You are on page 1of 14

Research Report

Effect of Virtual Reality Training on


Balance and Gait Ability in Patients
With Stroke: Systematic Review and
Meta-Analysis

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


Ilona J.M. de Rooij, Ingrid G.L. van de Port, Jan-Willem G. Meijer
I.J.M. de Rooij, MSc, Revant
Rehabilitation Centres, Breda, the
Background. Virtual reality (VR) training is considered to be a promising novel therapy for Netherlands.
balance and gait recovery in patients with stroke.
I.G.L. van de Port, PhD, Revant
Rehabilitation Centres, Brabant-
Purpose. The aim of this study was to conduct a systematic literature review with meta- laan 1, 4817 JW, Breda, the Neth-
analysis to investigate whether balance or gait training using VR is more effective than erlands. Address all correspon-
conventional balance or gait training in patients with stroke. dence to Dr van de Port at:
i.vandeport@revant.nl.
Data Sources. A literature search was carried out in the databases PubMed, Embase, J-W.G. Meijer, MD, PhD, Revant
MEDLINE, and Cochrane Library up to December 1, 2015. Rehabilitation Centres.

[de Rooij IJM, van de Port IGL,


Study Selection. Randomized controlled trials that compared the effect of balance or gait Meijer J-WG. Effect of virtual real-
training with and without VR on balance and gait ability in patients with stroke were included. ity training on balance and gait
ability in patients with stroke: sys-
Data Extraction and Synthesis. Twenty-one studies with a median PEDro score of tematic review and meta-analysis.
6.0 were included. The included studies demonstrated a significant greater effect of VR training Phys Ther. 2016;96:1905–1918.]
on balance and gait recovery after stroke compared with conventional therapy as indicated © 2016 American Physical Therapy
with the most frequently used measures: gait speed, Berg Balance Scale, and Timed “Up & Go” Association
Test. Virtual reality was more effective to train gait and balance than conventional training
when VR interventions were added to conventional therapy and when time dose was matched. Published Ahead of Print:
May 12, 2016
Accepted: May 1, 2016
Limitations. The presence of publication bias and diversity in included studies were Submitted: February 11, 2016
limitations of the study.

Conclusions. The results suggest that VR training is more effective than balance or gait
training without VR for improving balance or gait ability in patients with stroke. Future studies
are recommended to investigate the effect of VR on participation level with an adequate
follow-up period. Overall, a positive and promising effect of VR training on balance and gait
ability is expected.

Post a Rapid Response to


this article at:
ptjournal.apta.org

December 2016 Volume 96 Number 12 Physical Therapy f 1905


Virtual Reality in Stroke Rehabilitation

M any patients with stroke experi-


ence sensory, motor, cognitive,
and visual impairments, which
all have an impact on their ability to
perform daily life activities.1,2 Approxi-
can perform real-time tasks and antici-
pate and react to objects or events.13,17,18
It has been shown that VR can improve
upper extremity motor function in adults
with chronic hemiparesis as a result from
Method
Data Sources and Searches
A literature search was carried out using
the databases PubMed (since 1950),
Embase (since 1974), MEDLINE (since
mately 80% of patients with stroke are a stroke.18 It also is thought that VR con- 1946), and Cochrane Library (since
affected by motor impairment, which tributes to positive changes in neural 1993) from inception until December 1,
represents loss and limitation in muscle organization and walking ability.19 2015. Search terms included key words
strength and coordination. Motor impair- related to VR (eg, “game,” “gaming”),
ment in the legs greatly affects balance Multiple recent systematic reviews about stroke (“cerebrovascular accident/dis-
and walking ability.3 In a study by Pol- the effect of VR training supported the ease,” “brain attack”), balance (“pos-
lock et al,4 approximately 88% of all use of VR in lower extremity stroke reha- ture,” “postural control,” “mobility”), or

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


patients with stroke who were dis- bilitation to improve balance and gait gait (“ambulation,” “walking,” “lower
charged from hospital reported insuffi- ability.9,20 –23 Two of these reviews9,21 extremity,” “endurance”). These terms
cient walking ability. In addition, 26% to lacked a meta-analysis, and the majority were used as key words in the title and
33% of the home-dwelling patients with of the studies did not perform subanaly- abstract in all databases. In PubMed,
stroke were still unable to walk unsuper- ses of the results (eg, by making a divi- terms related to virtual reality also were
vised in the community,5–7 presumably sion between studies in which VR was searched in the full text. The search strat-
mainly because of difficulties with nego- time dose matched to conventional ther- egy used in PubMed is provided in the
tiating stairs, inclines, or unlevel sur- apy and studies in which VR training was Appendix. The titles and abstracts were
faces.6,7 Therefore, gait recovery has additional to conventional therapy). The displayed and screened by 2 reviewers to
been recognized as an important goal in most recent review about the effect of identify relevant studies.
stroke rehabilitation.8 –10 VR training on balance and gait ability
showed significant benefits of VR train- Study Selection
Impaired gait is highly associated with ing on gait speed, Berg Balance Scale Only RCTs that compared the effect of
balance dysfunction.4,11 In addition, (BBS) scores, and Timed “Up & Go” Test gait or balance training without VR with
improvement in balance has been shown (TUG) scores when VR was time dose the effect of gait or balance training with
to be the most important determinant for matched to conventional therapy.22 In VR in patients with stroke were
regaining gait as measured with the contrast to the studies supporting VR included. The VR intervention replaced
Functional Ambulation Categories.12 training, 2 recently published reviews the conventional therapy or was in addi-
During balance and gait recovery, using a commercial VR system con- tion to the conventional therapy. For
patients with stroke have to relearn vol- cluded that there was insufficient evi- inclusion, RCTs had to be peer-reviewed
untary control over the affected muscles. dence to ensure the effectiveness of VR articles and written in the Dutch, Ger-
In conventional therapy, this relearning training on balance ability.24,25 However, man, or English language. Studies that
is done through physical therapy and in the past year, new randomized con- compared VR interventions with no
occupational therapy, which focus trolled trials (RCTs) comparing the effect intervention or form of therapy were
on high-intensity, repetitive, and task- of VR training with conventional therapy excluded. Gait ability could be measured
specific practice.3,13 High-intensity, have been published. Because of the using parameters of spatiotemporal gait
repetitive, task-oriented, and task- inconclusive results in the previous ability, functional gait ability, or both,
specific practice has proven to be impor- reviews about the effect of VR training, and balance ability could be measured
tant for effective therapy in all stages the important question remains whether using static and dynamic balance param-
after stroke.14 However, the conven- VR interventions are more effective than eters. Furthermore, VR had to consist of
tional rehabilitation techniques are often balance or gait training without VR in a screen or a head-mounted device. The
labor- and resource-intensive, tedious, patients with stroke.9 Therefore, the patients with stroke had to perform gait
and result most of the time in modest and questions that are addressed in the pres- or balance exercises on the ground, a
delayed effects in patients with stroke.13 ent review are: (1) Are VR interventions balance board, or a treadmill while look-
In addition, the frequency and intensity to train gait or balance more effective ing at the VR scenes. This approach
of the conventional therapies as per- than conventional gait or balance train- means that studies using robots or stand-
formed in clinical practice have been ing on balance and gait ability in patients ing frames were excluded.
found to be insufficient to achieve max- with stroke when time dose is matched?
imum recovery.14,15 and (2) Are VR interventions in addition
Data Extraction and Quality
to conventional therapy more effective
than conventional therapy alone in
Assessment
In recent years, the use of virtual reality
The following data were extracted from
(VR) has been introduced in the field of improving balance and gait ability in
the included articles: sex, age, time since
stroke rehabilitation.16 Virtual reality is patients with stroke?
stroke, content of intervention, time
an advanced computer-human interface
dose of training, and significant main
with a variety of safe 3-dimensional envi-
findings in measures of balance and gait
ronments in which patients with stroke
ability between groups. Data extraction

