- Email: [email protected]
Therapeutic Effect of Virtual Reality on Post-Stroke Patients: Randomized Clinical Trial
ARTICLE IN PRESS
Therapeutic Effect of Virtual Reality on Post-Stroke Patients: Randomized Clinical Trial Erika Pedreira da Fonseca, PT, MSc,*† Nildo Manoel Ribeiro da Silva, and Elen Beatriz Pinto, PT, PhD†
PT, PhD,‡
Objectives: The study aimed to check the therapeutic effect of virtual reality associated with conventional physiotherapy on gait balance and the occurrence of falls after a stroke. Methods: This was a randomized, blinded clinical trial conducted with post-stroke patients, randomized into two groups—treatment group and control group—and subjected to balance assessments by the Dynamic Gait Index and investigation of falls before and after 20 intervention sessions. Statistically significant difference was considered at P < .05. Results: We selected 30 patients, but there were three segment losses, resulting in a total of 13 patients in the control group and 14 in the treatment group. There was an improvement in gait balance and reduced occurrence of falls in both groups. After intervention, the differences in gait balance in the control group (P = .047) and the reduction in the occurrence of falls in the treatment group (P = .049) were significant. However, in intergroup analysis, there was no difference in the two outcomes. Conclusions: Therapy with games was a useful tool for gait balance rehabilitation in post-stroke patients, with repercussions on the reduction of falls. Key Words: Stroke— balance—virtual reality—rehabilitation. © 2016 National Stroke Association. Published by Elsevier Inc. All rights reserved.
Introduction Stroke affects millions of people worldwide annually.1,2 Despite the decline in mortality of the disease in Brazil,3 the affected survivors may present with disabilities.4 The main consequence of stroke is hemiplegia or hemiparesis,5 which can result in sensory-motor deficit, and consequently change in balance, functional limitation, and risk of falls.5-10 Authors report that these falls frequently occurred more in a home environment and during gait.11 Most of these patients recover the ability to walk, but in many cases there is change in postural control.12-14 Balance From the *Católica University of Salvador, Salvador, Bahia, Brazil; †Bahia School of Medicine and Public Health, Salvador, Brazil; and ‡Federal University of Bahia, Salvador, Brazil. Received May 25, 2016; revision received August 15, 2016; accepted August 23, 2016. Address correspondence to Erika Pedreira da Fonseca, PT, MSc, Católica University of Salvador, Pinto de Aguiar av, n. 2589, Pituaçu, 41740-090, Salvador, Bahia, Brazil. E-mail: [email protected]. 1052-3057/$ - see front matter © 2016 National Stroke Association. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2016.08.035
is a functional motor skill6 that may be compromised in the hemiparetic patient, because of visual, vestibular sensory, somatosensory information, or motor changes.12-14 In some cases, strategies to maintain postural control are not effective enough, leading to falls.15 Various authors have reported that after a stroke, 25%-75% of patients have a history of falls, and 10% of those who fall suffer severe consequences,15,16 with 73% of these patients requiring hospitalization as a result of the fall.17 A tool used for assessment is the Dynamic Gait Index (DGI), which evaluates gait balance and is a predictor of falls.9 Rehabilitation of the body balance of post-stroke patients is indispensable9,18 to avoid episodes of falls—the main complications after a stroke.18 Among the different approaches for this purpose is virtual reality,19 which aims to simulate functional activities that are the basis for rehabilitation of neurologic patients.19-23 Several authors have observed improvement of body balance after a stroke in patients who underwent rehabilitation with virtual reality. These studies showed the feasibility of virtual reality as a therapeutic resource, although the studies were conducted with a small sample.7,8,20,23-27 Virtual reality has been reported as an adjunctive tool in the rehabilitation of
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post-stroke patients, as it is capable of generating more motivation and entertainment.21,23,27 However, balance during gait and the occurrence of falls have not been evaluated simultaneously in this population. The therapeutic effect of virtual reality on balance during gait may have an impact on reducing the occurrence of falls and their consequences. Thus, the aim of this study was to investigate the therapeutic effect of virtual reality associated with conventional physiotherapy on balance during gait and the occurrence of falls in poststroke patients.
