Effect of virtual reality-based balance training in multiple sclerosis Bina Eftekharsadat1, Arash Babaei-Ghazani2, Mehran Mohammadzadeh1, Mahnaz Talebi3, Fariba Eslamian1, Elnaz Azari1 1
Physical Medicine and Rehabilitation Research Center, Tabriz University of Medical Sciences, Iran, Department of Physical Medicine and Rehabilitation, Iran University of Medical Sciences, Iran, 3 Neuroscience Research Center, Tabriz University of Medical Sciences, Iran 2
Objectives: Balance and mobility impairments are common life-altering complications in patients with multiple sclerosis (MS). In this study, we aimed to investigate the efficacy of a short-term virtual reality (VR)-based balance training program on the balance ability of patients with MS. Methods: In this randomized controlled trial, 30 patients with relapsing–remitting or secondary-progressive MS were randomly assigned to an intervention or a control group. The intervention group performed a balance training program [postural stability training program (PST)] using the Biodex Balance System SD. Subjects in both groups were assessed using the manual muscle test (MMT), timed ‘up and go’ (TUG) test, the modified Ashworth scale, the Romberg test, the Berg balance scale (BBS), and the fall risk and postural stability tests, at baseline and after 12 weeks. Results: The TUG, fall risk index (FRi), and overall stability index (OSI) were significantly improved in the intervention group after 24 sessions of balance training. The changes in TUG, Fri, and OSi indices in the intervention group were significantly higher than the control group. Discussion: According to the fall risk and postural stability tests results, the VR-based balance training program could improve the balance ability of the patients with MS. Keywords: Multiple sclerosis, Balance training, Postural stability
Introduction
Different methods of physical therapy and training are introduced. Virtual reality (VR)-based balance training has shown promising results in treatment of different neuromuscular disease.14–17 The number of studies and experimental applications evaluating the beneficiary role of VR training on different neuromuscular disease has increased considerably over the last few years. Virtual reality-based trainings provide the patients with repetitive practice, feedback information, and motivation for endurance practice and could promote visual, auditory, tactile input, and motivation and motor learning.14,15 There are different VR-based balance training programs used for MS.17–23 Here, we investigated the efficacy of a VR-based balance rehabilitation program using Biodex Balance System on the speed and endurance of walking and the balance ability of patients with MS.
Multiple sclerosis (MS) is a chronic progressive autoimmune inflammatory disease of the central nervous system, which causes widespread dysfunction.1,2 Symptoms include sensory, cognitive, and motor impairment.2 Studies have reported a high prevalence of falls and balance or mobility impairments among people with MS.3–5 Balance dysfunction often occurs as a result of demyelination of the vestibular nerve or areas around vestibular nuclei in the brainstem.6 These impairments have a negative impact on personal activities and quality of life.7,8 Physical exercise and therapy are recommended to have considerable improvements in both physical and mental functioning of persons with MS and are becoming more commonly included as part of treatment interventions.9 It is reported that exercises could be beneficiary in improving muscular strength and aerobic capacity, mobility, mood, fatigue, and health-related quality of life.10–13
Methods
Correspondence to: Mahnaz Talebi, Neuroscience Research Center, Tabriz University of Medical Sciences, Golgasht Avenue, Tabriz 5166615556, Iran. email [email protected]
This single-blinded randomized clinical trial was conducted with the approval of Scientific and Ethical Review Boards of Tabriz University of Medical Sciences in 2011–2012. Thirty ambulatory patients
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with relapsing–remitting or secondary-progressive types of MS (most common types of MS in Iran) were selected randomly from among the patients who were referred to the Neurology Clinic of Tabriz University of Medical Sciences and were enrolled in this study after they have signed an informed consent to their participation. The patients were receiving standard treatment for MS. The participants were instructed by sealed envelopes. Patients with a background of diabetes mellitus, myasthenia gravis, myopathies, metabolic or toxic neuropathies, degenerative disorders of the musculoskeletal system, past history of trauma or surgery in the lower extremities, previous cerebrovascular accidents, or major cardiopulmonary disease were excluded from the study. Using a computer generated
table of random numbers, subjects were randomly assigned to an intervention or a control group, each comprising 15 patients. All outcome measures were assessed at approximately the same time of day and in the same order at the beginning of the study and after 12 weeks. No specific change was made to the medications of the subjects during the study period (Fig. 1). The manual muscle test (MMT) was performed to assess the muscle strength of the patients. The MMT evaluates the test movement and the test position of a muscle. It is graded from ‘zero’ (no movement even with therapist’s palpation) to grade ‘5’ (normal). The timed ‘up and go’ test (TUG) was performed to assess the mobility of the subjects. The TUG test assesses the
Randomly selected
Excluded: Did not wish to participate (n = 3) Assessed for eligibility
Excluded (n=7): a) Background of DM (n=4), b) previous history of trauma and surgery (n=3)
Randomized (n=30)
Intervention group (n = 15)
Postural stability training program 2 sessions per week for 12 weeks
Post intervention evaluation Figure 1 Flow diagram of the study protocol.
