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Research Report

Effect of Virtual Reality Training on


Balance and Gait Ability in Patients
W ith Stroke: Systematic Review and
Meta-Analysis
Ilona j.M. de Rooij, Ingrid C.L. van de Port, Jan-Willem G. Meijer
I.J.M. de Rooij, MSc, Revant
Rehabilitation Centres, Breda, the
B ackground. 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, 481 7 JW, Breda, the N e th ­
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.
D a ta 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
M eijer J-WG. Effect o f 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 w ith stroke: sys­
D a ta E xtraction and Synthesis. Twenty-one studies with a median PEDro score of tem atic review and meta-analysis.
6.0 were included. The included studies demonstrated a significant greater effect of VR training Phys Ther. 20 16 ;9 6 :1 9 0 5 -1 9 1 8 .]
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
Published Ahead of Print:
when VR interventions were added to conventional therapy and when time dose was matched.
May 12, 2016
Accepted: May 1, 2016
Lim itatio n s. 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.

s » : Post a Rapid Response to


(o) * h 's a rtic le at:
fep ptjournal.apta.org

December 2016 Volum e 96 Num ber 12 Physical Therapy ■ 1905


Virtual Reality in Stroke Rehabilitation

any patients with stroke experi­ can perform real-time tasks and antici­ Method

M ence sensory, motor, cognitive,


and visual impairments, which
all have an impact on their ability to
perform daily life activities.1-2 Approxi­
pate and react to objects or events.13'1718
It has been shown that VR can improve
upper extremity motor function in adults
Data Sources and Searches
A literature search was earned out using
the databases PubMed (since 1950),
with chronic hemiparesis as a result from 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 ail use of VR in lower extremity stroke reha­ ture,” “postural control,” “mobility”), or
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.810 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.411 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.313 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.1415 and (2) Are VR interventions in addition
Data Extraction and Q uality
to conventional therapy more effective
Assessment
In recent years, the use of virtual reality than conventional therapy alone in
The following data were extracted from
(VR) has been introduced in the field of improving balance and gait ability in
patients with stroke? the included articles: sex, age, time since
stroke rehabilitation.16 Virtual reality is
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 ■ 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 I 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
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.
F lo w c h a rt o f th e s tu d y selection. R C T= ra n d o m ize d c o n tro lle d tria l.
puted from the change scores between
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
Results played VR at home.4" Another reason for
In case of low heterogeneity, the fixed-
Identification of Studies exclusion was VR training that did not
effect model was used to pool study
In total, 398 relevant articles were found involve balance or gait training.11 Even­
results for the outcomes BBS, TUG, and
in PubMed, Embase, MEDLINE, and tually, 21 articles were included in the
gait speed. When significant heterogene­
Cochrane Library. In addition, 3 arti­ review.
ity was observed (I2 >50%), the random-
effects model was applied. In addition, a cles29-3233 were identified through hand
sensitivity analysis was conducted when searching reference lists. When dupli­ Description of Included Studies
heterogeneity was present. Forest plots cates were removed, 203 articles In the 21 included studies, the mean age
were generated to present the pooled remained. Based on title and abstract of of the participants varied between 45.9
effect, and the mean difference (MD) these 203 articles, 174 articles were and 65.9 years in the VR group and 46.3
with 95% confidence interval (Cl) was excluded (Fig. 1). The main reasons for and 65.7 years in the control group. Time
calculated for the BBS and TUG out­ excluding these articles were study since stroke ranged between 12.7 days
designs other than RCTs, interventions and 11.3 years in the VR group and

D e ce m b e r 2 0 1 6 V o lu m e 9 6 N u m b e r 12 Physical T h e ra p y ■ 19 07
Virtual Reality in Stroke Rehabilitation

Table 1.
Characteristics of the Selected Studies and Analysis of O utcom e Measures and of Gait A bility and Balance and Main Findings3

S tu d y N ( M a le ) M e a n A g e (S D ) (y ) T i m e S in c e S t r o k e ( S D ) V R In t e r v e n t io n C o n tr o l In te r v e n tio n

Givon et al,52 201 6 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 20 15 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
49.2 (12.9)
Lee et al,56 201 5 20(11) VR group: 57.2 (9.2) nr VR training with cognitive PNF exercise program
Control group: tasks
52.7 (11.7)
Llorens et al,49 201 5 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,51 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 20 14 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,33 201 4 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 20 14 20 (11) VR group: 65.6 (1 3.5) 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 20 13 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 20 13 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)

betw een 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 studies832’42' 47 extremities. In the study by Song et al,50 groups was equal. In 4 studies,16’29-50’54
w ere treadmill based and provided a VR however, the upper extremity was the participants in the VR group per­
intervention in combination w ith 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 w hich 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 w ith the control group (Tab. 1).

