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Published Ahead of Print on May 2, 2018 as 10.1212/WNL.

0000000000005603
VIEWS & REVIEWS

Advantages of virtual reality in the rehabilitation


of balance and gait
Systematic review
Desiderio Cano Porras, MSc, Petra Siemonsma, PhD, Rivka Inzelberg, MD, Gabriel Zeilig, MD, Correspondence
and Meir Plotnik, PhD Dr. Plotnik

®
meir.plotnik@
Neurology 2018;0:1-9. doi:10.1212/WNL.0000000000005603 sheba.health.gov.il

Abstract
Background
Virtual reality (VR) has emerged as a therapeutic tool facilitating motor learning for balance and
gait rehabilitation. The evidence, however, has not yet resulted in standardized guidelines. The
aim of this study was to systematically review the application of VR-based rehabilitation of
balance and gait in 6 neurologic cohorts, describing methodologic quality, intervention pro-
grams, and reported efficacy.

Methods
This study follows the Preferred Reporting Items for Systematic Reviews and Meta-Analyses.
VR-based treatments of Parkinson disease, multiple sclerosis, acute and chronic poststroke,
traumatic brain injury, and cerebral palsy were researched in PubMed and Scopus, including
earliest available records. Therapeutic validity (CONTENT scale) and risk of bias in ran-
domized controlled trials (RCT) (Cochrane Collaboration tool) and non-RCT (Newcastle-
Ottawa scale) were assessed.

Results
Ninety-seven articles were included, 68 published in 2013 or later. VR improved balance and
gait in all cohorts, especially when combined with conventional rehabilitation. Most studies
presented poor methodologic quality, lacked a clear rationale for intervention programs, and
did not utilize motor learning principles meticulously. RCTs with more robust methodologic
designs were widely recommended.

Conclusion
Our results suggest that VR-based rehabilitation is developing rapidly, has the potential to
improve balance and gait in neurologic patients, and brings additional benefits when combined
with conventional rehabilitation. This systematic review provides detailed information for
developing theory-driven protocols that may assist overcoming the observed lack of argued
choices for intervention programs and motor learning implementation and serves as a reference
for the design and planning of personalized VR-based treatments.

Registration
PROSPERO CRD42016042051.

From the Center of Advanced Technologies in Rehabilitation (D.C.P., M.P.) and Department of Neurological Rehabilitation (G.Z.), Sheba Medical Center, Tel Hashomer; Departments
of Neurology and Neurosurgery (R.I.), Physical and Rehabilitation Medicine (G.Z.), and Physiology and Pharmacology (M.P.), Sackler Faculty of Medicine (D.C.P.), and Sagol School of
Neuroscience (R.I., M.P.), Tel Aviv University, Israel; Perception and Action in Complex Environments (D.C.P.), Marie Curie International Training Network, European Union’s Horizons
2020 Research and Innovation Program, Brussels, Belgium; Division of Health Care (P.S.), University of Applied Science, Leiden; THIM International School for Physiotherapy (P.S.),
Nieuwegein; and Predictive Health Technologies (P.S.), Netherlands Organization for Applied Scientific Research, Leiden, the Netherlands.

Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

Copyright © 2018 American Academy of Neurology 1


Copyright ª 2018 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
Glossary
10-MWT = 10 Meter Walk Test; BBS = Berg Balance Scale; CP = cerebral palsy; CR = conventional rehabilitation; GS = gait
speed; MLS = motor learning strategies; MS = multiple sclerosis; NOS = Newcastle-Ottawa Scale; PD = Parkinson disease;
PRISMA = Preferred Reported Items for Systematic Reviews and Meta-Analyses; RCT = randomized controlled trials; TBI =
traumatic brain injury; TUG = Timed Up and Go; VR = virtual reality.

