Is virtual reality beneficial for dual-task gait training in patients with Parkinson's disease? A systematic review

Freitag, Fernanda; Brucki, Sonia Maria Dozzi; Barbosa, Alessandra Ferreira; Chen, Janini; Souza, Carolina de Oliveira; Valente, Débora Francato; Chien, Hsin Fen; Bedeschi, Cynthia; Voos, Mariana Callil

doi:10.1590/1980-57642018dn13-030002

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Original Article • Dement. neuropsychol. 13 (3) • Jul-Sep 2019 • https://doi.org/10.1590/1980-57642018dn13-030002 linkcopy

Is virtual reality beneficial for dual-task gait training in patients with Parkinson's disease? A systematic review

A REALIDADE VIRTUAL É BENÉFICA PARA O TREINO DE MARCHA COM TAREFA DUPLA EM PACIENTES COM DOENÇA DE PARKINSON? REVISÃO SISTEMÁTICA

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

This systematic review examined the evidence about the effects of virtual reality (VR) on dual-task gait training in Parkinson's disease (PD).

Methods: this study (PROSPERO registration CRD42019114736) aimed to answer the question: “Is VR beneficial for dual-task gait training in patients with PD?” We searched for studies from 2008 to 2018 on Medline/PubMed and Web of Science/Web of knowledge databases. The keywords were Parkinson AND gait training AND virtual reality OR Parkinson AND gait training AND game. A total of 55 articles were retrieved, of which 11 systematic reviews, 11 opinions, letters to the editor, posters or conferences abstracts and 17 studies not evaluating the effects of VR gait training were excluded. Three further studies addressing VR dual-task gait training in PD (found in references of studies selected) were also included. Therefore, 19 studies were included and analysed.

Results: all studies reported gait improvement after VR training. Many clinical scales were used, hampering comparison of the effects of each protocol.

Conclusion: VR dual-task gait training should be part of rehabilitation protocols for PD. The studies showed that VR training was effective, although specific guidelines have not yet been established.

