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research-article2019
CRE0010.1177/0269215519843174Clinical RehabilitationWang et al.

CLINICAL
Original article REHABILITATION

Clinical Rehabilitation

Effect of virtual reality on balance 1­–9


© The Author(s) 2019
Article reuse guidelines:
and gait ability in patients with sagepub.com/journals-permissions
DOI: 10.1177/0269215519843174
https://doi.org/10.1177/0269215519843174

Parkinson’s disease: a systematic journals.sagepub.com/home/cre

review and meta-analysis

Bo Wang1, Min Shen2, Yan-xue Wang1, Zhi-wen He1,


Shui-qing Chi3 and Zhao-hui Yang1

Abstract
Objective: The aim of this study was to evaluate the effectiveness of virtual reality interventions for
improving balance and gait in people with Parkinson’s disease.
Design: This is a systematic review and meta-analysis of randomized controlled trials.
Methods: Databases of MEDLINE, Cochran Central Register of Controlled Trials, EMBASE, PEDro,
Web of Science and China Biology Medicine disc were searched from their inception up to 1 March 2019.
Two reviewers individually appraised literatures for inclusion, extracted data and evaluated trial quality.
Results: A total of 12 studies with a median PEDro score of 6.4 and involving 419 participants were
included. This review first demonstrated significant improvements in Berg Balance Scale (mean difference
= 2.69; 95% confidence interval = 1.37 to 4.02; p < 0.0001), Timed Up and Go Test (mean difference =
−2.86; 95% confidence interval = −5.60 to −0.12; p = 0.04) and stride length (mean difference = 9.65;
95% confidence interval = 4.31 to 14.98; p = 0.0004) in Parkinson patients who received virtual reality
compared with controls. However, there was no significant difference in gait velocity and walk distance.
Conclusion: This systematic review and meta-analysis supports the use of virtual reality to enhance the
balance of patients with Parkinson’s disease. However, the review does not find any definite effect upon
gait by the use of virtual reality.

Keywords
Virtual reality, balance, gait, Parkinson’s disease, systematic review

Received: 15 September 2018; accepted: 14 March 2019

1Department of Rehabilitation, Union Hospital, Tongji Medical Corresponding author:


College, Huazhong University of Science and Technology, Zhao-hui Yang, Department of Rehabilitation, Union Hospital,
Wuhan, China Tongji Medical College, Huazhong University of Science and
2Department of Hematology, Tongji Hospital, Tongji Medical Technology, Wuhan 430022, China.
College, Huazhong University of Science and Technology, Email: annyhao430@hust.edu.cn
Wuhan, China
3Department of Pediatric Surgery, Union Hospital, Tongji

Medical College, Huazhong University of Science and


Technology, Wuhan, China
2 Clinical Rehabilitation 00(0)

