Archives of Physical Medicine and Rehabilitation

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Archives of Physical Medicine and Rehabilitation 2020;101:141-53

SYSTEMATIC REVIEW

Functional Balance and Postural Control

Improvements in Patients With Stroke After
Noninvasive Brain Stimulation: A Meta-analysis
Nyeonju Kang, PhD,a,b Ru Da Lee, MS,b Joon Ho Lee, BS,a,b Moon Hyon Hwang, PhDb,c
From the aDivision of Sport Science & Sport Science Institute, Incheon National University, Incheon; bDepartment of Human Movement
Science, Incheon National University, Incheon; and cDivision of Health and Kinesiology, Incheon National University, Incheon, South Korea.

Abstract
Objectives: The postural imbalance poststroke limits individuals’ walking abilities as well as increase the risk of falling. We investigated the
short-term treatment effects of noninvasive brain stimulation (NIBS) on functional balance and postural control in patients with stroke.
Data Sources: We started the search via PubMed and the Institute for Scientific Information’s Web of Science on March 1, 2019 and concluded
the search on April 30, 2019.
Study Selection: The meta-analysis included studies that used either repetitive transcranial magnetic stimulation (rTMS) or transcranial direct
current stimulation (tDCS) for the recovery of functional balance and postural control poststroke. All included studies used either randomized
controlled trial or crossover designs with a sham control group.
Data Extraction: Three researchers independently performed data extraction and assessing methodological quality and publication bias. We
calculated overall and individual effect sizes using random effects meta-analysis models.
Data Synthesis: The random effects meta-analysis model on the 18 qualified studies identified the significant positive effects relating to NIBS in
terms of functional balance and postural control poststroke. The moderator-variable analyses revealed that these treatment effects were only
significant in rTMS across patients with acute, subacute, and chronic stroke whereas tDCS did not show any significant therapeutic effects. The
meta-regression analysis showed that a higher number of rTMS sessions was significantly associated with more improvements in functional
balance and postural control poststroke.
Conclusions: Our systematic review and meta-analysis confirmed that NIBS may be an effective option for restoring functional balance and
postural control for patients with stroke.
Archives of Physical Medicine and Rehabilitation 2020;101:141-53
ª 2019 by the American Congress of Rehabilitation Medicine

Stroke typically causes long-term impairments such as asym-
metrical muscle weakness between limbs, impaired proprioceptive
capabilities, sensory loss, vision problems, and spasticity.1,2
Moreover, these sensorimotor deficits interfere with various
lower limb functions, including balance, postural control, and gait
capabilities, in patients with stroke.1,3 Specifically, 83% of pa-
tients with acute stroke experience difficulty in executing suc-
cessful balance and postural control.4 Common deficits in
functional balance and postural control include excessive weight-
Supported by Incheon National University, South Korea (grant no. 2017-0389).
Disclosures: none.
bearing asymmetry toward the nonparetic leg in a relatively static
position, greater postural sway, reduced limits of stability, and
impaired anticipatory postural adjustments.5 Further, the postural
imbalance could remain at a chronic stage poststroke, thereby
additionally limiting the individual’s walking abilities as well as
increasing his or her risk of falling.4,6,7 Functional balance and
postural control rehabilitation are therefore crucial for patients to
regain independence in activities of daily living and to enhance
their quality of life poststroke.5,7
Conventional balance and postural rehabilitation protocols
often advocate biofeedback training and repetitive task-specific
training.8 However, the treatment effects of these activity-
dependent therapies may be relatively constrained because the
intensity is insufficient to optimize neural plasticity.9 In recent

0003-9993/19/$36 - see front matter ª 2019 by the American Congress of Rehabilitation Medicine
https://doi.org/10.1016/j.apmr.2019.09.003
142 N. Kang et al

Fig 1 Flow chart for study identification.