Methods A clinical randomized trial was conducted, including patients of both sexes, with hemiparesis after a stroke, in the age group from 18 to 65 years. We excluded patients whose injury occurred fewer than 6 months previously, considering the expected time for spontaneous recovery; patients with associated disorders such as epilepsy, and sensory and perceptual deficits such as hemineglect and Pusher syndrome; patients with osteodegenerative disorders that would prevent participation in the games or that could influence the body balance; and individuals who had cognitive and communication disorders, affecting understanding, that could compromise performance in the games. In accordance with the CONSORT requirements, the patients included were randomized in blocks of ten, per lot by the RANDOM.ORG program, carried out by a third person to preserve allocation concealment, into two groups: treatment group with conventional physiotherapy associated with virtual rehabilitation with Nintendo Wii (Nintendo Company, Limited (NCL), Minami-ku-based, Kyoto, Japan) and control group with conventional physiotherapy. After selection and randomization, patients were evaluated at baseline, when demographic and clinical data were collected; the occurrence of falls was investigated in the 3 months prior to evaluation; and the gait balance was rated using the DGI.9 Patients were followed up throughout 20 physiotherapy sessions, in twice-weekly visits lasting an hour each. The exercises were performed under the direct and personal supervision of a previously trained physiotherapist. Balance assessments and investigation of the occurrence of falls were repeated at the end of treatment, which occurred on average 3 months after the interventions began, by the same examiner, who remained blind to the group to which the patient belonged. The group that underwent rehabilitation with Nintendo Wii was treated in a room with an area of 20 m2, equipped with the aforementioned apparatus and projector. The image was projected on the wall at a height of 1 m, and 20 patients had a large environment, free from external noise, in which to perform the activity. To follow up with virtual reality, a protocol was conducted, consisting of trunk mobilizations in the lateral, anterior, and posterior directions,
and stretching the arms and legs with a duration of 60 seconds, for a total time of 15 minutes, followed by 45 minutes of exercise with Nintendo Wii. The games used in the first session were tennis, which stimulates the lateralization of movements of the trunk; weight shift between the heel and forefoot; and hula hoop, working rotational movements of the trunk, weight transfer between the heel and forefoot, rotational movements of hip, and balance reaction time. The games were performed for 12 minutes each, with a 1-minute interval between the two games. In the second session, the following were used: soccer, with sideways, anterior, and posterior movements of the trunk, head movements, and balance reactions; and boxing, involving selective and rotational movements of the trunk and balance reactions, both with the same performance time. Conventional therapy consisted of stretching the arm and leg muscles for a total time of 10 minutes; trunk mobilization activities in the lateral, anterior, and posterior directions for 10 minutes; active or active assisted movement of the leg with the use of movements in diagonal for 15 minutes; balance training in standing position, when weight transfer activities were done, and balance reactions to a stable and unstable surface for 10 minutes; and free gait training for 10 minutes, with emphasis on weight transfer phase balance, average speed, and workout with obstacles. The present study was approved by the Research Ethics Committee in Report No. CAAE 19135213.2.0000.0046, and it was mandatory for patients to sign the Term of Free and Informed Consent in order to participate in the study, in accordance with Resolution 196/96. The study was registered on www.clinicaltrials.gov (NCT02475083). The database was created in Excel (Microsoft, Redmond, Washington, EUA) and analyzed in R v.3.1.3 software. A descriptive analysis was made (absolute frequency or relative, average, standard deviation, median, and quartiles) to identify the general and specific characteristics of the study sample. To check the normality of distribution, the Shapiro–Wilk test was used; and to check for the significant differences before and after the intervention, we used the t test for paired samples or the nonparametric Wilcoxon test. To test for differences between each group, the Student’s t test or the nonparametric Mann–Whitney test was used when variables were quantitative, or the chisquare test when they were qualitative. To identify correlations among variables of interest, the Spearman correlation was used. The level of significance established for this study was 5%. According to the study of DGI, validation identified that the boundary between deficit and normal balance was only 1 point9; thus, it is possible to consider that the score that defines the achievement of balance during gait is restricted. We chose to expand this difference to see the effects of the outcome in clinical practice. The sample size calculation was made in order to detect a difference of 5.5 points in the DGI to identify change of balance during gait, using a standard deviation of 5.1 for the experimental group
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Randomized selection of individuals (N = 30) Losses (N = 3)
Individuals who underwent treatment (N = 27)
Figure 1. Flowchart of study participants, according to CONSORT.
20 sessions
and 4.8 for the control group, and we would have an alpha error of 5% and a power of 80%.
Results We selected 30 patients for the study and the flowchart of the study participants is presented, in accordance with the CONSORT requirements (Fig 1). Analysis of the sociodemographic and clinical characteristics is presented in Table 1. There was no statistically significant difference between groups as regards these characteristics, thus confirming homogeneity between them. Figure 2 demonstrates that there was an increase in the DGI score in both groups, with initial values of the DGI for the treatment and control groups at 13.54 (±5.47)
Control Group (N = 13)
Experimental Group (N = 14)
After-test (N = 13)
After-test (N = 14)
and 16.29 (±5.01), respectively. However, when comparing the DGI values before and after treatment, statistically significant difference was observed only in the control group (P = .047). In both groups, the number of falls was reduced after the intervention, but this difference was statistically significant (P = .049) only in the treatment group (Table 2). In the intergroup analysis, there was no significant difference in balance during gait (P = .462) after rehabilitation or in reducing the incidence of falls (P = .653). This result is shown in Table 3. Table 4 shows that according to the result of total DGI, the gait balance performance in the two groups was not significantly correlated with the number of falls recorded after the intervention (P = .129 and P = .541,
Table 1. Demographic and clinical characteristics of 30 post-stroke patients Variable
Total (N = 30)
Control group (n = 15)
Treatment group (n = 15)
P value
Age in years (average/SD)* Female gender, n (%)† Right side of body affected, n (%)† Time from stroke in months (average/SD)*
52.4 ± 8.9 19 (63.3) 17 (56.7) 54.3 ± 35.5
50.9 ± 10.9 66.7 60 64.5 ± 41.9
53.8 ± 6.3 60 53.3 44.1 ± 25.0
.375 .705 .713 .117
Abbreviation: SD, standard deviation. *t Test. †Chi-square test.
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Figure 2. Balance gait performance—intergroup. Note: Paired t test was used.
DGI AFTER
DGI BEFORE
Note: Paired T test was used.
respectively). By correlating each DGI domain with the number of falls, the authors of this study observed that for the control group, only the eighth domain—“going up and down the stairs”—showed positive correlation (P = .043).
