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Clinical Rehabilitation 1 –8 © The Author(s) 2016 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0269215516639735 cre.sagepub.com CLINICAL REHABILITATION Effects of dual-task balance training on postural performance in patients with Multiple Sclerosis: A double-blind, randomized controlled pilot trial Saeideh Monjezi1, Hossein Negahban2, Shirin Tajali3, Nava Yadollahpour3 and Nastaran Majdinasab4 Abstract Objective: To investigate the effects of dual-task balance training on postural performance in patients with multiple sclerosis as compared with single-task balance training. Design: Double-blind, pretest-posttest, randomized controlled pilot trial. Setting: Local Multiple Sclerosis Society. Subjects: A total of 47 patients were randomly assigned to two equal groups labeled as single-task training and dual-task training groups. Interventions: All patients received supervised balance training sessions, 3 times per week for 4 weeks. The patients in the single-task group performed balance activities, alone. However, patients in dual-task group practiced balance activities while simultaneously performing cognitive tasks. Main measures: The 10-Meter Walk Test and Timed Up-and-Go under single-task and dual-task conditions, in addition to Activities-specific Balance Confidence, Berg Balance Scale, and Functional Gait Assessment were assessed pre-, and post intervention and also 6-weeks after the end of intervention. Results: Only 38 patients completed the treatment plan. There was no difference in the amount of improvement seen between the two study groups. In both groups there was a significant effect of time for dual-10 Meter Walk Test (F1, 36=11.33, p=0.002) and dual-Timed Up-and-Go (F1, 36=14.27, p=0.001) but not for their single-tasks. Moreover, there was a significant effect of time for Activities-specific Balance Confidence, Berg Balance Scale, and Functional Gait Assessment (P<0.01). 1 Musculoskeletal Rehabilitation Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran 2 Department of Physical Therapy, School of Paramedical Sciences, Mashhad University of Medical Sciences, Mashhad, Iran 3 Musculoskeletal Rehabilitation Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran 639735 CRE0010.1177/0269215516639735Clinical RehabilitationMonjezi et al. research-article2016 Original Article 4 Neurologist, Department of Neurology, Musculoskeletal Rehabilitation Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran Corresponding author: Hossein Negahban, Department of Physical Therapy, School of Paramedical Sciences, Mashhad University of Medical Sciences, Mashhad, Iran. Email: honegahban@yahoo.com at City University Library on April 14, 2016cre.sagepub.comDownloaded from mailto:honegahban@yahoo.com http://cre.sagepub.com/ 2 Clinical Rehabilitation Introduction Patients with Multiple Sclerosis (MS) exhibit postural instability as well as cognitive impair- ments even at the earliest stage of the disease.1–3 Although there are some evidences that postural instability in patients with MS can be minimized with single-task balance exercises,4–6 there have been limited evidences related to the effects of dual-task balance exercises in this specific patient population. Dual-task activities that involve both motor and cognitive resources (e.g. thinking while standing and talking while walking) constitute a significant portion of most activities of daily liv- ings.3 Patients with MS may have difficulty in concurrent execution of these activities. Given the apparent cognitive deficits (such as impaired information processing speed) in patients with MS,3 some evidences support the notion of decre- ment in balance performance when combined with simultaneous execution of a cognitive task.1,2,7 This cognitive-motor interference has been documented in dual-task studies in which postural control and gait of patients have been negatively affected by the addition of concurrent cognitive tasks.1,3,8,9 Some evidences have shown the positive effects of single-task balance exercises on patients with MS.4–6 However, no study has yet comprehensively evaluated the effects of dual-task balance-specific exercises and compared it with traditional single-task exercises in this specific patient population. To our knowledge, only one study has recently investigated the effectiveness of a video-game balance program by means of dual-task paradigm (i.e. exergaming with additional postural demands) in patients with MS.10 While the results were promising, this technol- ogy may not be available in all clinical settings and also may not be sufficiently adaptive for patients with moderate to severe disability.11 Therefore, the aim of this randomized con- trolled pilot study was to investigate the effects of dual-task balance training on postural performance of patients with MS as compared with single-task balance training. We hypothesized that