years, many stroke researchers have focused on the application of whereas tDCS may modify the transmembrane neuronal potentials
noninvasive brain stimulation (NIBS) for lower limb rehabilitation by delivering weak electrical currents to the targeted region.12,13
because NIBS may increase or decrease brain activity in specific Despite these different neurophysiological mechanisms, both
key regions.10,11 For balance and postural control rehabilitation, techniques can potentially cause excitatory and inhibitory effects
NIBS researchers frequently use repetitive transcranial magnetic on brain activity based on the specific stimulation protocol. For
stimulation (rTMS) and transcranial direct current stimulation example, rTMS can modulate cortical excitability in certain brain
(tDCS).10,11 rTMS may evoke action potentials by inducing regions through the delivery of repetitive single TMS with a
electrical currents into the targeted area using magnetic fields specific frequency: (1) high-frequency rTMS (
5Hz) increases
brain activation and (2) low-frequency rTMS (1Hz) decreases
brain activation. Similarly, tDCS can change cortical excitability
List of abbreviations: by stimulating the scalp with a certain electrode (1-2mA): (1)
CI confidence interval anodal tDCS increases brain activation and (2) cathodal tDCS
M1 primary motor cortex decreases brain activation. Although cortical representation of the
NIBS noninvasive brain stimulation leg muscles is located deep and near the midline, several previous
PEDro the Physiotherapy Evidence Database studies have provided the evidence that NIBS techniques can
rTMS repetitive transcranial magnetic stimulation reach the deep structures that modulate the brain activations
SMA supplementary motor area
related to the lower leg muscles.14,15
SMD standardized mean difference
Early rTMS and tDCS studies on lower limb recovery post-
tDCS transcranial direct current stimulation
stroke used techniques to balance the asymmetrical levels of

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NIBS and balance recovery poststroke 143

Table 1 Demographic and clinical information for participants

Study Total Affected Pretreatment Recovery
Study Design No. Age (y) Sex TSO (mo) Stroke Type Hemisphere Impairment Level Stage
rTMS Studies
Cha et al23 RCT 30 62.6 15 F, 15 M 2.5 19 I, 11 H NR WGCZ32.0/42 Subacute
Cha et al24 RCT 36 59.0 17 F, 19 M 1.8 NR NR BIZ5.8/100 Subacute
Choi et al26 Crossover 30 67.9 3 F, 27 M 46.8 20 I, 10 H 15 L, 15 R BBSZ34.5/56 Chronic
Forogh et al28 RCT 26 66.0 10 F, 16 M NR 26 I 18 L, 8R BBSZ44.6/56 Chronic
Huang et al30 RCT 38 61.6 15 F, 23 M 1.9 25 I, 13 H 21 L, 17 R NIHSSZ10.2/42 Subacute
Ji et al31 RCT 30 55.0 13 F, 17 M 1.7 21 I, 9H 13 L, 17 R MMSE-KZ26.9/29 Subacute
Kim et al32 RCT 32 66.0 15 F, 17 M 0.5 32 I NR BBSZ25.0/56 Acute
Lin et al33 RCT 32 60.3 11 F, 21 M 1.2 22 I, 10 H 17 L, 15 R BIZ36.2/100 Subacute
Vignon et al38 Crossover 9 NR NR NR NR NR NR Chronic
tDCS Studies
Andrade et al22 RCT 60 69.1 25 F, 35 M 2.7 60 I NR NIHSSZ9.5/42 Subacute
Chang et al25 RCT 24 62.8 9 F, 15 M 0.5 24 I 11 L, 13 R FMA-LEZ29.8/32 Acute
Danzl et al27 RCT 8 67.8 4 F, 4 M 48.0 6 I, 2 H 8L FACZ2.5/5 Chronic
Fruhauf et al29 Crossover 30 61.0 7 F, 23 M 37.0 22 I, 8 H 15 L, 15 R FMSZ65.5/226 Chronic
Manji et al34 Crossover 30 63.0 9 F, 21 M 4.7 17 I, 13 H NR FMA-LEZ21.9/32 Subacute
Saeys et al35 Crossover 31 63.2 14 F, 17 M 1.4 26 I, 5 H 17 L, 14 R POMAZ8.6/28 Subacute
Seo et al36 RCT 21 62.0 5 F, 16 M 114.0 16 I, 5 H 8 L, 13 R FACZ3.6/5 Chronic
Sohn et al37 Crossover 11 58.5 2 F, 9 M 2.1 4 I, 7 H 5 L, 6 R NR Subacute
Zandvliet et al39 RCT 25 57.5 7 F, 18 M 107.8 11 I, 4 H 6 L, 9 R BBSZ 53/56 Chronic
NOTE. The time since stroke onset is the interval between stroke onset and treatment initiation.
Abbreviations: BI, Barthel Index; F, female; FAC, functional ambulation category; FMS, Fugl-Meyer Scale; H, hemorrhagic; I, ischemic; L, left; FMA-LE,
lower limb subscale of Fugl-Meyer Assessment; M, male; MMSE-K, Mini-Mental State Examination-Korean; NIHSS, National Institutes of Health Stroke
Scale; NR, not reported; POMA, performance oriented mobility assessment; R, right; RCT, randomized controlled trial; TSO, time since stroke onset; WGC,
Wisconsin Gait Scale.

