578295
research-article2015
CRE0010.1177/0269215515578295Clinical RehabilitationWang et al.
CLINICAL REHABILITATION
Article
Cognitive motor intervention for gait and balance in Parkinson’s disease: Systematic review and meta-analysis
Clinical Rehabilitation 1–11 © The Author(s) 2015 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0269215515578295 cre.sagepub.com
Xue-Qiang Wang1*, Yan-Ling Pi2*, Bing-Lin Chen1, Ru Wang1, Xin Li1 and Pei-Jie Chen1
Abstract Objective: We performed a systematic review and meta-analysis to assess the effect of cognitive motor intervention (CMI) on gait and balance in Parkinson’s disease. Data sources: PubMed, Embase, Cochrane Library, CINAHL, Web of Science, PEDro, and China Biology Medicine disc. Methods: We included randomized controlled trials (RCTs) and non RCTs. Two reviewers independently evaluated articles for eligibility and quality and serially abstracted data. A standardized mean difference ± standard error and 95% confidence interval (CI) was calculated for each study using Hedge’s g to quantify the treatment effect. Results: Nine trials with 181 subjects, four randomized controlled trials, and five single group intervention studies were included. The pooling revealed that cognitive motor intervention can improve gait speed (Hedge’s g = 0.643 ± 0.191; 95% CI: 0.269 to 1.017, P = 0.001), stride time (Hedge’s g = -0.536 ± 0.167; 95% CI: -0.862 to -0.209, P = 0.001), Berg Balance Scale (Hedge’s g = 0.783 ± 0.289; 95% CI: 0.218 to 1.349, P = 0.007), Unipedal Stance Test (Hedge’s g = 0.440 ± 0.189; 95% CI: 0.07 to 0.81, P =0.02). Conclusions: The systematic review demonstrates that cognitive motor intervention is effective for gait and balance in Parkinson’s disease. However, the paper is limited by the quality of the included trials. Keywords Cognitive motor intervention, Parkinson’s disease, gait, balance, systematic review Received: 11 October 2014; accepted: 14 February 2015
Introduction Cognitive motor intervention is becoming an increasingly popular means of enhancing gait and balance ability.1 Cognitive motor intervention is where a cognitive exercise and a motor exercise are conducted simultaneously, such as performing balance exercise while doing cognitive exercise.2 In fact, most daily activities require the ability to maintain balance while performing various tasks.
1Sport
Medicine & Rehabilitation Center, Shanghai University of Sport, Shanghai, China 2Department of Rehabilitation Medicine, Shanghai Punan Hospital, Shanghai, China *These authors contributed equally to this study. Corresponding author: Peijie Chen, Sport Medicine & Rehabilitation Center, Shanghai University of Sport, Changhai Rd 399, Shanghai 200438, China. Email: [email protected]
2 Therefore, falling could be prevented by training to perform cognitive motor tasks simultaneously. Parkinson’s disease is a neurodegenerative disease that often leads to movement impairments, particularly gait and balance dysfunction.3 de Bruin showed that cognitive motor intervention, conversing whilst the music accompanied walks, can improve the gait and motor function of patients with Parkinson’s disease.4 And a recent systematic review with 15 randomized controlled trials demonstrated that cognitive motor intervention could be effective for improving gait speed, stride length, cadence and balance function for patients with stroke.5 Many studies found exercise was an effective strategy for improving gait and balance function.6–8 However, the effect of cognitive motor intervention on the gait and balance of Parkinson’s disease patients remains unclear. A published systematic review,9 which included 28 articles, reported that limited evidence is available on the ability of cognitive motor intervention to promote physical function in patients with neurological impairments. And another systematic review, which covered 30 randomized controlled trials with 1,206 subjects, showed that cognitive motor intervention was more effective than no intervention or single-task exercise for improving gait and balance function in older people.10 However, this review did not focus on Parkinson’s disease. To date, no systematic review or meta-analysis has been conducted on cognitive motor intervention in relation to the gait and balance function of patients with Parkinson’s disease. Moreover, the extent of cognitive motor intervention’s effectiveness to improve the gait and balance in Parkinson’s disease remains unclear. Thus, the aim of this systematic review and meta-analysis is to assess the effect of cognitive motor intervention for gait and balance functionin Parkinson’s disease.
Methods Relevant articles dated June 1980 to January 2015 were identified from the following databases: PubMed, Embase, Cochrane Library, Ebsco (CINAHL), Web of Science, PEDro, and China
Clinical Rehabilitation Biology Medicine disc. The electronic search strategies for all of the databases are provided in supplementary material Appendix 1. Manual searching was also performed. The protocol was registered on the international prospective register of systematic reviews (PROSPERO registration number: CRD42012002606). Inclusion criteria were as follows: types of studies were randomized controlled trials (RCTs) and non-RCTs; we included studies on patients with Parkinson’s disease; types of outcome measures were gait variables, such as gait speed and stride length, and balance function, such as Berg Balance Scale, center of pressure sway. Inclusion criteria interventions: (1) subjects who performed cognitive motor intervention were compared with those who underwent other therapies or no intervention; (2) subjects who performed cognitive motor intervention and were assessed before and after treatment. In cognitive motor intervention, subjects perform a motor task (e.g., balance exercise) while accomplishing a cognitive task exercise (e.g., addition/subtraction questions, 8 + 5 = 13).2 Other forms of feedback and attention strategies can also be included in cognitive motor exercise, such as the use of virtual reality techniques and electronic gaming (e.g., Wii).9 Two authors independently used the same selection criteria to screen titles, abstracts, and full papers of the relevant articles. Studies that failed to meet the inclusion criteria were removed. Any disagreement is resolved through discussion. A third author was consulted if any disagreement persisted. A standardized form was used to extract the data from the included studies. The following data were extracted: study characteristics (e.g., author and year), participant characteristics (e.g., age and number of subjects), description of interventions, duration of trial period, and types of outcomes assessed. The data extraction was performed by the same two authors who selected the studies. The Physiotherapy Evidence Database scale11 (with scores from 1 to 10) was used to assess the quality of the RCTs and non-RCTs with a control arm. We used modified Downs and Black tool12 to evaluate the quality of the single-group interventional studies. The modified Downs and Black
Wang et al. tool comprised 27 questions about study description, external validity, internal validity, and statistical power. Two review authors independently used a standardized assessment form to assess the methodological quality of each study. A third author was consulted if any disagreement occurred. A standardized mean difference (SMD) ± standard error and 95% confidence interval (CI) were calculated for each study by using Hedge’s g to quantify the treatment effect. The means and standard deviations could be estimated if the data are reported in a graph rather than a table. Authors were contacted if their standard deviations were not provided. Only the data from the cognitive motor intervention group were used in the pooled analyses if the trials estimated the treatment contrast of cognitive motor intervention versus an alternative intervention. We used the Comprehensive Meta-analysis software (version 2.0, Biostat, Englewood, NJ, USA)13 to analyze effect sizes, forest plots, and heterogeneity. Cohen14 suggested that an effect size greater than 0.5 is large, that ranging from 0.2 to 0.5 is moderate, and that lower than 0.2 is small. Q statistic and I2 statistic were used to assess heterogeneity among the studies. We used the random effects model. We considered P < 0.05 to be statistically significant. If a meta-analysis was not possible, the results from the clinical trials were described qualitatively.