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Virtual Reality in Stroke Rehabilitation

Table 1.
Continued

T im e D ose o f VR S ig n ific a n t
G ro u p C o m p a re d O u tc o m e M e as u re s o f S ig n ific a n t B e tw e e n - O u tc o m e M easures B e tw e e n -C ro u p s
S tud y W it h C o n tro l G ro u p G a it A b ility G rou ps Findings o f B alan ce Findings

Givon e t al,52 201 6 Equal Functional: 10M W T ns

Kim et al,47 20 1 5 Equal Static balance: PSPL PSPL (AP, ML, and
(AP, ML, and to ta l), to ta l), APSS (P C .05)
APSS

Lee et al,55 201 5 Equal Static balance: COP FRT (P C .0001)


path len g th , COP
velocity D ynam ic
balance: FRT

Lee et al,56 2015 Equal D ynam ic balance: BBS, BBS, TUG (PC .05)
TUG

Llorens e t al,49 2015 Equal Functional: 10M W T 10M W T (P*C.05) D ynam ic balance: BBS, BBS (PC .05)
T in e tti POMA, Brunei
Balance Assessment

Song et al,53 20 1 5 Equal Functional: 10M W T 10M W T (P < .05) Static balance: w e ig h t­ W eight-bearing ratio
bearing ratio affected affected side,
side, fo rw ard and forw ard and
backward LOS backward LOS, TUG
D ynam ic balance: TUG (P < .0 5 )

C ho et al,43 20 14 Equal Spatiotem poral: gait Gait speed, cadence, Static balance: AP-PSV, BBS, TUG (P = .0 0 1 )
speed, cadence, step single- and d ou b le -lim b ML-PSV, PSVM
len g th , stride length, su pp o rt period, step and D ynam ic balance: BBS,
d o u b le -lim b support stride length ( P c .029) TUG
period, single-lim b
supp o rt period

H ung et a l,33 20 1 4 Equal Static balance: SI, SI (P C .05)


w eig h t-b ea ring
asym m etry on affected
leg
D ynam ic balance:
TUG, FRT

M o ro n e et al,51 2014 Equal Functional: 10MW T, FAC 10M W T (P = .0 2 1 ) D ynam ic balance: BBS BBS (P = .0 0 4 )

Song et al,50 201 4 H igher Static balance: FI SI and WDI w hile


scores, SI, WDI standing w ith eyes
D ynam ic balance: BBS open and w hen
standing on a p illo w
w ith eyes open
( P c .01 7)

Barcala et al,29 2013 H igher D ynam ic balance: BBS, ns


TUG Static balance:
COP oscillations

Cho et al,42 2013 Equal Spatiotem poral: g ait G ait speed, cadence D ynam ic balance: BBS, BBS, TUG (P = ,0 1 )
speed, cadence, paretic (P = .0 1 ) TUG
side step length, stride
len g th , and single-lim b
su p p o rt period

Park e t al,48 201 3 Equal Spatiotem poral: g ait Stride length (P < .03)
speed, cadence, step
length, stride length
Functional: 10M W T

(Continued)

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Virtual Reality in Stroke Rehabilitation

Table 1.
Continued

Study N (M ale) M ean Age (SD) (y) Tim e Since Stroke (SD) VR In terven tio n Control In terven tio n
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,54 201 2 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

lung et al,44 201 2 21 (13) VR group: 60.5 (8.6) VR group: 12.6 (3.3) mo VR treadmill training Non-VR treadmill training
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,46 201 1 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,’ 8 2009 24 (1 4 ) 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,43 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