Virtual reality (VR) has emerged as a rehabilitation tech- Methods


nology for patients with neurologic conditions. Like in other
types of rehabilitation, VR-based interventions attempt to This study followed the Preferred Reported Items for Sys-
promote neuroplasticity and motor learning.1,2 To structure tematic Reviews and Meta-Analyses (PRISMA),17 and the
interventions promoting motor learning, therapists conduct protocol registration is in the PROSPERO International
clinical practices known as motor learning strategies (MLS) Prospective Register for Systematic Reviews (crd.york.ac.uk/
that take into consideration specific motor learning prospero/; registration CRD42016042051).
principles.3,4 A recent study defined MLS as “observable
therapeutic actions in which therapists consider task and Eligibility criteria
client-specific factors to select and to apply evidence-based A participants, interventions, comparisons, outcomes, and
practice and feedback variables for optimal motor learning.”4 study design (PICOS) model defined eligibility criteria.17
VR has several advantages over conventional rehabilitation
(CR) for implementing MLS, in particular facilitating the Participants: Patients with PD, MS, acute or chronic
(>6 months) poststroke, TBI, or CP.
incorporation of motor learning principles such as real-time
Interventions: Rehabilitation treatments implementing VR
multisensory feedback, task variation, objective progression,
for recovery of balance and gait.
and task-oriented repetitive training.5,6 Performing this type
Comparisons: Pretraining and posttraining or between
of training in a VR environment can induce the re-
interventions (e.g., VR vs CR such as physical therapy or
organization of the neural architecture7 and stimulates
treadmill training).
the recovery of motor skills after neurologic damage.1,7,8 VR
Outcomes: Measures of balance and gait.
also facilitates both standardization and personalized
Study design: Any design with measurement pre–post
interventions.5
training.
There is growing evidence of the benefits of VR for improving
Search strategy
balance and gait in neurologic patients.9–11 Balance and gait
Searches included the earliest available records on August
are significant predictors of functional independence and are 2016 in PubMed and Scopus. The search in PubMed included
associated with risk of falls,12,13 ambulation, and physical the builder “all fields” and the query (virtual reality or video
activity.13,14 Moreover, deficits in balance and gait limit games) and (motor learning or rehabilitation) and (posture
activities of daily living and quality of life.10 This growing or gait or balance or mobility). We conducted a similar
evidence has not yet resulted in guidelines for VR-based strategy in Scopus. A manual search identified additional
rehabilitation of balance and gait,15 and a consensus regarding records.
optimal intervention programs (for example, dosage and
tasks) and actual effects of VR is lacking. This hampers the Study selection
development of standardized interventions and the optimal One author (D.C.P.) performed 2-level eligibility assessment
use of VR in rehabilitation.1,15,16 by first checking the title and abstract and then checking the
full text. Two authors (P.S. and M.P.) checked the included
This study systematically reviews the implementation of VR articles. Disagreements were resolved by consulting R.I.
in the rehabilitation of balance and gait in patients with and G.Z.
Parkinson disease (PD), multiple sclerosis (MS), acute and
chronic poststroke, traumatic brain injury (TBI), and cerebral Data extraction
palsy (CP). The objective is to describe the application of VR We collected data on participants (medical condition, sample
and the reported outcomes and effects from individual size, age, and time of diagnosis), type of intervention (e.g., VR
publications, with the goal to provide detailed information for combined with CR), measures assessing balance and gait,
the design and planning of future VR-based interventions follow-up assessment (after intervention), and reported out-
among neurologic patients. We also aim to clarify aspects comes and effects of VR. In addition, we described the (1)
related to the emerging use of VR for each medical condition, characteristics of the study (design, country, and setting); (2)
in particular regarding (1) efficacy in improving balance and implementation of motor learning principles, i.e., feedback
gait, (2) intervention programs for VR-based rehabilitation, (intrinsic, from within [sensory], and extrinsic, from outside),
and (3) therapeutic validity. task variation (e.g., weight-shifting, obstacle negotiation),

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treatment intensity (e.g., total time in VR training) (indicating Synthesis of results and analysis
repetitions), and progression; and (3) VR system (equip- Studies were classified by design (RCT, cohort studies, and
ment, level of immersion based on previous definition18). case reports). Because of the high number of publications
included, tables e-1 and e-2 (links.lww.com/WNL/A497)
Assessment of methodologic quality report only about RCTs that (1) were labeled as therapeuti-
We used the CONTENT scale to assess therapeutic validity.19 cally valid, that is, scored ≥6 the CONTENT scale; and (2)
The scale includes 9 items accounting for patient eligibility, had the lowest risk of bias, that is, the highest fourth quartile
competences and settings, rationale, content, and adherence. (≥3 points) in the Cochrane Collaboration tool (table e-3).
Studies scoring under 6 points are considered to have poor
therapeutic quality.19 Assessment of risk of bias relied on the Primary outcome was efficacy of VR (outcomes and effects of
study design. The Cochrane Collaboration tool20 was used for individual publications on balance and gait).
randomized controlled trials (RCT) and quasi-RCT and the
Newcastle-Ottawa Scale (NOS) for cohort studies (non-
RCT) and case reports (5 participants or fewer) (ohri.ca/ Results
programs/clinical_epidemiology/oxford.asp). The Cochrane Study selection
tool analyzed 7 domains: random sequence generation, allo- Figure 1 shows the selection process in a PRISMA diagram
cation concealment, blinding of participants and personal resulting in the final inclusion of 97 studies.
data, blinding of outcome assessment, incomplete outcome
data, selective reporting, and other bias. The NOS comprised Years of publication and study design
8 items reporting on selection, comparability, and outcome. More than 70% (68 studies) were published in 2013 or later
All the studies were assigned 2 scores: 1 for therapeutic (figure 2). Designs were RCT or quasi-RCT (n = 49 [50%]),
validity (from 0 to 9) and the other for risk of bias (from 0 to 7 cohort studies (n = 34 [35%]), and case reports (n = 14
points for RCT and from 0 to 8 stars for non-RCT). [15%]) (tables e-1 and e-4, A–F, links.lww.com/WNL/A497).

Figure 1 Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram of study selection

The search strategy identified 1,333


records. The screening stage removed
32 duplicates, 1,175 studies based on
title and abstract, and assessed the
eligibility of 126 full texts, for a final
inclusion of 97 studies. Studies on
poststroke were divided into 2 main
groups according to chronicity: acute
and chronic (more than 6 months). VR
= virtual reality.

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Figure 2 Frequency of publications

The number of publications reporting on rehabilitation programs using virtual reality for training in balance and gait has been growing at an exponential rate
for the last few years, with a remarkable focus on poststroke studies.