Results Figure 1 shows the process of identifying eligible trials. Basing on their titles and abstracts, we included 43 potentially eligible studies (n = 181 patients) from 1048 identified records. After the full papers were reviewed, nine articles 9, 15–22 satisfied the inclusion criteria. The remaining 34 trials were excluded, because the participants considered had other neurological illness (e.g., cognitive impairment and stroke), no intervention or other interventions. Protocol articles were also excluded. Four RCTs conducted a comparison between an intervention group (cognitive motor intervention) and a control group (no treatment or other
3 interventions). Five articles were single-group intervention trials, in which all of the subjects were subjected to cognitive motor intervention. Table 1 presents the characteristics of each included study. We used the Physiotherapy Evidence Database scale (with scores from 1 to 10) to assess the methodological quality of RCTs. The PEDro score (mean ± SD) for the RCTs was 5.5±1. Three articles9,15,16 attempted to blind the assessors to the allocated treatment; one article17 reported allocation concealment; one article15 performed intention-to-treat analysis; and no article blinded the subjects and the therapist. The modified Downs and Black tool was used to evaluate the quality of the single-group interventional studies. The D owns and Black score (mean ± SD) for the singlegroup interventional studies was 15.5±1.30. Gait variables: three studies9,18,19 with six comparisons were included to assess the effect of cognitive motor intervention on gait speed. The results showed that cognitive motor intervention improves the gait speed of patients with Parkinson’s disease (Hedge’s g = 0.643 ± 0.191; 95% CI: 0.269 to 1.017, P = 0.001) (Figure 1A). Two studies 9,18 with four comparisons were included to assess the effect of cognitive motor intervention on stride length. We found that stride length presented no significant difference between pre- and post-intervention in Parkinson’s disease (Hedge’s g = 0.245 ± 0.181; 95% CI: –0.110 to 0.600, P = 0.176) (Figure 2B). Three studies9,18,19 with six comparisons were included to assess the effect of cognitive motor intervention on stride time. The results showed that cognitive motor intervention improves stride time (Hedge’s g = −0.536 ± 0.167; 95% CI: –0.862 to –0.209, P = 0.001) (Figure 2C). One study9 with two comparisons was included to estimate the effect of cognitive motor intervention on cadence. The results showed that cadence exhibited no significant difference between pre- and post-intervention (Hedge’s g = 0.484 ± 0.308; 95% CI: –0.118 to 1.087, P = 0.115) (Figure 2D). Balance function: three studies9,16,18 were included to assess the effect of cognitive motor intervention on the Unified Parkinson’s Disease Rating Scale. We found that cognitive motor intervention improves Unified Parkinson’s Disease
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Figure 1. Flow chart of the study selection procedure.
Clinical Rehabilitation
Yogev 201219 Single group intervention trail
Mirelman 201118 Single group intervention trail
Ma 201117 RCT
Pompeu 201216 RCT
Three times a week for 4 weeks
Gait (gait speed, stride time)
Gait (gait speed, stride length, stride time),balance (FSST) and UPDRS score
Three times a week for 6 weeks
Cognitive motor exercise
Movement time
1 hour per trail for 60 trails
G1: cognitive motor exercise G2: conventional balance training Cognitive motor exercise
Balance (BBS, UST) and UPDRS score
Gait (gait speed, stride length, stride time, cadence), UPDRS score
Balance performance (COP sway)
Outcome
Twice a week for 7 weeks
Three times a week for 13 weeks
Twice a week for 6 weeks
Duration of trial period
G1: cognitive motor exercise G2: balance training
G1: cognitive motor exercise G2: conventional balance training G3: No intervention G1: cognitive motor exercise G2: regular activities
Source: hospital 42 patients (G1=14, G2=14, G3=14). Mean age (SD): G1=70.4 y (6.5), G2=70.1 y (6.9), G3=71.6 y (5.8) Hoehn and Yahr stages: 2 to 3 Source: not specified 22 patients (G1=11, G2=11). Mean age (SD): G1=64.1 y (4.2), G2=67.0 y (8.1) Hoehn and Yahr stages: 2 to 3 Source: not specified 22 patients (G1=11, G2=11). Age range: 60 to 85 y Hoehn and Yahr stages: 1 to 2 Source: hospital 31 patients (G1=17, G2=16). Age range: 50 to 75 Hoehn and Yahr stages: 2 to 3 Source: not specified 20 patients. Age range: 55 to 79 Hoehn and Yahr stages: 2 to 3 UPDRS motor score mean (SD) = 26.5 (7.6) Source: hospital 7 patients. Age range: 50 to 90 Hoehn and Yahr stages: 2 to 3
Yen 201115 RCT
de Bruin 20109 RCT
Intervention
Patients characteristic
Study, study type
Table 1. Characteristics of included studies.