dual-task balance training would improve the postural per- formances and also, it would be more effective than single-task balance training. Materials and methods Patients The registration number in the Iranian Register for Clinical Trials is IRCT2014051917752N1. The method of this study was approved by the local Ethics Committee (ETH number: 1392.302). All patients were given the informed consent form and offered the opportunity to ask any questions regard- ing the study procedures. Following signed informed consent form, they completed the demographic vari- ables of interest including age, gender, height, weight, time since disease, and years of education. Patients’ disability level and cognitive impair- ments were evaluated by the Expanded Disability Status Scale12 and Mini-Mental State Examination,9 respectively. The inclusion criteria were (1) a neu- rologist-confirm diagnosis of MS, relapsing- remitting type, (2) an Expanded Disability Status Scale score of 2-5.5,13 since in our pilot study, patients with severe disability failed to perform/ complete the gait-related tests, (3) ability to stand without any support,1 and (4) ability to walk 100m independently. Patients were excluded if they had Conclusions: This pilot study did not show more benefits from undertaking dual-task training than single-task training. A power analysis showed 71 patients per group would be needed to determine whether there was a clinically relevant difference for dual-task gait speed between the groups. Keywords Dual-task, balance, training, multiple sclerosis, outcome Received: 18 August 2015; accepted: 25 February 2016 at City University Library on April 14, 2016cre.sagepub.comDownloaded from http://cre.sagepub.com/ Monjezi et al. 3 (1) Mini-Mental State Examination less than 24 as they potentially have problem with understanding instructions during dual-task activities, (2) any neuro-musculo-skeletal disorders except MS lim- iting gait and balance, (3) uncorrected visual dis- orders, and (4) ongoing exacerbation of the symptoms.6 The method of randomization was a balanced randomization process in which patients were matched based on age and sex and randomly assigned to either the single-task training group or the dual-task balance training group in equal sam- ple proportions using a table of random numbers. Study interventions This study was a double-blind, pretest-posttest, randomized controlled pilot trial in which neither the examiner nor the patients were aware of group assignment. All patients received 45-minute, supervised bal- ance training sessions, 3 times per week for 4 weeks, with a total of 12 training sessions. The balance- specific exercise program was based on the exer- cises provided in O’Sullivan and Schmitz14 Plummer-D’Amato et al.,15 and Silsupadol et al.,16 studies and has been described in details in Appendix 1 (Supplementary material). In brief, the exerciseprotocol was included exercise in double/single leg standing and tandem standing on a variety of differ- ent support surfaces (i.e. rigid and foam surfaces) with various sensory inputs (i.e. eyes open and closed). Also, walking activities including forward/ backward/side walking, walking on firm/foam sur- faces, walking through obstacles and walking up and down stairs were exercised by each patient. The patients in the single-task training group performed balance activities, alone. However, patients in dual-task training group practiced bal- ance activities while simultaneously performing cognitive task including naming objects, remem- bering things, and backward recitation of days, months, etc. Briefly, during the first training ses- sions, we asked patients to practice balance activi- ties while simultaneously perform an easy cognitive task (such as name words in category, backward recitation of days of week, and remembering 4-item grocery list or 4 numbers). In the final sessions, patients performed balance activities combined with a hard cognitive task (such as name words starting with a single letter, backward recitation of a group of alphabet, and remembering phone num- bers) (see Appendix 2, Supplementary material for details). Patients in both groups were advised to continue their usual medical care throughout the study. Outcome measurements The primary outcome measures were 10 Meter Walk test17 and Timed Up and Go test6 under sin- gle-task and dual-task conditions. The secondary outcome measures were Activities-specific Balance Confidence,7 Berg Balance Scale,4 and Functional Gait Assessment.18 Also, the cognitive scores of dual-10 Meter Walk test and dual-Timed Up and Go test were considered as secondary outcome measures. The order of all these measures was ran- domized between patients to control learning and fatigue effects. All outcome measures were col- lected at baseline (pretest), at the end of training session (posttest) and also at 6-weeks after the end of training sessions to test retention (follow-up). These measurements were performed by an exam- iner (ST) who was blinded to the group allocation. Before the baseline assessment, all patients were familiarized with the various test conditions and practiced them correctly. The 10 Meter Walk test was performed alone with no additional task (i.e. single-10 Meter Walk test) and also with a concurrent cognitive challenge (i.e. dual-10 Meter Walk test). During single test, patients walked 10m at their usual comfortable speed and the time to complete the middle 6m was recorded by a stopwatch.17 In dual-10 Meter Walk test patients were asked to walk 10m and at the same time count backward by three from a random number between 100 and 200. The cognitive score was based on the final number reported by patient and the number of subtractions. If the final number is accurate, one score would be added to the num- ber of subtracting items and if the final number is not accurate, only the number of subtracting items would be considered as cognitive score. The Timed Up and Go was performed both alone and with a concurrent cognitive task of backward at City University Library on April 14, 2016cre.sagepub.comDownloaded from http://cre.sagepub.com/ 4 Clinical Rehabilitation counting by three from a random number between 20 and 100.6,8 In this test, the total time require to rise from an armchair, walk 3m, turn around, walk back, and sit down again on a chair was recorded by a stopwatch.8,19 The test-retest reliability and valid- ity of Timed Up and Go was satisfactory for patients with MS.6,18 The Activities-specific Balance Confidence is a self-reported instrument of balance confidence during 16 different daily activities. A confidence rating scale ranges from 0% (not at all confident) to 100% (full confident).2,7 The reliability and valid- ity of this instrument has been established in patients with MS.7,20 The Berg Balance Scale consists of perfor- mance of 14 different activities common in every- day life and the patient’s score is rated by a clinician on a 0 (cannot perform) to 4 (normal per- formance) scale with a total scoring range of 0 to 56. The Berg Balance Scale is a reliable and valid instrument to examine functional balance in patients with MS.4,18,21 The Functional Gait Assessment consists of 10 items covering walking in different conditions. This scale ranges from 0 to 30, with lower scores indicating greater walking impairment.18 The Functional Gait Assessment is a valid measure of dynamic balance in patients with MS. Statistical analysis Data were analyzed using SPSS software (SPSS Inc., Chicago, IL, USA) version 18.0 for windows. The normality of the data distribution was assessed by the Shapiro-Wilk test. The balance training effects on all outcome measures were evaluated using 2-way mixed- effects repeated measures analysis of variance with group (2 levels: single-task training and dual- task training) as the between-subjects variable and time (2 levels: pretest and posttest) as within-sub- jects variable. For patients who completed the follow-up testing (n= 14 in single-task training group and n=16 in dual-task training group), a repeated measure analysis of variance was con- ducted to examine changes between pretest, post- test, and follow-up data. Results This study consisted of 47 ambulatory patients with MS recruited from the local Multiple Sclerosis Society at the School of Rehabilitation Sciences, AJUMS. During the 4-weeks intervention, nine patients in both groups dropped out of the protocol due to their work schedules (n=5), knee pain, back pain and ankle sprain (n=2 in the single-task and n=2 in the dual-task group) (Figure 1). Patients consisted of 15 females and 4 males in both experi- mental groups. From 38 patients (80.85%) who completed the treatment plan and underwent the posttest evaluation, 8 patients did not return for follow-up testing due to the trip in the summer and also their work schedules. Table 1 summarizes the results of demographics and clinical backgrounds which were equivalent (P<0.05) between the two study groups. The results of variance analysis showed that the group main effect was not significant for any primary and secondary outcomes (Supplementary Table). Therefore, there was an equivalent amount of improvement after the training across the both study groups. Moreover, there was a significant main effect of time for dual-10 Meter Walk test and dual-Timed Up and Go test but not for single-10 Meter Walk test and single-Timed Up and Go. Additionally, the cognitive score of dual-10 Meter Walk test was not different between pre-post train- ing while for the dual-Timed Up and Go test this was increased in the post-training. The results of pairwise comparisons for those who completed the follow-up testing showed that the benefits of improvement were maintained at follow-up test- ing; i.e. 6-weeks after completion of the interven- tion (P<0.01). Discussion As