Sample sizes ranged from an average of 12 patients with CP to a more effective reduction of risk of fall compared to a tread-
34 with MS. mill-only intervention.30 However, studies recommend
further RCTs with larger samples, e.g., reference 27.
Methodologic quality
Forty-nine studies (50%) lacked therapeutic validity and most Multiple sclerosis (n = 11)
studies presented high risk of bias (table e-3, links.lww.com/ Several outcome measures improved on BBS (3/5 studies),
WNL/A497). TUG (2/4), and the 4-Step Square Test (3/4). Three studies
reported maintained improvements between 1 and 2 months
Treatment intensity follow-up. One study,31 however, did not find significant
Total VR treatment period averaged 583 ± 430 minutes benefits using VR and another found a decline in physical
(figure 3). activity at week 14.32 Some authors suggested that VR should
complement CR,15,31 while others recommended its use as
Outcomes measuring balance and gait an alternative to CR,33 VR being more effective than CR in
Most reported balance measures were Berg Balance Scale improving balance in one study.34
(BBS, n = 38) and Timed Up and Go (TUG, n = 34); for
walking, these were gait speed (GS, n = 22), the 10 Meter Acute poststroke (n = 11)
Walk Test (10-MWT, n = 19), and the 6 Meter Walk Test Positive changes were found on BBS (in 6 out of 7 studies),
(n = 13) (tables e-1 and e-4, A–F, links.lww.com/WNL/ TUG (5/6), and 10-MWT (3/3). Three studies conducted
A497). Twelve studies performed dual-task conditions (e.g., 2–4 week follow-up assessments; one35 reported benefits in
motor-cognitive). walking ability at 1-month follow-up and 2 did not find
significant gains (or losses). One study36 suggested that
Findings and conclusions reported VR-based telerehabilitation provides similar outcomes of bal-
by publications ance and gait compared to CR, while another35 suggested that
Nearly all studies reported benefits of VR training on balance incorporating VR into CR may be more effective than CR only.
and gait (tables e-1 and e-4, A–F, links.lww.com/WNL/ However, it was also reported37 that the inclusion of VR into
A497). This section reports findings postintervention and CR does not lead to overall benefits in balance, although VR
during follow-up assessments. may improve balance in patients with normal sensory function.

Parkinson disease (n = 18) Chronic poststroke (n = 35)


All but one study21 found gains in TUG (n = 7) and BBS (n = Over 80% (13/16 studies) evaluating TUG reported gains.
9). Eight studies with follow-up assessments suggested that Improvements occurred on BBS (11/14) and GS (9/10).
gains might remain or continue to improve between 2 weeks Follow-up assessments in 10 studies lacked consensus.
and 6 months after intervention. Some concluded that VR is Half38–42 of the studies suggested that gains are not main-
useful as therapeutic intervention22 and proposed VR as an tained and 5 maintained or improved gains.43–47 A home-
alternative to independent exercise.23 Three home-based based telerehabilitation VR training41 improved balance and
interventions24–26 reported positive findings on gait and bal- gait as in-clinic VR intervention. Likewise, VR training was as
ance. Some authors stated that VR training brings benefits effective as CR.8,39,40 Some studies found that VR might
similar to CR.21,25,27–29 A multimodal intervention (motor- have an augmented effect, for example, combined with
cognitive) combining VR and treadmill training resulted in robotic-supported training,45,46 stepping over obstacles,44 and

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Figure 3 Treatment intensity

These histograms show the virtual reality (VR) rehabilitation strategies adopted in terms of treatment intensity among the included studies. The upper plots
express the time (in minutes) that patients effectively spent in VR intervention. This does not include time spent in other interventions (e.g., conventional
balance therapy or neurodevelopmental treatment). We observed that the majority of studies implemented interventions of 20–40 minutes of VR per session
for 3 sessions per week over 4–6 weeks. The total time of VR training generally lasted between 300 and 600 minutes.

CR.1,40,47 One study reported that further research is needed treatment,56 transcranial direct current stimulation,16 and
to demonstrate the effect of VR on balance and gait.38 robotic training57,58). Other authors reported on the feasi-
bility of VR for rehabilitation59 at home60 and in clinicse1
Traumatic brain injury (n = 6) (links.lww.com/WNL/A498).
Significant gains occurred in BBS, functional gait assessment,
and VR scores representing weight-shifting. Three studies
performing follow-up assessments suggested that gains may Application of VR and of motor learning
persist after VR training (2 days–3 months). One study48 principles: Level of immersion, multisensory
reported that VR only was more effective to improve GS and feedback, treatment intensity, task variation
weight-shifting compared to a combination of VR and vestibular and progression
therapy. Three other studies suggested that VR leads to nearly Tables e-2 and e-5, A–F (links.lww.com/WNL/A497), de-
equal outcomes of balance and gait compared to CR.49–51 scribe VR application. Most studies utilized semi-immersive
(n = 15 [16%]) or nonimmersive VR (n = 74 [76%]),
Cerebral palsy (n = 16) mainly low-cost commercial consoles such as Nintendo Wii
All studies (n = 11) evaluating 10-MWT, pediatric balance (n = 41).
scale, GS, and gross motor function measure, with the ex-
ception of one study,52 reported gains in these measures. Five Up to 88% (n = 85) of studies reported intrinsic feedback:
studies with follow-up assessments suggested maintained visual (n = 84 studies), auditory (n = 42), somatosensory
gains after 1–3 months of VR training (table e-4, A–F, links. (i.e., haptic, tactile, and vibratory; n = 8), and proprioceptive
lww.com/WNL/A497). Other authors suggested that VR is (n = 6). In addition, 79% (n = 77) reported extrinsic feedback:
not effective for balance training53 or that VR should be knowledge of performance (n = 70) and knowledge of results
viewed as an addition to CR.54,55 The need for studies with (n = 37). However, studies did not assess or discuss the
larger sample sizes was emphasized. benefits of feedback.

