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Effects of Exercise Therapy on Balance

Capacity in Chronic Stroke


Systematic Review and Meta-Analysis
Hanneke J.R. van Duijnhoven, MD, MSc; Anita Heeren, MD, MSc; Marlijn A.M. Peters, MSc;
Janne M. Veerbeek, PhD; Gert Kwakkel, PhD; Alexander C.H. Geurts, MD, PhD*;
Vivian Weerdesteyn, PhD*

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

A fter stroke, a main goal of rehabilitation is to promote


independence in activities of daily living. An important
determinant of activities of daily living performance is stand-
after stroke. Although the vast majority (75%) of people after
stroke regain independent standing-balance capacity,6 weight-
bearing asymmetry and increased postural sway often per-
ing balance, which is a strong predictor of functional recovery1,2 sist, as well as a diminished capacity to voluntarily shift body
and walking capacity3,4 and an important risk factor for falls5 weight or to withstand external perturbations.7 Hence, a key

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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be of high quality when the PEDro score was ≥6 and of moderate


particularly interested whether the type of intervention had a quality when the score was 4 or 5.23 Studies with a score <4 points
differential effect on gains in balance control, we conducted were excluded from further analysis.9,24,25
a subsequent sensitivity analysis. Interventions were catego-
rized based on the type of training regimen (balance and/or Meta-Analysis
functional weight-shifting training, gait training, multisensory For all selected studies, a stepwise categorization of the experimental
training, high-intensity aerobic training, and other training pro- training regimens was performed (Figure I in the online-only Data
grams), and we determined whether this categorization modi- Supplement). Five different categories were distinguished: (1) bal-
fied the overall effect. In addition, we examined whether there ance and/or functional weight-shifting training; (2) gait training;
(3) training with altered sensory input (multisensory training); (4)
was an influence of intensity of training on balance capacity.
high-intensity aerobic training; and (5) other training programs. The
classification process was based on hierarchical exclusion; a training
Methods intervention program was included in a specific category if its pri-
mary content (or added content compared with the control interven-
Definitions tion) did not fit in the categories specified before.
According to the definition of the World Health Organization, we defined From the selected studies, the following data were extracted:
stroke as rapidly developing signs of focal (or global) disturbance of sample size, mean age of participants, mean time post stroke, type
cerebral function lasting >24 hours (unless interrupted by surgery or of study population (ie, community-dwelling people or inpatients),
death), with no apparent nonvascular cause.17 Participants were in the training duration, type of experimental and control training, and
chronic phase after stroke if they were ≥6 months post onset. A study between-group differences in balance-specific outcome measures. If
was identified as a randomized controlled trial (RCT) if the individuals information was missing, we contacted the corresponding author.
(or other units) followed in the trial were definitely or possibly assigned Data were pooled when a particular outcome measure was used in
prospectively to one of 2 (or more) alternative forms of health care using at least 3 RCTs. We did not pool data between outcome measures, as
random allocation.18 We defined exercise therapy as a regimen or plan the reported measures of balance capacity encompass a variety of abil-
of physical activities designed and prescribed for specific therapeutic ities for maintaining, achieving, or restoring a state of balance during
goals with the purpose to restore normal musculoskeletal function or to any posture. Means and SDs of both the postintervention and follow-
reduce pain caused by diseases or injuries (Medline Subject Heading; up measurements were extracted from each study for both the experi-
MeSH). Training modalities using electric devices such as treadmills are mental and control groups. If a study did not report postintervention
included in our definition, but not those using assistive devices such as scores, we asked the authors to provide these. When the authors could
canes, walkers, splints, or functional electric stimulation. not be reached, we calculated the postintervention outcomes by using
Balance capacity was defined as the ability to maintain, achieve, or the mean preintervention scores and the pre- to postintervention differ-
restore a state of balance during any posture.19 This includes all dif- ence, assuming equal variance. A summary effect size (SES) with 95%
ferent aspects of balance capacity as described in a model by Tyson confidence interval (CI) was calculated based on the effect sizes (mean
et al,20 like static and dynamic balance, body alignment, and weight difference [MD]) of the individual studies, calculated as Hedges g.
distribution. Balance outcomes included in this study should assess Between-study variation (statistical consistency) was assessed with
van Duijnhoven et al   Exercise Therapy to Improve Balance After Stroke    2605