hypothesized, dual-task balance training was effective to improve balance performance as indi- cated by improvement in dual-task gait speed, dual- task Timed Up and Go time, cognitive score of dual-Timed Up and Go test, self-reported confi- dence, balance and gait in patients with MS. However, dual-task balance training does not lead to any greater improvement than single-task training at City University Library on April 14, 2016cre.sagepub.comDownloaded from http://cre.sagepub.com/ Monjezi et al. 5 Figure 1. Flow chart of the study process. Table 1. Demographic and functional characteristics of single- and dual-task balance training groups. STT group (n = 19 ) DTT (n = 19) P-value Mean (SD) Mean (SD) (Mean differences) Demographic data Age (yr) 36.2 (9.16) 35.8 (6.91) 0.87 Height (m) 1.6 (0.08) 1.6 (0.06) 0.13 Body mass index (kg/m2) 22.9 (3.19) 24.3 (4.06) 0.24 Time since disease (yr) 7.5 (4.62)7.2 (5.95) 0.87 Year of education (yr) 12.4 (4.42) 13.7 (3.65) 0.31 MMSEa 29.3 (0.82) 29.1 (1.05) 0.50 EDSSb 2.7 (0.91) 2.9 (1.25) 0.42 STT: Single-task training; DTT: Dual-task training; MMSE: Mini-Mental State Examination; EDSS: Expanded Disability Status Scale. aRange of scores is from 0 to 30.bRange of scores is from 0 to 10. at City University Library on April 14, 2016cre.sagepub.comDownloaded from http://cre.sagepub.com/ 6 Clinical Rehabilitation program. The results obtained in this study are con- sistent with results of the only study conducted on patients with MS in which balance training under dual-task conditions (i.e. playing Wii exergames on an unstable surface) was effective as traditional bal- ance training.10 We expected more improvement in dual-task group than single-task group. There are several pos- sible reasons that might explain these results. One reason is related to the large variability observed for the amount of improvement in both study groups (See Table 2). For instance, while the mean differ- ence between pretest-posttest times of the dual-10 Meter Walk test showed an improvement of 0.07sec for the single-task training group and 0.13sec for the dual-task training group, the standard deviation of these differences were also high (i.e. standard devia- tion of 0.17sec and 0.20sec for single-task and dual- task groups, respectively). Another explanation is that the counting cognitive task used in dual-task based outcome measures of this study (i.e. dual-10 Meter Walk test, dual-Timed Up and Go test) was not sufficiently difficult to compete with the atten- tional demands of the walking tasks. Therefore, in future studies, we recommend a more challenging cognitive task (such as Stroop task) or a secondary motor task (such as holding a tray while walking) to elicit dual-task training effects on postural control. Finally, we found that training balance under single- task situations resulted into the improvement in dual-task testing of gait and balance (i.e. dual-10 Meter Walk test and dual-Timed Up and Go test). This finding supported the Task Automization Hypothesis17 in which practicing only postural tasks at a time (i.e. single-task training) allows patients to gain automaticity in performing that activity. As a result, according to the attentional capacity theory, the attentional demands required to perform this task is decreased, freeing more capacity to perform another task concurrently.10,17 Table 2. Outcome measurements for the pretest-posttest times in both single- and dual-task training groups. Outcomes Pretest Posttest Difference 95% CI mean (SD) mean (SD) mean (SD) Single-task training Single-10MW (m/s) 1.03 (0.20) 1.03 (0.18) 0.003 (0.16) −0.08 to 0.08 Dual-10MW (m/s) 0.91 (0.19) 0.98 (0.19) 0.07 (0.17) −0.01 to 0.15 Single-TUG (sec) 10.54 (1.98) 10.17 (2.19) −0.37 (1.61) −1.15 to 0.41 Dual-TUG (sec) 12.65 (2.60) 11.24 (2.87) −1.40 (1.55) −2.15 to −0.66 ABC (0-100 point) 57.26 (20.54) 64.05 (18.53) 6.79 (13.99) 0.05 to 13.53 BBS (0-56 point) 44.32 (6.49) 48.42 (4.43) 4.11 (5.38) 1.51 to 6.7 FGA (0-30 point) 17.05 (5.63) 20.68 (4.46) 3.63 (3.27) 2.06 to 5.21 Cog score of dual-10MW 5.53 (1.95) 5.74 (1.85) 0.21 (1.36) −0.45 to 0.87 Cog score of Dual-TUG 4.82 (1.33) 5.00 (1.52) 0.18 (1.55) −0.56 to 0.93 Dual-task training Single-10MW (m/s) 1.04 (0.29) 1.06 (0.30) 0.02 (0.16) −0.06 to 0.10 Dual-10MW (m/s) 0.81 (0.29) 0.94 (0.33) 0.13 (0.20) 0.04 to 0.23 Single-TUG (sec) 10.27 (4.67) 9.52 (4.21) −0.75 (2.67) −2.04 to 0.54 Dual-TUG (sec) 12.30 (5.37) 10.87 (4.21) −1.43 (2.88) −2.82 to −0.04 ABC (0-100 point) 60.21 (17.51) 68.21 (14.86) 8 (16.74) −0.07 to 16.07 BBS (0-56 point) 45 (4.15) 49.26 (3.53) 4.26 (3.83) 2.42 to 6.11 FGA (0-30 point) 18.84 (4.71) 20.89 (4.93) 2.05 (3.19) 0.52 to 3.59 Cog score of dual-10MW 6.05 (3.06) 5.93 (2.57) 0.12 (2.69) −1.42 to 1.17 Cog score of dual-TUG 4.12 (1.49) 4.91 (1.41) 0.79 (1.11) 0.25 to 1.32 SD: standard deviation; CI: confidence interval.10MW: 10m walk test; TUG: time up and go; ABC: activities-specific balance