Key words: Parkinson's disease; gait; cognition; virtual reality; videogames

Authors	Participants	Method	Main findings
Espay et al., 2010¹⁸ At-home training with closed-loop augmented reality cueing device for improving gait in patients with PD.	• 13 PD patients • Age: 73.3±11.7 yrs • PD duration: 12.1±4.2 yrs • H&Y: not available	The efficacy of an accelerometer-driven, wearable, visual-auditory cueing device at baseline and after 2 weeks of twice daily (30 min) at-home use was examined. Gait velocity, stride length, and cadence were measured using a validated electronic gait-analysis system. FOG-Q was used for clinical assessment.	After training, patients improved velocity and stride length with the device. The effects were maintained even after the device was removed. Devices with closed-loop sensory feedback appear to be effective and desirable interventions to improve gait in PD patients. An overall improvement in gait was detected by the FOG-Q.
Mirelman et al., 2011a¹⁹ VR for gait training: can it induce motor learning to enhance complex walking and reduce fall risk in patients with PD?	• 20 PD patients • Age: 67.1±6.5 yrs • PD duration: 9.8±5.6 yrs • H&Y: 2-3	Eighteen sessions (three per week) of progressive intensive treadmill training with virtual obstacles. Outcome measures included gait with single and dual-tasks and while negotiating obstacles. Functional performance was assessed by UPDRS-III, four square step test, PDQ-39, MoCA and TMT.	Gait speed improved during single-tasks and while negotiating obstacles. Dual-task gait variability, TMT times (parts A and B), scores on UPDRS-III and four square step test performance improved). Functional gains were also observed one month later (retention effects). Quality of life increased after training.
Esculier et al., 2012²⁰ Home-Based balance training program using Wii Fit^TM with balance board for PD: A pilot study.	• 9 healthy subjects (age: 63.5±12.0 yrs) • 11 PD patients (age: 61.9±11.0 yrs, PD duration: 8.5±3.6).	Approximately 40 min, 3 days/week for 6 weeks (18 total training sessions) with pre-determined number of repetitions of game trials. Each training day included 30 min with the Wii Fit^TM using the balance board and 10 min with the Wii Sports^TM game (golf or bowling).	Balance, global mobility and functional abilities improved in PD patients (measured by UPDRS, Activities-specific Balance and Confidence Scale, TUG, Sit-to-Stand Test, Performance-Oriented Mobility Assessment, Community Balance and Mobility scale, 10MWT. Healthy subjects also improved, but to a lesser extent.
Mhatre et al., 2013²¹ Wii Fit balance board playing improves balance and gait in PD.	• 10 subjects with PD (4 men) • Age: 67.1 yrs (44-91 yrs), SD was not informed. • PD duration: 6.7 yrs (1-14 yrs), SD was not informed. • H&Y: 2.5-3.	Nintendo Wii Fit^TM and balance board system effects on balance and gait were evaluated with BBS, DGI and Romberg. Training occurred 3 times a week for 8 weeks for 30 min. Wii balance board^TM measured postural sway. Balance confidence was rated by the Activities-specific Balance Confidence scale and depression by GDS.	The Wii Fit^TM balance board training improved balance and gait. No significant changes were seen in mood or confidence. BBS increased significantly. DGI improved, as did postural sway (decreased 31% variance in stance with eyes open), but these differences were non-significant. Romberg with eyes closed increased significantly.
Pompeu et al., 2014²² Feasibility, safety and outcomes of playing Kinect Adventures! for people with Parkinson's disease: a pilot study.	• 7 PD patients (6 males) • Age: 72.0±9.0 yrs • PD duration: not informed • H&Y 2-3.	Kinect Adventures! training consisted of fourteen 60-min sessions, 3 times a week. Feasibility and safety outcomes included game performance and adverse events. Clinical outcomes were 6MWT, Balance Evaluation System Test, DGI and PDQ-39.	The scores of all games, 6MWT, Balance Evaluation System Test, DGI and PDQ-39 improved. Kinect-based training was safe and feasible. Kinect Adventures! improved balance, gait, cardiopulmonary aptitude and quality of life.
Esculier et al., 2014²³ Corticomotor excitability in PD during observation, imagery and imitation of action: effects of rehabilitation using Wii Fit and comparison to healthy controls.	• Eight subjects with moderate PD (age: 63.5±12 yrs, PD duration: 8.5±3,6 yrs) and eight controls (age: 61.9±12 yrs).	This study compared lower limb corticomotor activation during action observation, motor imagery, and imitation, and evaluated the effects of a 6-week training program using Wii Fit^TM on corticomotor excitability. Transcranial magnetic stimulation assessed motor evoked potentials in quadriceps femoris and soleus muscles after six weeks of training using Wii Fit^TM (mini-squat).	PD group showed less evoked potentials in quadriceps in observation, motor imagery and imitation compared to controls (baseline). In soleus, evoked potentials were reduced in PD group in imitation. PD group increased quadriceps evoked potentials in observation, in contrast to controls, after training. Both groups reduced motor evoked potentials in quadriceps and soleus in imitation. PD group improved on TUG and Sit-to-Stand.
Killane, et al., 2015²⁴ Dual motor-cognitive VR training impacts dual-task performance in freezing of gait.	• FOGPD (n=13): 64.2±2.4 yrs; H&Y: 2.6±0.1; • Non-FOGPD (n=7): 64.0±1.6 yrs; H&Y: 2.3±0.1; • PD duration: not available	A VR dual-task intervention combined motor and cognitive tasks to improve dual-task performance. Patients were assessed with MoCA, FAB, UPDRS III and FOG.	Dual-task performance improved post-intervention in patients with FOG, who also showed a decrease in the number of FOG episodes.
Liao et al., 2015²⁵ VR-based Wii fit training in improving muscle strength, sensory integration ability and walking abilities in patients with PD.	• 36 PD patients (H&Y 1-3) • Control 64.6±8.6 yrs; PD duration: 6.4±3.0 yrs • Traditional exercise: 65.1±6.7 yrs, PD duration: 6.9±2.8 yrs; • VR-based Wii Fit^TM exercise: 67.3±7.1 yrs; PD duration: 7.9±2.7 yrs	The effects of VR-based training in improving muscle strength, sensory integration ability, and walking abilities in PD patients after training and after 1-month follow-up were evaluated in this study. UPDRS, MMSE, GAITRite, Functional Gait Assessment, Body Mass Index were used for assessment.	Wii fit^TM improved stride length and velocity compared with the controls after training and at follow-up. No differences between Wii fit^TM and traditional exercises were found (both groups improved velocity and sensory integration compared to controls after training and at follow-up). VR-based Wii fit^TM exercise and traditional exercises improved gait, sensory integration, and muscle strength.
Liao et al., 2015²⁶ VR-based training to improve obstacle-crossing performance and dynamic balance in patients with PD.	• 36 PD patients (H&Y 1-3). • Control 64.6±8.6 yrs; PD duration: 6.4±3.0 yrs • Traditional exercise: 65.1±6.7 yrs, PD duration: 6.9±2.8 yrs; • VR-based Wii Fit^TM exercise: 67.3±7.1 yrs; PD duration: 7.9±2.7 yrs	The effects of virtual reality-based exercise on obstacle crossing performance and dynamic balance were evaluated in PD patients. PDQ-39, FES-I and TUG were used for assessment.	The VR Wii^TM group showed greater improvement in obstacle crossing velocity, crossing stride length, dynamic balance, sensory organization test, TUG, FES-I, and PDQ-39 than the control group. VR Wii^TM training also resulted in greater improvement in movement velocity of limits-of-stability test than traditional exercises.
Palacios-Navarro et al., 2015²⁷ A Kinect-based system for lower limb rehabilitation in PD: a pilot study.	• Seven PD patients • Age: 66.8±3.5 yrs • PD duration: not available • H&Y: not available.	The effects of VR-based exercise on obstacle crossing performance and dynamic balance were evaluated in PD patients by the MMSE and the 10MWT.	Patients improved on the 10 MWT. Feedback from participants supports the use of VR not only in rehabilitation centers but also at home.