cortical excitatory and interhemispheric inhibition between the Methods

ipsilesional and contralesional hemispheres.11,16 Recently, alter-
native perspectives have emphasized the supportive role of the
contralesional hemisphere during the bihemispheric control of
foot movements. Accordingly, NIBS protocols developed to
upregulate contralesional hemisphere activation may contribute to
lower limb rehabilitation.5,17 Previous meta-analyses found sig-
nificant quantitative findings that applying rTMS and tDCS to the
leg representation of either the ipsilesional or contralesional pri-
mary motor cortex (M1) improved gait functions in patients with
stroke.18-20 Despite the potential benefits of rTMS and tDCS on
lower limb function recovery, to date no studies have determined
via meta-analytic approaches whether rTMS and tDCS in-
terventions can improve functional balance and postural control in
patients with stroke.
The purpose of this systematic review and meta-analysis was
to investigate the effects of different rTMS and tDCS protocols on
functional balance and postural control in patients with stroke. In
this meta-analysis, we focused on the short-term effects by
quantifying the changes in functional balance and postural control
from the baseline to immediately posttest following the applica-
tion of NIBS techniques. Moreover, we addressed the following 3
specific questions: (1) Do the short-term treatment effects be-
tween rTMS and tDCS interventions differ? (2) Does NIBS
improve functional balance and postural control in patients with
acute and subacute stroke and also in patients with chronic
stroke? and (3) Are a higher number of NIBS treatment sessions
using rTMS and tDCS associated with greater short-term treat-
ment effects?
Literature search and study identification
Consistent with the Preferred Reporting Items for Systematic
Reviews and Meta-Analyses statement,21 we conducted a sys-
tematic review and meta-analysis. Our literature search focused on
stroke studies that used either tDCS or rTMS for the recovery of
functional balance and postural control. We started the search via
PubMed and Institute for Scientific Information’s Web of Science
on March 1, 2019, and concluded the search on April 30, 2019.
We used the following keywords: (1) “stroke or brain infarction or
cerebrovascular disease,” “tDCS or transcranial direct current
stimulation,” and “balance or posture or postural control” and (2)
“stroke or brain infarction or cerebrovascular disease,” “rTMS or
repetitive transcranial magnetic stimulation,” and “balance or
posture or postural control.” The inclusion criteria were: (1) a
randomized controlled trial or a crossover study; (2) the inclusion
of a sham control group; and (3) the testing of changes in func-
tional balance and postural control poststroke. We excluded re-
view articles, case studies, and animal studies. Three researchers
independently performed the literature search to minimize bias.
Figure 1 displays the study inclusion and exclusion procedures.
Initially, a computerized literature search found 227 potential ar-
ticles. After reading the titles, abstracts, and text, we excluded 209
articles because of (1) 52 duplicated articles; (2) 13 review arti-
cles; (3) 9 case studies; (4) 2 animal studies; and (5) 133 articles
that were not related to the topic of the current meta-analysis. The
remaining 18 studies qualified for the meta-analysis.22-39