1906 f Physical Therapy Volume 96 Number 12 December 2016


Virtual Reality in Stroke Rehabilitation

was performed by 2 independent


researchers (I.R., I.P.). They assessed the
methodological quality of the RCTs using
the PEDro scale.26 This scale consists of
11 items that can contribute 1 point to
the total score if they are satisfied,
except for item 1 (eligibility criteria),
which is scored “yes” or “no.” The PEDro
scale is proven to have sufficient reliabil-
ity to determine the quality of RCTs. Arti-
cles with a score of 6 or higher are con-
sidered as high quality, and those with

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


scores of less than 6 are defined as lower
quality.27 In case of disagreement in the
quality assessment of the 2 reviewers,
consensus was reached by discussion or
consulting a third person. Publication
bias was analyzed using forest plots for
the measures gait speed and TUG.

Data Synthesis and Analysis


The included studies were analyzed
based on participant characteristics, out-
come parameters, content of VR inter-
ventions, and main findings. A meta-
analysis of studies with a PEDro score of
6 or higher was performed using Review
Manager software, version 5.3 (The Nor-
dic Cochrane Centre, The Cochrane Col-
laboration, Copenhagen, Denmark).28
The pooled effect estimates were com- Figure 1.
puted from the change scores between Flowchart of the study selection. RCT⫽randomized controlled trial.
baseline and end of the intervention,
their standard deviations, and the num-
ber of participants. Authors were con-
comes. For the outcome gait speed, the focusing on the upper extremity or
tacted via email for unreported data.
standardized mean difference (SMD) was robotic devices, and participants who
Missing standard deviations of the
expressed because this outcome was experienced other forms of acquired
change values in the studies of Barcala et
obtained through multiple measurement brain injury. Furthermore, 8 articles
al29 and Rajaratnam et al30 were imputed
scales. A distinction was made between were excluded based on the full-text arti-
from other published literature. Other
studies in which the VR intervention cle. Two of these studies did not involve
standard deviations of change values that
replaced the conventional therapy (time randomization,34,35 1 study lacked a con-
were still not available after mail contact
dose matched) and studies in which the trol group,36 and 4 studies contained a
were estimated using the difference in
VR intervention was added to the con- control group that did not receive con-
means and P value, t value, or F value as
ventional therapy. ventional therapy37 or a control group
described in the Cochrane Handbook.31
that also watched at a VR screen38,39 or

In case of low heterogeneity, the fixed-


Results played VR at home.40 Another reason for
Identification of Studies exclusion was VR training that did not
effect model was used to pool study involve balance or gait training.41 Even-
results for the outcomes BBS, TUG, and In total, 398 relevant articles were found
in PubMed, Embase, MEDLINE, and tually, 21 articles were included in the
gait speed. When significant heterogene- review.
ity was observed (I2 ⬎50%), the random- Cochrane Library. In addition, 3 arti-
effects model was applied. In addition, a cles29,32,33 were identified through hand
searching reference lists. When dupli- Description of Included Studies
sensitivity analysis was conducted when
cates were removed, 203 articles In the 21 included studies, the mean age
heterogeneity was present. Forest plots
remained. Based on title and abstract of of the participants varied between 45.9
were generated to present the pooled
these 203 articles, 174 articles were and 65.9 years in the VR group and 46.3
effect, and the mean difference (MD)
excluded (Fig. 1). The main reasons for and 65.7 years in the control group. Time
with 95% confidence interval (CI) was
excluding these articles were study since stroke ranged between 12.7 days
calculated for the BBS and TUG out-
designs other than RCTs, interventions and 11.3 years in the VR group and

December 2016 Volume 96 Number 12 Physical Therapy f 1907


Virtual Reality in Stroke Rehabilitation

Table 1.
Characteristics of the Selected Studies and Analysis of Outcome Measures and of Gait Ability and Balance and Main Findingsa

Study N (Male) Mean Age (SD) (y) Time Since Stroke (SD) VR Intervention Control Intervention

Givon et al,52 2016 47 (28) VR group: 56.7 (9.3) VR group: 3.0 (1.8) y VR group training Conventional group
Control group: Control group: 2.6 (1.8) y therapy
62.0 (9.3)

Kim et al,47 2015 17 (9) VR group: 56.2 (7.56) VR group: 7.5 (4.4) mo Conventional therapy plus Conventional therapy
Control group: Control group: 16.6 (8.8) VR-based treadmill
48.7 (9.3) mo training

Lee et al,55 2015 24 (16) VR group: 45.9 (12.3) nr Conventional therapy plus Conventional therapy plus
Control group: VR training task-oriented training

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


49.2 (12.9)

Lee et al,56 2015 20 (11) VR group: 57.2 (9.2) nr VR training with cognitive PNF exercise program
Control group: tasks
52.7 (11.7)

Lloréns et al,49 2015 20 (9) VR group: 58.3 (11.6) VR group: 407.5 (232.4) d Conventional therapy plus Conventional therapy
Control group: Control group: VR therapy
55.0 (11.6) 587 (222.1) d

Song et al,53 2015 40 (22) VR group: 51.4 (40.6) VR group: 14.8 (6.1) mo VR training Ergometer bicycle training
Control group: Control group: 14.3 (3.4)
50.1 (7.8) mo

Cho et al,43 2014 30 (15) VR group: 65.9 (5.7) VR group: 414.5 (150.4) d Conventional therapy plus Conventional therapy plus
Control group: Control group: VR-based treadmill traditional non-VR
63.5 (5.5) 460.3 (186.8) d training treadmill training

Hung et al,33 2014 28 (18) VR group: 55.4 (10.0) VR group: 21.0 (11.3) mo Conventional therapy plus Conventional therapy plus
Control group: Control group: 15.9 (8.0) VR training weight-shift training
53.4 (10.0) mo

Morone et al,51 2014 50 (nr) VR group: 58.4 (9.6) VR group: 61.0 (36.5) d Conventional therapy plus Conventional therapy plus
Control group: Control group: 41.7 (36.9) VR therapy extra balance therapy
62.0 (10.3) d

Song et al,50 2014 20 (11) VR group: 65.6 (13.5) VR group: 12.7 (3.2) d Conventional therapy plus Conventional therapy
Control group: Control group: 13.2 (3.4) VR training
61.2 (13.8) d

Barcala et al,29 2013 20 (9) VR group: 65.2 (12.5) VR group: 12.3 (7.1) mo Conventional therapy plus Conventional therapy
Control group: Control group: 15.2 (6.6) VR training
63.5 (14.5) mo

Cho et al,42 2013 14 (7) VR group: 64.6 (4.4) VR group: 288.3 (69.2) d Conventional therapy plus Conventional therapy plus
Control group: Control group: VR-based treadmill traditional non-VR
65.1 (4.7) 312.4 (83.7) d training treadmill training

Park et al,48 2013 16 (11) VR group: 48.8 (8.8) VR group: 11.3 (4.5) y Conventional therapy plus Conventional therapy
Control group: Control group: 11.6 (4.4) reality-based training
46.3 (6.8) y

(Continued)

between 13.2 days and 11.6 years in the ance interventions was on the lower dose of therapy in the VR and control
control group. Eight studies8,32,42– 47 extremities. In the study by Song et al,50 groups was equal. In 4 studies,16,29,50,54
were treadmill based and provided a VR however, the upper extremity was the participants in the VR group per-
intervention in combination with walk- involved more directly because the par- formed the VR intervention in addition
ing. The other 13 studies focused on bal- ticipants had to accomplish tasks with to a conventional therapy program,
ance interventions by performing exer- their arms in order to direct their center which means that the time dose of ther-
cises on the ground16,48 –53 or a balance of pressure outside the feet. In 17 apy was higher in the VR group com-
board.29,30,33,54 –56 The focus of the bal- studies8,30,32,33,42– 49,51–53,55,56 the time pared with the control group (Tab. 1).