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mobility function. It records the time required for participant subject to stand up from a standard arm chair, walk 3 m around a cone and sit back down in the chair using their preferred assistive device. The test was repeated three times at a 2-minute intervals and the shortest time was recorded as the result. The reliability of this test in patients with MS is excellent: ICC50.91, 95% CI50.83–0.95.24 Subjects’ muscular tone was assessed using the modified Ashworth scale. The Modified Ashworth scale was developed in 1987 to assess muscle spasticity and tone. It is scored from ‘zero’ (no increase in muscle tone) to ‘4’ (rigidity of affected part(s) in flexion or extension). Balance ability was assessed using the Romberg test and the Berg balance scale (BBS). For the Romberg test, subjects stood with their feet together and their eyes closed. Irregular swaying and/or unsteadiness are recorded as positive in the Romberg test. The BBS assesses static and dynamic balance abilities with excellent test–retest reliability for patients with MS. It consists of 14 items of increasing difficulty, which are scored on a five-point Likert scale (0–4). The maximum possible score is 56, and lower scores indicate more impaired balance.25 In order to increase the diagnostic validity of our evaluation, we assessed all participants with Fall risk and postural stability tests using the Biodex Balance System SD (Biodex 945-302, Biodex Medical Systems Inc., Shirley, NY, USA). The Biodex Balance System is used to measure a subject’s ability to maintain balance while doing functional tasks. The Biodex Balance System assesses the static and dynamic balances by using usual tasks, such as reach, standing position, and transferences. The test includes 14 items that are common in everyday life. Each item of the Biodex Balance System is rated on a five-point scale. For the fall risk test (FRt), subjects were tested on the Biodex Balance System using the FRt protocol in order to evaluate the efficacy of the balance training intervention. In the FRt, the platform is unstable and subjects’ sway is used to calculate the Fall Risk index (FRi). According to the standard software configuration, three trials of 20 seconds each at a stability level of 8 were calculated with 10-second rest between trials. Fluctuations around the zero point, established prior to testing when the platform is stable, are presented as the findings of this test. For the postural stability test, three 20-second trials were conducted with 1 minute intervals between them. The platform is fixed and subjects’ sway is used to calculate the overall stability index (OSI). The BBS software sampled the deviations in the anterior–posterior (AP) and medial–lateral (ML) directions at a rate of 20 Hz and calculated the anterior/posterior index (API), medial/lateral index (MLI), and OSi during a given task. These indices were calculated using the degree of oscillation of the
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platform, in which low values indicated that the individual had good stability. For each mode, the average of three tests was considered as the subject index. All the subjects in the intervention group performed postural stability training (PST) using the Biodex Balance System SD for 20 minutes per session, twice a week for 12 weeks. Postural stability training simulates specific movement patterns or strategies by placing markers on specific locations on the screen grid. This training program is commercially available. In each session, the subjects attempted to touch targets nine times using an on-screen cursor, which is maneuvered by the subjects’ legs on the device’s platform. The platform stability was set to 6 (moderately stable). All the evaluations were repeated after 12 weeks. The subjects in the control group received no intervention, but were re-evaluated after 12 weeks for all of above mentioned outcome measures. The therapist who conducted the training program for the intervention group was not aware of the group composition and the investigators checked the training sessions several times to ensure that the therapist was following the training protocol. The assessor who performed the tests was blinded to the subjects’ grouping. The subjects completed the intervention or control programs as prescribed, and there were no drop-outs during the study. All the participants were re-evaluated at the end of study.
Statistical analysis All the statistical analyses were done using SPSS statistical software version 16.0 (SPSS Inc., Chicago, IL, USA). Values are presented as means + standard deviation. The values were compared between groups using the independent t-test, and before and after the intervention by the paired t-test. Values were recoded based on normal range limits, and the resulting categorical data were compared between groups using the chi-square test, or the Fisher’s exact test if needed. P values v0.05 were considered statistically significant.
Results In this randomized controlled trial, 15 patients with MS were enrolled in each of the intervention and control groups. The characteristics of both groups are shown in Table 1. There were no significant differences between the two groups’ characteristics, including age, sex, BMI, and the duration of disease. Manual muscle test (MMT) scores of the wrist, hip, and knee were not significantly different between the two groups before or after the intervention (Pw0.05). The Ashworth scale scores of the knee and hip were not significantly different between the two groups before or after the intervention either (Pw0.05). Only one subject in the control group was positive in the
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Table 1 Characteristics of the intervention and control groups
Age (years) Sex (M/F) BMI Duration of disease (years) Mobility (TUG)
Total
Intervention group (N515)
Control group (N515)
35?2+ 8?2 8/22 24?4+ 5?5 7?1+ 4?2 –
33?4+ 8?1 5/10 24?2+ 3?9 5?8+ 3?9 8?67+ 2?44
37?0+ 8?3 3/12 24?9+ 6?5 8?3+ 4?3 10?87+ 8?28
M: male; F: female; BMI: body mass index; TUG: timed ‘up and go’ test.