° n r= n o t reported, ns=nonsignificant, 6MWT=Six-Minute Walk Test, 10M W T=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, Fl=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, MM AS=Modified M otor Assessment Scale,
POMA=Performance-Oriented Mobility Assessment, PSPL=postural sway path length, PSVM = postural sway velocity moment, Sl=stability index, ss=self-
selected pace, stance time/P=stance time of the paretic limb, LOS = lim it of stability, step no./=step number of the paretic limb, TUG=Timed "Up & Co"
Test, WAQ=Walking Ability Questionnaire, W D I=w eight 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

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Virtual Reality in Stroke Rehabilitation

Table 1.
Continued

Tim e Dose o f VR Significant


Group Compared Outcom e Measures of Significant Between- Outcome Measures Between-Groups
Study W ith Control Group Gait A bility Groups Findings o f Balance Findings

Rajaratnam et a l,30 Equal Static balance: CoP FRT (P = .0 1 )


2013 sway Dynam ic
balance: BBS, TUG,
FRT

Cho e ta l,54 2012 H igher Static balance: AP-PSV BBS, TUG (P < .05)
and ML-PSV (w ith eyes
open or closed)
D ynam ic balance: BBS,
TUG

Jung et al,44 2012 Equal D ynam ic balance: TUG, ABC (PC .05)
TUG, ABC scale

Kang et al,32 2012 Equal Functional: 6M W T, 6M W T, 10 M W T (P c .0 5 ) D ynam ic balance: VR g rou p vs co ntro l


10M W T TUG, FRT g ro u p 1: TUG
(P C .05)
VR g ro u p vs co ntro l
g ro u p 2: TUG, FRT
(P c .0 5 )

Yang e t al,46 201 1 Equal Static balance: COPML (P = .038)


COPML, COPAP,
COPE, COPA,
sym m etry index (q uie t
stance and sit-to-stand
transfer), COPE/P (sit-
to-stand transfer)
stance tim e/P , step
no./P, co nta ct A/P
(level w alking )

Kim e t a l,’ 6 2009 H igher Spatiotem poral: Cadence, step length, Static balance: mean BBS, AP angle, and
cadence, step tim e, step tim e (P c .0 1 4 ) balance, sway area, M L angle (P c .0 1 )
stance tim e, swing tim e, sway path, m axim al
sing le /d ou b le supp o rt velocity D ynam ic
tim e , step/stride length balance: BBS, AP
Functional: 10MW T, angle, M L angle
MMAS

Yang e t al,8 2008 Equal Functional: 10MW T, Pretest-posttest: 10M W T, D ynam ic balance: ABC ns
co m m u n ity w alking c o m m u n ity w alking tim e scale
tim e, W AQ (PC .05)
Follow -up: W AQ (P = .03)

Jaffe e t al,45 2004 Equal Spatiotem poral: g ait Gait speed, stride length
speed, cadence, step (ss), obstacle clearance,
and stride length step length o f nonparetic
Functional: obstacle test, leg (ss) and paretic leg
distance on 6M W T (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,32'44'4548 and the VR was pro­ in favor of the VR intervention in differ­
able at ptjoumal.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-l6'29'30'33'42'43'46'47'49"56 except for the studies by Barcala et al29
training sessions a week. Eight and Givon et al52 (Tab. 1). Four studies
studies832 42-47 focused on a gait inter­ were not included in the meta-analysis: 3

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Virtual Reality in Stroke Rehabilitation

T a b le 2.
PEDro Scores o f th e In clu d e d Studies'3

P o i n t E s t im a te s a n d V a r i a b i l i t y
N o M is s in g D a t a o r I f M is s in g ,
D a ta f o r a t L e a s t 1 O u tc o m e
o f P a r tic ip a n ts

I n t e n t i o n - t o - T r e a t A n a ly s is

B e t w e e n - G r o u p s A n a ly s is
B a s e lin e C o m p a r a b i lit y
C o n c e a le d A llo c a tio n

P a r t i c ip a n t B lin d e d
R a n d o m A llo c a tio n
E lig ib ility C r ite r ia