1908 f Physical Therapy Volume 96 Number 12 December 2016


Virtual Reality in Stroke Rehabilitation

Table 1.
Continued

Time Dose of VR Significant


Group Compared Outcome Measures of Significant Between- Outcome Measures Between-Groups
Study With Control Group Gait Ability Groups Findings of Balance Findings

Givon et al,52 2016 Equal Functional: 10MWT ns

Kim et al,47 2015 Equal Static balance: PSPL PSPL (AP, ML, and
(AP, ML, and total), total), APSS (P⬍.05)
APSS

Lee et al,55 2015 Equal Static balance: COP FRT (P⬍.0001)

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


path length, COP
velocity Dynamic
balance: FRT

Lee et al,56 2015 Equal Dynamic balance: BBS, BBS, TUG (P⬍.05)
TUG

Lloréns et al,49 2015 Equal Functional: 10MWT 10MWT (P⬍.05) Dynamic balance: BBS, BBS (P⬍.05)
Tinetti POMA, Brunel
Balance Assessment

Song et al,53 2015 Equal Functional: 10MWT 10MWT (P⬍.05) Static balance: weight- Weight-bearing ratio
bearing ratio affected affected side,
side, forward and forward and
backward LOS backward LOS, TUG
Dynamic balance: TUG (P⬍.05)

Cho et al,43 2014 Equal Spatiotemporal: gait Gait speed, cadence, Static balance: AP-PSV, BBS, TUG (P⫽.001)
speed, cadence, step single- and double-limb ML-PSV, PSVM
length, stride length, support period, step and Dynamic balance: BBS,
double-limb support stride length (P⬍.029) TUG
period, single-limb
support period

Hung et al,33 2014 Equal Static balance: SI, SI (P⬍.05)


weight-bearing
asymmetry on affected
leg
Dynamic balance:
TUG, FRT

Morone et al,51 2014 Equal Functional: 10MWT, FAC 10MWT (P⫽.021) Dynamic balance: BBS BBS (P⫽.004)

Song et al,50 2014 Higher Static balance: FI SI and WDI while


scores, SI, WDI standing with eyes
Dynamic balance: BBS open and when
standing on a pillow
with eyes open
(P⬍.017)

Barcala et al,29 2013 Higher Dynamic balance: BBS, ns


TUG Static balance:
COP oscillations

Cho et al,42 2013 Equal Spatiotemporal: gait Gait speed, cadence Dynamic balance: BBS, BBS, TUG (P⫽.01)
speed, cadence, paretic (P⫽.01) TUG
side step length, stride
length, and single-limb
support period

Park et al,48 2013 Equal Spatiotemporal: gait Stride length (P⬍.03)


speed, cadence, step
length, stride length
Functional: 10MWT

(Continued)

December 2016 Volume 96 Number 12 Physical Therapy f 1909


Virtual Reality in Stroke Rehabilitation

Table 1.
Continued

Study N (Male) Mean Age (SD) (y) Time Since Stroke (SD) VR Intervention Control Intervention

Rajaratnam et al,30 19 (7) VR group: 58.7 (8.6) VR group: 14.7 (7.5) d Conventional therapy plus Conventional therapy
2013 Control group: Control group: 15.2 (6.3) VR balance training
65.3 (9.6) d

Cho et al,54 2012 22 (14) VR group: 65.3 (8.4) VR group: 12.5 (2.6) mo Conventional therapy plus Conventional therapy
Control group: Control group: 12.6 (2.5) VR balance training
63.1 (6.9) mo

Jung et al,44 2012 21 (13) VR group: 60.5 (8.6) VR group: 12.6 (3.3) mo VR treadmill training Non-VR treadmill training

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


Control group: Control group: 15.4 (4.7)
63.6 (5.1) mo

Kang et al,32 2012 30 (15) VR group: 55.9 (6.4) VR group: 14.1 (4.4) mo Conventional therapy plus Conventional therapy plus
Control group 1: Control group 1: VR treadmill training non-VR treadmill training
56.3 (7.6) 13.5 (4.0) mo (control group 1) or
Control group 2: Control group 2: stretching exercises
56.1 (7.8) 15.1 (7.4) mo (control group 2)

Yang et al,46 2011 14 (nr) VR group: 56.3 (10.2) VR group: 17.0 (8.6) mo VR treadmill training Non-VR treadmill training
Control group: Control group: 16.3 (10.4)
65.7 (5.9) mo

Kim et al,16 2009 24 (14) VR group: 52.4 (10.1) VR group: 25.9 (10.0) mo Conventional therapy plus Conventional therapy
Control group: Control group: 24.3 (8.9) VR therapy
51.75 (7.1) mo

Yang et al,8 2008 20 (10) VR group: 55.5 (12.2) VR group: 5.9 (4.2) y VR treadmill training Non-VR treadmill training
Control group: Control group: 6.1 (10.3)
60.9 (9.3) y

Jaffe et al,45 2004 20 (12) VR group: 58.2 (11.2) VR group: 3.9 (2.3) y Virtual object training Stepping over real foam
Control group: Control group: 3.6 (2.6) y objects on a 10-m
63.2 (8.3) walkway

a
nr⫽not reported, ns⫽nonsignificant, 6MWT⫽Six-Minute Walk Test, 10MWT⫽10-Meter Walk Test, ABC⫽Activities-specific Balance Confidence,
AP⫽anterior-posterior, AP-PSV⫽anterior-posterior postural sway velocity, AP and ML angle⫽angle between a vertical line from the spatial center of the
supporting feet and a second line connecting from the same point to the individual’s center of gravity, APSS⫽average postural sway speed, BBS⫽Berg
Balance Scale, contact A/P⫽contact area of the paretic limb, COP⫽center of pressure, COPA⫽center of pressure sway area, COPAP⫽center of pressure
displacement in anterior-posterior direction, COPE⫽center-of-pressure total path excursion, COPE/P⫽center-of-pressure path excursion under the paretic
limb, COPML⫽center-of-pressure displacement in medial-lateral direction, FI⫽falling index, fast⫽as fast as possible pace, FAC⫽Functional Ambulation
Categories, FRT⫽Functional Reach Test, ML⫽medial-lateral, ML-PSV⫽medial-lateral postural sway velocity, MMAS⫽Modified Motor Assessment Scale,
POMA⫽Performance-Oriented Mobility Assessment, PSPL⫽postural sway path length, PSVM⫽postural sway velocity moment, SI⫽stability index, ss⫽self-
selected pace, stance time/P⫽stance time of the paretic limb, LOS⫽limit of stability, step no./⫽step number of the paretic limb, TUG⫽Timed “Up & Go”
Test, WAQ⫽Walking Ability Questionnaire, WDI⫽weight distribution index.