Romberg test at the beginning of the study, and this subject was the only one to be noted positive in the Romberg test after 12weeks as well (P50.5). Tables 2 and 3 demonstrate TUG, BBS, Fri, and OSi before and after the study and their changes during the study period in each group. After the 12-week intervention, the TUG time had declined and improved significantly in the intervention group (P50.003), but it had increased in the control group (Pw0.05). The changes in TUG were significantly better in intervention group compared to control group (P50.01). The BBS score after 12 weeks had declined in both groups, but the decline was not significant (Pw0.05 for both groups). The BBS changes were not significantly different between groups (Pw0.05). There were also significant improvement in FRi and OSi in the intervention group (Pv0.001 and P50.005, respectively), but the change in control group was not significant (Pw0.05). Intervention group also had significantly better FRi and OSi changes during the study period compared to control group (P50.002 and P50.04, respectively).
Discussion In this study, we performed a short-term (12 weeks) balance training program using Biodex Balance
System SD and observed better gait and balancerelated measures in the intervention group showed compared to the control group after. These results showed that VR-based balance training could yield favorable results regarding the balance ability of patients with MS. Our findings are in accordance with the findings of some studies in the literature.21,25 Balance disorders are frequent symptoms in MS patients, which increase risk of falls and restrict patients’ daily living activities.21 Scientific evidence indicates that exercise training and physical activity might have beneficial effects on a number of outcomes including balance, fitness, mood, and quality of life MS.17,23 Patients with mild to moderate MS who are ambulatory and have disability are likely to benefit from an exercise program. Exercise has the potential to increase strength and improve balance and mood in people with MS.26 Few studies have investigated the effect of exercise training on balance and coordination in MS. Some has reported significant clinical improvement and some reported unsupportive results.27 Jackson et al.28 demonstrated that group kickboxing is a feasible exercise activity for patients with MS. Other aerobic or treadmill training programs have been studied for their effect on the walking and balance of patients
Table 2 The comparison of TUG, BBS, Fri, and OSi before and after the study in each group Intervention group
TUG (seconds) BBS FRi OSi
Control group
Beginning
End
95% CI
Beginning
End
95% CI
8?67+ 2?44 51?67+ 3?26 2?36+ 1?30 0?81+ 0?51
8?00+ 2?23* 51?87+ 3?24 0?87+ 0?48* 0?36+ 0?19*
0?26–1?06 {0?42 to 0?02 0?87–2?09 0?15–0?73
10?87+ 8?28 48?53+ 8?99 2?50+ 1?48 0?76+ 0?42
11?07+ 9?30 48?80+ 9?01 2?47+ 1?68 0?68+ 0?43
{0?79 to 0?39 {0?65 to 0?12 {0?62 to 0?67 {0?14 to 0?30
TUG: timed ‘up and go’ test; BBS: Berg balance scale; FRi: fall risk index; OSI: overall stability index. * Statistically significant (Pv0?05). Table 3 Comparison of the changes in TUG, BBS, Fri, and OSi among groups
TUG (seconds) BBS FRi OSi
Intervention group (N515)
Control group (N515)
95% CI
0?66+ 0?72* 0?20+ 0?41 1?48+ 1?10* 0?44+ 0?51*
0?20+ 1?08 0?26+ 0?70 0?02+ 1?16 0?08+ 0?40
0?17–1?50 {0?36 to 0?49 {2?31 to {0?60 {0?71 to {0?01
TUG: timed ‘up and go’ test; BBS: Berg balance scale; FRi: Fall Risk index; OSI: overall stability index. * Statistically significant (Pv0?05).
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with MS.18–20 Ahmadi and colleagues have reported significant changes in the balance of patients with mild to moderate MS following treadmill training.29 Balance training has been shown to improve the different aspects of postural control and prevent fall.30 Virtual reality-based interventions are recommended as an effective alternative to physical therapy in improving balance and gait of patients with different neurological disorders.31,32 It is reported that VR training can activate the cerebral cortex, which will improve the spatial orientation capacity of patients, ability to control balance and increase motion function, gross motor function, and coordination.32,33 In this study, MS patients underwent VR-based training using Biodex Balance System SD, which yielded significant improvement in balance and fall risk. The TUG, Fri, and OSi significantly improved in the intervention group, and their post-intervention changes were significantly different from those of the control group. Similar to our findings, Cattaneo et al. observed considerable reduction in the number of falls and an improvement in clinical tests of static balance (BBS) and dynamic balance (Dynamic Gait Index).21 Giesser et al.34 showed improvements in balance after 40 treadmill training sessions by MS individuals with severely impaired ambulation. Horlings and coworkers35 also reported that VR balance training improved the patient’s reaction time, postural stability, balance, and walking function effectively. However, Eser et al.36 did not find a statistically significant difference between VR therapy and conventional therapy on lower extremity motor recovery, mobility, or activity level among patients with stroke. In our study, there was no difference among the findings of Romberg test between the two groups, both at the beginning and at the end of the intervention. Only one patient in the control group was noted as positive in the Romberg test. There are reports that patients with MS can suffer from balance impairment, even when their Romberg test results are normal.25 This study has some strength and some limitations. In this study, we evaluated subjective methods to assess balance ability of subjects, whereas the majority of previous studies have examined the balance ability of patients with MS using some kind of subjective clinical test or self-report.5,18,22 Tests such as the BBS or Romberg test are based on clinical observations by a clinician, so they may be susceptible to observer error. It is shown that Biodex balance measures are reliable in study of balance disorders and for measuring the risk of falls.37 The objective methods used in this study are not observerdependent diagnostics, and they may even be able to detect minor balance deficits in mildly disabled MS patients.1 So, it seems that observed results in this study
Effect of virtual reality-based balance training
are more indicative of efficacy of balance training in MS patients. The limitations of this study were the short-term (12 weeks) intervention and the lack of home-based balance training programs. The authors suggest further studies on the effect of virtual balance training on patients with MS to confirm the findings of this study with other objective diagnostic tests in different settings. In performing VR-based balance training, there is no need for stabilized posture control, rehabilitation difficulty is reduced, and the safety of the rehabilitation exercise is increased. So, according to our findings it is suggestive that VR-based balance training programs are effective and successful at improving the balance performance of patients with MS according to the results of the fall risk and postural stability tests.
