The Clinical Utility of Virtual Reality in Neurorehabilitation: A Systematic Review

Background: Virtual reality (VR) experiences (through games and virtual environments) are increasingly being used in physical, cognitive, and psychological interventions. However, the impact of VR as an approach to rehabilitation is not fully understood, and its advantages over traditional rehabilitation techniques are yet to be established. Method: We present a systematic review which was conducted according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA). During February and March of 2018, we conducted searches on PubMed (Medline), Virtual Health Library Search Portal databases (BVS), Web of Science (WOS), and Embase for all VR-related publications in the past 4 years (2015, 2016, 2017, and 2018). The keywords used in the search were “neurorehabilitation” AND “Virtual Reality” AND “devices.” Results: We summarize the literature which highlights that a range of effective VR approaches are available. Studies identified were conducted with poststroke patients, patients with cerebral palsy, spinal cord injuries, and other pathologies. Healthy populations have been used in the development and testing of VR approaches meant to be used in the future by people with neurological disorders. A range of benefits were associated with VR interventions, including improvement in motor functions, greater community participation, and improved psychological and cognitive function. Conclusions: The results from this review provide support for the use of VR as part of a neurorehabilitation program in maximizing recovery.

[1]  Bruce H. Dobkin,et al.  A Rehabilitation-Internet-of-Things in the Home to Augment Motor Skills and Exercise Training , 2017, Neurorehabilitation and neural repair.

[2]  F. Fusco,et al.  Leap motion controlled videogame-based therapy for rehabilitation of elderly patients with subacute stroke: a feasibility pilot study , 2015, Topics in stroke rehabilitation.

[3]  L. Lucca.  Virtual reality and motor rehabilitation of the upper limb after stroke: a generation of progress? , 2009, Journal of rehabilitation medicine.

[4]  Young-Hyun Park,et al.  The effects of semi-immersive virtual reality therapy on standing balance and upright mobility function in individuals with chronic incomplete spinal cord injury: A preliminary study , 2018, The journal of spinal cord medicine.

[5]  Donatella Mattia,et al.  The 3Ts of the new millennium neurorehabilitation gym: therapy, technology, translationality , 2016, Expert review of medical devices.

[6]  Chi-Ying Lin,et al.  Development of a novel haptic glove for improving finger dexterity in poststroke rehabilitation. , 2015, Technology and health care : official journal of the European Society for Engineering and Medicine.

[7]  Peter Wolf,et al.  Cognitive and cognitive-motor interventions affecting physical functioning: A systematic review , 2011, BMC geriatrics.

[8]  Robert Riener,et al.  ChARMin: The First Actuated Exoskeleton Robot for Pediatric Arm Rehabilitation , 2016, IEEE/ASME Transactions on Mechatronics.

[9]  Andrea Cereatti,et al.  Effects of a virtual reality and treadmill training on gait of subjects with multiple sclerosis: a pilot study. , 2016, Multiple sclerosis and related disorders.

[10]  G. Burdea,et al.  Integrative rehabilitation of residents chronic post-stroke in skilled nursing facilities: the design and evaluation of the BrightArm Duo , 2016, Disability and rehabilitation. Assistive technology.

[11]  Márk Ágoston Pulay.  Eye-tracking and EMG supported 3D Virtual Reality - an integrated tool for perceptual and motor development of children with severe physical disabilities: a research concept , 2015, AAATE Conf..

[12]  Carlos B. M. Monteiro,et al.  Motor intervention in children with school learning difficulties , 2013 .

[13]  G. Oriolo,et al.  Non-invasive brain–computer interface system: Towards its application as assistive technology , 2008, Brain Research Bulletin.

[14]  Trieu Phat Luu,et al.  Gait adaptation to visual kinematic perturbations using a real-time closed-loop brain–computer interface to a virtual reality avatar , 2016, Journal of neural engineering.

[15]  Francisco J. Badesa,et al.  A Comparative Analysis of 2D and 3D Tasks for Virtual Reality Therapies Based on Robotic-Assisted Neurorehabilitation for Post-stroke Patients , 2016, Front. Aging Neurosci..

[16]  Gaetano Tieri,et al.  Virtual reality in cognitive and motor rehabilitation: facts, fiction and fallacies , 2018, Expert review of medical devices.