T o t a l S c o re ( / 1 0 )
C lin ic ia n B lin d e d

A s s e s s o r B lin d e d

>85%
F ro m
S tu d y

G ivon et al,52 201 6 Yes i 0 1 0 0 1 i i 0 i 6

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

Lee e t al,55 2015 Yes i 0 1 0 0 0 1 0 1 i 5

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

Llorens et al,49 20 1 5 Yes i 1 1 0 0 1 1 1 1 i 8

Song e t al,53 201 5 Yes 1 0 1 0 0 0 0 0 1 i 4

C ho et al,43 2014 Yes 1 1 1 0 0 1 1 0 1 i 7

Hung et al,33 20 1 4 Yes 1 1 1 0 0 1 1 0 1 1 7

M o ro n e e t al,51 2014 Yes i 1 1 0 0 1 1 1 1 i 8

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

Barcala et al,29 201 3 Yes i 1 1 0 0 1 1 0 1 i 7

Cho et al,42 20 1 3 Yes i 1 1 0 0 1 1 1 1 i 8

Park et al,48 201 3 Yes i 0 1 0 0 0 1 1 1 i 6

Rajaratnam et al,30 201 3 Yes 1 0 1 0 0 1 1 1 1 0 6

Cho e t al,54 201 2 Yes i 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 i 1 1 0 0 1 1 1 1 1 8

Yang et al, 2 0 1 146 Yes i 0 0 0 0 1 1 0 1 1 5

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

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

Jaffe et al,45 2 0 04 Yes i 0 0 0 0 0 1 0 1 0 3

° 1 =yes, 0 = n o .

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 outcom e 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 -.0 0 2 ). The I2 sta­
data of one study50 w ere 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
G a it a b ility . 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 w ith 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 W hen these studies w ere excluded, the
functional outcom e measures, and 6 examined by pooling the data of 8 stud­ I2 of the pooled effect becam e 0%, with
studies8-32-49-51-53 focused only on func­ ies in w hich VR training was time dose an SMD of 0.86 (95% CI=0.52, 1.20;
tional gait ability. Gait speed was the m atched to conventional therapy P C .0 0 1 ).
most frequently used measure of gait (Fig. 2A). The pooled SMD showed
ability, as all studies measuring gait abil­ that time dose-m atched VR training

1912 ■ Physical T h e ra p y V o lu m e 9 6 N u m b e r 12 D e ce m b e r 2 0 1 6
Virtual Reality in Stroke Rehabilitation

A. Tim e dose m atched


VR C ontrol Standardized Mean D ifference Standardized Mean D ifference
Study o r Subgroup Mean SD Total Mean SD Total W eight IV, Random, 95% Cl IV, Random, 95% Cl

Givon et al,52 2016 0.06 0.15 24 0.1 0.16 23 15.2% -0 .2 5 (-0.83, 0.32)

Llorens et al,49 2015 1.9 1.6 10 0 2.3 10 12.7% 0.92 (-0.01, 1.85) *

Cho et a l/ 3 2014 20.89 11.41 15 9.75 7.19 15 13.8% 1.14(0.36, 1.92)

Morone et al,51 2014 14.52 18.36 25 7.5 7.03 22 15.1% 0.48 (-0.10, 1.07)

Cho et al,42 201 3 25.4 12.86 7 9.75 6.55 7 10.7% 1.44 (0.21, 2.66)
Park et al,48 2013 6.74 6.76 8 1.94 3.09 8 12.0% 0.86 (-0.18, 1.90)

Kang et al,32 2012 0.21 0.06 10 0.01 0.02 10 7.8% 4.28 (2.56, 6.00)
Yang et al,8 2008 0.16 0.11 11 0.02 0.15 9 12.6% 1.04 (0.09, 1.99)

Total (95% Cl) 110 104 100.0% 1.03 (0.38,1.69) ♦


Heterogeneity: Tau2=0.64; x 2=31.12, df= 7 (P<.0001); l2=78%
-4 -2 2 4
Test for overall effect: Z=3.10 (P=.002)
Favors Control Favors VR Training

B. A d d itio n al
VR C ontrol Mean D ifference Mean D ifference
Study o r Subgroup Mean SD Total Mean SD Total W e igh t IV, Fixed, 95% Cl IV, Fixed, 95% Cl

Kim et al,16 2009 15.37 9.14 12 2.3 9.14 12 100.0% 13.07 (5.76, 20.38)

Total (95% Cl) 12 12 100.0% 13.07 (5.76, 20.38)

Heterogeneity: not applicable


-2 0 -1 0 0 10 20
Test for overall effect: Z=3.50 (*=.0005) Favors Contro| favors yR Training