Disclaimer Statements Contributors All authors cooperated in the study design, data collection and final anlysis and report. Funding Physical medicine and rehabilitation researches center, Tabriz University of medical sciences, Iran. Conflicts of interest No conflicts of interest. Ethics approval The study was approved by Scientific and Ethical Review Boards of Tabriz University of Medical Sciences, Tabriz, Iran.
References 1 Corporaal SH, Gensicke H, Kuhle J, Kappos L, Allum JH, ¨ . Balance control in multiple sclerosis: correlations Yaldizli O of trunk sway during stance and gait tests with disease severity. Gait Posture. 2013;37:55–60. 2 Socie MJ, Sosnoff JJ. Gait variability and multiple sclerosis. Mult Scler Int. 2013;2013:645197. 3 Coote S, Hogan N, Franklin S. Falls in people with multiple sclerosis who use a walking aid: prevalence, factors, and effect of strength and balance interventions. Arch Phys Med Rehabil. 2013;94:616–21. 4 Nilsaga˚rd Y, Lundholm C, Denison E, Gunnarsson LG. Predicting accidental falls in people with multiple sclerosis – a longitudinal study. Clin Rehabil. 2009;23:259–69. 5 Sosnoff JJ, Socie MJ, Boes MK, Sandroff BM, Pula JH, Suh Y, et al. Mobility, balance and falls in persons with multiple sclerosis. PLoS ONE. 2011;6:e28021. 6 McConvey J, Bennett SE. Reliability of the dynamic gait index in individuals with multiple sclerosis. Arch Phys Med Rehabil. 2005;86:130–3. 7 Pfaffenberger N, Pfeiffer K-P, Deibl M, Ho¨fer S, Gu¨nther V, Ulmer H. Association of factors influencing health-related quality of life in MS. Acta Neurol Scand. 2006;114:102–8. 8 Mitchell AJ, Benito-Leo´n J, Gonza´lez J-MM, Rivera-Navarro J. Quality of life and its assessment in multiple sclerosis: integrating physical and psychological components of wellbeing. Lancet Neurol. 2005;4:556–66. 9 Dalgas U, Stenager E, Ingemann-Hansen T. Multiple sclerosis and physical exercise: recommendations for the application of resistance-, endurance- and combined training. Mult Scler. 2008;14:35–53. 10 Do¨ring A, Pfueller CF, Paul F, Do¨rr J. Exercise in multiple sclerosis – an integral component of disease management. EPMA J. 2012;3:1–13. 11 Latimer-Cheung AE, Pilutti LA, Hicks AL, Martin Ginis KA, Fenuta AM, MacKibbon KA, et al. Effects of exercise training on fitness, mobility, fatigue, and health-related quality of life among adults with multiple sclerosis: a systematic review to inform guideline development. Arch Phys Med Rehabil. 2013;94:1800–28.e3.
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12 Sa´ MJ. Exercise therapy and multiple sclerosis: a systematic review. J Neurol. 2013;, doi: 10.1007/s00415-013-7183-9 [Epub ahead of print]. 13 Latimer-Cheung AE, Martin Ginis KA, Hicks AL, Motl RW, Pilutti LA, Duggan M, et al. Development of evidenceinformed physical activity guidelines for adults with multiple sclerosis. Arch Phys Med Rehabil. 2013;94:1829–36e7. 14 Lehrer N, Attygalle S, Wolf SL, Rikakis T. Exploring the base for a mixed reality stroke rehabilitation system, part I: a unified approach for representing action, quantitative evaluation, and interactive feedback. J Neuroeng Rehabil. 2011;8:51–65. 15 Laver K, George S, Ratcliffe J, Ratcliffe J, Crotty M. Virtual reality stroke rehabilitation-hype or hope? Aust Occup Ther J. 2011;58:215–9. 16 Adamovich SV, Fluet GG, Tunik E, Merians AS. Sensorimotor training in virtual reality: a review. NeuroRehabilitation. 2009;25(1):29–44. 17 Fulk GD. Locomotor training and virtual reality-based balance training for an individual with multiple sclerosis: a case report. J Neurol Phys Ther. 2005;29:34–42. 18 Kileff J, Ashburn A. A pilot study of the effect of aerobic exercise on people with moderate disability multiple sclerosis. Clin Rehabil. 2005;19:165–9. 19 Newman MA, Dawes H, van den Berg M, Wade DT, Burridge J, Izadi H. Can aerobic treadmill training reduce the effort of walking and fatigue in people with multiple sclerosis: a pilot study. Mult Scler. 2007;13:113–9. 20 van den Berg M, Dawes H, Wade DT, Wade DT, Newman M, Burridge J, et al. Treadmill training for individuals with multiple sclerosis: a pilot randomised trial. J Neurol Neurosurg Psychiatry. 2006;77:531–3. 21 Cattaneo D, Jonsdottir J, Zocchi M, Regola A. Effects of balance exercises on people with multiple sclerosis: a pilot study. Clin Rehabil. 2007;21:771–81. 22 Smedal T, Lygren H, Myhr KM, Moe-Nilssen R, Gjelsvik B, Gjelsvik O, et al. Balance and gait improved in patients with MS after physiotherapy based on the Bobath concept. Physiother Res Int. 2006;11:104–16. 23 Nilsaga˚rd YE, Forsberg AS, von Koch L. Balance exercise for persons with multiple sclerosis using Wii games: a randomised, controlled multi-centre study. Mult Scler. 2013;19:209–16. 24 Nilsagard Y, Lundholm C, Gunnarsson LG, Dcnison E. Clinical relevance using timed walk tests and ‘timed up and go’ testing in persons with multiple sclerosis. Physiother Res Int. 2007;12:105–14. 25 Cattaneo D, Jonsdottir J, Repetti S. Reliability of four scales on balance disorders in persons with multiple sclerosis. Disabil Rehabil. 2007;29:1920–5.