the I2 statistic.19 Because heterogeneity between studies is expected, a Results


random-effects model was used for all analyses.26 A sensitivity analy-
sis was performed for the type of experimental intervention, if this Study Identification
intervention type was investigated in at least 3 studies. When a sig- After electronic search of the databases, 43 out of 369 unique
nificant effect was found, we conducted subgroup analyses to iden- hits met the inclusion criteria (Figure 1). Table II in the
tify which intervention yielded improvement in balance outcome and online-only Data Supplement shows the characteristics of the
to identify whether there was an intensity difference in time spent included RCTs. Twelve studies involved balance and/or func-
in exercise therapy between the experimental and control groups. In
tional weight-shifting training, 14 gait training, 7 multisen-
addition, we investigated small-study effects (ie, a trend for smaller
studies to show larger treatment effects) by visual inspection of fun-
sory training, 4 high-intensity aerobic exercises, and 6 other
nel plots. When asymmetry of funnel plots was observed, this was training regimens. Overall, the mean time post stroke ranged
formally tested by Eggert regression intercept and Duval and Tweedie from 7 months to 7.7 years. The total training duration varied
trim and fill. For all analyses, Comprehensive Meta Analysis (Biostat, from 1.9 to 61.7 hours. Seven studies showed a difference in
Englewood, NJ) was used; 2-tailed α was set at 0.05. training intensity between the experimental and the control
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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
in training intensity between experimental and control groups 1. van de Port IG, Kwakkel G, Schepers VP, Lindeman E. Predicting mobil-
were not identified as an effect modifier in the present study ity outcome one year after stroke: a prospective cohort study. J Rehabil
should be interpreted cautiously because this analysis was pos- Med. 2006;38:218–223.
2. Tyson SF, Hanley M, Chillala J, Selley AB, Tallis RC. The relationship
sibly underpowered because of the small number of studies.
between balance, disability, and recovery after stroke: predictive valid-
Finally, the use of the BBS in our sensitivity analysis also ity of the Brunel Balance Assessment. Neurorehabil Neural Repair.
comes with a limitation because this outcome measure has a 2007;21:341–346. doi: 10.1177/1545968306296966.
ceiling effect particularly in the chronic phase after stroke.36 3. Kollen B, van de Port I, Lindeman E, Twisk J, Kwakkel G. Predicting
improvement in gait after stroke: a longitudinal prospective study. Stroke.
Indeed, 12 out of 28 studies reported near-normal BBS scores 2005;36:2676–2680. doi: 10.1161/01.STR.0000190839.29234.50.
(50–56 points) in their intervention groups directly after exer- 4. Dobkin BH, Nadeau SE, Behrman AL, Wu SS, Rose DK, Bowden
cise therapy; in the control groups, this was true for only 6 M, et al. Prediction of responders for outcome measures of locomotor
out of 28 studies. These ceiling effects may have resulted in Experience Applied Post Stroke trial. J Rehabil Res Dev. 2014;51:39–50.
doi: 10.1682/JRRD.2013.04.0080.
an underestimation of therapy effects in the higher functioning 5. Weerdesteyn V, de Niet M, van Duijnhoven HJ, Geurts AC. Falls in indi-
individuals, which effect seems to explain—at least partly—the viduals with stroke. J Rehabil Res Dev. 2008;45:1195–1213.
relatively modest gains on the BBS. Importantly, ceiling effects 6. Smith MT, Baer GD. Achievement of simple mobility milestones after
stroke. Arch Phys Med Rehabil. 1999;80:442–447.
do not seem to account for the differential effects between
Downloaded from http://ahajournals.org by on January 20, 2020