(Continued)
Downs and Black: 16
Downs and Black: 15
PEDro: 5
PEDro: 5
PEDro: 5
PEDro: 7
Quality assessment
Wang et al. 5
Three times a week for 6 weeks Two times a week for 7 weeks
Cognitive motor exercise
Cognitive motor exercise
Source: not specified 11 patients. Age range: 48 to 80 y UPDRS motor score mean (SD) = 18.4 (7.6) Source: hospital 16 patients. Mean age (SD): 68.6 y (8.0) Hoehn and Yahr stages: 1 to 2
Balance (STST, TUGT, POMA, CBM, ABC, UST, 10m walk test) Balance (FRT)
Balance (BBS, DGI,SRT, ABC, COP sway)
Outcome
Downs and Black: 14
Downs and Black: 14
Downs and Black: 17
Quality assessment
ABC: Activities-Specific Balance Confidence scale, BBS: Berg Balance Scale, CBM: Community Balance and Mobility assessment, COP: Center of pressure, DGI: Dynamic Gait Index, FRT: Functional Reach test, FSST: Four Square Step Test, PEDro: Physiotherapy Evidence Database, POMA: Tinetti Performance Oriented Mobility Assessment, RCT: randomized controlled trial, SRT: Sharpened Romberg Test, STST: Sit-to-Stand test, TUGT: Timed Up and Go test, UPDRS: Unified Parkinson’s Disease Rating Scale, UST: Unipedal Stance Test.
Three times a week for 8 weeks
Cognitive motor exercise
Source: hospital 10 patients. Mean age: 67.1 y Hoehn and Yahr stages: 2.5 to 3
Duration of trial period
Mhatre 201320 Single group intervention trail Esculier 201221 Single group intervention trail dos Santos 201222 Single group intervention trail
Intervention
Patients characteristic
Study, study type
Table 1. (Continued)
6 Clinical Rehabilitation
Wang et al.
Figure 2. Meta-analyses of cognitive motor intervention on gait function. A: gait speed, B: stride length, C: stride time and D: cadence. 95% CI=95% confidence intervals. CMI: cognitive motor intervention. *represents the performance under dual task test condition.
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8 Rating Scale (Hedge’s g = −0.492 ± 0.21; 95% CI: –0.903 to –0.081, P = 0.019) (Figure 3A). Two studies15,20 with four comparisons were included to assess the effect of cognitive motor intervention on center of pressure sway. We found that center of pressure sway significantly improved between preand post-intervention (Hedge’s g = −0.438 ± 0.071; 95% CI: –0.576 to –0.299, P < 0.001) (Figure 3B). Two studies16,20 were included to assess the effect of cognitive motor intervention on Berg Balance Scale. The results showed that cognitive motor intervention improved Berg Balance Scale after intervention (Hedge’s g = 0.783 ± 0.289; 95% CI: 0.218 to 1.349, P = 0.007) (Figure 3C). Two studies 16,21 with four comparisons were included to assess the effect of cognitive motor intervention on Unipedal Stance Test. We found that Unipedal Stance Test significantly improved between pre- and post-intervention (Hedge’s g = 0.440 ± 0.189; 95% CI: 0.07 to 0.81, P =0.02) (Figure 3D). These studies assessed the effect of cognitive motor intervention on different outcomes, demonstrating that cognitive motor intervention could improve the Four Square Step Test,18 the Dynamic Gait Index,20 the Sit-to-Stand test,21 the Timed Up and Go test,21 the Tinetti Performance Oriented Mobility Assessment,21 the 10 m walk test,21 and the Community Balance and Mobility assessment.21 However, no significant difference was found for Sharpened Romberg Test20 between preand post-intervention.
Discussion This systematic review and meta-analysis of articles from four RCTs and five single-group interventional studies, which included 181 subjects, verified the effect of cognitive motor intervention in Parkinson’s disease. Cognitive motor intervention was found to significantly benefit the following outcomes: gait speed, stride time, Unified Parkinson’s Disease Rating Scale, center of pressure sway, Berg Balance Scale, Unipedal Stance Test, Four Square Step Test, Dynamic Gait Index, Sit-to-Stand test, Timed Up and Go test, Tinetti Performance Oriented Mobility Assessment, 10 m walk test, and Community Balance and Mobility
Clinical Rehabilitation assessment. The sizes of the majority of the observed effects between pre- and post-intervention were predominantly not large. However, the levels of improvements for gait speed, Unified Parkinson’s Disease Rating Scale, center of pressure sway area, Berg Balance Scale, Dynamic Gait Index, Sit-to-Stand test, Timed Up and Go test, 10 m walk test, and Tinetti Performance Oriented Mobility Assessment may signify clinical importance in Parkinson’s disease. Moreover, no adverse events for cognitive motor intervention were found in nine studies. Various exercise interventions are used to improve the gait and balance function of patients with Parkinson’s disease. Previous most systematic reviews and meta-analyses23–26 have focused on motor exercise (e.g., resistance exercise and balance exercise). And previous5, 8, 9, 10, 27, 28 systematic reviews of cognitive motor intervention have either focused on qualitative synthesis or have not selected subjects with Parkinson’s disease. However, this work is the first systematic review and meta-analysis that estimates the effects of cognitive motor intervention on gait and balance function in Parkinson’s disease. Compared with previous reviews, the present systematic review and meta-analysis only included subjects with Parkinson’s disease for all articles. Most of the included studies were newly published. Moreover, we performed a meta-analysis of the effects of cognitive motor intervention between pre- and post-intervention of patients with Parkinson’s disease. We conducted a wide range of electronic search for the systematic review.29. No restrictions were placed on language or publication date. Study selection, data extraction, and quality evaluation were independently performed by two authors to minimize transcription errors and bias. In view of the abovementioned points, the results of our meta-analysis are considered extremely robust. However, several limitations were found in our review. First, high-quality studies remained inadequate despite our efforts to cover most of the studies within the last three years in our review. Four RCTs and five single-group interventional studies were found. According to their PEDro score, all of the
Wang et al.
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Figure 3. Meta-analyses of cognitive motor intervention on balance function. A: Unified Parkinson’s Disease Rating Scale (UPDRS), B: Center of pressure (COP) sway, C: Berg balance scale (BBS) and D: Unipedal Stance Test (UST). 95% CI=95% confidence intervals. CMI: cognitive motor intervention. *represents the performance under dual task test condition. # represents the performance under eye close.
