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0000000000005603
VIEWS & REVIEWS
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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.
Figure 1 Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram of study selection
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.
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).
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
Updated Information & including high resolution figures, can be found at:
Services http://n.neurology.org/content/early/2018/05/02/WNL.0000000000005
603.full.html
Subspecialty Collections This article, along with others on similar topics, appears in the
following collection(s):
All Clinical Neurology
http://n.neurology.org//cgi/collection/all_clinical_neurology
All Rehabilitation
http://n.neurology.org//cgi/collection/all_rehabilitation
Gait disorders/ataxia
http://n.neurology.org//cgi/collection/gait_disorders_ataxia
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