The additional training of the VR group 6 or higher and were considered of high used both point measures and measures
in these studies varied between 6029 and quality. All trials randomly allocated the of variability (90.5%). In total, 23 (10.0%)
12016 minutes a week. participants. Furthermore, the majority of the 231 items from the PEDro scale
of trials reported eligibility criteria were initially scored different by the 2
PEDro Scores (95.4%), had similar groups at baseline reviewers. After discussion, there was
The PEDro scores of the included studies (85.7%), performed between-group anal- agreement for all items.
varied between 3 and 8, with a median of yses (95.4%) and assessor blinding
6.0 and an interquartile range of 2.0 (61.9%), collected data of more than
(Tab. 2). Thirteen studies had a score of 85.0% of the participants (76.2%), and

1910 f Physical Therapy Volume 96 Number 12 December 2016


Virtual Reality in Stroke Rehabilitation

Table 1.
Continued

Time Dose of VR Significant


Group Compared Outcome Measures of Significant Between- Outcome Measures Between-Groups
Study With Control Group Gait Ability Groups Findings of Balance Findings

Rajaratnam et al,30 Equal Static balance: CoP FRT (P⫽.01)


2013 sway Dynamic
balance: BBS, TUG,
FRT

Cho et al,54 2012 Higher Static balance: AP-PSV BBS, TUG (P⬍.05)
and ML-PSV (with eyes
open or closed)

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


Dynamic balance: BBS,
TUG

Jung et al,44 2012 Equal Dynamic balance: TUG, ABC (P⬍.05)


TUG, ABC scale

Kang et al,32 2012 Equal Functional: 6MWT, 6MWT, 10MWT (P⬍.05) Dynamic balance: VR group vs control
10MWT TUG, FRT group 1: TUG
(P⬍.05)
VR group vs control
group 2: TUG, FRT
(P⬍.05)

Yang et al,46 2011 Equal Static balance: COPML (P⫽.038)


COPML, COPAP,
COPE, COPA,
symmetry index (quiet
stance and sit-to-stand
transfer), COPE/P (sit-
to-stand transfer)
stance time/P, step
no./P, contact A/P
(level walking)

Kim et al,16 2009 Higher Spatiotemporal: Cadence, step length, Static balance: mean BBS, AP angle, and
cadence, step time, step time (P⬍.014) balance, sway area, ML angle (P⬍.01)
stance time, swing time, sway path, maximal
single/double support velocity Dynamic
time, step/stride length balance: BBS, AP
Functional: 10MWT, angle, ML angle
MMAS
Yang et al,8 2008 Equal Functional: 10MWT, Pretest-posttest: 10MWT, Dynamic balance: ABC ns
community walking community walking time scale
time, WAQ (P⬍.05)
Follow-up: WAQ (P⫽.03)
Jaffe et al,45 2004 Equal Spatiotemporal: gait Gait speed, stride length
speed, cadence, step (ss), obstacle clearance,
and stride length step length of nonparetic
Functional: obstacle test, leg (ss) and paretic leg
distance on 6MWT (fs) (P⬍.05)

Content of the VR Interventions vention, and 13 studies16,29,30,33,48 –56 Outcome Measures and Main
of Included Studies focused on balance interventions. To Findings of Included Studies
There was wide variety in frequency, project the virtual environment, a head- All studies showed a significant differ-
intervention setup, and content of the mounted device was used in 4 ence between the VR and control groups
VR intervention (eTabs. 1 and 2, avail- studies,32,44,45,48 and the VR was pro- in favor of the VR intervention in differ-
able at ptjournal.apta.org). The fre- jected on a screen in the other 17 ent measures of balance or gait ability,
quency varied between 2 and 5 VR studies.8,16,29,30,33,42,43,46,47,49 –56 except for the studies by Barcala et al29
training sessions a week. Eight and Givon et al52 (Tab. 1). Four studies
studies8,32,42– 47 focused on a gait inter- were not included in the meta-analysis: 3

December 2016 Volume 96 Number 12 Physical Therapy f 1911


Virtual Reality in Stroke Rehabilitation

Table 2.
PEDro Scores of the Included Studiesa

Point Estimates and Variability


No Missing Data or If Missing,
Data for at Least 1 Outcome
From >85% of Participants

Intention-to-Treat Analysis

Between-Groups Analysis
Baseline Comparability
Concealed Allocation

Participant Blinded
Random Allocation
Eligibility Criteria

Total Score (/10)


Clinician Blinded

Assessor Blinded

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


Study

Givon et al,52 2016 Yes 1 0 1 0 0 1 1 1 0 1 6

Kim et al,47 2015 No 1 0 0 0 0 0 0 0 1 1 3

Lee et al,55 2015 Yes 1 0 1 0 0 0 1 0 1 1 5

Lee et al,56 2015 Yes 1 0 1 0 0 0 0 0 1 1 4

Lloréns et al,49 2015 Yes 1 1 1 0 0 1 1 1 1 1 8

Song et al,53 2015 Yes 1 0 1 0 0 0 0 0 1 1 4

Cho et al,43 2014 Yes 1 1 1 0 0 1 1 0 1 1 7

Hung et al,33 2014 Yes 1 1 1 0 0 1 1 0 1 1 7

Morone et al,51 2014 Yes 1 1 1 0 0 1 1 1 1 1 8

Song et al,50 2014 Yes 1 0 1 0 0 0 0 0 1 1 4

Barcala et al,29 2013 Yes 1 1 1 0 0 1 1 0 1 1 7

Cho et al,42 2013 Yes 1 1 1 0 0 1 1 1 1 1 8

Park et al,48 2013 Yes 1 0 1 0 0 0 1 1 1 1 6

Rajaratnam et al,30 2013 Yes 1 0 1 0 0 1 1 1 1 0 6

Cho et al,54 2012 Yes 1 0 1 0 0 0 1 0 1 1 5

Jung et al,44 2012 Yes 1 0 1 0 0 1 1 0 1 1 6

Kang et al,32 2012 Yes 1 1 1 0 0 1 1 1 1 1 8

Yang et al, 201146 Yes 1 0 0 0 0 1 1 0 1 1 5

Kim et al,16 2009 Yes 1 0 1 1 0 1 1 1 1 1 8

Yang et al,8 2008 Yes 1 1 1 0 0 1 0 1 1 1 7

Jaffe et al,45 2004 Yes 1 0 0 0 0 0 1 0 1 0 3


a
1⫽yes, 0⫽no.

studies46,47,55 did not report gait speed, ity included gait speed as an outcome improved gait speed significantly more
BBS scores, or TUG scores and reported measure. This outcome measure was than conventional therapy (SMD⫽1.03;
only on static balance parameters, and obtained using pressure-sensitive equip- 95% CI⫽0.38, 1.69; P⫽.002). The I2 sta-
data of one study50 were not available for ment or the 10-Meter Walk Test. Eight tistic of 78% represents substantial heter-
a pooled analysis. of the 11 studies (n⫽211) showed ogeneity. A sensitivity analysis showed
significantly greater increases in gait that this heterogeneity was mainly due to
Gait ability. Of the studies measuring speed in the VR group (n⫽108) com- the magnitude of the effect of the studies
gait ability, 2 studies42,43 reported on spa- pared with the control group by Kang et al32 and Givon et al52 (eFigs.
tiotemporal parameters, 3 studies16,45,48 (n⫽103).8,32,42,43,45,49,51,53 The effect of 1 and 2, available at ptjournal.apta.org).
used both spatiotemporal and VR training on gait speed was further When these studies were excluded, the
functional outcome measures, and 6 examined by pooling the data of 8 stud- I2 of the pooled effect became 0%, with
studies8,32,49,51–53 focused only on func- ies in which VR training was time dose an SMD of 0.86 (95% CI⫽0.52, 1.20;
tional gait ability. Gait speed was the matched to conventional therapy P⬍.001).
most frequently used measure of gait (Fig. 2A). The pooled SMD showed
ability, as all studies measuring gait abil- that time dose–matched VR training

1912 f Physical Therapy Volume 96 Number 12 December 2016


Virtual Reality in Stroke Rehabilitation

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


Figure 2.
Forest plot of the pooled results of the effect of VR training on gait speed in (A) time dose–matched studies (n⫽214) and (B) studies in which
VR was additional to conventional therapy (n⫽24). VR⫽virtual reality, IV⫽inverse variance, CI⫽confidence interval.