10 RCTs were of moderate quality. Only one study conducted concealed allocation and intention-to-treat analyses. All studies failed to blind the subjects and therapists. Three studies attempted to blind assessors. Second, only a limited number of comparisons (one to three) were made in the systematic review with regard to the effect of cognitive motor intervention on the following outcomes: cadence, Unified Parkinson’s Disease Rating Scale, Berg Balance Scale, Four Square Step Test, Dynamic Gait Index, Sit-to-Stand test, Timed Up and Go test, Tinetti Performance Oriented Mobility Assessment, 10 m walk test, and Community Balance and Mobility assessment. In fact, the number of articles may be too small to discover the differences between preand post-intervention on these outcomes. Furthermore, the total number of subjects was small for the systematic review. Slight differences between pre and post-intervention were also difficult to estimate. Third, we intended to perform the meta-analysis on long-term gait and balance. However, most of the articles reported short follow-up periods and involved short intervention durations. Overall, our systematic review lacked highquality articles. The methodological standards must be improved in future studies to reduce possible biases. We should improve the following standards: conduct random allocation and concealed allocation; attempt to blind assessors, therapists, and subjects; perform intention-totreat analysis; and employ adequate follow-up period. Moreover, studies should be registered to reduce bias and should be conducted in accordance with the standards of clinical trials (e.g., the Consolidated Standards of Reporting Trials statement).30 As previously mentioned, most of the studies in this systematic review had small sample size. Thus, additional large-scale RCTs should be performed to evaluate the effect of cognitive motor intervention. To estimate the duration for any improvement outcome to be sustained for cognitive motor intervention, future studies should have follow-up sessions with longer durations. In addition, different training programs for cognitive motor intervention can be used, which may lead to different results. Therefore, a systematic review and meta-analysis
Clinical Rehabilitation of different cognitive motor interventions should be conducted to determine the optimal intervention program for patients with Parkinson’s disease. The results of our systematic review and metaanalysis show that cognitive motor intervention can significantly improve the following outcomes: gait speed, stride time, Unified Parkinson’s Disease Rating Scale, center of pressure sway, Berg Balance Scale, Unipedal Stance Test, Four Square Step Test, Dynamic Gait Index, Sit-to-Stand test, Timed Up and Go test, Tinetti Performance Oriented Mobility Assessment, 10 m walk test, and Community Balance and Mobility assessment. Therefore, our review results should be useful for patients with Parkinson’s disease, healthcare decision makers, and medical staff. Clinical messages •• Cognitive motor intervention is effective for gait and balance function in Parkinson’s disease. •• In the future, it is necessary to have more high quality RCTs to confirm these results. Acknowledgements We would like to thank Prof Chetwyn Chan for his advice.
Conflict of interest The authors declare that there is no conflict of interest.
Funding This study was supported by the Key Laboratory of Exercise and Health Sciences (Shanghai University of Sport), Ministry of Education, Shanghai University of Sport; Ministry of Education, the First-class Disciplines of Shanghai Colleges and Universities (Psychology); Shanghai Committee of Science and Technology (14490503800); Shanghai Youth Science and Technology Sail Project (15YF1411400).
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Wang et al. 2. Al-Yahya E, Dawes H, Smith L, Dennis A, Howells K and Cockburn J. Cognitive motor interference while walking: a systematic review and meta-analysis. Neurosci Biobehav Rev 2011; 35: 715–728. 3. Li F, Harmer P, Fitzgerald K, et al. Tai chi and postural stability in patients with Parkinson’s disease. N Engl J Med 2012; 366: 511–519. 4. de Bruin N, Doan JB, Turnbull G, et al. Walking with music is a safe and viable tool for gait training in Parkinson’s disease: the effect of a 13-week feasibility study on single and dual task walking. Parkinsons Dis 2010; 2010: 483530. 5. Wang XQ, Pi YL, Chen BL, et al. Cognitive motor interference for gait and balance in stroke: a systematic review and meta-analysis. Eur J Neurol. 2015. Epub ahead of print Jan 5 2015, DOI: 10.1111/ene.12616. 6. Sheehan DP and Katz L. The effects of a daily, 6-week exergaming curriculum on balance in fourth grade children. Journal of Sport and Health Science 2013; 2(3): 131–137. 7. Li FZ. Transforming traditional Tai Ji Quan techniques into integrative movement therapy-Tai Ji Quan: Moving for Better Balance. Journal of Sport and Health Science 2013; 3: 9–15. 8. Riner WF and Sellhorst SH. Physical activity and exercise in children with chronic health conditions. Journal of Sport and Health Science 2013; 2: 12–20. 9. Pichierri G, Wolf P, Murer K and de Bruin ED. Cognitive and cognitive-motor interventions affecting physical functioning: a systematic review. BMC Geriatr 2011; 11: 29. 10. Wang X, Pi Y, Chen P, Liu Y, Wang R and Chan C. Cognitive motor interference for preventing falls in older adults: a systematic review and meta-analysis of randomised controlled trials. Age Ageing 2014. Epub ahead of print Nov 5 2014, pii: afu175. 11. Coombes BK, Bisset L and Vicenzino B. Efficacy and safety of corticosteroid injections and other injections for management of tendinopathy: a systematic review of randomised controlled trials. Lancet 2010; 376: 1751–1767. 12. Downs SH and Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health 1998; 52: 377–384. 13. Foley N, Murie-Fernandez M, Speechley M, Salter K, Sequeira K and Teasell R. Does the treatment of spastic equinovarus deformity following stroke with botulinum toxin increase gait velocity? A systematic review and meta-analysis. Eur J Neurol 2010; 17:1419–1427. 14. Cohen J. Statistical power analysis for the behavioral sciences, 2nd Edn. New York: Academic Press, 1988. 15. Yen CY, Lin KH, Hu MH, Wu RM, Lu TW and Lin CH. Effects of virtual reality-augmented balance training on sensory organization and attentional demand for postural control in people with Parkinson disease: a randomized controlled trial. Phys Ther 2011; 91: 862–874. 16. Pompeu JE, Mendes FA, Silva KG, et al. Effect of Nintendo Wii™-based motor and cognitive training on activities of daily living in patients with Parkinson’s disease: a randomised clinical trial. Physiotherapy 2012; 98: 196–204.