Introduction Methods
Parkinson’s disease is a neurodegenerative disease Data sources and searches
that is often associated with movement impairments
such as reduced balance and gait control.1,2 The loss All procedures mentioned below were performed in
of gait and balance with progression of the disease accordance with PRISMA Checklist and Cochrane
has an impact on their ability to perform daily life Collaboration protocols.15,16 Databases of MEDLINE
activities.3,4 Virtual reality is increasingly being used (via PubMed), Web of Science, EMBASE, PEDro,
in neurological conditions including Parkinson’s Cochran Central Register of Controlled Trials and
disease, but that its effects are not yet well proven.5,6 China Biology Medicine disc were thoroughly exam-
Virtual reality is a high-tech computer–human ined using the search term “virtual reality or exer-
interface system which can make subjects engaged gaming or game or gaming,” “Parkinson’s Disease or
in environments that feel similar to real-world Parkinson or Parkinsonism,” “balance or posture or
objects and events.7 A recent meta-analysis with 21 postural control or mobility” or “gait or ambulation
randomized controlled trials (RCTs) demonstrated or walking” and their synonyms, from their inception
that virtual reality was more effective in training gait to 1 March 2019. The detailed example of the full
and balance than conventional methods in patients electronic search strategy for MEDLINE is provided
with stroke.8 The potential reasons are as follows: in Supplementary Material Appendix A. Additional
not only it can strengthen feedback by visual, ves- records were searched through other sources to sup-
tibular and somatosensory input but it also enhances plement the database results. Also, manual search of
the personalized training of gait and balance control. reference lists of related reviews was adopted. Two
However, the effect of virtual reality on gait and bal- investigators carried out study selection and data
ance of Parkinson’s disease remains unclear. extraction independently, while any discrepancy was
Recently, a growing number of studies demon- resolved by mutual discussion. All results involving
strated that the ability of gait and balance of title, abstract and reference were imported into
patients with Parkinson’s disease can be signifi- EndNote X8 for screening.
cantly improved via virtual reality when compared
with conventional therapy.9–12 But, another two
Inclusion and exclusion criteria
studies pointed out that no significant difference
between virtual reality intervention and conven- Studies that met the following criteria were eventu-
tional therapy was observed in Berg Balance Scale, ally included: (1) participants were clinically diag-
Timed Up and Go Test and gait.13,14 Unfortunately, nosed as Parkinson’s disease, which was defined by
although there are already two systematic reviews the UK Parkinson’s Disease Society Brain Bank or
discussing this topic, this controversy has not been other diagnostic criteria; (2) there were no restrictions
solved and there exist some problems in these about participants’ age, gender, disease severity and
reviews. First, one review mainly focused on older disease duration; (3) only RCTs that evaluated effects
adults and only one study involving Parkinson’s of virtual reality interventions on balance and gait in
disease was included in this review, thus the evi- patients with Parkinson’s disease were selected; (4)
dence was low. Second, another review lacked a trials that compared two or more interventions (at
meta-analysis. Finally, in the past year, new RCTs least one of which was an ongoing virtual reality
comparing the effect of virtual reality training with training) were also included; (5) at least one quantita-
conventional therapy have been published. tive outcome of balance and gait was measured and
Therefore, we performed this systematic review by no restrictions in frequency and duration of these vir-
a comprehensive meta-analysis via an updated lit- tual reality interventions; (6) the effectiveness of vir-
erature search and evaluated RCTs in order to tual reality interventions versus an alternative
explain the evidence-based effectiveness of virtual intervention such as a placebo control intervention, or
reality for Parkinson’s disease. any other exercise intervention without virtual reality
Wang et al. 3

was assessed; and (7) non-English language trials model was preferred. The statistical significance
were also included. The eliminated criteria were as within all comparisons was mathematically signified
follows: (1) overlapped or duplicated articles; (2) as p < 0.05. The potential publication bias was
reviews, case reports, letters, unpublished articles and assessed using Egger’s test.
conference abstracts; and (3) inadequate original data. The overall quality evidence was appraised using
GRADE (Grading of Recommendations, Assessment,
Development and Evaluation) approach.19 Through
Data extraction and quality assessment this measure, the evidence was assessed not by indi-
Two investigators (M.S. and Y.W.) extracted rele- vidual trail but across studies for special outcomes.
vant data independently and reached agreement on Factors that may reduce the quality of the evidence
all items. The following data were extracted from include the following: study design, risk of bias,
selected studies: general characteristics (title, first inconsistency of results, indirectness and imprecision.
author and year published), demographic charac- We adjusted the quality of evidence by a level based
teristics of the study sample sizes, age, disease on five factors.20 Levels of evidence were defined as
stage and duration, study characteristics (content of follows: (1) high-quality evidence: further studies are
intervention, training intensity and frequency, very unlikely to change the estimate or the confidence
comparators and outcome measures) and signifi- in the result. There are at least 75% of RCTs with no
cant main findings in measures of balance and gait limitations of study design, low risk of bias, consist-
ability between groups. Two reviewers (Z.H. and ent finding, direct, and precise data and no known or
S.C.) independently evaluated the included articles suspected publication biases; (2) moderate-quality
according to the PEDro scale. A PEDro scale is evidence: further studies are likely to have an impor-
composed of 11 items that can contribute one point tant impact on our confidence in the estimate of effect
to 10 score, except for the first item, eligibility cri- and may change the estimate. One of the factors is not
teria. A PEDro scale is an effective measure of met; (3) low-quality evidence; (4) very low-quality
methodological quality of clinical trials.17,18 evidence; and (5) no evidence.21
Articles with a score of 6 or higher are considered
as high quality, and those with scores of less than 6
are defined as lower quality.17 In case of disagree- Results
ment in the quality assessment of two reviewers, Identification of studies
consensus was conducted by a third reviewer.
A total of 586 related articles were identified
through database searching. In addition, three stud-
Data synthesis and analysis ies were found by manually searching reference
Our quantitative meta-analysis was performed using lists. When duplicates were removed and titles and
both fixed- or random-effects model in Review abstracts of all remaining unique articles were
Manager 5.3 under Cochrane Collaboration proto- screened, there were 36 articles needed to be fully
cols. Forest plots were generated to present the evaluated for the final inclusion. Eventually, only
pooled effect, and the mean difference (MD) with 12 of them were selected for this review.9–14,22–27
95% confidence interval (CI) was calculated for the The selection flow chart is depicted in Figure 1.
all outcomes because the pooled studies used the
same rating scale or test. Heterogeneity was assessed
Description of included studies
by means of the value of the I2 statistic. We acknowl-
edged I2 as a heterogeneity indicator with its value The participants and study characteristics are shown
<25%, 25%–50% and >50% defined as low, mod- in Table 1 and Supplementary Material Appendix B.
erate and significant heterogeneity, respectively. A In the selected studies, 12 parallel groups rand-
moderate or significant heterogeneity was adjusted omized controlled studies involving 419 participants
by a random-effects model; otherwise, a fixed-effects published between 2012 and 2018. Six trials were
4 Clinical Rehabilitation 00(0)