[17]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. , 2010, International journal of surgery.

[18]  N. A. Borghese,et al.  Autonomous rehabilitation at stroke patients home for balance and gait: safety, usability and compliance of a virtual reality system. , 2018, European journal of physical and rehabilitation medicine.

[19]  Katherine Isbister,et al.  Player-video game interaction: A systematic review of current concepts , 2015, Comput. Hum. Behav..

[20]  Walter Ricciardi,et al.  Evaluation of the Endorsement of the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) Statement on the Quality of Published Systematic Review and Meta-Analyses , 2013, PloS one.

[21]  E. Yanovich,et al.  The Use of Virtual Reality in Motor Learning: A Multiple Pilot Study Review , 2015 .

[22]  Emilia Biffi,et al.  Immersive Virtual Reality to Improve Walking Abilities in Cerebral Palsy: A Pilot Study , 2018, Annals of Biomedical Engineering.

[23]  Giuseppe Riva,et al.  A Psychometric Tool for a Virtual Reality Rehabilitation Approach for Dyslexia , 2017, Comput. Math. Methods Medicine.

[24]  Silvia Regina Pinheiro Malheiros,et al.  Motor learning through virtual reality in cerebral palsy – a literature review , 2014 .

[25]  David Blatner,et al.  Silicon Mirage: The Art and Science of Virtual Reality , 1992 .

[26]  G. Savelsbergh,et al.  Transfer of motor learning from virtual to natural environments in individuals with cerebral palsy. , 2014, Research in developmental disabilities.

[27]  Rafael Rieder,et al.  Motion Rehab AVE 3D: A VR-based exergame for post-stroke rehabilitation , 2017, Comput. Methods Programs Biomed..

[28]  Patrice L Tamar Weiss,et al.  Improving physical fitness of individuals with intellectual and developmental disability through a Virtual Reality Intervention Program. , 2009, Research in developmental disabilities.

[29]  Kristian Thorlund,et al.  The PRISMA Extension Statement for Reporting of Systematic Reviews Incorporating Network Meta-analyses of Health Care Interventions: Checklist and Explanations , 2015, Annals of Internal Medicine.

[30]  James M. Finley,et al.  Walking in fully immersive virtual environments: an evaluation of potential adverse effects in older adults and individuals with Parkinson’s disease , 2017, Journal of NeuroEngineering and Rehabilitation.

[31]  Mansueto Gomes Neto,et al.  Virtual rehabilitation via Nintendo Wii® and conventional physical therapy effectively treat post-stroke hemiparetic patients , 2015, Topics in stroke rehabilitation.

[32]  M. L. Nicolelis,et al.  Assimilation of virtual legs and perception of floor texture by complete paraplegic patients receiving artificial tactile feedback , 2016, Scientific Reports.

[33]  Corey J. Bohil,et al.  Virtual reality in neuroscience research and therapy , 2011, Nature Reviews Neuroscience.

[34]  Nancy Byl,et al.  Upper limb bilateral symmetric training with robotic assistance and clinical outcomes for stroke: A pilot study , 2016, Int. J. Intell. Comput. Cybern..

[35]  Derek G Kamper,et al.  Training finger individuation with a mechatronic-virtual reality system leads to improved fine motor control post-stroke , 2014, Journal of NeuroEngineering and Rehabilitation.

[36]  Oded Nov,et al.  Can Force Feedback and Science Learning Enhance the Effectiveness of Neuro-Rehabilitation? An Experimental Study on Using a Low-Cost 3D Joystick and a Virtual Visit to a Zoo , 2013, PloS one.

[37]  Hubertus J.A. van Hedel,et al.  Weight-supported training of the upper extremity in children with cerebral palsy: a motor learning study , 2017, Journal of NeuroEngineering and Rehabilitation.

[38]  S. Perrey,et al.  Does a Combination of Virtual Reality, Neuromodulation and Neuroimaging Provide a Comprehensive Platform for Neurorehabilitation? – A Narrative Review of the Literature , 2016, Front. Hum. Neurosci..