Table 2. Occurrence of falls—intergroup
Occurrence of falls‡
Before treatment
After treatment
Median/ Quartiles
Median/ Quartiles
P value
1 (0-2)† 0 (0-1)†
1 (0-1)† 0 (0-0)†
.257 .049*
Control group (n = 13) Experimental group (n = 14)
Discussion The results of this study showed that after a stroke, patients undergoing treatment that included virtual reality and patients receiving conventional therapy showed an improvement in balance during gait and a reduction in the occurrence of falls. The differences in gait balance after intervention in the control group and the reduction in the occurrence of falls in the treatment group were significant. However, the intergroup analysis showed no difference between the two outcomes. Some authors suggest that the rehabilitation of balance should involve the task performed, the particularities of the individual, and the environment in which the
Table 4. Correlation between the scores of Dynamic Gait Index (DGI) domains and number of falls
*Significant difference. †Quartiles 25-75. ‡Wilcoxon test.
Table 3. Gait balance performance and occurrence of falls—intergroup
▲DGI* ▲Number of falls†
Control group
Treatment group
P value
−2.84 (4.63) 1 (0-1)
−1.71 (3.14) 0 (0-0)
.462 .653
Note: ▲DGI represented in average/SD and ▲number of falls represented in median/quartiles 25-75. *Non–paired t test. †Mann–Whitney test.
Item 1 DGI Item 2 DGI Item 3 DGI Item 4 DGI Item 5 DGI Item 6 DGI Item 7 DGI Item 8 DGI DGI total
Control group
Experimental group
Number of falls
Number of falls
r
P value
r
P value
.306 .262 .364 .364 .328 .411 .048 .567 .444
.309 .338 .222 .222 .274 .163 .887 .043* .129
.122 −.081 −.028 −.030 −.413 −.302 −.287 −.190 −.179
.679 .782 .434 .920 .142 .295 .319 .515 .541
Spearman nonparametric test. *Significant difference.
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rehabilitation is being carried out. Balance training with virtual reality provides patients with enriched environments and the ability to solve motor problems.23 Different studies corroborate that therapy with virtual reality associated with conventional therapy can improve the performance of balance in post-stroke patients.7,8,13,20,22,23 In this study, the improvement in balance during gait in both groups can be explained by the fact that all patients performed task-oriented trainings. Moreover, virtual reality (VR) therapy is capable of motivating patients to a larger extent and thereby stimulating new motor and sensory abilities responsible for maintaining balance.9,24 A clinical trial that evaluated the motivational aspects found that the group that underwent treatment with VR was more motivated than the control group.28 A recent systematic review drew attention to the need to include the outcome of motivation after training with VR in the study.29 The VR can be an important tool in sensorimotor training of individuals after a stroke, as the visual feedback provided by this training can modulate a neural network in the motor, premotor, and parietal cortex. This suggests that sensory information can promote cortical reorganization.30,31 Some authors have indicated that this visual feedback imposed by VR may generate an immediate self-correction in the patient, thereby facilitating the activation of neuronal plasticity,32,33 which increases its clinical applicability.34 Other authors have suggested that a higher number of repetitions and a longer treatment time facilitate neuroplasticity,35 and the association of task-oriented training with a suitable treatment time may influence the rehabilitation.36,37 The use of VR favors longer sessions and greater variability of tasks,38 capable of facilitating this cortical reorganization. The duration of treatment with VR, presented in a recent review that included different studies, ranged from 2 to 22 hours,36 similar to the treatment time of 20 hours used in the present study for both groups. In post-stroke patients, reduced gait velocity and risk of falls are known to occur.39 Although there is no evidence that the stimuli generated by the virtual and real environments have equivalence in neural activation,40 the scenes of varying capacity and movement trajectories provided by VR can stimulate gait training.34 This was verified in studies that observed an increase in gait speed41 and reduced time of implementing the 10-m walk test42 after gait training with VR. However, a systematic review considered that VR was a safe tool for rehabilitation but was not a substitute for conventional physical therapy.43 There was no difference in improvement of balance during gait and the occurrence of falls between the groups in this study. The authors of this study recognize that the selection of games may have influenced this result. The two protocols had similar goals: the activities carried out in the conventional therapy were directed to balance
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training on a static basis, and the balance in gait and the games used in VR therapy gave priority to balance training on a static base. This reaffirms the importance of planning the intervention protocols and pairing goals more specifically, advocated in a previous clinical trial that also did not observe significant differences between the groups.7 In disagreement with these findings, the authors observed that the experimental group had boosted control of balance after the intervention.8 This difference in findings may be due to changes in the approach to balance outcome. In the present study, we evaluated the balance during gait by DGI,9 and in different clinical trials the performance of balance evaluated was not specifically in walking and different assessment tools were used.7,8,15,17,26,44 Authors who used the DGI to assess the outcome of balance after intervention with VR in post-stroke patients corroborated the results of the present study.27,45 Post-stroke patients can evolve with limitations of balance skills and gait, with consequent increase in the occurrences of falls.27,39 In the present study, investigation of the occurrence of falls after 3 months found a reduction in this occurrence in both groups, but it was significant only in the group that underwent therapy with Nintendo Wii. This investigation period was similar to that used by other authors.27,39 This finding corroborates those of a study including patients with different neurologic disorders, which found the reduction in falls was achieved after training based on VR games.41 Various authors have reported that training with VR resulted in improved balance and auto safety balance, reported by post-stroke patients,27,31 which may reflect on performing daily activities.46,47 The results of a clinical trial showed that treatment with VR was effective in improving the balance and functional independence of individuals after a subacute stroke.42 Despite the risk of falls identified in the study population, with an average DGI value ≤19, there was no correlation between the result of the DGI and the number of falls. Only in the domain—going up and down the stairs—was DGI correlated with decreases in the control group. This can be justified by the fact that after a stroke individuals became more unstable in the medial-lateral displacement of the center of gravity,45 which may hinder the task. In contrast, the variation of sensory environments provided by the training with VR27,46 can improve patient safety in carrying out activities that require greater control of postural stability, such as going up and down the stairs. The advantage of this study was the fact that it expanded the investigation of the effects of VR gamesbased therapy on gait balance rehabilitation and the occurrence of falls in post-stroke patients. As limitation, there is the fact that the games are not specifically marketed for the purpose of rehabilitation, which could limit physiotherapists in adapting them to specific objectives of the visits. In addition, the small sample size and the treatment time may have had a negative influence on
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obtaining some inferences and could not provide information on the severity of stroke in regard to motor weakness, and involvement of sensory and visual impairment, and their impact upon balance.