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26 Padgett PK, Kasser SL. Exercise for managing the symptoms of multiple sclerosis. PhysTher. 2013;93:723–8. 27 Romberg A, Virtanen A, Ruutiainen J, Aunola S, Karppi S-L, Vaara M, et al. Effects of a 6-month exercise program on patients with multiple sclerosis: a randomized study. Neurology. 2004;63(11):2034–8. 28 Jackson K, Edginton-Bigelow K, Bowsheir C, Weston M, Grant E. Feasibility and effects of a group kickboxing program for individuals with multiple sclerosis: a pilot report. J Bodyw Mov Ther. 2012;16:7–13. 29 Ahmadi A, Arastoo AA, Nikbakht M, Zahednejad S, Rajabpour M. Comparison of the effect of 8 weeks aerobic and yoga training on ambulatory function, fatigue and mood status in MS patients. Iran Red Crescent Med J. 2013;15(6):449–54. 30 Silsupadol P, Siu KC, Shumway-Cook A, Woollacott MH. Training of balance under single- and dual-task conditions in older adults with balance impairment. Phys Ther. 2006;86:269–81. 31 Saposnik G, Teasell R, Mamdani M, Hall J, McIlroy W, Cheung D, et al. Stroke Outcome Research Canada (SORCan) Working Group: effectiveness of virtual reality using Wii gaming technology in stroke rehabilitation: a pilot randomized clinical trial and proof of principle. Stroke. 2010;41:1477–84. 32 Butler DP, Willett K. Wii-habilitation: is there a role in trauma? Injury. 2010;41:883–5. 33 Mao YR, Chen PM, Li L, Huang DF. Virtual reality training improves balance function. Neural Regen Res. 2014;9(17):1628–34. 34 Giesser B, Beres-Jones J, Budovitch A, Herlihy E, Harkema S. Locomotor training using body weight support on a treadmill improves mobility in persons with multiple sclerosis: a pilot study. Mult Scler. 2007;13(2):224–31. 35 Horlings CG, Carpenter MG, Kung UM, Honegger F, Wiederhold B, Allum JH. Influence of virtual reality on postural stability during movements of quiet stance. Neurosci Lett. 2009;451:227–31. 36 Eser F, Yavuzer G, Karakus D, Karaoglan B. The effect of balance training on motor recovery and ambulation after stroke: a randomized controlled trial. Eur J Phys Rehabil Med. 2008;44:19–25. 37 Parraca JA, Olivares PR, Carbonell-Baeza A, Aparicio VA, Adsuar JC, Gusi N. Test-retest reliability of biodex balance SD on physically active old people. J Hum Sport Exercise. 2011;6(2):444–51. 38 Cameron MH, Horak FB, Herndon RR, Bourdette D. Imbalance in multiple sclerosis: a result of slowed spinal somatosensory conduction. Somatosens Mot Res. 2008;25:113–122, .