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144 N. Kang et al

Table 2 Specific parameters for stimulation protocol

Retention Active
Study Treatment Test Session Stimulation Site Parameter Setup
rTMS studies
Cha et al23 rTMS before MRT N 20 L-rTMS (1Hz) iCerebellum 100% RMT, 900 pulses, 15 min, 70-mm
figure-8 coil
Cha et al24 rTMS before MRT N 20 L-rTMS (1Hz) iM1* 20 min, 70-mm figure-8 coil
Choi et al26 rTMS during CTx Y (4wk) 20 H-rTMS (10Hz) iM1y 90% RMT, 1000 pulses, 10 min, figure-8
coil
Forogh et al28 rTMS Y (12wk) 5 L-rTMS (1Hz) cM1* 1200 pulses, 20 min, 70-mm figure-8 coil
Huang et al30 rTMS before PT Y (12wk) 15 L-rTMS (1Hz) cM1y 120% MT, 900 pulses, 15 min, 110-mm
double-cone coil
Ji et al31 rTMS before CPT N 20 H-rTMS (10Hz) iM1* 2000 pulses, 15 min, 70-mm figure-8 coil
Kim et al32 rTMS and CRS Y (4wk) 5 L-rTMS (1Hz) iCerebellum 100% RMT, 900 pulses, 75-mm figure-8
coil
Lin et al33 rTMS before PT N 15 L-rTMS (1Hz) cM1y 130% MT, 900 pulses, 15 min, 70-mm
figure-8 coil
Vignon et al38 rTMS N 10 L-rTMS (1Hz) cM1* NR
tDCS studies
Andrade et al22 tDCS and PRP Y (12wk) 10 A-tDCS iM1* 2 mA, 35 cm2, 0.06 mA/cm2
Chang et al25 tDCS during CPT N 10 A-tDCS iM1y 2 mA, 7.07 cm2, 0.28 mA/cm2, 10 min
Danzl et al27 tDCS before LT-RGO Y (4wk) 12 A-tDCS iM1y 2 mA, 25 cm2, 0.08 mA/cm2, 20 min
Fruhauf et al29 tDCS N 1 A-tDCS iM1* 2 mA, 35 cm2, 0.06 mA/cm2, 20 min
Manji et al34 tDCS during BWSTT N 14 A-tDCS SMA 1 mA, 35 cm2, 0.03 mA/cm2, 20 min
Saeys et al35 tDCS and PT þ OT N 16 Bi-tDCS biM1* 1.5 mA, 35 cm2, 0.04 mA/cm2, 20 min
Seo et al36 tDCS before RAGT Y (4wk) 10 A-tDCS iM1y 2 mA, 35 cm2, 0.06 mA/cm2, 20 min
Sohn et al37 tDCS N 1 A-tDCS iM1y 2 mA, 25 cm2, 0.08 mA/cm2, 10 min
Zandvliet et al39 tDCS N 1 A-tDCS cCerebellum 1.5mA, 3.14 cm2, 0.48 mA/cm2, 20 min
Abbreviations: A-tDCS, anodal tDCS; bi, bilateral hemispheres; BWSTT, body weight-supported treadmill training; c, contralesional hemisphere; C-tDCS,
cathodal tDCS; CPT, conventional physical therapy; CRS, conventional rehabilitation service; CTx, conservative treatment; H-rTMS, high-frequency of
rTMS; i, ipsilesional hemisphere; L-rTMS, low-frequency of rTMS; LT-RGO, locomotor training with a robotic gait orthosis; M1, primary motor cortex;
MLPTT, mediolateral postural tracking task; MRT, mirror therapy; MT, motor threshold; N, no; OT, occupational therapy; PRP, physical rehabilitation
program; PT, physical therapy; RAGT, robot-assisted gait training; RMT, resting motor threshold; Y, yes.
* Indicates studies that used either rTMS or tDCS on the M1 (ie, C3 or C4 in the electroencephalography 10/20 system).
y
Denotes studies that applied either rTMS or tDCS on the leg area of the M1 (ie, CZ in the electroencephalography 10/20 system).

Functional balance and postural control
assessments
The primary outcome measures for assessing functional balance
and postural control changes from the 18 qualified studies
involved: (1) the Berg Balance Scale (BBS); (2) postural sway; (3)
postural assessment scale for stroke; (4) the Tinetti test (balance
section); and (5) the trunk control test. Twelve of the 18 included
studies reported clinical scores to estimate functional balance and
postural control (ie, 8 BBS comparisons, 2 postural assessment
scale for stroke comparisons, and 1 Tinetti test comparison; 1
trunk control test comparison). The remaining 6 studies used
functional assessments that quantified postural sway changes (eg,
spatial amplitude and variability of the center of pressure) during
the specific static balance tests.
Meta-analytic approaches
We executed all the statistical data synthesis procedures using
Comprehensive Meta-Analysis softwarea version 3.0. The individ-
ual and overall effect sizes were calculated using standardized mean
difference (SMD) with a 95% confidence interval (CI).40 Increased
positive SMD values denoted that active rTMS and tDCS protocols
showed greater improvements in functional balance and postural
control than the sham control conditions. Based on the traditional
assumption that no common effects exist across individual
studies,40,41 we used random effects meta-analysis models.
To measure the variability levels across the qualified studies,
we used the Higgins and Green I2 test.42 An I2 greater than 75%
indicated substantial heterogeneity levels. The publication bias
tests included: (1) comparing an original funnel plot with a revised
funnel plot after applying the trim-and-fill technique43 and (2)
Egger regression test.44 Egger regression test was based on the
null hypothesis that symmetry exists in the funnel plot. Thus, a P
value for the intercept (b0) less than .05 indicated a violation of
the symmetry assumption, representing high publication bias.44
Finally, for each qualified study, we estimated a methodological
quality using the Physiotherapy Evidence Database (PEDro)
scale45 and Cochrane risk of bias assessment.46
Moreover, we performed 2 moderator-variable analyses: (1)
rTMS vs tDCS and (2) acute and subacute vs chronic stages
poststroke.47 Finally, we conducted a random effects meta-
regression analysis to determine how many NIBS treatment ses-
sions (ie, the explanatory variable) were associated with levels of