Some authors suggested additional benefits of VR in combi- Patients performed a variety of task-oriented and repetitive
nation with other therapies (e.g., neurodevelopmental activities (tables e-2 and e-5, A–F, links.lww.com/WNL/A497).

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Table e-6 identifies the application of treatment progression CP studies (n = 16) presented poor methodologic quality. For
and additional measures for VR application (e.g., safety, preintervention/postintervention comparisons, 3 (therapeu-
adherence, and self-efficacy). tically valid) studies found significant improvements in
balance and gait52,59,e9 (links.lww.com/WNL/A498). In
contrast, 3 studies lacking therapeutic validity did not find
Discussion significant results to conclude that VR is effective.54,55,e1 This
suggests that for patients with CP, possibly due to their young
This systematic review assessed and compared VR-based age, more rigorous intervention programs are required for
strategies for rehabilitation of balance and gait across dif- achieving clinical efficacy.
ferent neurologic conditions, while previous reviews focused
on a sole cohort (e.g., poststroke or MS,10,e2 links.lww.com/ Finally, follow-up assessments suggest that VR contributes to
WNL/A498). Our results suggest that VR has additional maintain benefits for weeks or even months after intervention
benefits for rehabilitation of balance and gait, especially (the only exception to this consistent trend was in chronic
when combined with other interventions such as CR. poststroke). Others support our findings that improvements
However, most studies presented poor methodologic remain for 2 months after intervention for PD.9
quality and intervention programs lacked a clear rationale, in
particular regarding treatment intensity, personalized Interpretation of results
training, and task variation. Indeed, the worst scores in VR implementation is developing rapidly (figure 2). Most
therapeutic validity were in items 6 (“Was the intensity of studies in all 6 cohorts showed certain levels of evidence of the
the therapeutic exercise selected and adjusted on theoreti- efficacy of VR for improving balance and gait. Levels of ad-
cally driven and/or argued choices?”) and 8 (“Was the herence, motivation, and enjoyment consistently favored VR
therapeutic exercise personalized and contextualized to the (table e-6, links.lww.com/WNL/A497). Despite the encour-
individual participants?”) (table e-3, links.lww.com/WNL/ aging results, we found some weaknesses on the imple-
A497). mentation of VR. One main source of weakness relates to the
fact that most of the studies do not define a priori rationalized
Summary of main findings MLS for the interventions. The lack of rational intervention
For PD (18 studies), most studies comparing VR to CR found programs and personalized interventions are a methodologic
similar improvements in balance and gait.21,25,28,29 This sup- problem that hinder therapeutic validity and represent a seri-
ports rehabilitation strategies using VR. ous limitation.

For MS (n = 11), we found discrepancies in the outcomes of Incorporating MLS into the design and planning of VR
balance and gait among studies with different levels of interventions and treatment intensity may overcome these
methodologic quality. Two studies (therapeutically valid, low challenges.3,4 Researchers recognized that VR is notably
risk of bias, and one utilizing immersive VR) suggested that useful to incorporate MLS that optimize motor learning for
VR has similar benefits compared to CR15,e3 (links.lww.com/ a successful rehabilitation program.4–6 The use of MLS may
WNL/A498). On the other hand, 2 studies (not therapeuti- contribute to reaching homogeneity in the description and
cally valid, with high risk of bias, and using nonimmersive VR) quantification of VR interventions in future studies.
suggested that VR is more effective than CR.33,34 Marked
differences in patient heterogeneity and treatment intensity We define theory-driven VR-based rehabilitation protocols as
may explain these discrepancies. The 4 MS studies with the evidence-based description and quantification of inter-
shortest exposure to VR (260–360 minutes) did not present ventions aiming to promote motor learning using VR tech-
significant advantage of VR15,31,e3,e4 (tables e-1 and e-4, A–F, nology. Such protocols will facilitate the exploitation of MLS.
links.lww.com/WNL/A497). Wuest et al.e10 (links.lww.com/WNL/A498) reported such an
example with a set of VR applications that systematically exploit
For poststroke (n = 11 acute and n = 35 chronic), VR seemed “variance practice” and “progression,” alternating training ses-
to be more effective at improving dynamic balance than static sions with different tasks. Similar initiatives may address mul-
balance for both chronice5,e6 (links.lww.com/WNL/A498) tisensory feedback, treatment intensity (i.e., repetitions), or task
and acute poststroke.e7 Studies of acute poststroke suggest specificity.
that VR is safe and improves balance and gait even after recent
episodes of stroke.14 VR to enhance motor learning
VR enhanced motor learning principles (as shown for ex-
For TBI (n = 6), the additional benefits of VR warrant further ample in CP,11 MS [links.lww.com/WNL/A498],e2 post-
investigation. Although balance and gait improved within VR- stroke,e11,e12 and PD9,e13).
only interventionse7,e8 (links.lww.com/WNL/A498), there
was no consensus in effects when VR was compared to other For treatment intensity, some authors suggest a minimum of
interventions. Only 1 study found significant benefits of VR 10 sessions for poststroke18 or 14 sessions for PD.9 This
compared to traditional vestibular therapy.48 review found that treatment intensity was heterogeneous with