13. 14.
Conclusions The rehabilitation of gait balance in post-stroke patients using virtual reality had repercussions on the reduction of falls. Considering the functional and motivational aspects involved in performing the therapy with games, this was shown to be a useful tool to achieve these goals. We suggest conducting further clinical trials with the use of virtual reality games specifically for rehabilitation purposes. Acknowledgments: The authors would like to thank Daniel Dominguez, Igor Matos, Marília Lira, and Marcelo Masruha for their help in the acquisition of data.
References 1. Health Ministry of Brazil. Acidente vascular cerebral (AVC). Available at: http://www.brasil.gov.br/saude/ 2012/04/acidente-vascular-cerebral-avc. Accessed March 8, 2015. 2. World Health Organization. Stroke, cerebrovascular accident. Available at: http://www.who.int/topics/ cerebrovascular_accident/en/. Accessed March 08, 2015. 3. de Carvalho JJF, Alves MB, Viana GÁ, et al. Stroke epidemiology, patterns of management, and outcomes in Fortaleza, Brazil: a hospital-based multicenter prospective study. Stroke 2011;42:3341-3346. 4. Wen H, Dou Z, Cheng S, et al. Activity of thing muscles during static and dynamics stances in stroke patients: a pilot case-control study. Top Stroke Rehabil 2014;21:163175. 5. Geurts ACH, Haart M, Nes IJW, et al. A review of standing balance recovery from stroke. Gait Posture 2005;65:267-281. 6. Horak FB, Henry SM, Shumway-Cook A. Postural perturbations: new insights for treatment of balance disorders. Phys Ther 1997;77:517-533. 7. Barcala L, Grecco LAC, Colella F, et al. Visual biofeedback balance training using Wii Fit after stroke: a randomized controlled trial. J Phys Ther Sci 2013;25:1027-1032. 8. Kim JH, Jang SH, Kim CS, et al. Use of virtual reality to enhance balance and ambulation in chronic stroke: a double-blind, randomized controlled study. Am J Phys Med Rehabil 2009;88:693-701. 9. Jonsdottir J, Cattaneo D. Reliability and validity of the Dynamic Gait Index in persons with chronic stroke. Arch Phys Med Rehabil 2007;88:1410-1415. 10. Belgen B, Beninato M, Sullivan PE, et al. The association of balance capacity and falls self-efficacy with history of falling in community-dwelling people with chronic stroke. Arch Phys Med Rehabil 2006;87:554-561. 11. Pinto EB, Nascimento C, Marinho C, et al. Risk factors associated with falls in adults patients after stroke living in the community: baseline data from a stroke cohort in Brazil. Top Stroke Rehabil 2014;21:220-227. 12. Liu-Ambrose T, Pang MYC, Eng JJ. Executive function is independently associated with performances of balance
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and mobility in community-dwelling older adults after mild stroke: implications for falls prevention. Cerebrovasc Dis 2007;23:203-210. Tyson SF, Hanley M, Chillala J, et al. Balance disability after stroke. Phys Ther 2006;86:30-38. de Haart M, Geurts AC, Huidekoper SC, et al. Recovery of standing balance in postacute stroke patients: a rehabilitation cohort study. Arch Phys Med Rehabil 2004;85:886-895. Cho K, Lee G. Impaired dynamic balance is associated with falling in post-stroke patients. Tohoku J Exp Med 2013;230:233-239. Campbell GB, Matthews JT. An integrative review of factors associated with falls during post-stroke rehabilitation. J Nurs Scholarsh 2010;42:395-404. Rajaratnam BS, Gui Kaien J, Lee Jialin K, et al. Does the inclusion of the virtual reality games within conventional rehabilitation enhance balance retraining after a recent episode of stroke? Rehabil Res Pract 2013;2013:1-6. Weerdesteyn V, de Niet M, van Duijnhoven HJ, et al. Falls in individuals with stroke. J Rehabil Res Dev 2008;45:1195-1213. Laver KE, George S, Thomas S, et al. Virtual reality for stroke rehabilitation. Cochrane Database Syst Rev 2015;(9):CD008349. Cikajlo I, Rudolf M, Goljar N, et al. Telerehabilitation using virtual reality task can improve balance in patients with stroke. Disabil Rehabil 2012;1:13-18. Baumeister J, Kirsten R, Cordes M, et al. Brain activity in goal-directed movements in a real compared to a virtual environment using the Nintendo Wii. Neurosci Lett 2010;481:47-50. Crosbie JH, Lennon S, Basford JR, et al. Virtual reality in stroke rehabilitation: still more virtual than real. Disabil Rehabil 2007;29:1139-1146. Flynn S, Palma P, Bender A. Feasibility of using the Sony PlayStation 2 gaming platform for an individual poststroke: a case report. J Neurol Phys Ther 2007;4:180189. Cho KH, Lee KJ, Song CH. Virtual-reality balance training with a video-game system improves dynamic balance in chronic patients. Tohoku J Exp Med 2012;228:6974. Gómez JAG, Lloréns R, Alcaniz M, et al. Effectiveness of a Wii balance board-based system (eBaViR) for balance rehabilitation: a pilot randomized clinical trial in patients with acquired brain injury. J Neuroeng Rehabil 2011; 8:30. Barcala L, Colella F, Araujo MC, et al. Análise do equilíbrio em pacientes hemiparéticos após treino com o programa Wii Fit. Fisiot Mov 2011;24:337-343. Fritz SL, Peters DM, Merlo AM, et al. Active videogaming effects on balance and mobility in individuals with chronic stroke: a randomized controlled trial. Top Stroke Rehabil 2013;20:218-225. Hung JW, Chou CX, Hsieh YW, et al. Randomized comparison trial of balance training by using exergaming and conventional weight-shift therapy in patients with chronic stroke. Arch Phys Med Rehabil 2014;95:16291637. Li Z, Han XG, Sheng J, et al. Virtual reality for improving balance in patients after stroke: a systematic review and meta-analysis. Clin Rehabil 2015;9:432-440. Graziano MS, Gross CG. Visual responses with and without fixation: neurons in premotor cortex encode spatial locations independently of eye position. Exp Brain Res 1998;118:373-380.