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NIBS and balance recovery poststroke

Table 3 Methodological quality assessment using PEDro score
rTMS Studies tDCS Studies
Cha Cha Choi Huang Fruhauf Ji Kim Lin Vignon Andrade Chang Danzl Forogh Manji Saeys Seo Sohn Zandvliet
Criteria et al23 et al24 et al26 et al30 et al29 et al31 et al32 et al33 et al38 et al22 et al25 et al27 et al28 et al34 et al35 et al36 et al37 et al39
1. Eligibility criteria were 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1 1
specified.
2. Subjects were randomly 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
allocated to groups (in a
crossover study, subjects
were randomly allocated an
order in which treatments
were received).
3. Allocation was concealed. 1 1 1 0 0 1 1 0 0 1 1 0 1 0 1 1 0 1
4. The groups were similar at 1 0 1 0 1 1 0 1 0 1 1 1 1 1 1 1 0 0
baseline regarding the most
important prognostic
indicators.
5. There was blinding of all 1 0 0 1 1 1 1 1 1 1 0 1 1 1 1 1 1 1
subjects.
6. There was blinding of all 0 0 0 0 1 0 0 0 0 0 0 1 0 0 1 1 0 0
therapists who administered
the therapy.
7. There was blinding of all 1 1 1 1 1 1 1 1 1 1 0 1 1 1 1 1 1 0
assessors who measured at
least 1 key outcome.
8. Measures of at least 1 key 0 1 1 1 1 1 0 1 0 1 1 0 1 1 1 0 1 1
outcome were obtained from
more than 85% of the
subjects initially allocated to
groups.
9. All subjects for whom 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
outcome measures were
available received the
treatment or control
condition as allocated or,
where this was not the case,
data for at least 1 key
outcome was analyzed by
“intention to treat.”
10. The results of between- 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
group statistical
comparisons are reported for
at least 1 key outcome.

145
(continued on next page)
146 N. Kang et al

improvement in functional balance and postural control (ie, the

Sohn Zandvliet
dependent variable).46,48

et al25 et al27 et al28 et al34 et al35 et al36 et al37 et al39

1

8
Results
1

8
Participant and study characteristics
Vignon Andrade Chang Danzl Forogh Manji Saeys Seo

10
A total of 18 studies qualified for this meta-analysis. We therefore
examined the therapeutic effects of either rTMS or tDCS in-
terventions on postural imbalance in 503 patients with stroke.
1

11
tDCS Studies

Eleven studies investigated patients with acute and subacute stroke

(ie, 2 acute studies and 9 subacute studies), and 7 studies focused
on patients in a chronic stage poststroke. Twelve studies were
1

randomized controlled trials, and 6 studies used a crossover

design. Table 1 shows the specific details of the participants’
characteristics.
1

10

NIBS protocols
1

For this meta-analysis, 9 rTMS and 9 tDCS studies were assessed.

Ten studies used excitatory NIBS protocols: (1) 2 used high-
frequency rTMS and 6 used anodal tDCS on the ipsilesional M1;
1

(2) 1 used anodal tDCS on the supplementary motor area (SMA);

et al23 et al24 et al26 et al30 et al29 et al31 et al32 et al33 et al38 et al22

and (3) one used anodal tDCS on the cerebellum. On the other
hand, 7 studies used inhibitory NIBS protocols: (1) 4 used low-
10
1

frequency rTMS on the contralesional M1; (2) 1 used low-

frequency rTMS on the ipsilesional hemisphere; and (3) 2 used
low-frequency rTMS on the cerebellum. One study applied both
1

anodal tDCS on the ipsilesional M1 and cathodal tDCS on the

contralesional M1. Thirteen studies (ie, 7 rTMS studies and 6
Lin

tDCS studies) applied NIBS together with motor training, whereas

5 studies (ie, 2 rTMS studies and 3 tDCS studies) used only NIBS.
Kim

Fifteen studies administered multiple sessions (ie, 5-20 sessions)

1

of NIBS, and 3 studies used a single session of NIBS. Table 2

shows the specific details of the NIBS protocols.
10
1
Huang Fruhauf Ji
rTMS Studies

Methodological quality assessments

10
1

For the 18 qualified studies, the mean and SD of the PEDro scores,
which included 11 items, were 8.91.2 (range, 6-11). Given that a
PEDro score between 7 and 11 indicates a high-quality study, the
included studies had relatively good methodological quality.
1

Table 3 displays the specific PEDro scores for each included study.
Choi

Moreover, although the Cochrane risk of bias assessment revealed

1

some risk of bias concerns regarding allocation concealment, se-

lective reporting, and other forms of bias, all the included studies
Cha

revealed a relatively low risk across the selection, performance

1

detection, and attrition bias sections (fig 2).