Physical Medicine and Rehabilitation Research Center, Tabriz University of Medical Sciences, Iran, Department of Physical Medicine and Rehabilitation, Iran University of Medical Sciences, Iran, 3 Neuroscience Research Center, Tabriz University of Medical Sciences, Iran 2
Objectives: Balance and mobility impairments are common life-altering complications in patients with multiple sclerosis (MS). In this study, we aimed to investigate the efficacy of a short-term virtual reality (VR)-based balance training program on the balance ability of patients with MS. Methods: In this randomized controlled trial, 30 patients with relapsing–remitting or secondary-progressive MS were randomly assigned to an intervention or a control group. The intervention group performed a balance training program [postural stability training program (PST)] using the Biodex Balance System SD. Subjects in both groups were assessed using the manual muscle test (MMT), timed ‘up and go’ (TUG) test, the modified Ashworth scale, the Romberg test, the Berg balance scale (BBS), and the fall risk and postural stability tests, at baseline and after 12 weeks. Results: The TUG, fall risk index (FRi), and overall stability index (OSI) were significantly improved in the intervention group after 24 sessions of balance training. The changes in TUG, Fri, and OSi indices in the intervention group were significantly higher than the control group. Discussion: According to the fall risk and postural stability tests results, the VR-based balance training program could improve the balance ability of the patients with MS. Keywords: Multiple sclerosis, Balance training, Postural stability
Introduction
Different methods of physical therapy and training are introduced. Virtual reality (VR)-based balance training has shown promising results in treatment of different neuromuscular disease.14–17 The number of studies and experimental applications evaluating the beneficiary role of VR training on different neuromuscular disease has increased considerably over the last few years. Virtual reality-based trainings provide the patients with repetitive practice, feedback information, and motivation for endurance practice and could promote visual, auditory, tactile input, and motivation and motor learning.14,15 There are different VR-based balance training programs used for MS.17–23 Here, we investigated the efficacy of a VR-based balance rehabilitation program using Biodex Balance System on the speed and endurance of walking and the balance ability of patients with MS.
Multiple sclerosis (MS) is a chronic progressive autoimmune inflammatory disease of the central nervous system, which causes widespread dysfunction.1,2 Symptoms include sensory, cognitive, and motor impairment.2 Studies have reported a high prevalence of falls and balance or mobility impairments among people with MS.3–5 Balance dysfunction often occurs as a result of demyelination of the vestibular nerve or areas around vestibular nuclei in the brainstem.6 These impairments have a negative impact on personal activities and quality of life.7,8 Physical exercise and therapy are recommended to have considerable improvements in both physical and mental functioning of persons with MS and are becoming more commonly included as part of treatment interventions.9 It is reported that exercises could be beneficiary in improving muscular strength and aerobic capacity, mobility, mood, fatigue, and health-related quality of life.10–13
Methods
Correspondence to: Mahnaz Talebi, Neuroscience Research Center, Tabriz University of Medical Sciences, Golgasht Avenue, Tabriz 5166615556, Iran. email [email protected]
This single-blinded randomized clinical trial was conducted with the approval of Scientific and Ethical Review Boards of Tabriz University of Medical Sciences in 2011–2012. Thirty ambulatory patients
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with relapsing–remitting or secondary-progressive types of MS (most common types of MS in Iran) were selected randomly from among the patients who were referred to the Neurology Clinic of Tabriz University of Medical Sciences and were enrolled in this study after they have signed an informed consent to their participation. The patients were receiving standard treatment for MS. The participants were instructed by sealed envelopes. Patients with a background of diabetes mellitus, myasthenia gravis, myopathies, metabolic or toxic neuropathies, degenerative disorders of the musculoskeletal system, past history of trauma or surgery in the lower extremities, previous cerebrovascular accidents, or major cardiopulmonary disease were excluded from the study. Using a computer generated
table of random numbers, subjects were randomly assigned to an intervention or a control group, each comprising 15 patients. All outcome measures were assessed at approximately the same time of day and in the same order at the beginning of the study and after 12 weeks. No specific change was made to the medications of the subjects during the study period (Fig. 1). The manual muscle test (MMT) was performed to assess the muscle strength of the patients. The MMT evaluates the test movement and the test position of a muscle. It is graded from ‘zero’ (no movement even with therapist’s palpation) to grade ‘5’ (normal). The timed ‘up and go’ test (TUG) was performed to assess the mobility of the subjects. The TUG test assesses the
Randomly selected
Excluded: Did not wish to participate (n = 3) Assessed for eligibility
Excluded (n=7): a) Background of DM (n=4), b) previous history of trauma and surgery (n=3)
Randomized (n=30)
Intervention group (n = 15)
Postural stability training program 2 sessions per week for 12 weeks
Post intervention evaluation Figure 1 Flow diagram of the study protocol.
