure II in the online-only at the level of body functions and structures were limited by
Data Supplement). Eleven studies reported follow-up data, the number of studies that used the same outcome measure
with a time range after termination of the intervention of 1 (SOT, n=4; postural sway velocity, n=3). In the 43 studies
to 5 months. Pooling showed significant SES after retention, that met our inclusion criteria, we identified a myriad of other
favoring the intervention group, for the BBS (8 studies; n=338; measures at this ICF level, sometimes within a single study,
MD=1.65 points [random]; 95% CI, 0.22–3.07; P=0.02; I2=0%; that often yielded an inconsistent pattern of results.
Figure 3) and the SOT (3 studies; n=151; MD=3.91% [random]; An important finding of the present work is that the benefi-
95% CI, 0.10–7.73; P=0.04; I2=0%; Figure 3). cial effect of exercise therapy was restricted to balance and/or
Sensitivity analysis, which could only be conducted for the functional weight-shifting and gait training. The finding that
immediate postintervention measurement of the BBS, yielded gait training was also effective in improving balance capacities
a significant effect of intervention type (P=0.02). Subgroup may seem somewhat surprising, in light of the critical impor-
analyses for the various types of experimental interventions tance of task specificity of exercise therapy after stroke.25,29
(P<0.01; I2=52%; Figure III in the online-only Data Supplement), Yet, on closer inspection (Table III in the online-only Data
and gait training (10 studies; MD=2.26 points [random]; 95% Supplement), the individual gait training studies that did not
CI, 0.94–3.58; P<0.01; I2=21%). Nonsignificant SES were yield improvements in BBS scores mainly involved treadmill
van Duijnhoven et al Exercise Therapy to Improve Balance After Stroke 2607
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Figure 2. Summary effect sizes immediately post intervention for studies reporting Berg Balance Scale (BBS), Functional Reach Test
(FRT), and Sensory Organization Test (SOT). The diamond is the summary effect size. C indicates control group; E1, experimental group
1; and E2, experimental group 2.
training with (partial) body weight support or robotic gait train- training studies that did report improvements in BBS scores
ing with pelvic stabilization, which procedures greatly assist in often involved additional challenges to balance control during
controlling upright balance during walking. In contrast, the gait walking, such as walking on a treadmill while interacting with
2608 Stroke October 2016
Figure 3. Summary effect sizes of follow-up for studies reporting Berg Balance Scale (BBS) and Sensory Organization Test (SOT). The
diamond is the summary effect size.
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a virtual reality environment or walking while making turn- showed on average 1.6 to 3.3 points improvement in BBS score
ing movements. These observations therefore suggest that, for in the active control condition but yielded superior improve-
gait training to be effective in improving balance capacity, it ments in the experimental intervention groups. Future research
is crucial to include challenging walking exercises, preferably is needed to definitively address the mechanisms underlying
without reduction in degrees of freedom by, for instance, an training-induced balance gains in the chronic phase of stroke.
exoskeleton around the pelvis in robotic gait trainers or by a The presently applied hierarchical classification of train-
harnessed body weight support.30 Yet, establishing the mutual ing regimens allowed us to group interventions that included
effectiveness of various gait training modalities on balance the same type of exercises and to evaluate—in a sensitivity
capacity remains an important subject for future research. analysis—their combined effects on BBS scores relative to
The question arises whether the beneficial effects of balance other intervention types. It must be mentioned, although, that
and/or functional weight-shifting training and of gait train- this method of categorization still left a substantial degree of
ing can be explained by additional improvement of balance heterogeneity in the content of the interventions categorized.
capacities (on top of the level achieved at the end of primary For example, the interventions in the balance and/or func-
rehabilitation), or whether it reflects the reacquisition of skills tional weight-shifting group varied from circuit class training
that have been lost because the cessation of the primary reha- focusing on agility and dynamic balance control34 to hydro-
bilitation process (because of inactivity and related disuse31). therapy-based tai-chi exercises.35 Similarly, the control inter-
Consistent with the latter notion, a previous study32 investigat- ventions were heterogeneous in nature as well. Because of this
ing a community-based, adaptive physical activity program heterogeneity within the relatively small number of studies
for people with chronic stroke reported an average decline in per group (n=8 for balance and/or functional weight-shifting
BBS score of 1.5 points in the inactive control group during training and n=10 for gait training), it is not possible to deter-
a period of 6 months. On the contrary, the plateau phase that mine whether all forms of balance, functional weight-shifting,
is commonly reached ≈6 months post stroke onset may also or gait exercises included in these categories were equally
be because of saturation of the training regimens used during effective. Thus, we recommend future research to focus on the
primary rehabilitation.33 This saturation may be overcome by identification of optimal forms of exercise therapy for improv-
introducing new types of training (eg, dynamic and challenging ing standing balance in the chronic phase post stroke.
balance training, including balance perturbations, dual tasks, This systematic review and meta-analysis was limited by the
and/or gait adaptability exercises) that exploit residual (latent) number of studies included, particularly in the subgroup analy-
recovery potential.33 In favor of this latter notion, the studies in ses, which may have resulted in a type II error (ie, false-nega-
the balance and/or functional weight-shifting training category tive outcome). We considered including studies with an average
van Duijnhoven et al Exercise Therapy to Improve Balance After Stroke 2609
time post onset of >6 months that did not exclusively recruit analysis. A.C.H. Geurts and V. Weerdesteyn performed funding and
participants in the chronic phase after stroke. This would have supervision. H.J.R.v. Duijnhoven, A. Heeren, A.C.H. Geurts, and V.
Weerdesteyn helped with drafting of the article. H.J.R.v. Duijnhoven,
borne the risk, however, of our results being confounded by
A. Heeren, M.A.M. Peters, J.M. Veerbeek, G. Kwakkel, A.C.H. Geurts,
differential effects of training in the various poststroke phases. and V. Weerdesteyn assisted in critical revision of the article.
We therefore decided to adhere to a rigorous inclusion criterion
regarding the minimal time post stroke. In addition, balance
Sources of Funding
capacities after stroke can be influenced by stroke severity and The contribution of V. Weerdesteyn was supported by Veni Grant
stroke location.7 Both factors, however, were not systemati- 916-10-106 of The Netherlands Organization for Scientific Research
cally reported in the included RCTs, and we therefore could (NWO).
not determine the impact of stroke location and stroke sever-
ity on the effects of balance training. Another limitation was Disclosures
the variety of outcome measures used in the literature, which None.
restricted the number of studies that could be considered in
the meta-analysis. Furthermore, the finding that differences References
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