ARTICLE IN PRESS VIRTUAL REALITY ON POST-STROKE PATIENTS 31. Kakei S, Hoffman DS, Strick PL. Sensorimotor transformations in cortical motor areas. Neurosci Res 2003;46:1-10. 32. Bray S, Shimojo S, O’Doherty JP. Direct instrumental conditioning of neural activity using functional magnetic resonance imaging-derived reward feedback. J Neurosci 2007;27:7498-7507. 33. Wise SP, Moody SL, Blomstrom KL, et al. Changes in motor cortical activity during visuomotor adaptation. Exp Brain Res 1998;121:285-299. 34. Adamovich SV, Fluet GG, Tunik E, et al. Sensorimotor training in virtual reality: a review. Neurorehabilitation 2009;25:29-49. 35. Kitago T, Krakauer JW. Motor learning principles for neurorehabilitation. Handb Clin Neurol 2013;110:93-103. 36. Darekar A, McFadyen BJ, Lamontagne A, et al. Efficacy of virtual reality-based intervention on balance and mobility disorders post-stroke: a scoping review. J Neuroengineering Rehabil 2015;12:46. 37. Fluet GG, Deutsch JJ. Virtual reality for sensorimotor rehabilitation post-stroke: the promise and current state of the field. Curr Phys Med Rehabil Rep 2013;1:9-20. 38. Holden MK. Virtual environments for motor rehabilitation: review. Cyber Psychol Behav 2005;3:187-211. 39. Kao PC, Dingwell JB, Higginson JS, et al. Dynamic instability during post-stroke hemiparetic walking. Gait Posture 2014;40:457-463.
7 40. Perani D, Fazio F, Borghese NA, et al. Different brain correlates for watching real and virtual hand actions. Neuroimage 2001;14:749-758. 41. Lamontagne A, Fung J, McFadyen BJ, et al. Modulation of walking speed by changing optic flow in persons with stroke. J Neuroeng Rehabil 2007;4:22. 42. Morone G, Tramontano M, Iosa M, et al. The efficacy of balance training with video game-based therapy in subacute stroke patients: a randomized controlled trial. Biomed Res Int 2014;2014:580861. 43. Dos Santos LRA, Carregosa AA, Masruha MR, et al. The use of Nintendo Wii in the rehabilitation of poststroke patients: a systematic review. J Stroke Cerebrovasc Dis 2015;24:2298-2305. 44. Singh DKA, Nordin NAM, Aziz NAA, et al. Effects of substituting a portion of standard physiotherapy time with virtual reality games among community-dwelling stroke survivors. BMC Neurol 2013;13:199. 45. Betker AL, Szturm T, Moussavi ZK, et al. Video gamebased exercises for balance rehabilitation: a single-subject design. Arch Phys Med Rehabil 2006;87:1141-1149. 46. Jung J, Yu J, Kang H. Effects of virtual reality treadmill training on balance self-efficacy in stroke patients with a history of falling. J Phys Ther Sci 2012;24:1133-1136. 47. Cho K, Lee G. Impaired dynamic balance is associated with falling in post-stroke patients. Tohoku J Exp Med 2013;230:233-239.
Therapeutic Effect of Virtual Reality on Post-Stroke Patients: Randomized Clinical Trial Erika Pedreira da Fonseca, PT, MSc,*† Nildo Manoel Ribeiro da Silva, and Elen Beatriz Pinto, PT, PhD†
PT, PhD,‡
Objectives: The study aimed to check the therapeutic effect of virtual reality associated with conventional physiotherapy on gait balance and the occurrence of falls after a stroke. Methods: This was a randomized, blinded clinical trial conducted with post-stroke patients, randomized into two groups—treatment group and control group—and subjected to balance assessments by the Dynamic Gait Index and investigation of falls before and after 20 intervention sessions. Statistically significant difference was considered at P < .05. Results: We selected 30 patients, but there were three segment losses, resulting in a total of 13 patients in the control group and 14 in the treatment group. There was an improvement in gait balance and reduced occurrence of falls in both groups. After intervention, the differences in gait balance in the control group (P = .047) and the reduction in the occurrence of falls in the treatment group (P = .049) were significant. However, in intergroup analysis, there was no difference in the two outcomes. Conclusions: Therapy with games was a useful tool for gait balance rehabilitation in post-stroke patients, with repercussions on the reduction of falls. Key Words: Stroke— balance—virtual reality—rehabilitation. © 2016 National Stroke Association. Published by Elsevier Inc. All rights reserved.