Figure 1.  The selection flow chart of our systematic review.

undertaken in China, three from Brazil, the rest of 10 trials10–13,22–27 using basic virtual reality where 2
three were conducted in the Netherlands, Korea and trials9,14 using augmented virtual reality.
Italy, individually. The mean age of the participants
varied between 50.9 and 80.9 years in virtual reality Content of the interventions of included
group and 48.9 and 81.7 years in control group. The
studies
mean Hoehn and Yahr stage of the subjects varied
between 0.9 and 3.6 in virtual reality group and 0.87 The intervention approaches differed with each other.
and 3.6 in control group. In addition, the mean Five studies used the Nintendo Wii Fit. Three trials
Parkinson’s disease duration of the patients varied used Kinect X-BOX or Sensor. The majority of stud-
between 0.29 and 13 years in virtual reality group ies (n = 10) compared the virtual reality intervention
and 0.64 and 12.4 years in control group. Moreover, with a comparable alternative intervention. The alter-
only four studies involved sample sizes of less than native intervention in most of the studies was con-
30 participants. In virtual reality group, there were ventional physiotherapy (n = 7). Two studies
Wang et al. 5

Table 1.  Characteristics of included studies.

References Experiment Control Dosage Outcomes Major findings Quality


Shen (2014)9 BAL Muscle strength 100 min/d, 5 SLS, stride Significant 8
training d/w, 12w length, gait improvement in SLS
velocity and stride length
Lee (2015)10 VR plus NDT NDT and FES 45 min/d, 5 BBS Significant 4
and FES d/w, 6w improvement in BBS
Liao (2015)11 Wii Fit VR Traditional 1 h/d, 2 d/w, LOS, TUG, Significant 7
exercise exercise 6w obstacle improvement in
crossing obstacle crossing
performance velocity, crossing
stride length, TUG
Shih (2016)12 VR balance Balance training 50 min/d, 2 LOS, OLS, Significant 6
training d/w, 8w BBS, TUG improvement in LOS
and OLS
Pompeu Global Global exercise 1 h/d, 2 d/w, BBS, UST No significant 5
(2012)13 exercise plus plus balance 7w differences were
Wii Fit VR exercise found in BBS, UST
Van (2014)14 VFT CBT 1 h/d, 2 d/w, FRT, BBS, SLS, No significant 8
5w 10MWT differences were
found in FRT, BBS,
SLS and 10MWT
Yang (2016)22 VR balance CBT 50 min/d, 2 BBS, TUG, No significant 7
training d/w, 6w Gait differences were
found in BBS, TUG,
gait
Lin (2016)23 VR balance CBT 30 min/d, 5 BBS, TUG Significant 7
training d/w, 4w improvement in BBS,
TUG
Ribas (2017)24 Wii Fit VR Conventional 30 min/d, 2 BBS, 6MWT Significant 7
exercise exercise d/w, 12w improvement in BBS
Gandolfi VR balance SIBT 50 min/d, 3 BBS, ABC, Significant 6
(2017)25 training d/w, 7w 10MWT improvement in BBS
and Dynamic Gait
Index
Chen (2017)26 VR balance CBT 50 min/d, 5 BBS, TUG Significant 6
training d/w, 6w improvement in BBS,
TUG
Melo (2018)27 VR gait Conventional 20 min/d, 3 6MWT, speed Significant 6
training gait training d/w, 4w improvement in
6MWT, gait speed