In one study,16 VR training was addi- represents low heterogeneity. The heter- ment in time of the TUG in favor of the
tional to conventional therapy. This ogeneity between the 2 studies in which VR group (Fig. 4B).
study showed a significant improvement VR was added to the conventional ther-
in gait speed in favor of the VR group apy was high (I2⫽98%). The pooled MD Discussion
(Fig. 2B). did not show a significant effect of VR This systematic review provided evi-
training compared with conventional dence for a stronger effect of VR training
Balance. Regarding studies on bal- therapy (MD⫽1.17; 95% CI⫽⫺6.54, compared with conventional therapy, as
ance, 7 studies8,32,42,44,49,51,56 reported 8.88; P⫽.77) (Fig. 3B). suggested by the significantly greater
on dynamic balance, 2 studies46,47 improvements in balance and gait ability.
reported on static balance, and 9 stud- Time of the TUG improved signi- Gait speed, BBS score, and time of TUG
ies16,29,30,33,43,50,53–55 reported on both ficantly more in the VR group of 7 stud- were the most frequently used measures
dynamic and static balance outcome ies.32,42– 44,53,54,56 Only Barcala et al,29 to underpin the stronger effect of VR
measures. Significant differences in the Rajaratnam et al,30 and Hung et al33 did training. Pooled effect estimates showed
effect on static balance between the VR not find significant results for the TUG in significant improvements in these 3 out-
group (n⫽47) and control group (n⫽44) favor of the VR group. The pooled results come measures in favor of the VR group
were found in 4 of the 11 studies re- for the TUG showed a significant MD of for both time dose–matched VR interven-
porting on static balance.46,47,50,53 The 2.48 (95% CI⫽1.28, 3.67; P⬍.001) in tions and VR interventions in addition to
dynamic balance of patients with stroke favor of the VR group. However, substan- conventional therapy. The positive find-
seems to improve significantly more after tial heterogeneity was indicated with an ings of VR training are in line with pre-
a VR intervention compared with a con- I2 statistic of 85% (Fig. 4A). When vious reviews on the effect of VR on the
ventional intervention. Significant differ- excluding the studies by Rajaratnam lower extremity in patients with
ences were found for the BBS in favor et al30 and Kang et al,32 no heterogeneity stroke.9,20 –23,57 The systematic reviews
of the VR group in 7 out of 10 (I2⫽0%) was observed. The MD was 1.35 by Dos Santos et al24 and Cheok et al25
studies reporting on this scale and remained significant in favor of the did not support these positive findings.
(n⫽180).16,42,43,49,51,54,56 The pooled MD VR group (95% CI⫽1.02, 1.67; P⬍.001) This conflicting finding may be due to
for VR training time dose matched to (eFigs. 1 and 2). The pooled MD for VR the fact that these reviews included only
conventional therapy showed that VR training in addition to conventional ther- RCTs that used a Nintendo Wii (Nin-
training significantly improved the BBS apy was reported in just one study.29 tendo, Kyoto, Japan) intervention as VR
score with 2.18 (95% CI⫽1.52, 2.85; This study showed a significant improve- and, therefore, included only 524 or 625
P⬍.001) (Fig. 3A). The I2 statistic of 9% studies. In addition, 2 of the included

December 2016 Volume 96 Number 12 Physical Therapy f 1913


Virtual Reality in Stroke Rehabilitation

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


Figure 3.
Forest plot of the pooled results for effect of VR training on Berg Balance Scale in (A) time dose–matched studies (n⫽130) and (B) studies
in which VR was additional to conventional therapy (n⫽44). VR⫽virtual reality, IV⫽inverse variance, CI⫽confidence interval.

Figure 4.
Forest plot of the pooled results for the effect of VR training on Timed “Up & Go” Test in (A) time dose–matched studies (n⫽132) and (B)
studies in which VR was additional to conventional therapy (n⫽20). VR⫽virtual reality, IV⫽inverse variance, CI⫽confidence interval.

RCTs in both reviews concentrated on pooled effect for the BBS when VR was included in the analysis of the BBS may
upper extremity motor function58 or added to conventional therapy was the explain why there was no significant
global motor function59 and did not only measure that did not significantly pooled effect of VR training in addition
include dynamic balance measures (BBS, improve more after VR training. The high to conventional therapy. The meta-
TUG) or static balance measures. The heterogeneity between the 2 studies analysis included only studies of high

1914 f Physical Therapy Volume 96 Number 12 December 2016


Virtual Reality in Stroke Rehabilitation

quality, as indicated by a PEDro score of sic or augmented feedback is provided population in detail and reported their
6 or higher. However, when performing through an external source.62,63 This results completely. We tried to retrieve
the same meta-analyses using all studies so-called augmented feedback can be most of the unreported data by contact-
for which data were available, the con- provided in knowledge of results at the ing the authors through email. Regarding
clusions were the same. end of a training task or knowledge of the stroke population, disease status or
performance concurrent with the perfor- severity may influence the effect of
The added value of VR on balance and mance of the training task.64 It is well VR interventions. Because half of the
gait ability compared with most of the known that feedback improves the learn- included studies did not report
currently provided conventional thera- ing rate64 and that patients with stroke Brunnstrom stages or other measures of
pies may be explained by multiple benefit from practice with augmented disease status, this stroke characteristic
aspects. Virtual reality creates patient- feedback.65 Visual feedback, specifically, could not be included in this review.
specific motor training with a high level has been shown to play a role in improv-