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mobility function. It records the time required for participant subject to stand up from a standard arm chair, walk 3 m around a cone and sit back down in the chair using their preferred assistive device. The test was repeated three times at a 2-minute intervals and the shortest time was recorded as the result. The reliability of this test in patients with MS is excellent: ICC50.91, 95% CI50.83–0.95.24 Subjects’ muscular tone was assessed using the modified Ashworth scale. The Modified Ashworth scale was developed in 1987 to assess muscle spasticity and tone. It is scored from ‘zero’ (no increase in muscle tone) to ‘4’ (rigidity of affected part(s) in flexion or extension). Balance ability was assessed using the Romberg test and the Berg balance scale (BBS). For the Romberg test, subjects stood with their feet together and their eyes closed. Irregular swaying and/or unsteadiness are recorded as positive in the Romberg test. The BBS assesses static and dynamic balance abilities with excellent test–retest reliability for patients with MS. It consists of 14 items of increasing difficulty, which are scored on a five-point Likert scale (0–4). The maximum possible score is 56, and lower scores indicate more impaired balance.25 In order to increase the diagnostic validity of our evaluation, we assessed all participants with Fall risk and postural stability tests using the Biodex Balance System SD (Biodex 945-302, Biodex Medical Systems Inc., Shirley, NY, USA). The Biodex Balance System is used to measure a subject’s ability to maintain balance while doing functional tasks. The Biodex Balance System assesses the static and dynamic balances by using usual tasks, such as reach, standing position, and transferences. The test includes 14 items that are common in everyday life. Each item of the Biodex Balance System is rated on a five-point scale. For the fall risk test (FRt), subjects were tested on the Biodex Balance System using the FRt protocol in order to evaluate the efficacy of the balance training intervention. In the FRt, the platform is unstable and subjects’ sway is used to calculate the Fall Risk index (FRi). According to the standard software configuration, three trials of 20 seconds each at a stability level of 8 were calculated with 10-second rest between trials. Fluctuations around the zero point, established prior to testing when the platform is stable, are presented as the findings of this test. For the postural stability test, three 20-second trials were conducted with 1 minute intervals between them. The platform is fixed and subjects’ sway is used to calculate the overall stability index (OSI). The BBS software sampled the deviations in the anterior–posterior (AP) and medial–lateral (ML) directions at a rate of 20 Hz and calculated the anterior/posterior index (API), medial/lateral index (MLI), and OSi during a given task. These indices were calculated using the degree of oscillation of the
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platform, in which low values indicated that the individual had good stability. For each mode, the average of three tests was considered as the subject index. All the subjects in the intervention group performed postural stability training (PST) using the Biodex Balance System SD for 20 minutes per session, twice a week for 12 weeks. Postural stability training simulates specific movement patterns or strategies by placing markers on specific locations on the screen grid. This training program is commercially available. In each session, the subjects attempted to touch targets nine times using an on-screen cursor, which is maneuvered by the subjects’ legs on the device’s platform. The platform stability was set to 6 (moderately stable). All the evaluations were repeated after 12 weeks. The subjects in the control group received no intervention, but were re-evaluated after 12 weeks for all of above mentioned outcome measures. The therapist who conducted the training program for the intervention group was not aware of the group composition and the investigators checked the training sessions several times to ensure that the therapist was following the training protocol. The assessor who performed the tests was blinded to the subjects’ grouping. The subjects completed the intervention or control programs as prescribed, and there were no drop-outs during the study. All the participants were re-evaluated at the end of study.
Statistical analysis All the statistical analyses were done using SPSS statistical software version 16.0 (SPSS Inc., Chicago, IL, USA). Values are presented as means + standard deviation. The values were compared between groups using the independent t-test, and before and after the intervention by the paired t-test. Values were recoded based on normal range limits, and the resulting categorical data were compared between groups using the chi-square test, or the Fisher’s exact test if needed. P values v0.05 were considered statistically significant.
Results In this randomized controlled trial, 15 patients with MS were enrolled in each of the intervention and control groups. The characteristics of both groups are shown in Table 1. There were no significant differences between the two groups’ characteristics, including age, sex, BMI, and the duration of disease. Manual muscle test (MMT) scores of the wrist, hip, and knee were not significantly different between the two groups before or after the intervention (Pw0.05). The Ashworth scale scores of the knee and hip were not significantly different between the two groups before or after the intervention either (Pw0.05). Only one subject in the control group was positive in the
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Table 1 Characteristics of the intervention and control groups
Age (years) Sex (M/F) BMI Duration of disease (years) Mobility (TUG)
Total
Intervention group (N515)
Control group (N515)
35?2+ 8?2 8/22 24?4+ 5?5 7?1+ 4?2 –
33?4+ 8?1 5/10 24?2+ 3?9 5?8+ 3?9 8?67+ 2?44
37?0+ 8?3 3/12 24?9+ 6?5 8?3+ 4?3 10?87+ 8?28
M: male; F: female; BMI: body mass index; TUG: timed ‘up and go’ test.
Romberg test at the beginning of the study, and this subject was the only one to be noted positive in the Romberg test after 12weeks as well (P50.5). Tables 2 and 3 demonstrate TUG, BBS, Fri, and OSi before and after the study and their changes during the study period in each group. After the 12-week intervention, the TUG time had declined and improved significantly in the intervention group (P50.003), but it had increased in the control group (Pw0.05). The changes in TUG were significantly better in intervention group compared to control group (P50.01). The BBS score after 12 weeks had declined in both groups, but the decline was not significant (Pw0.05 for both groups). The BBS changes were not significantly different between groups (Pw0.05). There were also significant improvement in FRi and OSi in the intervention group (Pv0.001 and P50.005, respectively), but the change in control group was not significant (Pw0.05). Intervention group also had significantly better FRi and OSi changes during the study period compared to control group (P50.002 and P50.04, respectively).