Cha

Meta-analytic findings
point measures and measures
of variability for at least 1

The random effects meta-analysis model identified significant

11. The study provides both

positive effects relating to NIBS in terms of functional balance

and postural control poststroke (SMD, 0.380; SE, 0.108; 95% CI,
Table 3 (continued )

0.169-0.592; zZ3.523; P<.0001 [18 total comparisons; fig 3]).

The heterogeneity level was moderate (I2Z49.5%), and the pub-
key outcome.

lication bias was relatively minimal: (1) a revised funnel plot

with 1 imputed value (fig 4) and (2) Egger regression intercept
Criteria

(b0)Z1.31 and PZ.19.

Total

The first moderator-variable analysis showed that rTMS and

tDCS had different treatment effects (see fig 3). Nine of the rTMS

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NIBS and balance recovery poststroke
Fig 2 Cochrane risk of bias assessment.
comparisons revealed a significant therapeutic effect on functional
balance and postural control poststroke (SMD, 0.475; SE, 0.145;
95% CI, 0.192-0.759; zZ3.284; PZ.001; I2Z36.6%), whereas 9
of the tDCS comparisons did not show significant effects (SMD,
0.294; SE, 0.162; 95% CI, -0.024 to 0.611; zZ1.813;
PZ.070; I2Z58.7%).
Given that the treatment effects of rTMS and tDCS were
different, we performed a second moderator-variable analysis and
meta-regression analysis for each NIBS protocol, respectively.
The second moderator-variable analysis of the rTMS protocols
revealed significant positive effects for both acute and subacute
patients (6 comparisons; SMD, 0.574; SE, 0.229; 95% CI, 0.126-
1.021; zZ2.510; PZ.012; I2Z57.0%; fig 5) and chronic patients
(3 comparisons; SMD, 0.328; SE, 0.159; 95% CI, 0.016-0.641;
zZ2.059; PZ.040; I2Z0.0%; see fig 5). However, the analysis of
the tDCS protocols failed to reveal any significant treatment ef-
fects (fig 6): (1) patients with acute and subacute stroke based on 5
comparisons (SMD, 0.419; SE, 0.314; 95% CI, -0.196 to 1.034;
zZ1.336; PZ.181; I2Z75.6%); and (2) chronic patients based on
4 comparisons (SMD, 0.220; SE, 0.134; 95% CI, -0.043 to 0.483;
zZ1.637; PZ.102; I2Z0.0%).
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147
The random effects meta-regression analysis revealed a sig-
nificant relationship between the number of stimulation sessions
and the treatment effects of rTMS on functional balance and
postural control: YZ-0.0932þ0.0424X; PZ.03; R2Z0.60 (fig 7).
According to this finding, a higher number of rTMS sessions
were associated with increased improvements in functional bal-
ance and postural control poststroke. However, the analysis did
not reveal a significant relationship for the tDCS: YZ0.4711-
0.0212X; PZ.24.
Discussion
The current systematic review and meta-analysis investigated the
effects of rTMS and tDCS on functional balance and postural
control in patients with stroke. The meta-analytic findings indi-
cated that the application of NIBS provided significant positive
short-term effects on postural imbalance poststroke. However, the
moderator-variable analyses revealed that these treatment effects
were only significant for rTMS across the patients with acute,
subacute, and chronic stroke. tDCS, on the other hand, did not
148 N. Kang et al

Fig 3 Short-term treatment effects of NIBS.

show any significant therapeutic effects. Finally, the meta- The meta-analytic findings demonstrated the significant posi-
regression analysis showed that a higher number of rTMS ses- tive effects of NIBS on balance and posture control function in
sions was significantly associated with more improvements in patients with stroke. Although many studies have provided evi-
functional balance and postural control poststroke. dence that NIBS effectively improves upper limb function such as

Fig 4 Publication bias estimation. Funnel plot of SE by SMD. White circles denote original 18 comparisons and a white diamond means an
original overall effect size. Black circles indicate imputed values and a black diamond means a revised overall effect size after applying the trim-
and-fill technique.