11 17. Ma HI, Hwang WJ, Fang JJ, et al. Effects of virtual reality training on functional reaching movements in people with Parkinson’s disease: a randomized controlled pilot trial. Clin Rehabil 2011; 25: 892–902. 18. Mirelman A, Maidan I, Herman T, Deutsch JE, Giladi N and Hausdorff JM. Virtual reality for gait training: can it induce motor learning to enhance complex walking and reduce fall risk in patients with Parkinson’s disease? J Gerontol A Biol Sci Med Sci 2011; 66: 234–240. 19. Yogev-Seligmann G, Giladi N, Brozgol M and Hausdorff JM. A training program to improve gait while dual tasking in patients with Parkinson’s disease: a pilot study. Arch Phys Med Rehabil 2012; 93: 176–181. 20. Mhatre PV, Vilares I, Stibb SM, et al. Wii fit balance board playing improves balance and gait in Parkinson disease. PM R 2013; 5: 769–777. 21. Esculier JF, Vaudrin J, Bériault P, Gagnon K and Tremblay LE. Home-based balance training programme using Wii Fit with balance board for Parkinsons’s disease: a pilot study. J Rehabil Med 2012; 44: 144–150. 22. dos Santos Mendes FA, Pompeu JE, Modenesi Lobo A, et al. Motor learning, retention and transfer after virtual-reality-based training in Parkinson’s disease–effect of motor and cognitive demands of games: a longitudinal, controlled clinical study. Physiotherapy 2012; 98: 217–223. 23. Lima LO, Scianni A and Rodrigues-de-Paula F. Progressive resistance exercise improves strength and physical performance in people with mild to moderate Parkinson’s disease: a systematic review. J Physiother 2013; 59: 7–13. 24. Allen NE, Sherrington C, Paul SS and Canning CG. Balance and falls in Parkinson’s disease: a meta-analysis of the effect of exercise and motor training. Mov Disord 2011; 26: 1605–1615. 25. Tomlinson CL, Patel S, Meek C, et al. Physiotherapy versus placebo or no intervention in Parkinson’s disease. Cochrane Database Syst Rev 2013; 9: CD002817. 26. Allen NE, Sherrington C, Suriyarachchi GD, Paul SS, Song J and Canning CG. Exercise and motor training in people with Parkinson’s disease: a systematic review of participant characteristics, intervention delivery, retention rates, adherence, and adverse events in clinical trials. Parkinsons Dis 2012; 2012: 854328. 27. Verhaeghen P, Steitz DW, Sliwinski MJ and Cerella J. Aging and dual-task performance: a meta-analysis. Psychol Aging 2003; 18: 443–460. 28. Lee H, Sullivan SJ and Schneiders AG. The use of the dual-task paradigm in detecting gait performance deficits following a sports-related concussion: a systematic review and meta-analysis. J Sci Med Sport 2013; 16: 2–7. 29. Egger M, Juni P, Bartlett C, Holenstein F and Sterne J. How important are comprehensive literature searches and the assessment of trial quality in systematic reviews? Empirical study. Health Technol Assess 2003; 7: 1–76. 30. CONSORT GROUP (Consolidated Standards of Reporting Trials). The CONSORT statement: revised recommendations for improving the quality of reports of parallel-group randomized trials. Ann Intern Med 2001; 134: 657–662.
research-article2015
CRE0010.1177/0269215515578295Clinical RehabilitationWang et al.
CLINICAL REHABILITATION
Article
Cognitive motor intervention for gait and balance in Parkinson’s disease: Systematic review and meta-analysis
Clinical Rehabilitation 1–11 © The Author(s) 2015 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0269215515578295 cre.sagepub.com
Xue-Qiang Wang1*, Yan-Ling Pi2*, Bing-Lin Chen1, Ru Wang1, Xin Li1 and Pei-Jie Chen1
Abstract Objective: We performed a systematic review and meta-analysis to assess the effect of cognitive motor intervention (CMI) on gait and balance in Parkinson’s disease. Data sources: PubMed, Embase, Cochrane Library, CINAHL, Web of Science, PEDro, and China Biology Medicine disc. Methods: We included randomized controlled trials (RCTs) and non RCTs. Two reviewers independently evaluated articles for eligibility and quality and serially abstracted data. A standardized mean difference ± standard error and 95% confidence interval (CI) was calculated for each study using Hedge’s g to quantify the treatment effect. Results: Nine trials with 181 subjects, four randomized controlled trials, and five single group intervention studies were included. The pooling revealed that cognitive motor intervention can improve gait speed (Hedge’s g = 0.643 ± 0.191; 95% CI: 0.269 to 1.017, P = 0.001), stride time (Hedge’s g = -0.536 ± 0.167; 95% CI: -0.862 to -0.209, P = 0.001), Berg Balance Scale (Hedge’s g = 0.783 ± 0.289; 95% CI: 0.218 to 1.349, P = 0.007), Unipedal Stance Test (Hedge’s g = 0.440 ± 0.189; 95% CI: 0.07 to 0.81, P =0.02). Conclusions: The systematic review demonstrates that cognitive motor intervention is effective for gait and balance in Parkinson’s disease. However, the paper is limited by the quality of the included trials. Keywords Cognitive motor intervention, Parkinson’s disease, gait, balance, systematic review Received: 11 October 2014; accepted: 14 February 2015
Introduction Cognitive motor intervention is becoming an increasingly popular means of enhancing gait and balance ability.1 Cognitive motor intervention is where a cognitive exercise and a motor exercise are conducted simultaneously, such as performing balance exercise while doing cognitive exercise.2 In fact, most daily activities require the ability to maintain balance while performing various tasks.