Ginis et al., 2016²⁸ Feasibility and effects of home-based smartphone-delivered automated feedback training for gait in people with PD: a pilot randomized controlled trial.	• Smartphone application group (CuPiD-systems, n=22): 67.3±8.1 yrs. PD duration: 10.6±5.3 yrs. H&Y: 2-3. • Control group (n=18): 66.1±8.0 yrs. PD duration: 11.6±7.6 yrs. H&Y: 2-3. Distribution was randomized.	The smartphone provided feedback on gait performance. Feasibility and effectiveness were investigated in home environment. Gait training lasted for 30 min, 3 times a week, for 6 weeks. Gait, balance, endurance and quality of life were assessed with MiniBESTest and SF-36 after training and at 1 month-follow-up.	Both groups improved in single- and dual-task gait speed at post-test and follow-up. The smartphone group improved significantly more on balance at post-test and maintained quality of life at follow-up. whereas the control group deteriorated. The smartphone system was well-tolerated, and participants found the tool user-friendly.
Yang et al., 2016²⁹ Home-based virtual reality balance training and conventional balance training in PD: a randomized controlled trial.	• VR (n=11): 72.5±8.4 yrs, PD duration: 9.4±3.6 yrs, H&Y: 3. • Control (n=12): 75.4±6.3 yrs, PD duration: 8.3±4.1 yrs, H&Y: 3.	The effects of VR balance training were evaluated in patients with PD to investigate whether VR balance training would be superior to conventional balance training. Patients were evaluated with BBS, DGI, TUG, PDQ-39, UPDRS III.	No differences between VR training and conventional training were found.
Strouwen et al., 2017³⁰ Training dual tasks together or apart in PD: results from the duality trial.	• 121 PD patients • group 1: age: 66.1±9.3 yrs; PD duration: 8.9±6.3 • group 2: age: 65.8±9.2; PD duration: 8.4±5.3 • H&Y: 2-3 • Distribution was randomized	Two training programs (six weeks) were compared: consecutive (gait and cognitive tasks trained separately) and integrated (gait and cognitive tasks trained simultaneously). Two baseline tests were performed as a six-week control period before training (MoCA and FAB). Post-tests were performed after training and at 12-week follow-up. Falls risk was determined by weekly calls for 24 weeks.	Both protocols had similar effects on dual-task gait. Improvements in dual-task gait velocity were found and were retained at 12-week follow-up. No significant change in fall risk occurred in either group.
Gandolfi et al., 2017³¹ VR telerehabilitation for postural instability in PD: a multicenter, single-blind, randomized, controlled trial.	• 76 PD patients • Nintendo Wii Fit^TM (n=36): 67.5±7.2 yrs, PD duration: 6.2±3.8 yrs, H&Y: 2.5. • sensory integration balance training (n=34): 69.8±9.4 yrs, PD duration: 7.5±3.9 yrs, H&Y: 2.5-3.0.	Postural stability after in home VR-based balance training with the Nintendo Wii Fit^TM and after in-clinic sensory integration balance training were compared. Balance confidence, mobility-related function, quality of life, falls, UPDRS, GDS and the costs of the rehabilitation programs were evaluated.	BBS scores improvement was significant after 7 weeks (completion of training programs) and at follow-up evaluation. Both groups showed improvement on the 10MWT, DGI, and PDQ-39. Nintendo Wii Fit^TM holds promise and potential to enrich rehabilitation care at home in patients with PD.
Ferraz et al., 2018³² The effects of functional training, bicycle exercise, and exergaming on walking capacity of elderly patients with PD: a pilot randomized controlled single-blinded trial.	• Group 1 (n=22, 16 men): 71.0 ±5.0 yrs, H&Y: 2.5-3.0. PD duration: 4.0±3.0 yrs • Group 2 (n=20, 11 men): 67.0 ±4.0 yrs, H&Y:2.0-3.0. PD duration: 6.0±4.0 yrs • Group 3 (n=20,10 men): 67.0 ±4.0 yrs, H&Y: 2.0-2.5. PD duration: 4.0±3.0 yrs	This study compared the effects of 3 treatment modalities (functional training, bicycle exercise, and exergaming) on gait of PD patients. Patients were evaluated with UPDRS, MMSE, 6MWT, 10MWT, PDQ-39, body mass index, world health organization disability assessment schedule, sitting-rising test and GDS.	All groups showed significant improvements on 6MWT and SRT. Group 3 improved gait speed on 10MWT. Groups 1 and 3 improved quality of life. Functional training, bicycle exercise, and Kinect Adventures exergames were safe and improved the walking capacity of patients with PD.
Dantas et al., 2018³³ Training healthy persons and individuals with PD to use Xbox Kinect games: a preliminary study.	• 19 adults (8 with PD and 11 healthy adults). • PD Group: 65.6±11.8 yrs. H&Y: 1-3, PD duration: not mentioned • Healthy Adults Group: 70.0±7.7 yrs	This study investigated the effects of motor and cognitive demands of six Kinect for Xbox 360^TM games (Target Kick, Stack 'em Up, Wall Breaker, Super Saver, Paddle Panic and Bump Bash) on the learning of PD patients, compared to healthy individuals. MMSE were used in the assessment.	Both groups improved their performances in terms of the scores obtained in each session compared to the first session on Target Kick, Stack 'em Up, Wall Breaker and Super Saver. Motor and cognitive abilities improved with the use of VR. Some of the games and devices can influence the learning process, even in healthy adults.
Melo et al., 2018³⁴ Effect of virtual reality training on walking distance and physical fitness in individuals with PD.	• 37 PD patients. • Control group (n=12): 65.6±13.0 yrs, H&Y: 2.08±0.9 • Treadmill group (n=13): 61.0±10.7 yrs, H&Y: 1.53±0.66 • VR group (n=12): 60.3±9.3 yrs, H&Y1.41±0.51 • PD duration: not mentioned	This study evaluated the effects of VR gait training on walking distance and physical fitness. The control group was submitted to conventional training, the treadmill group was submitted to gait training on a treadmill and the VR group was submitted to gait training using the Xbox^TM. Patients were evaluated with 6MWT, UPDRS III and PDQ-39.	Heart rate increased during the intervention in VR and treadmill groups. HR variation was more intense in VR group after the ﬁrst training session and after training. Gains were not maintained at 30 days after training. Treadmill training was more effective at maintaining physical ﬁtness than VR activities. VR was as effective as treadmill training for improving walking distance and temporal gait variables.
Alves et al., 2018³⁵ Nintendo Wii versus Xbox Kinect for assisting people with PD.	• 27 patients (25 men): 61±10.7 yrs. • Nintendo Wii^TM group (n=9): 58.9±11.2 yrs, H&Y: 1.9± 0.9. • Xbox Kinect group (n=9): 62.7±13.8 yrs, H&Y: 1.6± 0.7. • Control group (n=9): 61.7±10.7 yrs, H&Y: 1.8± 0.8.	This study compared the effects of 10 VR sessions with Nintendo Wii^TM and Xbox Kinect on motor and cognitive performance, anxiety levels, and perceived quality of life changes in patients with PD. Patients were evaluated with MMSE, GDS, WHOQOL-OLD, Beck Anxiety Inventory, VFT, Digit Span (forward and backward), TUG, 10MWT, 30-Second Walk Test.	Improvements in gait performance after Nintendo Wii^TM training were evident on the 30-Second Walk Test on both single and dual tasks (increase in distance covered and decrease in number of steps taken). Anxiety scores and Digit Span Backward scores decreased after Nintendo Wii^TM training. The Xbox Kinect^TM did not facilitate these improvements. Greater benefits were observed in the simpler and less distracting interface of the Nintendo Wii^TM.
Song et al., 2018³⁶ Home-based step training using videogame technology in people with Parkinson's disease: a single-blinded randomised controlled trial.	• Intervention group: n=31, 68.0±7.0, PD duration: 7±4 yrs and control group: n=29, 65.0±7.0, PD duration: 9±6 yrs	This study aimed to determine whether 12-week home-based exergame step training could improve stepping performance, gait and neuropsychological measures associated with falls in PD. Choice stepping reaction time test, Functional Gait Assessment and neuropsychological functions, number of falls over six months and self-reported mobility and balance were evaluated.	Post-intervention, there were no differences between the intervention and control groups except for the TUG (the difference favoured the control group). Intervention participants reported mobility improvement, whereas control participants reported mobility deterioration. Interaction effects between intervention and disease severity on physical function measures were observed with seemingly positive effects for the low-severity group and potentially negative effects for the high-severity group.