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


of repetitive and variable training. Repet- ing balance in patients with stroke.66,67 Study Limitations
itive training has been hypothesized to All studies in this review included visual, The review identified some limitations
form the physiological basis of motor auditory, or sensory augmented feed- that should be taken into account when
learning.60 The majority of studies back, for instance, derived from real- interpreting the effect of VR training on
included in this review provided highly world video recording or an avatar that balance and gait ability in patients recov-
repetitive VR training. However, notice- copies the individual’s movements. ering from stroke. First, the broad inclu-
able differences among the studies could Therefore, this aspect of VR may play a sion and diversity in the included studies
be found in the intensity of training. In crucial role in the positive effect of VR bring some limitations with it. The
the studies by Jaffe et al45 and Park on improving balance and gait ability. included studies were diverse regarding
et al,48 the number of steps or correc- the population of patients with stroke,
tions in balance that participants had to Lastly, VR is thought to improve motiva- especially regarding the wide variation in
take were small, which is in contrast to tion and enjoyment, to decrease the per- time since stroke. It was expected that
the highly repetitive training in the other ception of exertion, and to increase the the effect of VR training was higher in
19 studies. Because repetitive training activity adherence in training.68 The patients early after stroke because brain
has proven to be an important principle degree to which participants feel moti- plasticity and structural reorganization is
of motor learning,60 these 2 studies may vated and engaged during VR training higher early after lesions69 and endoge-
not have fully optimized the benefits of can depend on the individual and nous recovery after stroke has been
VR. This possibility is confirmed by the the intervention. None of the studies reported to reach a plateau in 6
results for gait speed, which showed a included in the present review measured months.70 However, this expectation
nonsignificant or minor effect of VR in motivation. However, Lloréns et al40 was not supported by our results
the studies by Park et al48 and Jaffe et already assessed motivation and showed because the 3 studies30,50,51 with a mean
al,45 respectively. that people with stroke considered a time since stroke that did not exceed 2
VR-based balance intervention as highly months did not report another trend in
Besides repetitive training, variability in motivating. To study the role of motiva- the results compared with the other 18
practice is important for motor learning tion as one of the underlying mecha- studies with a mean time since stroke of
because it will lead to improvement in nisms for the effect of VR training, future more than 7 months. Because of a lack of
the ability to adapt to novel situations.13 studies need to include motivation as an a clear definition of VR, there is diversity
Virtual reality also enables therapists to outcome measure. in the VR interventions included in the
provide individualized training in which review. In addition, there is diversity in
the intensity and difficulty of the training The majority of the included studies pro- control interventions, leading to a varia-
exercises can easily be adjusted to the vided high methodological quality. How- tion in contrast between intervention
characteristics and needs of the ever, most studies did not perform and control groups among the included
patient.61 Controlled constraints can be concealed allocation and lacked an studies.
applied to patients with stroke who intention-to-treat analysis, which could
are performing exercises, which is nec- have led to bias in the included trials. In It is important to point out that the
essary for optimal learning.9,17 addition, the majority of studies did not reported control group mostly repre-
provide participant and clinician blind- sents conventional therapy, which may
Besides, more feedback about the perfor- ing, which was expected in this kind of not actually and truly control for the VR
mance of participants can be given in VR intervention. However, the assessor intervention. An appropriate control
training than would be possible in real- who performed the measurements was group should match the VR inter-
world practice. Feedback can be divided blinded in the majority of the studies. vention in dose, intensity, structure,
into intrinsic and extrinsic. Intrinsic feed- Besides methodological quality, the goal-oriented focus, progressive increase
back refers to somatic information, transparency of the included studies may of task demands, and inclusion of an
including tactile, proprioceptive, and have had an influence on the results of explicit balance or walking compo-
kinesthetic information, and may be this review. Not all included studies nent.71 For example, in the balance study
damaged in patients with stroke. Extrin- described the intervention and stroke by Morone et al,51 the control therapy

December 2016 Volume 96 Number 12 Physical Therapy f 1915


Virtual Reality in Stroke Rehabilitation

consisted of both walking and balance virtual environment might improve qual- ment and fund procurement. Dr van de Port
exercises, whereas the VR training was ity of life and feeling of safety. Further- and Dr Meijer provided consultation (includ-
specifically focused on balance. In the more, most of the studies measured the ing review of manuscript before submission).
treadmill studies, the control therapy effect of VR directly after the interven- The authors thank Thamar Bovend’Eerdt,
often consisted of treadmill training, but tion; only 4 studies8,33,48,52 also mea- PhD, for his contribution as scientific adviser
without VR. Using this design, the true sured the effect of VR after 1 or 3 months for the establishment of the research ques-
additional value of VR could be studied. of follow-up. However, it would be inter- tions and specification of the study design.
In this review, both VR in addition to esting to investigate the long-term effects
DOI: 10.2522/ptj.20160054
conventional therapy and VR training of VR training to ascertain whether
time dose matched to conventional ther- VR-induced improvement can be sus-
apy showed a significantly greater effect tained over time and how the improve- References
on balance and gait ability compared ments translate into home or community 1 Laver K, George S, Thomas S, et al.

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


with conventional therapy. The addition environments.16 To improve the strength Cochrane review: virtual reality for stroke
rehabilitation. Eur J Phys Rehabil Med.
of VR appeared to have a smaller effect of evidence on the effects of VR, future 2012;48:523–530.
on improving balance and gait ability studies need to be large RCTs investigat- 2 Laver KE, George S, Thomas S, et al. Vir-
than time dose–matched VR training. ing the effect of VR from body function tual reality for stroke rehabilitation.
However, the meta-analysis for addi- to participation level and have to be con- Cochrane Database Syst Rev. 2015;2:
CD008349.
tional VR training comprised only 3 ducted with standardized training doses
studies. and adequate follow-up. 3 Langhorne P, Coupar F, Pollock A. Motor
recovery after stroke: a systematic review.
Lancet Neurol. 2009;8:741–754.
Second, the generalizability of this Lastly, we included 21 studies using 4 Pollock C, Eng J, Garland S. Clinical mea-
review regarding age is questionable broad inclusion criteria regarding the VR surement of walking balance in people
because only relatively young patients interventions, suggesting that we did not post stroke: a systematic review. Clin
Rehabil. 2011;25:693–708.
with stroke were included. It might be miss studies comparing VR training with
assumed that implementing VR in an gait or balance training without VR. 5 van de Port IG, Kwakkel G, Lindeman E.
Community ambulation in patients with
older population is more challenging. In However, visual inspection of funnel chronic stroke: how is it related to gait
addition, the generalizability of the plots in which the SMDs for the TUG and speed? J Rehabil Med. 2008;40:23–27.
results of this review is limited to gait and gait speed were plotted against the stan- 6 Mayo NE, Wood-Dauphinée S, Côté R,
balance outcomes and specifically gait dard error of the SMD shows asymmetry, et al. Activity, participation, and quality of
life 6 months poststroke. Arch Phys Med
speed, BBS scores, and TUG scores. We which suggests the presence of publica- Rehabil. 2002;83:1035–1042.
chose to include these uniform outcome tion bias. As most published studies 7 Lord SE, McPherson K, McNaughton HK,
measures to perform a valuable meta- showed a positive effect, it might be sug- et al. Community ambulation after stroke:
analysis. However, in several of the gested that studies with a negative out- how important and obtainable is it and
what measures appear predictive? Arch
included studies, other balance and gait come were missed. Phys Med Rehabil. 2004;85:234 –239.
outcomes were performed, and some of
8 Yang YR, Tsai MP, Chuang TY, et al. Vir-
these performance-based outcome mea- In conclusion, this review suggests that tual reality-based training improves com-
sures did not demonstrate significant dif- VR training is more effective than con- munity ambulation in individuals with
ferences between VR training and con- stroke: a randomized controlled trial. Gait
ventional therapy without VR in improv- Posture. 2008;28:201–206.
ventional therapy. In addition, there is a ing balance and gait ability in patients
9 Moreira MC, de Amorim Lima AM, Ferraz
lack of outcome measures on participa- with stroke, both when VR interventions KM, Benedetti Rodrigues MA. Use of vir-
tion level and follow-up analysis. The are added to conventional therapy and tual reality in gait recovery among post
effectiveness of the VR intervention is when time dose is matched. Keeping in stroke patients: a systematic literature
review. Disabil Rehabil Assist Technol.
measured using spatiotemporal or func- mind that different interventions and 2013;8:357–362.
tional gait measures and dynamic or outcome measures were used, no defi- 10 Makizako H, Kabe N, Takano A, Isobe K.
static balance measures. However, to our nite conclusions can be drawn about the Use of the Berg Balance Scale to predict
knowledge, how these outcome mea- most effective sort of VR training inter- independent gait after stroke: a study of an
inpatient population in Japan. PM&R.
sures translate into daily life participation vention. Future studies are recom- 2015;7:392–399.
levels and quality of life has not been mended to investigate the effect of VR on 11 Michael KM, Allen JK, Macko RF. Reduced
investigated. Other reviews18,72 also con- participation level with large sample ambulatory activity after stroke: the role of
cluded that there is a lack of RCTs that sizes and an adequate follow-up period. balance, gait, and cardiovascular fitness.
measure the effect of VR on participation Arch Phys Med Rehabil. 2005;86:1552–
Overall, a positive and promising effect 1526.
level. The inclusion of outcome mea- of VR training on balance and gait ability
12 Kollen B, van de Port I, Lindeman E, et al.
sures focusing on improvement of par- is expected. Predicting improvement in gait after
ticipation levels and quality of life would stroke: a longitudinal prospective study.
have strengthened the results on the Stroke. 2005;36:2676 –2680.
effect of VR on balance and gait and the All authors provided concept/idea/research 13 Imam B, Jarus T. Virtual reality rehabilita-
translation to real life, especially as a pre- design and writing. Ms de Rooij and Dr van tion from social cognitive and motor learn-
de Port provided data collection and data ing theoretical perspectives in stroke pop-
vious study73 suggested that training in a ulation. Rehabil Res Pract. 2014;2014:
analysis. Dr Meijer provided project manage- 594540.