[39]  Zahra Moussavi,et al.  Design and Application of a Novel Virtual Reality Navigational Technology (VRNChair) , 2014, Journal of experimental neuroscience.

[40]  R. Calabró,et al.  The role of virtual reality in improving motor performance as revealed by EEG: a randomized clinical trial , 2017, Journal of NeuroEngineering and Rehabilitation.

[41]  T. Campos,et al.  Brain activity during a lower limb functional task in a real and virtual environment: A comparative study. , 2017, NeuroRehabilitation.

[42]  Joseph J. LaViola,et al.  A discussion of cybersickness in virtual environments , 2000, SGCH.

[43]  Rudy McDaniel,et al.  User experience design considerations for healthcare games and applications , 2016, 2016 IEEE International Conference on Serious Games and Applications for Health (SeGAH).

[44]  E. Stokes,et al.  Addition of motivational interventions to exercise and traditional physiotherapy: a review and meta-analysis. , 2015, Physiotherapy.

[45]  Silvia Comani,et al.  A Post-Stroke Rehabilitation System Integrating Robotics, VR and High-Resolution EEG Imaging , 2013, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[46]  Jong-Ling Fuh,et al.  Virtual Reality–Based Training to Improve Obstacle-Crossing Performance and Dynamic Balance in Patients With Parkinson’s Disease , 2015, Neurorehabilitation and neural repair.

[47]  K. Bodin,et al.  RehAtt – scanning training for neglect enhanced by multi-sensory stimulation in Virtual Reality , 2016, Topics in stroke rehabilitation.

[48]  F. Fávero,et al.  Virtual reality in multiple sclerosis - A systematic review. , 2016, Multiple sclerosis and related disorders.

[49]  Olivier Lambercy,et al.  The Virtual Peg Insertion Test as an assessment of upper limb coordination in ARSACS patients: A pilot study , 2014, Journal of the Neurological Sciences.

[50]  S. Viñas-Diz,et al.  Virtual reality for therapeutic purposes in stroke: A systematic review , 2016 .

[51]  F Cincotti,et al.  Video-game based therapy performed by children with cerebral palsy: a cross-over randomized controlled trial and a cross-sectional quantitative measure of physical activity. , 2015, European journal of physical and rehabilitation medicine.

[52]  Jordan W. Smith,et al.  Immersive Virtual Environment Technology to Supplement Environmental Perception, Preference and Behavior Research: A Review with Applications , 2015, International journal of environmental research and public health.

[53]  F. Valero-Cuevas,et al.  The potential of virtual reality and gaming to assist successful aging with disability. , 2010, Physical medicine and rehabilitation clinics of North America.

[54]  S. Adamovich,et al.  Does training with traditionally presented and virtually simulated tasks elicit differing changes in object interaction kinematics in persons with upper extremity hemiparesis? , 2015, Topics in stroke rehabilitation.

[55]  Antonio Frisoli,et al.  Integration of serious games and wearable haptic interfaces for Neuro Rehabilitation of children with movement disorders: A feasibility study , 2017, 2017 International Conference on Rehabilitation Robotics (ICORR).

[56]  E. Noé,et al.  Feasibility of a walking virtual reality system for rehabilitation: objective and subjective parameters , 2016, Journal of NeuroEngineering and Rehabilitation.

[57]  K. Caeyenberghs,et al.  What do randomized controlled trials say about virtual rehabilitation in stroke? A systematic literature review and meta-analysis of upper-limb and cognitive outcomes , 2018, Journal of NeuroEngineering and Rehabilitation.

[58]  M. Morris,et al.  Complementary physical therapies for movement disorders in Parkinson's disease: a systematic review. , 2015, European journal of physical and rehabilitation medicine.

[59]  Sadasivan Puthusserypady,et al.  BCI inside a virtual reality classroom: a potential training tool for attention , 2015 .

[60]  Sara Basso Moro,et al.  A novel semi-immersive virtual reality visuo-motor task activates ventrolateral prefrontal cortex: a functional near-infrared spectroscopy study , 2016, Journal of neural engineering.

[61]  Uttama Lahiri,et al.  A Low-Cost Adaptive Balance Training Platform for Stroke Patients: A Usability Study , 2017, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[62]  P. Verschure,et al.  Neurorehabilitation using the virtual reality based Rehabilitation Gaming System: methodology, design, psychometrics, usability and validation , 2010, Journal of NeuroEngineering and Rehabilitation.