1Sport
Medicine & Rehabilitation Center, Shanghai University of Sport, Shanghai, China 2Department of Rehabilitation Medicine, Shanghai Punan Hospital, Shanghai, China *These authors contributed equally to this study. Corresponding author: Peijie Chen, Sport Medicine & Rehabilitation Center, Shanghai University of Sport, Changhai Rd 399, Shanghai 200438, China. Email: [email protected]
2 Therefore, falling could be prevented by training to perform cognitive motor tasks simultaneously. Parkinson’s disease is a neurodegenerative disease that often leads to movement impairments, particularly gait and balance dysfunction.3 de Bruin showed that cognitive motor intervention, conversing whilst the music accompanied walks, can improve the gait and motor function of patients with Parkinson’s disease.4 And a recent systematic review with 15 randomized controlled trials demonstrated that cognitive motor intervention could be effective for improving gait speed, stride length, cadence and balance function for patients with stroke.5 Many studies found exercise was an effective strategy for improving gait and balance function.6–8 However, the effect of cognitive motor intervention on the gait and balance of Parkinson’s disease patients remains unclear. A published systematic review,9 which included 28 articles, reported that limited evidence is available on the ability of cognitive motor intervention to promote physical function in patients with neurological impairments. And another systematic review, which covered 30 randomized controlled trials with 1,206 subjects, showed that cognitive motor intervention was more effective than no intervention or single-task exercise for improving gait and balance function in older people.10 However, this review did not focus on Parkinson’s disease. To date, no systematic review or meta-analysis has been conducted on cognitive motor intervention in relation to the gait and balance function of patients with Parkinson’s disease. Moreover, the extent of cognitive motor intervention’s effectiveness to improve the gait and balance in Parkinson’s disease remains unclear. Thus, the aim of this systematic review and meta-analysis is to assess the effect of cognitive motor intervention for gait and balance functionin Parkinson’s disease.
Methods Relevant articles dated June 1980 to January 2015 were identified from the following databases: PubMed, Embase, Cochrane Library, Ebsco (CINAHL), Web of Science, PEDro, and China
Clinical Rehabilitation Biology Medicine disc. The electronic search strategies for all of the databases are provided in supplementary material Appendix 1. Manual searching was also performed. The protocol was registered on the international prospective register of systematic reviews (PROSPERO registration number: CRD42012002606). Inclusion criteria were as follows: types of studies were randomized controlled trials (RCTs) and non-RCTs; we included studies on patients with Parkinson’s disease; types of outcome measures were gait variables, such as gait speed and stride length, and balance function, such as Berg Balance Scale, center of pressure sway. Inclusion criteria interventions: (1) subjects who performed cognitive motor intervention were compared with those who underwent other therapies or no intervention; (2) subjects who performed cognitive motor intervention and were assessed before and after treatment. In cognitive motor intervention, subjects perform a motor task (e.g., balance exercise) while accomplishing a cognitive task exercise (e.g., addition/subtraction questions, 8 + 5 = 13).2 Other forms of feedback and attention strategies can also be included in cognitive motor exercise, such as the use of virtual reality techniques and electronic gaming (e.g., Wii).9 Two authors independently used the same selection criteria to screen titles, abstracts, and full papers of the relevant articles. Studies that failed to meet the inclusion criteria were removed. Any disagreement is resolved through discussion. A third author was consulted if any disagreement persisted. A standardized form was used to extract the data from the included studies. The following data were extracted: study characteristics (e.g., author and year), participant characteristics (e.g., age and number of subjects), description of interventions, duration of trial period, and types of outcomes assessed. The data extraction was performed by the same two authors who selected the studies. The Physiotherapy Evidence Database scale11 (with scores from 1 to 10) was used to assess the quality of the RCTs and non-RCTs with a control arm. We used modified Downs and Black tool12 to evaluate the quality of the single-group interventional studies. The modified Downs and Black
Wang et al. tool comprised 27 questions about study description, external validity, internal validity, and statistical power. Two review authors independently used a standardized assessment form to assess the methodological quality of each study. A third author was consulted if any disagreement occurred. A standardized mean difference (SMD) ± standard error and 95% confidence interval (CI) were calculated for each study by using Hedge’s g to quantify the treatment effect. The means and standard deviations could be estimated if the data are reported in a graph rather than a table. Authors were contacted if their standard deviations were not provided. Only the data from the cognitive motor intervention group were used in the pooled analyses if the trials estimated the treatment contrast of cognitive motor intervention versus an alternative intervention. We used the Comprehensive Meta-analysis software (version 2.0, Biostat, Englewood, NJ, USA)13 to analyze effect sizes, forest plots, and heterogeneity. Cohen14 suggested that an effect size greater than 0.5 is large, that ranging from 0.2 to 0.5 is moderate, and that lower than 0.2 is small. Q statistic and I2 statistic were used to assess heterogeneity among the studies. We used the random effects model. We considered P < 0.05 to be statistically significant. If a meta-analysis was not possible, the results from the clinical trials were described qualitatively.
Results Figure 1 shows the process of identifying eligible trials. Basing on their titles and abstracts, we included 43 potentially eligible studies (n = 181 patients) from 1048 identified records. After the full papers were reviewed, nine articles 9, 15–22 satisfied the inclusion criteria. The remaining 34 trials were excluded, because the participants considered had other neurological illness (e.g., cognitive impairment and stroke), no intervention or other interventions. Protocol articles were also excluded. Four RCTs conducted a comparison between an intervention group (cognitive motor intervention) and a control group (no treatment or other
3 interventions). Five articles were single-group intervention trials, in which all of the subjects were subjected to cognitive motor intervention. Table 1 presents the characteristics of each included study. We used the Physiotherapy Evidence Database scale (with scores from 1 to 10) to assess the methodological quality of RCTs. The PEDro score (mean ± SD) for the RCTs was 5.5±1. Three articles9,15,16 attempted to blind the assessors to the allocated treatment; one article17 reported allocation concealment; one article15 performed intention-to-treat analysis; and no article blinded the subjects and the therapist. The modified Downs and Black tool was used to evaluate the quality of the single-group interventional studies. The D owns and Black score (mean ± SD) for the singlegroup interventional studies was 15.5±1.30. Gait variables: three studies9,18,19 with six comparisons were included to assess the effect of cognitive motor intervention on gait speed. The results showed that cognitive motor intervention improves the gait speed of patients with Parkinson’s disease (Hedge’s g = 0.643 ± 0.191; 95% CI: 0.269 to 1.017, P = 0.001) (Figure 1A). Two studies 9,18 with four comparisons were included to assess the effect of cognitive motor intervention on stride length. We found that stride length presented no significant difference between pre- and post-intervention in Parkinson’s disease (Hedge’s g = 0.245 ± 0.181; 95% CI: –0.110 to 0.600, P = 0.176) (Figure 2B). Three studies9,18,19 with six comparisons were included to assess the effect of cognitive motor intervention on stride time. The results showed that cognitive motor intervention improves stride time (Hedge’s g = −0.536 ± 0.167; 95% CI: –0.862 to –0.209, P = 0.001) (Figure 2C). One study9 with two comparisons was included to estimate the effect of cognitive motor intervention on cadence. The results showed that cadence exhibited no significant difference between pre- and post-intervention (Hedge’s g = 0.484 ± 0.308; 95% CI: –0.118 to 1.087, P = 0.115) (Figure 2D). Balance function: three studies9,16,18 were included to assess the effect of cognitive motor intervention on the Unified Parkinson’s Disease Rating Scale. We found that cognitive motor intervention improves Unified Parkinson’s Disease
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Figure 1. Flow chart of the study selection procedure.