Authors	1	2	3	4	5	6	7	8	9	10	11	Total
Espay et al., 2010¹⁸	Yes	Yes	No	Yes	No	No	No	Yes	Yes	Yes	Yes	7
Mirelman et al., 2011¹⁹	Yes	No	No	No	No	No	No	Yes	Yes	No	Yes	4
Esculier et al., 2012²⁰	Yes	No	No	No	No	No	No	Yes	Yes	No	Yes	4
Mhatre et al., 2013²¹	Yes	Yes	No	Yes	No	No	No	Yes	Yes	Yes	Yes	7
Esculier et al., 2014²²	Yes	No	No	Yes	No	No	No	Yes	Yes	No	Yes	5
Pompeu et al., 2014²³	Yes	No	No	Yes	Yes	Yes	Yes	Yes	Yes	No	Yes	8
Killane, et al., 2015²⁴	Yes	No	No	Yes	No	No	No	Yes	Yes	Yes	Yes	6
Liao et al., 2015^a²⁵	Yes	Yes	Yes	Yes	No	Yes	Yes	Yes	Yes	Yes	Yes	10
Liao et al., 2015^b²⁶	Yes	Yes	Yes	Yes	No	Yes	Yes	Yes	Yes	Yes	Yes	10
Palacios-Navarro et al., 2015²⁷	Yes	No	No	Yes	No	No	No	Yes	Yes	No	Yes	5
Ginis et al., 2016²⁸	Yes	Yes	No	Yes	Yes	No	No	Yes	Yes	Yes	Yes	8
Strouwen et al., 2017²⁹	Yes	No	Yes	Yes	Yes	Yes	Yes	No	Yes	Yes	Yes	9
Yang et al., 2016³⁰	Yes	Yes	Yes	Yes	No	No	No	Yes	Yes	Yes	Yes	8
Gandolfi et al, 2017³¹	Yes	Yes	No	Yes	No	Yes	Yes	Yes	Yes	Yes	Yes	9
Ferraz et al., 2018³²	Yes	Yes	Yes	Yes	Yes	No	No	Yes	Yes	Yes	Yes	9
Dantas et al., 2018³³	Yes	No	No	No	No	No	No	Yes	Yes	Yes	Yes	5
Melo et al., 2018³⁴	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	11
Alves et al., 2018³⁵	Yes	Yes	Yes	Yes	No	No	No	Yes	Yes	Yes	Yes	8
Song et al., 2018³⁶	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	11