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NIBS and balance recovery poststroke
Fig 5 Moderator-variable analysis on rTMS treatment effects. Acute and subacute stages vs chronic stage.
muscle strength and movement control,49,50 findings regarding the
potential treatment effects of NIBS interventions on the functional
activities of the lower extremities are limited. Recently, several
stroke meta-analyses revealed that NIBS effectively increases
walking speed and mobility.18-20 Beyond gait function improve-
ments poststroke, a prior meta-analysis study failed to show sig-
nificant positive effects on balance function; however, these
findings were based on only 3 comparisons.18 To the best of our
knowledge, the current meta-analytic findings are the first to
report the treatment effects of NIBS on reducing postural imbal-
ance poststroke using a relatively high number of studies.
Differences in the treatment effects of rTMS
and tDCS
Interestingly, despite the therapeutic effects on functional balance
and postural control collapsed across the rTMS and tDCS
Fig 6 Moderator-variable analysis on tDCS treatment effects. Acute and subacute stages vs chronic stage.
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149
interventions, our moderator-variable analysis identified a signif-
icant overall effect size for the rTMS protocols. The different
treatment effects between the rTMS and tDCS were consistent
with previous meta-analytic findings that rTMS combined with
movement training significantly improved gait speed in patients
with stroke whereas tDCS combined with movement training did
not enhance gait speed.20,51 In particular, Vaz et al20 suggested the
lower rate of tDCS treatment effects on lower limb function may
be related to low-intensity stimulation (eg, 1-1.5mA), and this
may be insufficient to trigger the deep structures that modulate the
brain activations related to the lower leg muscles. In this meta-
analysis, although low levels of stimulation intensity (1-1.5mA)
were used in 3 out of 9 tDCS studies, the 3 comparisons did not
necessarily indicate lower treatment effects (the individual effect
sizes ranged from 0.09-0.62) than the overall effect size of tDCS
(0.29). These findings could not fully support the proposition that
lower levels of stimulation intensity may suppress the treatment
150
Fig 7 Meta-regression analysis. A higher number of rTMS sessions was significantly associated with more treatment effects on functional
balance and postural control poststroke.
effects of tDCS on lower limb function. Instead, we identified a
relatively lower number of stimulation sessions across the tDCS
studies included in this meta-analysis. A 2-sample t test indicated
that the number of sessions for the studies using the tDCS pro-
tocols was significantly less than those for the studies using the
rTMS protocols (PZ.049). The mean sessions  SD of the
stimulation sessions were: (1) 9 rTMS studiesZ14.4  6.3 and (2)
9 tDCS studiesZ8.3  5.9. Given that multiple sessions of NIBS
therapy presumably reveal better treatment effects,52,53 a higher
number of tDCS sessions may be necessary to increase their
therapeutic effects on functional balance and postural control
poststroke.
Recovery stages poststroke
The treatment effects of rTMS were found to be significant in the
early and chronic stages of recovery poststroke in our study. These
findings expand prior findings that NIBS improves gait speed
across patients with acute, subacute, and chronic stroke.20 More-
over, the overall effect size for the patients with acute and sub-
acute stroke in our study (6 comparisons; SMDZ0.574) was
relatively higher than that for the patients with chronic stroke (3
comparisons; SMDZ0.328). Within 6 months of stroke onset,
which represents the acute and subacute phases, these patients
presumably experienced spontaneous recoveries, and additional
movement therapies and neurorehabilitation during these early
periods also facilitated their progress toward stroke motor recov-
ery.54-56 Previous studies have suggested that providing early
neuromodulation treatment before a chronic stage may promote
further functional recovery in patients with stroke.55,57 However,
the current moderator-variable analysis findings need to be inter-
preted cautiously because of the relatively small size for each
recovery stage. Overall, applying rTMS in the early recovery
phases may effectively improve functional balance and postural
control in patients with stroke.
N. Kang et al
Relationship between the number of NIBS sessions
and treatment effects
Our meta-regression analysis identified that a higher number of
rTMS treatment sessions was significantly associated with greater
improvements in functional balance and postural control post-
stroke. However, no related significant relationship was observed
for tDCS. This result is consistent with a prior meta-analysis that
failed to identify any significant immediate treatment effects using
multiple tDCS sessions on upper limb recovery.58 Contrary to
these tDCS findings, we found cumulative effects on functional
balance and postural control in patients with stroke as the number
of rTMS sessions increased. The current findings support the
growing body of evidence indicating that multiple sessions of
rTMS may facilitate positive changes in motor and cognitive
function in patients with various neurologic diseases.59-63
Study limitations and future directions
Despite the findings of the positive short-term effects of NIBS on