F ig u re 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 m ent in time of the TUG in favor of the
tional to conventional therapy. This ogeneity betw een the 2 studies in w hich VR group (Fig. 4B).
study show ed 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 D is c u s s io n
(Fig. 2B). did not show a significant effect of VR This systematic review provided evi­
training com pared with conventional dence for a stronger effect of VR training
B alan ce. Regarding studies on bal­ therapy (MD=1.17; 95% C I= —6.54, com pared 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- w ere the most frequently used measures
dynamic and static balance outcom e 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 betw een the VR not find significant results for the TUG in significant improvements in these 3 out­
group (n = 4 7 ) and control group (n =44) favor of the VR group. The pooled results come measures in favor of the VR group
w ere found in 4 of the 11 studies re­ for the TUG show ed a significant MD of for both time dose-m atched VR interven­
porting on static balance.46’47'50'53 The 2.48 (95% 0 = 1 .2 8 , 3.67; P C .001) in tions and VR interventions in addition to
dynamic balance of patients w ith stroke favor of the VR group. However, substan­ conventional therapy. The positive find­
seems to improve significantly m ore after tial heterogeneity was indicated with an ings of VR training are in line with pre­
a VR intervention com pared w ith 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 low er extremity in patients with
ences w ere 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 ,«,43,49,51,54,56 The pooled MD VR group (95% 0 = 1 .0 2 , 1.67; PC.001) This conflicting finding may be due to
for VR training time dose m atched to (eFigs. 1 and 2). The pooled MD for VR the fact that these reviews included only
conventional therapy show ed 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 w ith 2.18 (95% CI=1.52, 2.85; This study show ed a significant improve­ and, therefore, included only 524 or 625
PC. 001) (Fig. 3A). The I2 statistic of 9% studies. In addition, 2 of the included

December 2016 Volume 96 Number 12 Physical Therapy ■ 1913


Virtual Reality in Stroke Rehabilitation

A. Time dose matched


VR Control Mean Difference Mean Difference
Study or Subgroup Mean SD Total Mean SD Total Weight IV, Fixed, 95% Cl IV, Fixed, 95% Cl
Llorens et al,49 2015 3.8 2.6 10 1.8 1.4 10 13.3% 2.00 (0.17, 3.83)
C h o e ta l« 2014 3.34 1.63 15 1.53 0.91 15 49.8% 1.81 (0.87, 2.75)
Morone et al,5’ 2014 8.68 5.81 25 5.14 3.54 22 6.0% 3.54 (0.82, 6.26)
Cho et al,42 201 3 4.14 1.21 7 1.86 1.21 7 27.7% 2.28 (1.01, 3.55) — a—

Rajaratnam et al,30 2013 8 5.78 10 2.67 1.48 9 3.2% 5.33 (1.62, 9.04)

Total (95% Cl) 67 63 100.0% 2.18(1.52, 2.85) ♦


1
1
-10 -5 5 10
Test for overall effect: Z=6.42 (Pc.00001)
Favors Control Favors VR Training

B. Additional
VR Control Mean Difference Mean Difference
Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% Cl IV, Random, 95% Cl
Barcala et al,29 2013 2.3 1.42 10 5 0.4 10 50.8% -2.70 (-3.61,-1.79)
Kim et al,14 2009 6.75 2.68 12 1.58 2.68 12 49.2% 5.17(3.03, 7.31) — ■—

Total (95% Cl) 22 22 100.0% 1.17 (-6.54, 8.88)


Heterogeneity; TauMO.26 x;=43.78, dfc 1 (P=.00001); |4=98% ------------------1-------- 1-------- 1-------- 1-------- 1-----------------
Test for overall effect: Z==0.30 (P=,77) -4 -2 0 2 4
Favors Control Favors VR Training
Figure 3.
Forest plot of the pooled results for effect of VR training on Berg Balance Scale in (A) time dose-matched studies (n=1 30) and (B) studies
in which VR was additional to conventional therapy (n=44). VR=virtual reality, IV=inverse variance, CI=confidence interval.