1916 f Physical Therapy Volume 96 Number 12 December 2016


Virtual Reality in Stroke Rehabilitation

14 Veerbeek JM, van Wegen E, van Peppen R, 28 Review Manager (RevMan) [computer 42 Cho KH, Lee WH. Virtual walking training
et al. What is the evidence for physical program]. Version 5.3. Copenhagen, Den- program using a real-world video record-
therapy poststroke? A systematic review mark: The Nordic Cochrane Centre, The ing for patients with chronic stroke: a
and meta-analysis. PLoS One. 2014;9: Cochrane Collaboration; 2014. pilot study. Am J Phys Med Rehabil. 2013;
e87987. 92:371–380.
29 Barcala L, Grecco LA, Colella F, et al.
15 Teasell RW, Foley NC, Salter KL, Jutai JW. Visual biofeedback balance training using 43 Cho KH, Lee WH. Effect of treadmill train-
A blueprint for transforming stroke reha- wii fit after stroke: a randomized con- ing based real-world video recording on
bilitation care in Canada: the case for trolled trial. J Phys Ther Sci. 2013;25: balance and gait in chronic stroke
change. Arch Phys Med Rehabil. 2008;89: 1027–1032. patients: a randomized controlled trial.
575–578. Gait Posture. 2014;39:523–528.
30 Rajaratnam BS, Gui Kaien J, Lee Jialin K,
16 Kim JH, Jang SH, Kim CS, et al. Use of et al. Does the inclusion of virtual reality 44 Jung J, Yu J, Kang H. Effects of virtual
virtual reality to enhance balance and games within conventional rehabilitation reality treadmill training on balance and
ambulation in chronic stroke: a double- enhance balance retraining after a recent balance self-efficacy in stroke patients
blind, randomized controlled study. Am J episode of stroke? Rehabil Res Pract. with a history of falling. J Phys Ther Sci.
Phys Med Rehabil. 2009;88:693–701. 2013;2013:649561. 2012;24:1133–1136.

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


17 Fung J, Richards CL, Malouin F, et al. A 31 Higgins JPT, Green S, eds. Cochrane 45 Jaffe DL, Brown DA, Pierson-Carey CD,
treadmill and motion coupled virtual real- Handbook for Systematic Reviews of et al. Stepping over obstacles to improve
ity system for gait training post-stroke. Interventions. Version 5.1.0 [updated walking in individuals with poststroke
Cyberpsychol Behav. 2006;9:157–162. March 2011]. The Cochrane Collabora- hemiplegia. J Rehabil Res Dev. 2004;
tion, 2011. Available at: http://handbook. 41(3A):283–292.
18 Saposnik G, Levin M; for the Stroke Out- cochrane.org/. Accessed December 15,
2015. 46 Yang S, Hwang W-H, Liu F-K, et al. Improv-
come Research Canada Working Group. ing balance skills in patients who had
Virtual reality in stroke rehabilitation: a 32 Kang HK, Kim Y, Chung Y, Hwang S. stroke through virtual reality treadmill
meta-analysis and implications for clini- Effects of treadmill training with optic training. Am J Phys Med Rehabil. 2011;
cians. Stroke. 2011;42:1380 –1386. flow on balance and gait in individuals fol- 90:969 –978.
19 You SH, Jang SH, Kim YH, et al. Virtual lowing stroke: randomized controlled tri-
als. Clin Rehabil. 2012;26:246 –255. 47 Kim N, Park Y, Lee BH. Effects of
reality-induced cortical reorganization and community-based virtual reality treadmill
associated locomotor recovery in chronic 33 Hung JW, Chou CX, Hsieh YW, et al. Ran- training on balance ability in patients with
stroke: an experimenter-blind randomized domized comparison trial of balance train- chronic stroke. J Phys Ther Sci. 2015;27:
study. Stroke. 2005;36:1166 –1171. ing by using exergaming and conventional 655– 658.
weight-shift therapy in patients with
20 Rodrigues-Baroni JM, Nascimento LR, Ada chronic stroke. Arch Phys Med Rehabil. 48 Park YH, Lee CH, Lee BH. Clinical useful-
L, Teixeira-Salmela LF. Walking training 2014;95:1629 –1637. ness of the virtual reality-based postural
associated with virtual reality-based train- control training on the gait ability in
ing increases walking speed of individuals 34 Singh DKA, Nordin NAM, Aziz NAA, et al. patients with stroke. J Exerc Rehabil.
with chronic stroke: systematic review Effects of substituting a portion of stan- 2013;9:489 – 494.
with meta-analysis. Braz J Phys Ther. dard physiotherapy time with virtual real-
2014;18:502–512. ity games among community-dwelling 49 Lloréns R, Gil-Gómez JA, Alcañiz M, et al.
stroke survivors. BMC Neurol. 2013;13: Improvement in balance using a virtual
21 Luque-Moreno C, Ferragut-Garcias A, 199. reality-based stepping exercise: a random-
Rodriguez-Blanco C, et al. A decade of ized controlled trial involving individuals
progress using virtual reality for post- 35 Cikajlo I, Rudolf M, Goljar N, et al. Telere- with chronic stroke. Clin Rehabil. 2015;
stroke lower extremity rehabilitation: sys- habilitation using virtual reality task can 29:261–268.
tematic review of the intervention meth- improve balance in patients with stroke.
ods. Biomed Res Int. 2015;2015:342529. Disabil Rehabil. 2012;34:13–18. 50 Song YB, Chun MH, Kim W, et al. The
effect of virtual reality and tetra-
22 Corbetta D, Imeri F, Gatti R. Rehabilitation 36 Omiyale O, Crowell CR, Madhavan S. ataxiometric posturography programs on
that incorporates virtual reality is more Effect of Wii-based balance training on cor- stroke patients with impaired standing bal-
effective than standard rehabilitation for ticomotor excitability post stroke. J Mot ance. Ann Rehabil Med. 2014;38:160 –
improving walking speed, balance and Behav. 2015;47:190 –200. 166.
mobility after stroke: a systematic review. 37 Fritz SL, Peters DM, Merlo AM, Donley J. 51 Morone G, Tramontano M, Iosa M, et al.
J Physiother. 2015;61:117–124. Active video-gaming effects on balance The efficacy of balance training with video
23 Li Z, Han XG, Sheng J, Ma SJ. Virtual reality and mobility in individuals with chronic game-based therapy in subacute stroke
for improving balance in patients after stroke: a randomized controlled trial. Top patients: a randomized controlled trial.
stroke: a systematic review and meta-anal- Stroke Rehabil. 2013;20:218 –225. Biomed Res Int. 2014;2014:580861.
ysis. Clin Rehabil. 2016;30:432– 440. 38 McEwen D, Taillon-Hobson A, Bilodeau M, 52 Givon N, Zeilig G, Weingarden H, Rand D.
et al. Virtual reality exercise improves Video-games used in a group setting is fea-
24 Dos Santos LR, Carregosa AA, Masruha mobility after stroke: an inpatient random- sible and effective to improve indicators of
MR, et al. The use of Nintendo Wii in the ized controlled trial. Stroke. 2014;45: physical activity in individuals with
rehabilitation of poststroke patients: a sys- 1853–1855. chronic stroke: a randomized controlled
tematic review. J Stroke Cerebrovasc Dis. trial. Clin Rehabil. 2016;30:383–392.
2015;24:2298 –2305. 39 Yom C, Cho HY, Lee B. Effects of virtual
reality-based ankle exercise on the 53 Song GB, Park EC. Effect of virtual reality
25 Cheok G, Tan D, Low A, Hewitt J. Is Nin- dynamic balance, muscle tone, and gait of games on stroke patients’ balance, gait,
tendo Wii an effective intervention for stroke patients. J Phys Ther Sci. 2015;27: depression, and interpersonal relation-
individuals with stroke? A systematic 8458 – 49. ships. J Phys Ther Sci. 2015;27:2057–
review and meta-analysis. J Am Med Dir 2060.
Assoc. 2015;16:923–932. 40 Lloréns R, Noé E, Colomer C, Alcañiz M.
Effectiveness, usability, and cost-benefit of 54 Cho KH, Lee KJ, Song CH. Virtual-reality
26 The George Institute for Global Health. a virtual reality-based telerehabilitation balance training with a video-game system
PEDro scale 1999 [updated April 8, 2015]. program for balance recovery after stroke: improves dynamic balance in chronic
Available at: http://www.pedro.org.au/ a randomized controlled trial. Arch Phys stroke patients. Tohoku J Exp Med. 2012;
english/downloads/pedro-scale. Accessed Med Rehabil. 2015;96:418 –25e2. 228:69 –74.
January 4, 2016.
41 Mirelman A, Bonato P, Deutsch JE. Effects 55 Lee HY, Kim YL, Lee SM. Effects of virtual
27 Maher CG, Sherrington C, Herbert RD, of training with a robot-virtual reality sys- reality-based training and task-oriented
et al. Reliability of the PEDro scale for rat- tem compared with a robot alone on the training on balance performance in stroke
ing quality of randomized controlled trials. gait of individuals after stroke. Stroke. patients. J Phys Ther Sci. 2015;27:1883–
Phys Ther. 2003;83:713–721. 2009;40:169 –174. 1888.