VR, virtual reality; BBS, Berg Balance Scale; UST, Unipedal Stance Test; VFT, virtual feedback training; CBT, conventional balance
training; FRT, functional reach test; SLS, single leg stance test; 10MWT, 10-meter walk test; BAL, technology-assisted balance and
gait training; NDT, neurodevelopment treatment; FES, functional electrical stimulation; LOS, limits of stability; TUG, Timed Up
and Go Test; OLS: one-leg stance; 6MWT, 6-minute walk test; ABC, Activities Balance Confidence scale.

combined physical therapy as an experimental inter- from 20 to 100 minutes. In addition, the duration of
vention. Moreover, 10 studies focused on balance interventions varied between 4 and 12 weeks and the
interventions and 2 studies focused on gait training. frequency of interventions ranged from 2 to 5 day/
The intensity of different trainings of all trials ranged week. Furthermore, in terms of outcome measures,
6 Clinical Rehabilitation 00(0)

Figure 2.  Meta-analysis results using the random-effects model for (a) BBS and (b) TUG. Study effect, weightage
and confidence interval are represented by box position, size and the horizontal line. The pooled effect of the
studies is shown by the diamond and its width represents the confidence interval.

there were all kinds of methods. Both Berg Balance the two reviewers. After discussion, there was in
Scale and Timed Up and Go Test were used to assess agreement for all items.
the function balance. And the gait ability was
appraised by 10-meter walk test or 6-minute walk Outcome measures and main findings of
test. All studies measured outcomes promptly post-
intervention and post-intervention scores were used
included studies
to compare between groups in this review. Balance.  Nine studies provided Berg Balance Scale
data including 299 participants in this meta-analysis
(Figure 2(a)). The comprehensive results demon-
PEDro scores strated significant effect on Berg Balance Scale
The PEDro scores of the included studies varied score after a virtual reality intervention compared
between 4 and 8, and the average score was 6.4 with a control intervention (MD = 2.69; 95% CI =
(Supplementary Material Appendix C). In total, 10 1.37 to 4.02; p < 0.0001). However, substantial het-
studies had a score of 6 or higher and were consid- erogeneity was indicated with an I2 statistic of 69%.
ered of high quality. All trials randomly allocated When excluding the studies by Chen et al. and Shih
the subjects. Moreover, the majority of trials et al., low heterogeneity (I2 = 9%) was observed.
reported eligibility criteria, had similar groups at The MD was 2.71 and remained significant in favor
baseline, assessor blinding and concealed alloca- of the virtual reality group (95% CI = 1.80 to 3.63;
tion and used both point measures and measures of p < 0.0001) (Supplementary Material Appendix D).
variability. In summary, 13 of the 132 items from There was no publication bias within the included
the PEDro scale were initially scored different by cohorts according to the Egger’s test (p = 0.49).
Wang et al. 7

Figure 3.  Meta-analysis results using the fixed-effects model for (a) gait velocity, (b) walk distance and (c) stride
length. Study effect, weightage and confidence interval are represented by box position, size and the horizontal line.
The pooled effect of the studies is shown by the diamond and its width represents the confidence interval.