A. Time dose matched


VR Control Mean Difference Mean Difference
Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% Cl IV, Random, 95% Cl
Cho et al,"45 2014 2.42 1.12 15 1.16 0.79 15 24.1% 1.26 (0.57, 1.95)
Hung et al,33 2014 5.18 8.18 13 2.84 8.18 15 3.4% 2.34 (-3.74, 8.42)
Cho et al,42 201 3 2.26 0.32 7 0.95 0.42 7 25.6% 1.31 (0.92, 1.70)
Rajaratnam et al,30 2013 16.27 4.8 10 10.86 4.1 9 6.6% 5.41 (1.41, 9.41)
Jung et al,44 2012 2.7 1.9 11 0.8 0.7 10 20.7% 1.90 (0.70, 3.10)
Kang etal,32 2012 5.55 2.04 10 0.4 0.84 10 19.5% 5.15 (3.78, 6.52)

Total (95% Cl) 66 66 100.0% 2.48 (1.28, 3.67)


Heterogeneity: Tau2=1.41; x2=32.68, df=5 (P<.00001); l2=85%
-5 0 5 10
Test for overall effect: Z=4.07 (P<.0001)
Favors Control Favors VR Training

B. Additional
Control Mean Difference Mean Difference

Barcala et al,29 2013 3,6 0.42 10 2.9 0.52 10 100.0% 0.70(0.29, 1.11) *
Total (95% Cl) 10 10 100.0% 0.70 (0.29, 1.11)
I |
Heterogeneity: not applicable 1
-4 -2 2 4
Test for overall effect: Z=3.31 (P=.0009)
Favors Control Favors VR Training

Figure 4.
Forest plot of the pooled results for the effect of VR training on Timed "Up & Co" Test in (A) time dose-matched studies (n = l 32) 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 w hen VR was included in the analysis of the BBS may
u pper extremity m otor function'’8 or added to conventional therapy was the explain why there was no significant
global m otor function59 and did not only measure that did not significantly pooled effect of VR training in addition
include dynamic balance measures (BBS, improve m ore after VR training. The high to conventional therapy. The m eta­
TUG) or static balance measures. The heterogeneity betw een the 2 studies analysis included only studies of high

1914 ■ 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.6263 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
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, Llorens 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.917 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

D e ce m b e r 2 0 1 6 V o lu m e 9 6 N u m b e r 12 Physical T h e ra p y ■ 1915
Virtual Reality in Stroke Rehabilitation

consisted of both walking and balance virtual environment might improve qual­ m e n t and fu n d p ro c u re m e n t. D r van de Port
exercises, whereas the VR training was ity of life and feeling of safety. Further­ an d D r M e ije r p ro v id e d c o n s u lta tio n (in c lu d ­
specifically focused on balance. In the more, most of the studies measured the in g review o f m a n u s c rip t b e fore subm ission).
treadmill studies, the control therapy effect of VR directly after the interven­ T he a u thors th a n k T h a m a r B ovend'E erdt,
often consisted of treadmill training, but tion; only 4 studies8-33-48-52 also mea­ PhD, fo r his c o n trib u tio n as scie n tific adviser
without VR. Using this design, the true sured the effect of VR after 1 or 3 months fo r th e e sta b lish m e n t o f th e research ques­
additional value of VR could be studied. of follow-up. However, it would be inter­ tio n s and sp e cifica tio n o f th e s tu d y design.
In this review, both VR in addition to esting to investigate the long-term effects
D O I: 1 0 .2 5 2 2 /p tj.2 0 1 6 0 0 5 4
conventional therapy and VR training of VR training to ascertain whether
time dose matched to conventional ther­ VR-induced improvement can be sus­
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Appendix.
Search String in PubMed

((((((((Virtual reality[Title/Abstract]) OR G am ing[Title/Abstract]) OR G am e[Title/Abstract]) OR Virtual reality) OR G am ing) OR Game))) AND


((((G ait[Title/Abstract] OR W alking[Title/Abstract] OR Am bulation[Title/A bstract] OR Lower extrem it*[T itle/A bstract] OR Balance[Title/Ab-
stract] OR M ob ility[T itle/A b stra ct] OR PosturefTitle/Abstract] OR Postural con trol[T itle/A bstract] OR Endurance[Title/Abstract]))) AND
((Stroke[Title/Abstract] OR Cerebrovascular accident[Title/Abstract] OR Cerebrovascular disease[Title/Abstract] OR Hem ipare*[Title/Abstract]
OR Brain attack[Title/Abstract])))

1918 ■ Physical Therapy Volum e 96 Num ber 12 December 2016


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