7. Geurts AC, de Haart M, van Nes IJ, Duysens J. A review of standing


intervention types, as revealed by the sensitivity analysis. The balance recovery from stroke. Gait Posture. 2005;22:267–281. doi:
mean baseline BBS score across studies was <48 points for 10.1016/j.gaitpost.2004.10.002.
each intervention type, and there were only 5 out of 28 studies 8. Langhorne P, Bernhardt J, Kwakkel G. Stroke rehabilitation. Lancet.
2011;377:1693–1702. doi: 10.1016/S0140-6736(11)60325-5.
reporting BBS scores of >50 points (divided for 3 interven- 9. Peppen Rv, Kwakkel G, Wood-Dauphinee S, Hendriks H, Wees Pvd,
tion types). This leaves sufficient room for improvement and, Dekker J. The impact of physical therapy on functional outcomes after
therefore, cannot explain the lack of training-induced gains stroke: what’s the evidence? Clin Rehabil. 2004;18:833–862.
after multisensory and aerobic training. Yet, for future studies 10. French B, Thomas L, Leathley M, Sutton C, McAdam J, Forster A, et
al. Does repetitive task training improve functional activity after stroke?
evaluating training effects in high-functioning stroke survivors, A Cochrane systematic review and meta-analysis. J Rehabil Med.
we recommend to use a different primary outcome on the ICF 2010;42:9–14. doi: 10.2340/16501977-0473.
level of activities. One such alternative may be the mini-Bal- 11. Barclay-Goddard R, Stevenson T, Poluha W, Moffatt M, Taback S. Force
ance Evaluation System Test (mini-BESTest), which is a test platformfeedback for standing balance training after stroke (review).
Cochrane Database Syst Rev. 2004;CD004129.
of dynamic balance that has shown high reliability and a lower 12. Lubetzky-Vilnai A, Kartin D. The effect of balance training on balance
ceiling effect than the BBS in people after stroke.37,38 performance in individuals poststroke: a systematic review. J Neurol
Phys Ther. 2010;34:127–137. doi: 10.1097/NPT.0b013e3181ef764d.
13. Heeren A, van Ooijen M, Geurts AC, Day BL, Janssen TW, Beek PJ,
Conclusions et al. Step by step: a proof of concept study of C-Mill gait adaptability
Our systematic review and meta-analysis shows that balance training in the chronic phase after stroke. J Rehabil Med. 2013;45:616–
capacity can be improved by exercise therapy in the chronic 622. doi: 10.2340/16501977-1180.
14. Dean CM, Rissel C, Sherrington C, Sharkey M, Cumming RG, Lord
phase after stroke. Specifically, balance and/or functional
SR, et al. Exercise to enhance mobility and prevent falls after stroke: the
weight-shifting training and gait training were identified as suc- community stroke club randomized trial. Neurorehabil Neural Repair.
cessful training regimens. We therefore recommend exercise 2012;26:1046–1057. doi: 10.1177/1545968312441711.
therapy for people in the chronic phase after stroke for improv- 15. Kwakkel G, Kollen B, Twisk J. Impact of time on improvement of
outcome after stroke. Stroke. 2006;37:2348–2353. doi: 10.1161/01.
ing balance capacities, provided that training regimens include STR.0000238594.91938.1e.
exercises targeting balance, weight-shifting, and/or gait. 16. Kwakkel G, Kollen BJ. Predicting activities after stroke: what is clinically rel-
evant? Int J Stroke. 2013;8:25–32. doi: 10.1111/j.1747-4949.2012.00967.x.
17. Truelsen T, Mähönen M, Tolonen H, Asplund K, Bonita R, Vanuzzo
Acknowledgments D; WHO MONICA Project. Trends in stroke and coronary heart dis-
A.C.H. Geurts and V. Weerdesteyn assisted in study conception and ease in the WHO MONICA Project. Stroke. 2003;34:1346–1352. doi:
design. H.J.R.v. Duijnhoven, A. Heeren, and M.A.M. Peters helped 10.1161/01.STR.0000069724.36173.4D.
with search and quality appraisal. H.J.R.v. Duijnhoven, A. Heeren, J.M. 18. Higgins JPT, Green S, eds. Cochrane Handbook for Systematic Reviews
Veerbeek, A.C.H. Geurts, and V. Weerdesteyn done analysis and inter- of Interventions Version 5.1.0 [updated March 2011]. The Cochrane
pretation. H.J.R.v. Duijnhoven and J.M. Veerbeek performed statistical Collaboration. 2011. https://www.cochrane-handbook.org.
2610  Stroke  October 2016