Clinical Rehabilitation
Yogev 201219 Single group intervention trail
Mirelman 201118 Single group intervention trail
Ma 201117 RCT
Pompeu 201216 RCT
Three times a week for 4 weeks
Gait (gait speed, stride time)
Gait (gait speed, stride length, stride time),balance (FSST) and UPDRS score
Three times a week for 6 weeks
Cognitive motor exercise
Movement time
1 hour per trail for 60 trails
G1: cognitive motor exercise G2: conventional balance training Cognitive motor exercise
Balance (BBS, UST) and UPDRS score
Gait (gait speed, stride length, stride time, cadence), UPDRS score
Balance performance (COP sway)
Outcome
Twice a week for 7 weeks
Three times a week for 13 weeks
Twice a week for 6 weeks
Duration of trial period
G1: cognitive motor exercise G2: balance training
G1: cognitive motor exercise G2: conventional balance training G3: No intervention G1: cognitive motor exercise G2: regular activities
Source: hospital 42 patients (G1=14, G2=14, G3=14). Mean age (SD): G1=70.4 y (6.5), G2=70.1 y (6.9), G3=71.6 y (5.8) Hoehn and Yahr stages: 2 to 3 Source: not specified 22 patients (G1=11, G2=11). Mean age (SD): G1=64.1 y (4.2), G2=67.0 y (8.1) Hoehn and Yahr stages: 2 to 3 Source: not specified 22 patients (G1=11, G2=11). Age range: 60 to 85 y Hoehn and Yahr stages: 1 to 2 Source: hospital 31 patients (G1=17, G2=16). Age range: 50 to 75 Hoehn and Yahr stages: 2 to 3 Source: not specified 20 patients. Age range: 55 to 79 Hoehn and Yahr stages: 2 to 3 UPDRS motor score mean (SD) = 26.5 (7.6) Source: hospital 7 patients. Age range: 50 to 90 Hoehn and Yahr stages: 2 to 3
Yen 201115 RCT
de Bruin 20109 RCT
Intervention
Patients characteristic
Study, study type
Table 1. Characteristics of included studies.
(Continued)
Downs and Black: 16
Downs and Black: 15
PEDro: 5
PEDro: 5
PEDro: 5
PEDro: 7
Quality assessment
Wang et al. 5
Three times a week for 6 weeks Two times a week for 7 weeks
Cognitive motor exercise
Cognitive motor exercise
Source: not specified 11 patients. Age range: 48 to 80 y UPDRS motor score mean (SD) = 18.4 (7.6) Source: hospital 16 patients. Mean age (SD): 68.6 y (8.0) Hoehn and Yahr stages: 1 to 2
Balance (STST, TUGT, POMA, CBM, ABC, UST, 10m walk test) Balance (FRT)
Balance (BBS, DGI,SRT, ABC, COP sway)
Outcome
Downs and Black: 14
Downs and Black: 14
Downs and Black: 17
Quality assessment
ABC: Activities-Specific Balance Confidence scale, BBS: Berg Balance Scale, CBM: Community Balance and Mobility assessment, COP: Center of pressure, DGI: Dynamic Gait Index, FRT: Functional Reach test, FSST: Four Square Step Test, PEDro: Physiotherapy Evidence Database, POMA: Tinetti Performance Oriented Mobility Assessment, RCT: randomized controlled trial, SRT: Sharpened Romberg Test, STST: Sit-to-Stand test, TUGT: Timed Up and Go test, UPDRS: Unified Parkinson’s Disease Rating Scale, UST: Unipedal Stance Test.
Three times a week for 8 weeks
Cognitive motor exercise
Source: hospital 10 patients. Mean age: 67.1 y Hoehn and Yahr stages: 2.5 to 3
Duration of trial period
Mhatre 201320 Single group intervention trail Esculier 201221 Single group intervention trail dos Santos 201222 Single group intervention trail
Intervention
Patients characteristic
Study, study type
Table 1. (Continued)
6 Clinical Rehabilitation
Wang et al.
Figure 2. Meta-analyses of cognitive motor intervention on gait function. A: gait speed, B: stride length, C: stride time and D: cadence. 95% CI=95% confidence intervals. CMI: cognitive motor intervention. *represents the performance under dual task test condition.
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8 Rating Scale (Hedge’s g = −0.492 ± 0.21; 95% CI: –0.903 to –0.081, P = 0.019) (Figure 3A). Two studies15,20 with four comparisons were included to assess the effect of cognitive motor intervention on center of pressure sway. We found that center of pressure sway significantly improved between preand post-intervention (Hedge’s g = −0.438 ± 0.071; 95% CI: –0.576 to –0.299, P < 0.001) (Figure 3B). Two studies16,20 were included to assess the effect of cognitive motor intervention on Berg Balance Scale. The results showed that cognitive motor intervention improved Berg Balance Scale after intervention (Hedge’s g = 0.783 ± 0.289; 95% CI: 0.218 to 1.349, P = 0.007) (Figure 3C). Two studies 16,21 with four comparisons were included to assess the effect of cognitive motor intervention on Unipedal Stance Test. We found that Unipedal Stance Test significantly improved between pre- and post-intervention (Hedge’s g = 0.440 ± 0.189; 95% CI: 0.07 to 0.81, P =0.02) (Figure 3D). These studies assessed the effect of cognitive motor intervention on different outcomes, demonstrating that cognitive motor intervention could improve the Four Square Step Test,18 the Dynamic Gait Index,20 the Sit-to-Stand test,21 the Timed Up and Go test,21 the Tinetti Performance Oriented Mobility Assessment,21 the 10 m walk test,21 and the Community Balance and Mobility assessment.21 However, no significant difference was found for Sharpened Romberg Test20 between preand post-intervention.