[63]  Fátima L. S. Nunes,et al.  Achievement of Virtual and Real Objects Using a Short-Term Motor Learning Protocol in People with Duchenne Muscular Dystrophy: A Crossover Randomized Controlled Trial. , 2018, Games for health journal.

[64]  Felipe Fregni,et al.  Short-term motor learning through non-immersive virtual reality task in individuals with down syndrome , 2017, BMC Neurology.

[65]  Philip Grewe,et al.  Learning real-life cognitive abilities in a novel 360°-virtual reality supermarket: a neuropsychological study of healthy participants and patients with epilepsy , 2011, Journal of NeuroEngineering and Rehabilitation.

[66]  Hossein Mousavi Hondori,et al.  Choice of Human–Computer Interaction Mode in Stroke Rehabilitation , 2016, Neurorehabilitation and neural repair.

[67]  Athanasios Vourvopoulos,et al.  Motor priming in virtual reality can augment motor-imagery training efficacy in restorative brain-computer interaction: a within-subject analysis , 2016, Journal of NeuroEngineering and Rehabilitation.

[68]  K. Knobloch,et al.  Preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement and publication bias. , 2011, Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery.

[69]  Robert Teasell,et al.  Efficacy and safety of non-immersive virtual reality exercising in stroke rehabilitation (EVREST): a randomised, multicentre, single-blind, controlled trial , 2016, The Lancet Neurology.

[70]  Itshak Melzer,et al.  Parameters and Measures in Assessment of Motor Learning in Neurorehabilitation; A Systematic Review of the Literature , 2017, Front. Hum. Neurosci..

[71]  C. Caltagirone,et al.  The Efficacy of Balance Training with Video Game-Based Therapy in Subacute Stroke Patients: A Randomized Controlled Trial , 2014, BioMed research international.

[72]  Matt C. Howard.  A meta-analysis and systematic literature review of virtual reality rehabilitation programs , 2017, Comput. Hum. Behav..

[73]  Roseli de Deus Lopes,et al.  An augmented reality system for upper-limb post-stroke motor rehabilitation: a feasibility study , 2016, Disability and rehabilitation. Assistive technology.

[74]  Brett M. Kissela,et al.  Early Rehabilitation After Stroke: a Narrative Review , 2017, Current Atherosclerosis Reports.

[75]  L. C. Abreu,et al.  Motor Learning and Virtual Reality in Down Syndrome; a Literature Review , 2015 .

[76]  Roberto Cano de la Cuerda,et al.  A telerehabilitation program by virtual reality-video games improves balance and postural control in multiple sclerosis patients. , 2013, NeuroRehabilitation.

[77]  A. Howard,et al.  Effectiveness of Virtual Reality in Children With Cerebral Palsy: A Systematic Review and Meta‐Analysis of Randomized Controlled Trials , 2018, Physical therapy.

[78]  Zhang Tong,et al.  Virtual Reality in Neurorehabilitation , 2016 .

[79]  Marco Ferrari,et al.  A semi-immersive virtual reality incremental swing balance task activates prefrontal cortex: A functional near-infrared spectroscopy study , 2014, NeuroImage.

[80]  Luciano Vieira de Araújo,et al.  Virtual reality software package for implementing motor learning and rehabilitation experiments , 2017, Virtual Reality.

[81]  Ángel Gil-Agudo,et al.  Upper limb rehabilitation after spinal cord injury: a treatment based on a data glove and an immersive virtual reality environment , 2016, Disability and rehabilitation. Assistive technology.

[82]  M Saadat,et al.  Test–retest reliability of Kinect’s measurements for the evaluation of upper body recovery of stroke patients , 2015, Biomedical engineering online.

[83]  Jörg Krüger,et al.  Movement visualisation in virtual reality rehabilitation of the lower limb: a systematic review , 2016, BioMedical Engineering OnLine.

[84]  Albert A. Rizzo,et al.  Clinical Virtual Reality tools to advance the prevention, assessment, and treatment of PTSD , 2017, European journal of psychotraumatology.