Introduction Stroke affects millions of people worldwide annually.1,2 Despite the decline in mortality of the disease in Brazil,3 the affected survivors may present with disabilities.4 The main consequence of stroke is hemiplegia or hemiparesis,5 which can result in sensory-motor deficit, and consequently change in balance, functional limitation, and risk of falls.5-10 Authors report that these falls frequently occurred more in a home environment and during gait.11 Most of these patients recover the ability to walk, but in many cases there is change in postural control.12-14 Balance From the *Católica University of Salvador, Salvador, Bahia, Brazil; †Bahia School of Medicine and Public Health, Salvador, Brazil; and ‡Federal University of Bahia, Salvador, Brazil. Received May 25, 2016; revision received August 15, 2016; accepted August 23, 2016. Address correspondence to Erika Pedreira da Fonseca, PT, MSc, Católica University of Salvador, Pinto de Aguiar av, n. 2589, Pituaçu, 41740-090, Salvador, Bahia, Brazil. E-mail: [email protected]. 1052-3057/$ - see front matter © 2016 National Stroke Association. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2016.08.035
is a functional motor skill6 that may be compromised in the hemiparetic patient, because of visual, vestibular sensory, somatosensory information, or motor changes.12-14 In some cases, strategies to maintain postural control are not effective enough, leading to falls.15 Various authors have reported that after a stroke, 25%-75% of patients have a history of falls, and 10% of those who fall suffer severe consequences,15,16 with 73% of these patients requiring hospitalization as a result of the fall.17 A tool used for assessment is the Dynamic Gait Index (DGI), which evaluates gait balance and is a predictor of falls.9 Rehabilitation of the body balance of post-stroke patients is indispensable9,18 to avoid episodes of falls—the main complications after a stroke.18 Among the different approaches for this purpose is virtual reality,19 which aims to simulate functional activities that are the basis for rehabilitation of neurologic patients.19-23 Several authors have observed improvement of body balance after a stroke in patients who underwent rehabilitation with virtual reality. These studies showed the feasibility of virtual reality as a therapeutic resource, although the studies were conducted with a small sample.7,8,20,23-27 Virtual reality has been reported as an adjunctive tool in the rehabilitation of
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post-stroke patients, as it is capable of generating more motivation and entertainment.21,23,27 However, balance during gait and the occurrence of falls have not been evaluated simultaneously in this population. The therapeutic effect of virtual reality on balance during gait may have an impact on reducing the occurrence of falls and their consequences. Thus, the aim of this study was to investigate the therapeutic effect of virtual reality associated with conventional physiotherapy on balance during gait and the occurrence of falls in poststroke patients.
Methods A clinical randomized trial was conducted, including patients of both sexes, with hemiparesis after a stroke, in the age group from 18 to 65 years. We excluded patients whose injury occurred fewer than 6 months previously, considering the expected time for spontaneous recovery; patients with associated disorders such as epilepsy, and sensory and perceptual deficits such as hemineglect and Pusher syndrome; patients with osteodegenerative disorders that would prevent participation in the games or that could influence the body balance; and individuals who had cognitive and communication disorders, affecting understanding, that could compromise performance in the games. In accordance with the CONSORT requirements, the patients included were randomized in blocks of ten, per lot by the RANDOM.ORG program, carried out by a third person to preserve allocation concealment, into two groups: treatment group with conventional physiotherapy associated with virtual rehabilitation with Nintendo Wii (Nintendo Company, Limited (NCL), Minami-ku-based, Kyoto, Japan) and control group with conventional physiotherapy. After selection and randomization, patients were evaluated at baseline, when demographic and clinical data were collected; the occurrence of falls was investigated in the 3 months prior to evaluation; and the gait balance was rated using the DGI.9 Patients were followed up throughout 20 physiotherapy sessions, in twice-weekly visits lasting an hour each. The exercises were performed under the direct and personal supervision of a previously trained physiotherapist. Balance assessments and investigation of the occurrence of falls were repeated at the end of treatment, which occurred on average 3 months after the interventions began, by the same examiner, who remained blind to the group to which the patient belonged. The group that underwent rehabilitation with Nintendo Wii was treated in a room with an area of 20 m2, equipped with the aforementioned apparatus and projector. The image was projected on the wall at a height of 1 m, and 20 patients had a large environment, free from external noise, in which to perform the activity. To follow up with virtual reality, a protocol was conducted, consisting of trunk mobilizations in the lateral, anterior, and posterior directions,