19. Pollock AS, Durward BR, Rowe PJ, Paul JP. What is balance? Clin 30. Mehrholz J, Pohl M, Elsner B. Treadmill training and body weight sup-
Rehabil. 2000;14:402–406. port for walking after stroke (review). Cochrane Database Syst Rev.
20. Tyson SF, DeSouza LH. A clinical model for the assessment of posture 2014;CD002840.
and balance in people with stroke. Disabil Rehabil. 2003;25:120–126. 31. Wolfe CD, Crichton SL, Heuschmann PU, McKevitt CJ, Toschke AM,
doi: 10.1080/0963828021000013944. Grieve AP, et al. Estimates of outcomes up to ten years after stroke:
21. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred analysis from the prospective South London Stroke Register. PLoS Med.
reporting items for systematic reviews and meta-analyses: the PRISMA 2011;8:e1001033. doi: 10.1371/journal.pmed.1001033.
statement. J Clin Epidemiol. 2009;62:1006–1012. doi: 10.1016/j. 32. Stuart M, Benvenuti F, Macko R, Taviani A, Segenni L, Mayer F, et al.
jclinepi.2009.06.005. Community-based adaptive physical activity program for chronic stroke:
22. Morton NAd. The pedro scale is a valid measure of the methodologi- feasibility, safety, and efficacy of the Empoli model. Neurorehabil
cal quality of clinical trials: a demographic study. Aust J Physiother. Neural Repair. 2009;23:726–734. doi: 10.1177/1545968309332734.
2009;55:129–133. 33. Page SJ, Gater DR, Bach-Y-Rita P. Reconsidering the motor recovery
23. Maher CG, Sherrington C, Herbert RD, Moseley AM, Elkins M. plateau in stroke rehabilitation. Arch Phys Med Rehabil. 2004;85:1377–
Reliability of the PEDro scale for rating quality of randomized con-
1381. doi: 10.1016/j.apmr.2003.12.031.
trolled trials. Phys Ther. 2003;83:713–721.
34. Marigold DS, Eng JJ, Dawson AS, Inglis JT, Harris JE, Gylfadóttir S.
24. Kwakkel G, Veerbeek JM, van Wegen EE, Wolf SL. Constraint-induced
Exercise leads to faster postural reflexes, improved balance and mobility,
movement therapy after stroke. Lancet Neurol. 2015;14:224–234. doi:
and fewer falls in older persons with chronic stroke. J Am Geriatr Soc.
10.1016/S1474-4422(14)70160-7.
2005;53:416–423. doi: 10.1111/j.1532-5415.2005.53158.x.
25. Veerbeek JM, van Wegen E, van Peppen R, van der Wees PJ, Hendriks E,
35. Noh DK, Lim JY, Shin HI, Paik NJ. The effect of aquatic therapy
Rietberg M, et al. What is the evidence for physical therapy poststroke?
A systematic review and meta-analysis. PLoS One. 2014;9:e87987. doi: on postural balance and muscle strength in stroke survivors–a ran-
10.1371/journal.pone.0087987. domized controlled pilot trial. Clin Rehabil. 2008;22:966–976. doi:
26. Riley RD, Higgins JP, Deeks JJ. Interpretation of random effects meta- 10.1177/0269215508091434.
analyses. BMJ. 2011;342:d549. 36. Blum L, Korner-Bitensky N. Usefulness of the Berg Balance Scale in
27. Schmid AA, Van Puymbroeck M, Altenburger PA, Schalk NL, Dierks stroke rehabilitation: a systematic review. Phys Ther. 2008;88:559–566.
TA, Miller KK, et al. Poststroke balance improves with yoga: a pilot doi: 10.2522/ptj.20070205.
study. Stroke. 2012;43:2402–2407. doi: 10.1161/STROKEAHA. 37. Tsang CS, Liao LR, Chung RC, Pang MY. Psychometric properties of
112.658211. the Mini-Balance Evaluation Systems Test (Mini-BESTest) in commu-
28. Dias D, Laíns J, Pereira A, Nunes R, Caldas J, Amaral C, et al. Can we nity-dwelling individuals with chronic stroke. Phys Ther. 2013;93:1102–
improve gait skills in chronic hemiplegics? A randomised control trial 1115. doi: 10.2522/ptj.20120454.
with gait trainer. Eura Medicophys. 2007;43:499–504. 38. Chinsongkram B, Chaikeeree N, Saengsirisuwan V, Viriyatharakij
29. Langhorne P, Coupar F, Pollock A. Motor recovery after stroke: a N, Horak FB, Boonsinsukh R. Reliability and validity of the Balance
systematic review. Lancet Neurol. 2009;8:741–754. doi: 10.1016/ Evaluation Systems Test (BESTest) in people with subacute stroke. Phys
S1474-4422(09)70150-4. Ther. 2014;94:1632–1643. doi: 10.2522/ptj.20130558.
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