confidence; BBS: berg balance scale; FGA: functional gait assessment. at City University Library on April 14, 2016cre.sagepub.comDownloaded from http://cre.sagepub.com/ Monjezi et al. 7 The results of this study showed that in contrast to single-task testing of balance and gait, testing under dual-task conditions was able to discriminate differences between pretest-posttest times. This finding suggests that the postural performance measures under dual-task conditions are more sen- sitive to record the training effects than postural measurements in isolation.3, 6 Therefore, in contrast to single-task measures of postural performance, the outcome measures based on dual-tasking, may represent a promising tool for detecting the training effects, since they truly reflect everyday activities compared to assessing postural and cognitive skills, separately.1 This hypothesis is supported by evidences that fall risks are increased in activities performed under cognitive loading in patients with MS.22,23 Consistent with finding of our study, Nilsagard et al. observed that the Nintendo Wii Fit balance exercise improved the dual-Timed Up and Go test not the single-Timed Up and Go in patients with MS.6 Also, these authors in an observation study performed on 70 patients reported that the performance of dual-Timed Up and Go test was a predictor for future falls in MS.23 This study has several strengths in terms of the interpretation of the findings. First, one of the important issues in randomized controlled trials is whether the positive training effects are retained several months after the end of training. We included a follow-up period after the end of inter- vention to assess the long-term effects of the bal- ance program and found that the balance training effects were maintained at 6-weeks follow-up. Second, a posttest analysis was performed for 80% of the patients enrolled into the study. As most drop-out was due to their work schedules, we rec- ommend fewer treatment sessions for encouraging patients to complete the treatment plan. Third, we conducted a double-blind study in which both the patients and examiner were blinded to the group assignment. We acknowledge the following study limitations. While in the single-center study we can include more homogenous sample, a sufficient large sample size may not possible in this case. Therefore, a first limitation of this study is that commonly observed in pilot rehabilitation studies (i.e. small sample size) that limits the generalizability of the results and reduces the observed power to detect a true differ- ence. A post-study calculation showed that a sample of 71 patients per group would be needed to be ade- quately powered to determine if there is any differ- ence for dual-task gait speed (as an example) between the two groups. Second; our sample com- prised patients with mild to moderate disability (as indexed by the Expanded Disability Status Scale), so the findings cannot be generalized to patients with a more severe disability. Third, due to the ethi- cal considerations, there was no true control group with no exercise program. Another limitation may be not assessing falls-related outcome measures in this study. As falls is affected by postural instability, many patients with MS reported falls as a common concern.24 Therefore, future research should evalu- ate falls outcome measures when training balance in patients with MS. Overall, this pilot study did not show any bene- fit from undertaking dual-task balance training. A power analysis showed that a sample of 71 patients per group would be needed to determine whether there was a clinically relevant difference for dual- task gait speed between the groups. Clinical Messages •• Dual-task balance training does not lead to any greater improvement than single- task training program. •• Outcome measuresbased on dual-task- ing are more sensitive to detect the train- ing effects than postural measurements in isolation. Acknowledgements This study is part of MSc thesis of Mrs. Monjezi. Special thanks to Ahvaz Jundishapur University of Medical Sciences for the financial support. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publica- tion of this article. at City University Library on April 14, 2016cre.sagepub.comDownloaded from http://cre.sagepub.com/ 8 Clinical Rehabilitation Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by a Master thesis grant (no: PHT-9229) in Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran References 1. Prosperini L, Castelli L, Sellitto G, et al. Investigating the phenomenon of “cognitive-motor interference” in multi- ple sclerosis by means of dual-task posturography. Gait Posture. 2015; 41: 780–785. 2. Wajda DA, Motl RW and Sosnoff JJ. Correlates of dual task cost of standing balance in individuals with multiple sclerosis. Gait Posture. 2014; 40: 352–356. 3. Wajda DA and Sosnoff JJ. 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