and stretching the arms and legs with a duration of 60 seconds, for a total time of 15 minutes, followed by 45 minutes of exercise with Nintendo Wii. The games used in the first session were tennis, which stimulates the lateralization of movements of the trunk; weight shift between the heel and forefoot; and hula hoop, working rotational movements of the trunk, weight transfer between the heel and forefoot, rotational movements of hip, and balance reaction time. The games were performed for 12 minutes each, with a 1-minute interval between the two games. In the second session, the following were used: soccer, with sideways, anterior, and posterior movements of the trunk, head movements, and balance reactions; and boxing, involving selective and rotational movements of the trunk and balance reactions, both with the same performance time. Conventional therapy consisted of stretching the arm and leg muscles for a total time of 10 minutes; trunk mobilization activities in the lateral, anterior, and posterior directions for 10 minutes; active or active assisted movement of the leg with the use of movements in diagonal for 15 minutes; balance training in standing position, when weight transfer activities were done, and balance reactions to a stable and unstable surface for 10 minutes; and free gait training for 10 minutes, with emphasis on weight transfer phase balance, average speed, and workout with obstacles. The present study was approved by the Research Ethics Committee in Report No. CAAE 19135213.2.0000.0046, and it was mandatory for patients to sign the Term of Free and Informed Consent in order to participate in the study, in accordance with Resolution 196/96. The study was registered on www.clinicaltrials.gov (NCT02475083). The database was created in Excel (Microsoft, Redmond, Washington, EUA) and analyzed in R v.3.1.3 software. A descriptive analysis was made (absolute frequency or relative, average, standard deviation, median, and quartiles) to identify the general and specific characteristics of the study sample. To check the normality of distribution, the Shapiro–Wilk test was used; and to check for the significant differences before and after the intervention, we used the t test for paired samples or the nonparametric Wilcoxon test. To test for differences between each group, the Student’s t test or the nonparametric Mann–Whitney test was used when variables were quantitative, or the chisquare test when they were qualitative. To identify correlations among variables of interest, the Spearman correlation was used. The level of significance established for this study was 5%. According to the study of DGI, validation identified that the boundary between deficit and normal balance was only 1 point9; thus, it is possible to consider that the score that defines the achievement of balance during gait is restricted. We chose to expand this difference to see the effects of the outcome in clinical practice. The sample size calculation was made in order to detect a difference of 5.5 points in the DGI to identify change of balance during gait, using a standard deviation of 5.1 for the experimental group
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Randomized selection of individuals (N = 30) Losses (N = 3)
Individuals who underwent treatment (N = 27)
Figure 1. Flowchart of study participants, according to CONSORT.
20 sessions
and 4.8 for the control group, and we would have an alpha error of 5% and a power of 80%.
Results We selected 30 patients for the study and the flowchart of the study participants is presented, in accordance with the CONSORT requirements (Fig 1). Analysis of the sociodemographic and clinical characteristics is presented in Table 1. There was no statistically significant difference between groups as regards these characteristics, thus confirming homogeneity between them. Figure 2 demonstrates that there was an increase in the DGI score in both groups, with initial values of the DGI for the treatment and control groups at 13.54 (±5.47)
Control Group (N = 13)
Experimental Group (N = 14)
After-test (N = 13)
After-test (N = 14)
and 16.29 (±5.01), respectively. However, when comparing the DGI values before and after treatment, statistically significant difference was observed only in the control group (P = .047). In both groups, the number of falls was reduced after the intervention, but this difference was statistically significant (P = .049) only in the treatment group (Table 2). In the intergroup analysis, there was no significant difference in balance during gait (P = .462) after rehabilitation or in reducing the incidence of falls (P = .653). This result is shown in Table 3. Table 4 shows that according to the result of total DGI, the gait balance performance in the two groups was not significantly correlated with the number of falls recorded after the intervention (P = .129 and P = .541,
Table 1. Demographic and clinical characteristics of 30 post-stroke patients Variable
Total (N = 30)
Control group (n = 15)
Treatment group (n = 15)
P value
Age in years (average/SD)* Female gender, n (%)† Right side of body affected, n (%)† Time from stroke in months (average/SD)*
52.4 ± 8.9 19 (63.3) 17 (56.7) 54.3 ± 35.5
50.9 ± 10.9 66.7 60 64.5 ± 41.9
53.8 ± 6.3 60 53.3 44.1 ± 25.0
.375 .705 .713 .117
Abbreviation: SD, standard deviation. *t Test. †Chi-square test.
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Figure 2. Balance gait performance—intergroup. Note: Paired t test was used.
DGI AFTER
DGI BEFORE
Note: Paired T test was used.
respectively). By correlating each DGI domain with the number of falls, the authors of this study observed that for the control group, only the eighth domain—“going up and down the stairs”—showed positive correlation (P = .043).
Table 2. Occurrence of falls—intergroup
Occurrence of falls‡
Before treatment
After treatment
Median/ Quartiles
Median/ Quartiles
P value
1 (0-2)† 0 (0-1)†
1 (0-1)† 0 (0-0)†
.257 .049*
Control group (n = 13) Experimental group (n = 14)
Discussion The results of this study showed that after a stroke, patients undergoing treatment that included virtual reality and patients receiving conventional therapy showed an improvement in balance during gait and a reduction in the occurrence of falls. The differences in gait balance after intervention in the control group and the reduction in the occurrence of falls in the treatment group were significant. However, the intergroup analysis showed no difference between the two outcomes. Some authors suggest that the rehabilitation of balance should involve the task performed, the particularities of the individual, and the environment in which the
Table 4. Correlation between the scores of Dynamic Gait Index (DGI) domains and number of falls
*Significant difference. †Quartiles 25-75. ‡Wilcoxon test.
Table 3. Gait balance performance and occurrence of falls—intergroup
▲DGI* ▲Number of falls†
Control group
Treatment group
P value
−2.84 (4.63) 1 (0-1)
−1.71 (3.14) 0 (0-0)
.462 .653
Note: ▲DGI represented in average/SD and ▲number of falls represented in median/quartiles 25-75. *Non–paired t test. †Mann–Whitney test.