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a minimum of 9 sessions in acute poststroke and of 8 sessions neuroplasticitye19 (links.lww.com/WNL/A498), and partly
in PD. Task variations included weight-shifting, obstacle ne- explains the benefits of VR on balance and gait in PD21 and
gotiation, dual tasking, and treadmill training, among others. CP.16 Progression might be adjusted according to extrinsic
feedback and motivation. For instance, if the patient is tired or
Motivation and enjoyment may assist motor learning. One- bored, she or he should be engaged in less difficult tasks.
third of studies (n = 32, table e-6, links.lww.com/WNL/ Alternatively, if the knowledge of results (extrinsic feedback)
A497) evaluated these features. Lack of motivation or en- reports very high scores, the therapist can consider engaging
joyment may lead to the interruption or cessation of re- the patient to a more demanding task.
habilitation treatment (i.e., adherence), which in turn can
hamper the potential of the patient to improve balance and This study presents the most frequently reported measures
gaite14–e16 (links.lww.com/WNL/A498). measuring balance and gait in each cohort, enabling clinicians
to compare their results with previous studies. BBS, TUG, and
Nearly 60% of studies (table e-6, links.lww.com/WNL/A497) GS-related measures were the most commonly reported, and
reported progression adjustments9,e16 (links.lww.com/ they matched the results of other systematic reviews9,18,e14,e15
WNL/A498) for an efficient control of the level of difficulty (links.lww.com/WNL/A498).
per VR tasks within and across sessions.
Safety is a high priority in clinical interventions (58 studies
Immediate multisensory feedback is important10,e17 (links. evaluated safety levels or adverse events) (table e-6, links.lww.
lww.com/WNL/A498). Adding somatosensory and pro- com/WNL/A497), yet the results are controversiale11,e15
prioceptive inputs enriches intrinsic feedback (mainly visual- (links.lww.com/WNL/A498). We recommend using objec-
auditory in VR studies). Moreover, extrinsic feedback tive and subjective measures of safety.9
(knowledge of results and knowledge of performance) is
highly relevant in VR interventions because it facilitates an Finally, we encourage conducting follow-up assessments to
objective measure of progress and increases motivation (e.g., better understand long-term outcomes of VR rehabilitatione16
in poststroke10,e11 and PDe13). (links.lww.com/WNL/A498), as VR is an emerging technology.

Comparison with the literature Implications for future research


Our results are consistent with a meta-analysis in post- Although training in fully immersive VR may present eco-
strokee12 (links.lww.com/WNL/A498) and a review in MSe2 logical validity and seems to bring additional benefits com-
supporting the efficacy of VR for balance and gait re- pared to training in less immersive VR systemse15 (links.lww.
habilitation. We also observed that combining VR with CR in com/WNL/A498), further work needs to establish whether
poststroke,10,18,e14 CP,11 and PD30 is beneficial. Our findings the outcomes transfer to the real worlde17 and investigate how
on follow-up assessments for acute poststroke corroborate the level of immersion may influence balance and gait.
others,e12 suggesting that patients may improve in balance
and gait 1–6 months after stroke. Nonetheless, interventions Finally, further research might attempt differentiating clini-
in acute poststroke applied less intense treatments than in cally oriented VR vs commercial video games. Several authors
chronic poststroke (figure 3). insist that video games were originally designed for healthy
people and therefore are unsuitable for the recovery of sen-
Clinical relevance sorimotor impairments40,e20 (links.lww.com/WNL/A498)
The results of this systematic review should benefit clinical (for a comparison of clinically oriented VR vs commercial
practice with protocols or guidelines incorporating both the video games, see reference e12).
provisional evidence and rational treatment choices. A good
start would be illness-related protocols facilitating the design Strengths and limitations
of patient-tailored VR interventions. This systematic review evaluated 97 studies using VR for
improving balance and gait in 6 neurologic cohorts and de-
We thus encourage researchers and clinical experts to take tailed the strategies for applying VR. The study was limited to
initiatives to develop theory-driven VR-based rehabilitation balance and gait; however, there are tangential domains (e.g.,
protocols (e.g., references e10 and e18) incorporating MLS.4 cognitive function) not considered in this review. Another
This systematic review provides ample information for the limitation is the inclusion of low-quality studies. Nevertheless,
realization of such protocols (e.g., motor tasks and VR games considering the novelty of VR for neurologic rehabilitation,
for each cohort). this review may contribute to rational treatment choices in
future VR interventions.
Clinicians should strike the right balance between too difficult
and too easy tasks, and as such keeping the patient’s moti- Our results suggest that VR has the ability to improve balance
vation high. This delicate balance deserves much attention. It and gait in neurologic patients, and creates additional benefits
seems that extrinsic feedback and progression play a critical when combined with other interventions such as CR. These
role. Objective progression encourages training,58 elicits additional benefits seem to rely on the capability of VR to