Discussion In this study, we performed a short-term (12 weeks) balance training program using Biodex Balance
System SD and observed better gait and balancerelated measures in the intervention group showed compared to the control group after. These results showed that VR-based balance training could yield favorable results regarding the balance ability of patients with MS. Our findings are in accordance with the findings of some studies in the literature.21,25 Balance disorders are frequent symptoms in MS patients, which increase risk of falls and restrict patients’ daily living activities.21 Scientific evidence indicates that exercise training and physical activity might have beneficial effects on a number of outcomes including balance, fitness, mood, and quality of life MS.17,23 Patients with mild to moderate MS who are ambulatory and have disability are likely to benefit from an exercise program. Exercise has the potential to increase strength and improve balance and mood in people with MS.26 Few studies have investigated the effect of exercise training on balance and coordination in MS. Some has reported significant clinical improvement and some reported unsupportive results.27 Jackson et al.28 demonstrated that group kickboxing is a feasible exercise activity for patients with MS. Other aerobic or treadmill training programs have been studied for their effect on the walking and balance of patients
Table 2 The comparison of TUG, BBS, Fri, and OSi before and after the study in each group Intervention group
TUG (seconds) BBS FRi OSi
Control group
Beginning
End
95% CI
Beginning
End
95% CI
8?67+ 2?44 51?67+ 3?26 2?36+ 1?30 0?81+ 0?51
8?00+ 2?23* 51?87+ 3?24 0?87+ 0?48* 0?36+ 0?19*
0?26–1?06 {0?42 to 0?02 0?87–2?09 0?15–0?73
10?87+ 8?28 48?53+ 8?99 2?50+ 1?48 0?76+ 0?42
11?07+ 9?30 48?80+ 9?01 2?47+ 1?68 0?68+ 0?43
{0?79 to 0?39 {0?65 to 0?12 {0?62 to 0?67 {0?14 to 0?30
TUG: timed ‘up and go’ test; BBS: Berg balance scale; FRi: fall risk index; OSI: overall stability index. * Statistically significant (Pv0?05). Table 3 Comparison of the changes in TUG, BBS, Fri, and OSi among groups
TUG (seconds) BBS FRi OSi
Intervention group (N515)
Control group (N515)
95% CI
0?66+ 0?72* 0?20+ 0?41 1?48+ 1?10* 0?44+ 0?51*
0?20+ 1?08 0?26+ 0?70 0?02+ 1?16 0?08+ 0?40
0?17–1?50 {0?36 to 0?49 {2?31 to {0?60 {0?71 to {0?01
TUG: timed ‘up and go’ test; BBS: Berg balance scale; FRi: Fall Risk index; OSI: overall stability index. * Statistically significant (Pv0?05).
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with MS.18–20 Ahmadi and colleagues have reported significant changes in the balance of patients with mild to moderate MS following treadmill training.29 Balance training has been shown to improve the different aspects of postural control and prevent fall.30 Virtual reality-based interventions are recommended as an effective alternative to physical therapy in improving balance and gait of patients with different neurological disorders.31,32 It is reported that VR training can activate the cerebral cortex, which will improve the spatial orientation capacity of patients, ability to control balance and increase motion function, gross motor function, and coordination.32,33 In this study, MS patients underwent VR-based training using Biodex Balance System SD, which yielded significant improvement in balance and fall risk. The TUG, Fri, and OSi significantly improved in the intervention group, and their post-intervention changes were significantly different from those of the control group. Similar to our findings, Cattaneo et al. observed considerable reduction in the number of falls and an improvement in clinical tests of static balance (BBS) and dynamic balance (Dynamic Gait Index).21 Giesser et al.34 showed improvements in balance after 40 treadmill training sessions by MS individuals with severely impaired ambulation. Horlings and coworkers35 also reported that VR balance training improved the patient’s reaction time, postural stability, balance, and walking function effectively. However, Eser et al.36 did not find a statistically significant difference between VR therapy and conventional therapy on lower extremity motor recovery, mobility, or activity level among patients with stroke. In our study, there was no difference among the findings of Romberg test between the two groups, both at the beginning and at the end of the intervention. Only one patient in the control group was noted as positive in the Romberg test. There are reports that patients with MS can suffer from balance impairment, even when their Romberg test results are normal.25 This study has some strength and some limitations. In this study, we evaluated subjective methods to assess balance ability of subjects, whereas the majority of previous studies have examined the balance ability of patients with MS using some kind of subjective clinical test or self-report.5,18,22 Tests such as the BBS or Romberg test are based on clinical observations by a clinician, so they may be susceptible to observer error. It is shown that Biodex balance measures are reliable in study of balance disorders and for measuring the risk of falls.37 The objective methods used in this study are not observerdependent diagnostics, and they may even be able to detect minor balance deficits in mildly disabled MS patients.1 So, it seems that observed results in this study
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are more indicative of efficacy of balance training in MS patients. The limitations of this study were the short-term (12 weeks) intervention and the lack of home-based balance training programs. The authors suggest further studies on the effect of virtual balance training on patients with MS to confirm the findings of this study with other objective diagnostic tests in different settings. In performing VR-based balance training, there is no need for stabilized posture control, rehabilitation difficulty is reduced, and the safety of the rehabilitation exercise is increased. So, according to our findings it is suggestive that VR-based balance training programs are effective and successful at improving the balance performance of patients with MS according to the results of the fall risk and postural stability tests.
Disclaimer Statements Contributors All authors cooperated in the study design, data collection and final anlysis and report. Funding Physical medicine and rehabilitation researches center, Tabriz University of medical sciences, Iran. Conflicts of interest No conflicts of interest. Ethics approval The study was approved by Scientific and Ethical Review Boards of Tabriz University of Medical Sciences, Tabriz, Iran.
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