Five studies involving 144 participants meas- showed no significantly greater increases in walk
ured the effect of virtual reality versus control ther- distance in virtual reality group compared with the
apy on the Timed Up and Go Test (Figure 2(b)). control group using 6-minute walk test (MD = 8.91,
The impact was statistical significant: MD = 95% CI = −43.32 to 61.13; p = 0.74) (Figure 3(b)).
−2.86; 95% CI = −5.60 to −0.12; p = 0.04. No heterogeneity (I2 = 0%) was observed. How-
Heterogeneity was high (I2 = 73%). However, ever, in terms of stride length, there was a significant
excluding the studies by Chen et al., no heteroge- difference when virtual reality group was compared
neity (I2 = 0%) was observed. The MD was −1.74 with the control group (MD = 9.65; 95% CI = 4.31
and remained significant in favor of the virtual to 14.98; p = 0.0004) (Figure 3(c)). And there is no
reality group (95% CI = −3.21 to −0.27; p = 0.02) statistical heterogeneity (I2 = 0%). An Egger’s test
(Supplementary Material Appendix D). Also, there was not applied due to the very small number of
was no publication bias within the included cohorts studies.
according to the Egger’s test (p = 0.089). As for subgroup analysis, the different Hoehn
and Yahr stage of included studies were compared
Gait ability.  Gait velocity was recorded in five stud- in the Berg Balance Scale and Timed Up and Go
ies (n = 203), but there was no significant difference Test, and no significant differences were observed
between groups (MD = −0.00; 95% CI = −0.06 to between groups in Berg Balance Scale (p = 0.27)
0.06; p = 0.98) (Figure 3(a)) and no heterogeneity and groups in Timed Up and Go Test (p = 0.30)
(I2 = 0%). Also, two of the six studies (n = 45) (Supplementary Material Appendix E).
8 Clinical Rehabilitation 00(0)

In summary, using GRADE criteria, this review may have missed some literatures through the
found moderate evidence that virtual reality inter- search terms we have used. Finally, although the
ventions are more effective than control interven- majority of the selected studies provided high
tions in Berg Balance Scale and low evidence that methodological quality, the most did not conduct
virtual reality training is more effective than con- participant and clinician blinding, which could
trol training in Timed Up and Go Test in Parkinson’s lead to bias in the included trials.
disease. Furthermore, there is very low-quality evi- Even though there exist some limitations in
dence that virtual reality interventions are more this systematic review, there remain some impli-
effective than control interventions in stride length cations for practice and future research. First, vir-
(Supplementary Material Appendix F). tual reality therapies are thought to improve
motivation and enjoyment, to increase the activ-
ity adherence in training and to decrease the per-
Discussion ception of exertion. However, none of included
This meta-analysis demonstrated significant results studies in this review assessed the motivation.
of virtual reality training on the improvement of Further study should consider motivation as an
Berg Balance Scale based on moderate evidence outcome measure. Second, to assess the duration
according to GRADE criteria and Timed Up and of any improvement outcome to be sustained for
Go Test with low evidence according to GRADE virtual reality intervention, future trials should
criteria. In addition, with respect to gait ability, sig- have longer follow-up duration. Furthermore,
nificant improvements in stride length were additional large-scale RCTs should be conducted
reported in two studies, although this finding was to appraise the effect of virtual reality interven-
supported only by very low evidence according to tion because of the small sample size of included
GRADE criteria. studies in this review. Finally, future researchers
The positive findings of virtual reality training are should compare the effects between different vir-
consistent with a previous review on the effect of vir- tual reality interventions and investigate the most
tual reality on balance including Berg Balance Scale effective virtual reality method and dosage.
and Timed Up and Go Test in patients with Parkinson’s
disease.28 However, the systematic review by Dockx Clinical Messages
et al.29 did not support these positive results. The
•• This systematic review suggests that
potential conflicts may be due to the fact that the
“virtual reality” interventions are effec-
review included only seven studies for meta-analysis.
tive at improving balance in people with
And five additional studies were included in our
Parkinson’s disease.
review, which were published after its publication.
•• The review did not find any definite
However, there exist some limitations in our
effect upon gait and mobility, but the
study. First, the majority of 12 included studies
total number of studies and the total
had small sample size and intervention approaches
number of patients were both low leaving
varied considerably in this review. Not only the
some uncertainty on this matter.
devices of virtual reality come from different cor-
porations but also the contents of virtual reality
differ with each other. Moreover, there are some Declaration of Conflicting Interests
variabilities in the number of intervention ses- The author(s) declared no potential conflicts of interest
sions, frequency and duration in the included stud- with respect to the research, authorship and/or publica-
ies. In addition, the majority of post-intervention tion of this article.
follow-up ranges from 1 month to 3 months and
only one study reported the effects after 15 months. Funding
Furthermore, virtual reality is not a very accurate The author(s) received no financial support for the
description, although it is widely used. Thus, we research, authorship and/or publication of this article.
Wang et al. 9

Supplemental material 14. van den Heuvel MR, Kwakkel G, Beek PJ, et al. Effects
of augmented visual feedback during balance training
Supplemental material for this article is available online. in Parkinson’s disease: a pilot randomized clinical trial.
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