functional balance and postural control poststroke, this meta-
analysis had some limitations. First, given that we included 5
different types of measurements (ie, BBS, postural sway, postural
assessment scale for stroke, Tinetti test, and trunk control test) to
estimate functional balance and postural control, the effect sizes
could have been influenced by the heterogeneity of the outcome
measures. Second, the studies included in this meta-analysis tar-
geted various brain regions (ie, 14 studies stimulated the M1, 1
study stimulated the SMA, and 3 studies stimulated the cere-
bellum). Moreover, only 7 of the 14 studies that stimulated the M1
mentioned that they exactly triggered the leg area of the M1 (eg,
CZ in the electroencephalography 10/20 system). Thus, these
methodological differences between rTMS and tDCS protocols
may additionally have influenced the treatment effects on func-
tional balance and postural control poststroke.
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NIBS and balance recovery poststroke
Importantly, 13 studies used either excitatory NIBS on the
ipsilesional M1 or inhibitory NIBS on the contralesional M1 based
on the interhemispheric competition model.16 Although 1 study
used low-frequency rTMS on the ipsilesional M1,24 the individual
effect size was not significant (SMD, 0.355; SE, 0.336; 95% CI,
-0.304 to 1.015; zZ1.056; PZ.291). Nevertheless, given that
recent studies have suggested the supportive role of the con-
tralesional hemisphere for lower limb recovery in patients with
stroke and more serious impairments,5,17 applying excitatory
NIBS on the contralesional M1 may advance improvements in
functional balance and postural control. Moreover, previous brain
imaging studies have indicated the involvement of the prefrontal
cortex, SMA, and premotor cortex during static balance control.64
Thus, future NIBS studies may be necessary to simultaneously
target these key regions to optimize functional balance and
postural control recovery poststroke.
Prior studies have argued that administering NIBS with either
conventional motor training or task-specific training effectively
promote motor recovery poststroke compared with the provision
of NIBS without additional motor training.65,66 A recent meta-
analysis examining the restoration of lower limb function
showed significant gait speed improvements in patients with
stroke following the application of rTMS with additional move-
ment training.20 In this meta-analysis, 13 studies (ie, 7 rTMS
studies and 6 tDCS studies) provided NIBS combined with motor
training, whereas 5 studies (ie, 2 rTMS studies and 3 tDCS
studies) used only NIBS. It can be surmised that the inconsistency
in administering movement training in addition to NIBS across
individual studies perhaps influenced the treatment effects. Thus,
applying additional motor training to NIBS is a viable option for
optimizing progress toward functional balance and postural con-
trol recovery poststroke.
One remaining issue is how specifically NIBS techniques deal
with the functional and anatomical limitations of the leg area of
the M1.10 Given the region of leg representations in the motor
areas on the medial wall of the hemisphere within the longitudinal
fissure,67 NIBS techniques for functional balance and postural
control rehabilitation need to be more precise and in-depth
regarding the triggering of exact lower limb cortical motor
areas. For rTMS, the double-cone coil and H-coil are presumably
more effective for stimulating deeper brain areas (depth of the
stimulated structure: 3-4cm by double-cone coil and 4-6cm by H-
coil) than the conventional figure-of-8 coil rTMS technique.68,69
For tDCS, high-definition tDCS targeting a focal area using
specialized small electrodes are potentially more beneficial than
conventional tDCS using relatively wide electrodes (eg, the area
of electrodeZ25-36cm2) because this technique may stimulate
specific targeted cortical as well as deep brain structures.70,71
These advanced NIBS techniques that stimulate more precise
lower limb cortical motor areas than conventional approaches may
optimize the treatment effects of NIBS on postural imbalance
poststroke.
Conclusions
The current systematic review and meta-analysis found that the
short-term treatment effects of NIBS on functional balance and
postural control poststroke were significantly positive. Further,
these effects were significant for patients with acute, subacute, and
chronic stroke following rTMS treatment. Furthermore, a higher
number of rTMS sessions significantly increased improvements in
www.archives-pmr.org
151
functional balance and postural control. Future studies should
therefore investigate whether specialized NIBS techniques (eg,
double-cone coil, H-coil rTMS, and high-definition tDCS) tar-
geting multiple key regions are more effective for optimizing the
short- and long-term treatment effects of NIBS treatment on
functional balance and postural control poststroke.
Supplier
a. Comprehensive Meta-Analysis software version 3; Biostat.
Keywords
Meta-analysis; Postural balance; Rehabilitation; Stroke;
Systematic review; Transcranial direct current stimulation;
Transcranial magnetic stimulation
Corresponding author
Nyeonju Kang, PhD, Neuromechanical Rehabilitation Research
Laboratory, Division of Sport Science & Sport Science Institute,
Incheon National University, 119 Academy-ro, Yeonsu-gu,
Incheon, South Korea. E-mail address: nyunju@inu.ac.kr.
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