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Academia Brasileira de Neurologia, Departamento de Neurologia Cognitiva e Envelhecimento R. Vergueiro, 1353 sl.1404 - Ed. Top Towers Offices, Torre Norte, São Paulo, SP, Brazil, CEP 04101-000, Tel.: +55 11 5084-9463 | +55 11 5083-3876 - São Paulo - SP - Brazil
E-mail: revistadementia@abneuro.org.br | demneuropsy@uol.com.br

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[TFN1] BBS: Berg Balance Scale; DGI: Dynamic Gait Index; FAB: Frontal Assessment Battery; FES-I: Fall Efficacy Scale; FOG-Q: Freezing of gait questionnaire; GAITRite: Assessment of level of walking performance; GDS: Geriatric Depression Scale; H&Y: Hoehn & Yahr Staging Scale; MiniBESTest: Mini Balance Evaluation Systems Test; MMSE: Mini-Mental State Examination; min: minutes; MoCA: Montreal Cognitive Assessment; PD: Parkinson's disease; PDQ-39: Parkinson's Disease Questionnaire-39; SD: standard deviation; SRT: serial reaction time; SF-36: Short Form Health Survey; TMT: Trail-Making Test; TUG: Timed Get Up and Go Test; UPDRS-III: Unified Parkinson's Disease Rating Scale - Part III; VFT: Verbal Fluency Test; VR: virtual reality; WAIS-III: Wechsler Adult Intelligence Scale; WHOQOL-OLD: World Health Organization Quality of Life for Older Persons; yrs: years; 6MWT: Six-Minute Walk Test; 10 MWT: Ten-Meter Walk Test.