December 2016 Volume 96 Number 12 Physical Therapy f 1917


Virtual Reality in Stroke Rehabilitation

56 Lee IW, Kim YN, Lee DK. Effect of a virtual 62 Winstein CJ. Knowledge of results and 69 Felling RJ, Song H. Epigenetic mechanisms
reality exercise program accompanied by motor learning: implications for physical of neuroplasticity and the implications for
cognitive tasks on the balance and gait of therapy. Phys Ther. 1991;71:140 –149. stroke recovery. Exp Neurol. 2015;268:
stroke patients. J Phys Ther Sci. 2015;27: 37– 45.
2175–2177. 63 Subramanian SK, Massie CL, Malcolm MP,
Levin MF. Does provision of extrinsic feed- 70 Kwakkel G, Kollen BJ. Predicting activities
57 Darekar A, McFadyen BJ, Lamontagne A, back result in improved motor learning in after stroke: what is clinically relevant? Int
Fung J. Efficacy of virtual reality– based the upper limb poststroke? A systematic J Stroke. 2013;8:25–32.
intervention on balance and mobility dis- review of the evidence. Neurorehabil
orders post-stroke: a scoping review. Neural Repair. 2010;24:113–124. 71 Nadeau SE, Wu SS, Dobkin BH; for The
J Neuroeng Rehabil. 2015;12:46. LEAPS Investigative Team. Effects of task-
64 Holden MK. Virtual environments for specific and impairment-based training
58 Saposnik G, Teasell R, Mamdani M; for the motor rehabilitation: review. Cyber Psy- compared with usual care on functional
Stroke Outcome Research Canada Work- chol Behav. 2005;8:187–211. walking ability after inpatient stroke reha-
ing Group. Effectiveness of virtual reality bilitation: LEAPS Trial. Neurorehabil Neu-
using Wii gaming technology in stroke 65 Winstein CJ, Merians AS, Sullivan KJ. ral Repair. 2013;27:370 –380.
rehabilitation: a pilot randomized clinical Motor learning after unilateral brain dam-

Downloaded from https://academic.oup.com/ptj/article/96/12/1905/2866292 by guest on 09 November 2020


trial and proof of principle. Stroke. 2010; age. Neuropsychologia. 1999;37:975–987. 72 Lohse KR, Hilderman CG, Cheung KL,
41:1477–1484. et al. Virtual reality therapy for adults post-
66 Walker ER, Hyngstrom AS, Schmit BD. stroke: a systematic review and meta-
59 Kim EK, Kang JH, Park JS, Jung BH. Clini- Influence of visual feedback on dynamic analysis exploring virtual environments
cal feasibility of interactive commercial balance control in chronic stroke survi- and commercial games in therapy. PLoS
nintendo gaming for chronic stroke reha- vors. J Biomech. 2016;49:6987– 03. One. 2014;9:e93318.
bilitation. J Phys Ther Sci. 2012;24:901–
903. 67 Barclay-Goddard R, Stevenson T, Poluha 73 Broeren J, Sunnerhagen K, Rydmark M.
60 French B, Thomas LH, Leathley MJ, et al. W, et al. Force platform feedback for Haptic virtual rehabilitation in stroke:
Repetitive task training for improving standing balance training after stroke. transferring research into clinical practice.
functional ability after stroke. Cochrane Cochrane Database Syst Rev. 2004;4: Phys Ther Rev. 2009;14:322–335.
Database Syst Rev. 2007;4:CD006073. CD004129.
61 Merians AS, Poizner H, Boian R, et al. Sen- 68 Sveistrup H. Motor rehabilitation using vir-
sorimotor training in a virtual reality envi- tual reality. J Neuroeng Rehabil. 2004;1:
ronment: does it improve functional 10.
recovery poststroke? Neurorehabil Neu-
ral Repair. 2006;20:252–267.

Appendix.
Search String in PubMed

((((((((Virtual reality[Title/Abstract]) OR Gaming[Title/Abstract]) OR Game[Title/Abstract]) OR Virtual reality) OR Gaming) OR Game))) AND


((((Gait[Title/Abstract] OR Walking[Title/Abstract] OR Ambulation[Title/Abstract] OR Lower extremit*[Title/Abstract] OR Balance[Title/Ab-
stract] OR Mobility[Title/Abstract] OR Posture[Title/Abstract] OR Postural control[Title/Abstract] OR Endurance[Title/Abstract]))) AND
((Stroke[Title/Abstract] OR Cerebrovascular accident[Title/Abstract] OR Cerebrovascular disease[Title/Abstract] OR Hemipare*[Title/Abstract]
OR Brain attack[Title/Abstract])))

1918 f Physical Therapy Volume 96 Number 12 December 2016

You might also like