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exploit MLS (i.e., task variation and repetition, multisensory 8. Singh DKA, Nordin NAM, Aziz NAA, Lim BK, Soh LC. Effects of substituting
a portion of standard physiotherapy time with virtual reality games among
feedback, and motivation). This systematic review provides community-dwelling stroke survivors. BMC Neurol 2013;13:1.
detailed information for VR-based interventions in different 9. Barry G, Galna B, Rochester L. The role of exergaming in Parkinson’s disease
rehabilitation: a systematic review of the evidence. J Neuroeng Rehabil 2014;11:33.
neurologic cohorts and may serve as a reference for the design 10. Darekar A, McFadyen BJ, Lamontagne A, Fung J. Efficacy of virtual reality-based
and planning of future VR-based rehabilitation programs. intervention on balance and mobility disorders post-stroke: a scoping review. J Neu-
roeng Rehabil 2015;12:1.
11. Dewar R, Love S, Johnston LM. Exercise interventions improve postural control in
There are 2 clinical implications. First, given the growing children with cerebral palsy: a systematic review. Dev Med Child Neurol 2015;57:
evidence of the advantages of VR and the lack of argued 504–520.
12. Newstead AH, Walden GJ, Gitter AJ. Gait variables differentiating fallers from non-
choices in VR interventions setup, a clinical practice guide for fallers. J Geriatr Phys Ther 2007;30:93–101.
VR-based rehabilitation is necessary. This guide should focus 13. Tatla SK, Radomski A, Cheung J, Maron M, Jarus T. Wii-habilitation as balance
therapy for children with acquired brain injury. Dev Neurorehabil 2014;17:1–15.
on incorporating MLS and VR-related values.4 Second, 14. Rajaratnam B, Gui KaiEn J, Lee JiaLin K, et al. Does the inclusion of virtual reality
interventions should be personalized according to individual games within conventional rehabilitation enhance balance retraining after a recent
episode of stroke? Rehabil Res Pract 2013;2013:649561.
sensorimotor and cognitive impairments and environmental 15. Kalron A, Fonkatz I, Frid L, Baransi H, Achiron A. The effect of balance training on
factors (e.g., social and family support), regardless of the postural control in people with multiple sclerosis using the CAREN virtual reality
system: a pilot randomized controlled trial. J Neuroeng Rehabil 2016;13:1.
neurologic condition. 16. Grecco LAC, Duarte NdAC, Mendonça ME, Galli M, Fregni F, Oliveira CS. Effects of
anodal transcranial direct current stimulation combined with virtual reality for im-
proving gait in children with spastic diparetic cerebral palsy: a pilot, randomized,
Author contributions controlled, double-blind, clinical trial. Clin Rehabil 2015;29:1212–1223.
D. Cano Porras: study concept and design, acquisition of data, 17. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting sys-
tematic reviews and meta-analyses of studies that evaluate health care interventions:
analysis and interpretation, critical revision of the manuscript explanation and elaboration. PLOS Med 2009;6:e1000100.
for important intellectual content. Dr. Siemonsma: study 18. Luque-Moreno C, Ferragut-Garcı́as A, Rodrı́guez-Blanco C, et al. A decade of
concept and design, analysis and interpretation, critical re- progress using virtual reality for poststroke lower extremity rehabilitation: systematic
review of the intervention methods. Biomed Res Int 2015;2015:342529.
vision of the manuscript for important intellectual content. 19. Hoogeboom TJ, Oosting E, Vriezekolk JE, et al. Therapeutic validity and effectiveness
Prof. Inzelberg: critical revision of the manuscript for im- of preoperative exercise on functional recovery after joint replacement: a systematic
review and meta-analysis. PLoS One 2012;7:e38031.
portant intellectual content, study supervision. Prof. Zeilig: 20. Higgins JP, Altman DG, Gøtzsche PC, et al. The Cochrane Collaboration’s tool for
critical revision of the manuscript for important intellectual assessing risk of bias in randomised trials. BMJ 2011;343:d5928.
21. van den Heuvel MR, Kwakkel G, Beek PJ, Berendse HW, Daffertshofer A, van Wegen
content, study supervision. Dr. Plotnik: study concept EE. Effects of augmented visual feedback during balance training in Parkinson’s dis-
and design, analysis and interpretation, critical revision of ease: a pilot randomized clinical trial. Parkinsonism Relat Disord 2014;20:1352–1358.
22. Zettergren K, Franca J, Antunes M, Lavallee C. The effects of Nintendo Wii Fit
the manuscript for important intellectual content, study training on gait speed, balance, functional mobility and depression in one person with
supervision. Parkinson’s disease. Med Health Sci J 2011;9:18–24.