Discussion This systematic review and meta-analysis of articles from four RCTs and five single-group interventional studies, which included 181 subjects, verified the effect of cognitive motor intervention in Parkinson’s disease. Cognitive motor intervention was found to significantly benefit the following outcomes: gait speed, stride time, Unified Parkinson’s Disease Rating Scale, center of pressure sway, Berg Balance Scale, Unipedal Stance Test, Four Square Step Test, Dynamic Gait Index, Sit-to-Stand test, Timed Up and Go test, Tinetti Performance Oriented Mobility Assessment, 10 m walk test, and Community Balance and Mobility
Clinical Rehabilitation assessment. The sizes of the majority of the observed effects between pre- and post-intervention were predominantly not large. However, the levels of improvements for gait speed, Unified Parkinson’s Disease Rating Scale, center of pressure sway area, Berg Balance Scale, Dynamic Gait Index, Sit-to-Stand test, Timed Up and Go test, 10 m walk test, and Tinetti Performance Oriented Mobility Assessment may signify clinical importance in Parkinson’s disease. Moreover, no adverse events for cognitive motor intervention were found in nine studies. Various exercise interventions are used to improve the gait and balance function of patients with Parkinson’s disease. Previous most systematic reviews and meta-analyses23–26 have focused on motor exercise (e.g., resistance exercise and balance exercise). And previous5, 8, 9, 10, 27, 28 systematic reviews of cognitive motor intervention have either focused on qualitative synthesis or have not selected subjects with Parkinson’s disease. However, this work is the first systematic review and meta-analysis that estimates the effects of cognitive motor intervention on gait and balance function in Parkinson’s disease. Compared with previous reviews, the present systematic review and meta-analysis only included subjects with Parkinson’s disease for all articles. Most of the included studies were newly published. Moreover, we performed a meta-analysis of the effects of cognitive motor intervention between pre- and post-intervention of patients with Parkinson’s disease. We conducted a wide range of electronic search for the systematic review.29. No restrictions were placed on language or publication date. Study selection, data extraction, and quality evaluation were independently performed by two authors to minimize transcription errors and bias. In view of the abovementioned points, the results of our meta-analysis are considered extremely robust. However, several limitations were found in our review. First, high-quality studies remained inadequate despite our efforts to cover most of the studies within the last three years in our review. Four RCTs and five single-group interventional studies were found. According to their PEDro score, all of the
Wang et al.
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Figure 3. Meta-analyses of cognitive motor intervention on balance function. A: Unified Parkinson’s Disease Rating Scale (UPDRS), B: Center of pressure (COP) sway, C: Berg balance scale (BBS) and D: Unipedal Stance Test (UST). 95% CI=95% confidence intervals. CMI: cognitive motor intervention. *represents the performance under dual task test condition. # represents the performance under eye close.
10 RCTs were of moderate quality. Only one study conducted concealed allocation and intention-to-treat analyses. All studies failed to blind the subjects and therapists. Three studies attempted to blind assessors. Second, only a limited number of comparisons (one to three) were made in the systematic review with regard to the effect of cognitive motor intervention on the following outcomes: cadence, Unified Parkinson’s Disease Rating Scale, Berg Balance Scale, Four Square Step Test, Dynamic Gait Index, Sit-to-Stand test, Timed Up and Go test, Tinetti Performance Oriented Mobility Assessment, 10 m walk test, and Community Balance and Mobility assessment. In fact, the number of articles may be too small to discover the differences between preand post-intervention on these outcomes. Furthermore, the total number of subjects was small for the systematic review. Slight differences between pre and post-intervention were also difficult to estimate. Third, we intended to perform the meta-analysis on long-term gait and balance. However, most of the articles reported short follow-up periods and involved short intervention durations. Overall, our systematic review lacked highquality articles. The methodological standards must be improved in future studies to reduce possible biases. We should improve the following standards: conduct random allocation and concealed allocation; attempt to blind assessors, therapists, and subjects; perform intention-totreat analysis; and employ adequate follow-up period. Moreover, studies should be registered to reduce bias and should be conducted in accordance with the standards of clinical trials (e.g., the Consolidated Standards of Reporting Trials statement).30 As previously mentioned, most of the studies in this systematic review had small sample size. Thus, additional large-scale RCTs should be performed to evaluate the effect of cognitive motor intervention. To estimate the duration for any improvement outcome to be sustained for cognitive motor intervention, future studies should have follow-up sessions with longer durations. In addition, different training programs for cognitive motor intervention can be used, which may lead to different results. Therefore, a systematic review and meta-analysis
Clinical Rehabilitation of different cognitive motor interventions should be conducted to determine the optimal intervention program for patients with Parkinson’s disease. The results of our systematic review and metaanalysis show that cognitive motor intervention can significantly improve the following outcomes: gait speed, stride time, Unified Parkinson’s Disease Rating Scale, center of pressure sway, Berg Balance Scale, Unipedal Stance Test, Four Square Step Test, Dynamic Gait Index, Sit-to-Stand test, Timed Up and Go test, Tinetti Performance Oriented Mobility Assessment, 10 m walk test, and Community Balance and Mobility assessment. Therefore, our review results should be useful for patients with Parkinson’s disease, healthcare decision makers, and medical staff. Clinical messages •• Cognitive motor intervention is effective for gait and balance function in Parkinson’s disease. •• In the future, it is necessary to have more high quality RCTs to confirm these results. Acknowledgements We would like to thank Prof Chetwyn Chan for his advice.
Conflict of interest The authors declare that there is no conflict of interest.
Funding This study was supported by the Key Laboratory of Exercise and Health Sciences (Shanghai University of Sport), Ministry of Education, Shanghai University of Sport; Ministry of Education, the First-class Disciplines of Shanghai Colleges and Universities (Psychology); Shanghai Committee of Science and Technology (14490503800); Shanghai Youth Science and Technology Sail Project (15YF1411400).
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