Item 1 DGI Item 2 DGI Item 3 DGI Item 4 DGI Item 5 DGI Item 6 DGI Item 7 DGI Item 8 DGI DGI total
Control group
Experimental group
Number of falls
Number of falls
r
P value
r
P value
.306 .262 .364 .364 .328 .411 .048 .567 .444
.309 .338 .222 .222 .274 .163 .887 .043* .129
.122 −.081 −.028 −.030 −.413 −.302 −.287 −.190 −.179
.679 .782 .434 .920 .142 .295 .319 .515 .541
Spearman nonparametric test. *Significant difference.
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rehabilitation is being carried out. Balance training with virtual reality provides patients with enriched environments and the ability to solve motor problems.23 Different studies corroborate that therapy with virtual reality associated with conventional therapy can improve the performance of balance in post-stroke patients.7,8,13,20,22,23 In this study, the improvement in balance during gait in both groups can be explained by the fact that all patients performed task-oriented trainings. Moreover, virtual reality (VR) therapy is capable of motivating patients to a larger extent and thereby stimulating new motor and sensory abilities responsible for maintaining balance.9,24 A clinical trial that evaluated the motivational aspects found that the group that underwent treatment with VR was more motivated than the control group.28 A recent systematic review drew attention to the need to include the outcome of motivation after training with VR in the study.29 The VR can be an important tool in sensorimotor training of individuals after a stroke, as the visual feedback provided by this training can modulate a neural network in the motor, premotor, and parietal cortex. This suggests that sensory information can promote cortical reorganization.30,31 Some authors have indicated that this visual feedback imposed by VR may generate an immediate self-correction in the patient, thereby facilitating the activation of neuronal plasticity,32,33 which increases its clinical applicability.34 Other authors have suggested that a higher number of repetitions and a longer treatment time facilitate neuroplasticity,35 and the association of task-oriented training with a suitable treatment time may influence the rehabilitation.36,37 The use of VR favors longer sessions and greater variability of tasks,38 capable of facilitating this cortical reorganization. The duration of treatment with VR, presented in a recent review that included different studies, ranged from 2 to 22 hours,36 similar to the treatment time of 20 hours used in the present study for both groups. In post-stroke patients, reduced gait velocity and risk of falls are known to occur.39 Although there is no evidence that the stimuli generated by the virtual and real environments have equivalence in neural activation,40 the scenes of varying capacity and movement trajectories provided by VR can stimulate gait training.34 This was verified in studies that observed an increase in gait speed41 and reduced time of implementing the 10-m walk test42 after gait training with VR. However, a systematic review considered that VR was a safe tool for rehabilitation but was not a substitute for conventional physical therapy.43 There was no difference in improvement of balance during gait and the occurrence of falls between the groups in this study. The authors of this study recognize that the selection of games may have influenced this result. The two protocols had similar goals: the activities carried out in the conventional therapy were directed to balance
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training on a static basis, and the balance in gait and the games used in VR therapy gave priority to balance training on a static base. This reaffirms the importance of planning the intervention protocols and pairing goals more specifically, advocated in a previous clinical trial that also did not observe significant differences between the groups.7 In disagreement with these findings, the authors observed that the experimental group had boosted control of balance after the intervention.8 This difference in findings may be due to changes in the approach to balance outcome. In the present study, we evaluated the balance during gait by DGI,9 and in different clinical trials the performance of balance evaluated was not specifically in walking and different assessment tools were used.7,8,15,17,26,44 Authors who used the DGI to assess the outcome of balance after intervention with VR in post-stroke patients corroborated the results of the present study.27,45 Post-stroke patients can evolve with limitations of balance skills and gait, with consequent increase in the occurrences of falls.27,39 In the present study, investigation of the occurrence of falls after 3 months found a reduction in this occurrence in both groups, but it was significant only in the group that underwent therapy with Nintendo Wii. This investigation period was similar to that used by other authors.27,39 This finding corroborates those of a study including patients with different neurologic disorders, which found the reduction in falls was achieved after training based on VR games.41 Various authors have reported that training with VR resulted in improved balance and auto safety balance, reported by post-stroke patients,27,31 which may reflect on performing daily activities.46,47 The results of a clinical trial showed that treatment with VR was effective in improving the balance and functional independence of individuals after a subacute stroke.42 Despite the risk of falls identified in the study population, with an average DGI value ≤19, there was no correlation between the result of the DGI and the number of falls. Only in the domain—going up and down the stairs—was DGI correlated with decreases in the control group. This can be justified by the fact that after a stroke individuals became more unstable in the medial-lateral displacement of the center of gravity,45 which may hinder the task. In contrast, the variation of sensory environments provided by the training with VR27,46 can improve patient safety in carrying out activities that require greater control of postural stability, such as going up and down the stairs. The advantage of this study was the fact that it expanded the investigation of the effects of VR gamesbased therapy on gait balance rehabilitation and the occurrence of falls in post-stroke patients. As limitation, there is the fact that the games are not specifically marketed for the purpose of rehabilitation, which could limit physiotherapists in adapting them to specific objectives of the visits. In addition, the small sample size and the treatment time may have had a negative influence on
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obtaining some inferences and could not provide information on the severity of stroke in regard to motor weakness, and involvement of sensory and visual impairment, and their impact upon balance.
13. 14.
Conclusions The rehabilitation of gait balance in post-stroke patients using virtual reality had repercussions on the reduction of falls. Considering the functional and motivational aspects involved in performing the therapy with games, this was shown to be a useful tool to achieve these goals. We suggest conducting further clinical trials with the use of virtual reality games specifically for rehabilitation purposes. Acknowledgments: The authors would like to thank Daniel Dominguez, Igor Matos, Marília Lira, and Marcelo Masruha for their help in the acquisition of data.
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