23. Killane I, Fearon C, Newman L, et al. Dual motor-cognitive virtual reality training
impacts dual-task performance in freezing of gait. IEEE J Biomed Health Inform 2015;
Study funding 19:1855–1861.
24. Esculier JF, Vaudrin J, Bériault P, Gagnon K, Tremblay LE. Home-based balance
This work received support from the Perception and Action in training programme using Wii Fit with balance board for Parkinson’s disease: a pilot
Complex Environments (PACE) project, which has received study. J Rehabil Med 2012;44:144–150.
funding from the European Union’s Horizon 2020 Research 25. Yang WC, Wang HK, Wu RM, Lo CS, Lin KH. Home-based virtual reality balance
training and conventional balance training in Parkinson’s disease: a randomized
and Innovation Program under the Marie Sklodwska-Curie controlled trial. J Formos Med Assoc 2016;115:734–743.
grant agreement no. 642961. 26. Zalecki T, Gorecka-Mazur A, Pietraszko W, et al. Visual feedback training using Wii
Fit improves balance in Parkinson’s disease. Folia Med Cracov 2013;53:65–78.
27. Liao YY, Yang YR, Cheng SJ, Wu YR, Fuh JL, Wang RY. Virtual reality–based training
Disclosure to improve obstacle-crossing performance and dynamic balance in patients with
Parkinson’s disease. Neurorehabil Neural Repair 2015;29:658–667.
The authors report no disclosures relevant to the manuscript. 28. Pompeu JE, dos Santos Mendes FA, da Silva KG, et al. Effect of Nintendo
Go to Neurology.org/N for full disclosures. Wii™-based motor and cognitive training on activities of daily living in patients with
Parkinson’s disease: a randomised clinical trial. Physiotherapy 2012;98:196–204.
29. Yen CY, Lin KH, Hu MH, Wu RM, Lu TW, Lin CH. Effects of virtual reality–
Received September 7, 2017. Accepted in final form March 12, 2018. augmented balance training on sensory organization and attentional demand for
postural control in people with Parkinson disease: a randomized controlled trial. Phys
Ther 2011;91:862–874.
References 30. Mirelman A, Rochester L, Maidan I, et al. Addition of a non-immersive virtual reality
1. Cho KH, Lee WH. Virtual walking training program using a real-world video re-
cording for patients with chronic stroke: a pilot study. Am J Phys Med Rehabil 2013; component to treadmill training to reduce fall risk in older adults (V-TIME):
92:371–384. a randomised controlled trial. Lancet 2016;388:1170–1182.
2. Kleim JA, Jones TA. Principles of experience-dependent neural plasticity: implications 31. Nilsagård YE, Forsberg AS, von Koch L. Balance exercise for persons with multiple
sclerosis using Wii games: a randomised, controlled multi-centre study. Mult Scler
for rehabilitation after brain damage. J Speech Lang Hear Res 2008;51:S225–S239.
2013;19:209–216.
3. Levac D, Missiuna C, Wishart L, DeMatteo C, Wright V. Documenting the content of
32. Plow M, Finlayson M. Potential benefits of Nintendo Wii Fit among people with
physical therapy for children with acquired brain injury: development and validation
multiple sclerosis: a longitudinal pilot study. Int J MS Care 2011;13:21–30.
of the Motor Learning Strategy Rating Instrument. Phys Ther 2011;91:689–699.
33. Lozano-Quilis JA, Gil-Gómez H, Gil-Gómez JA, et al. Virtual rehabilitation for
4. Levac DE, Glegg SM, Sveistrup H, et al. Promoting therapists’ use of motor learning
multiple sclerosis using a kinect-based system: randomized controlled trial. JMIR
strategies within virtual reality-based stroke rehabilitation. PLoS One 2016;11: Serious Games 2014;2:e12.
e0168311. 34. Brichetto G, Spallarossa P, de Carvalho MLL, Battaglia MA. The effect of Nintendo®
5. Keshner EA, Fung J. The quest to apply VR technology to rehabilitation: tribulations Wii® on balance in people with multiple sclerosis: a pilot randomized control study.
and treasures. J Vestib Res 2017;27:1–5. Mult Scler 2013;19:1219–1221.
6. Levin MF, Weiss PL, Keshner EA. Emergence of virtual reality as a tool for upper limb 35. Morone G, Tramontano M, Iosa M, et al. The efficacy of balance training with video
rehabilitation: incorporation of motor control and motor learning principles. Phys game-based therapy in subacute stroke patients: a randomized controlled trial.
Ther 2015;95:415–425. Biomed Res Int 2014;2014:580861.
7. You SH, Jang SH, Kim YH, et al. Virtual reality–induced cortical reorganization and 36. Krpic A, Savanovic A, Cikajlo I. Telerehabilitation: remote multimedia-supported
associated locomotor recovery in chronic stroke an experimenter-blind randomized assistance and mobile monitoring of balance training outcomes can facilitate the
study. Stroke 2005;36:1166–1171. clinical staff’s effort. Int J Rehabil Res 2013;36:162–171.

8 Neurology | Volume , Number  | Month 0, 2018 Neurology.org/N


Copyright ª 2018 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
37. Song YB, Chun MH, Kim W, Lee SJ, Yi JH, Park DH. The effect of virtual reality and 49. Cuthbert JP, Staniszewski K, Hays K, Gerber D, Natale A, O’Dell D. Virtual reality-
tetra-ataxiometric posturography programs on stroke patients with impaired standing based therapy for the treatment of balance deficits in patients receiving inpatient
balance. Ann Rehabil Med 2014;38:160–166. rehabilitation for traumatic brain injury. Brain Inj 2014;28:181–188.
38. Fritz SL, Peters DM, Merlo AM, Donley J. Active video-gaming effects on balance and 50. Sveistrup H, McComas J, Thornton M, et al. Experimental studies of virtual reality-
mobility in individuals with chronic stroke: a randomized controlled trial. Top Stroke delivered compared to conventional exercise programs for rehabilitation.
Rehabil 2013;20:218–225. CyberPsychology Behav 2003;6:245–249.
39. Givon N, Zeilig G, Weingarden H, Rand D. Video-games used in a group setting is 51. Thornton M, Marshall S, McComas J, Finestone H, McCormick A, Sveistrup H.
feasible and effective to improve indicators of physical activity in individuals with Benefits of activity and virtual reality based balance exercise programmes for adults
chronic stroke: a randomized controlled trial. Clin Rehabil 2016;30:383–392. with traumatic brain injury: perceptions of participants and their caregivers. Brain Inj
40. Hung JW, Chou CX, Hsieh YW, et al. Randomized comparison trial of balance 2005;19:989–1000.
training by using exergaming and conventional weight-shift therapy in patients with 52. Brien M, Sveistrup H. An intensive virtual reality program improves functional bal-
chronic stroke. Arch Phys Med Rehabil 2014;95:1629–1637. ance and mobility of adolescents with cerebral palsy. Pediatr Phys Ther 2011;23:
41. Lloréns R, Noé E, Colomer C, Alcañiz M. Effectiveness, usability, and cost-benefit of 258–266.
a virtual reality–based telerehabilitation program for balance recovery after stroke: 53. Ramstrand N, Lygnegård F. Can balance in children with cerebral palsy improve
a randomized controlled trial. Arch Phys Med Rehabil 2015;96:418–425.e2. through use of an activity promoting computer game? Technol Health Care 2012;20:
42. Yatar GI, Yildirim SA. Wii Fit balance training or progressive balance training in 531–540.
patients with chronic stroke: a randomised controlled trial. J Phys Ther Sci 2015;27: 54. Jelsma J, Pronk M, Ferguson G, Jelsma-Smit D. The effect of the Nintendo Wii Fit on
1145–1151. balance control and gross motor function of children with spastic hemiplegic cerebral
43. Flynn S, Palma P, Bender A. Feasibility of using the Sony PlayStation 2 gaming platform palsy. Dev Neurorehabil 2013;16:27–37.
for an individual poststroke: a case report. J Neurol Phys Ther 2007;31:180–189. 55. Tavares CN, Carbonero FC. Finamore PdS, Kós RS. Uso do Nintendo® Wii para
44. Jaffe DL, Brown DA, Pierson-Carey CD, Buckley EL, Lew HL. Stepping over reabilitação de crianças com paralisia cerebral: estudo de caso. Rev Neurocien 2013;
obstacles to improve walking in individuals with poststroke hemiplegia. J Rehabil Res 21:286–293.
Dev 2004;41:283. 56. Tarakci D, Ersoz Huseyinsinoglu B, Tarakci E, Razak Ozdinçler A. The effects of
45. Mirelman A, Bonato P, Deutsch JE. Effects of training with a robot-virtual reality Nintendo Wii-fit video games on balance in children with mild cerebral palsy. Pediatr
system compared with a robot alone on the gait of individuals after stroke. Stroke Int 2016;58:1042–1050.
2009;40:169–174. 57. Burdea GC, Cioi D, Kale A, Janes WE, Ross SA, Engsberg JR. Robotics and gaming to
46. Mirelman A, Patritti BL, Bonato P, Deutsch JE. Effects of virtual reality training on gait improve ankle strength, motor control, and function in children with cerebral palsy:
biomechanics of individuals post-stroke. Gait Posture 2010;31:433–437. a case study series. IEEE Trans Neural Syst Rehabil Eng 2013;21:165–173.
47. Yang YR, Tsai MP, Chuang TY, Sung WH, Wang RY. Virtual reality-based training 58. Patritti BL, Sicari M, Deming LC, et al. The role of augmented feedback in pediatric
improves community ambulation in individuals with stroke: a randomized controlled robotic-assisted gait training: a case series. Technol Disabil 2010;22:215–227.
trial. Gait Posture 2008;28:201–206. 59. Jaume-i-Capó A, Martı́nez-Bueso P, Moya-Alcover B, Varona J. Interactive re-
48. Sessoms PH, Gottshall KR, Collins JD, Markham AE, Service KA, Reini SA. habilitation system for improvement of balance therapies in people with cerebral
Improvements in gait speed and weight shift of persons with traumatic brain injury palsy. IEEE Trans Neural Syst Rehabil Eng 2014;22:419–427.
and vestibular dysfunction using a virtual reality computer-assisted rehabilitation 60. AlSaif AA, Alsenany S. Effects of interactive games on motor performance in children
environment. Mil Med 2015;180:143–149. with spastic cerebral palsy. J Phys Ther Sci 2015;27:2001.

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Advantages of virtual reality in the rehabilitation of balance and gait: Systematic
review
Desiderio Cano Porras, Petra Siemonsma, Rivka Inzelberg, et al.
Neurology published online May 2, 2018
DOI 10.1212/WNL.0000000000005603

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