Advertisement
Systematic review| Volume 101, ISSUE 1, P130-140, January 2020

Download started.

Ok

Effect of Repetitive Transcranial Magnetic Stimulation on Gait and Freezing of Gait in Parkinson Disease: A Systematic Review and Meta-analysis

  • Author Footnotes
    ∗ Xie and Gao contributed equally to this work.
    Yun-Juan Xie
    Footnotes
    ∗ Xie and Gao contributed equally to this work.
    Affiliations
    Department of Rehabilitation Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan Province, People’s Republic of China
    Search for articles by this author
  • Author Footnotes
    ∗ Xie and Gao contributed equally to this work.
    Qiang Gao
    Footnotes
    ∗ Xie and Gao contributed equally to this work.
    Affiliations
    Department of Rehabilitation Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan Province, People’s Republic of China

    Key Laboratory of Rehabilitation Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan Province, People’s Republic of China
    Search for articles by this author
  • Cheng-Qi He
    Correspondence
    Corresponding author Cheng-Qi He, PhD, Department of Rehabilitation Medicine, West China Hospital, Sichuan University, No. 37 Guo-xue-xiang St, Chengdu, Sichuan Province, People's Republic of China.
    Affiliations
    Department of Rehabilitation Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan Province, People’s Republic of China

    Key Laboratory of Rehabilitation Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan Province, People’s Republic of China
    Search for articles by this author
  • Rong Bian
    Affiliations
    Department of Rehabilitation, The First Affiliated Hospital of Nanjing Medical University, Nanjing, Jiangsu Province, People’s Republic of China
    Search for articles by this author
  • Author Footnotes
    ∗ Xie and Gao contributed equally to this work.
Published:August 26, 2019DOI:https://doi.org/10.1016/j.apmr.2019.07.013

      Abstract

      Objective

      The purpose of this review was to systematically assess the effectiveness of repetitive transcranial magnetic stimulation (rTMS) intervention on gait in individuals with Parkinson disease (PD).

      Data Sources

      We searched online electronic databases up to March 28, 2019, including MEDLINE, Embase, the Cochrane Library, and so on.

      Study Selection

      The inclusion criteria for this review were randomized controlled trials (RCTs), exploring the effect of rTMS in patients diagnosed with idiopathic PD.

      Data Extraction

      Data extraction was performed independently by 2 reviewers based on predefined criteria and the methodologic quality of included studies was quantified by the Physiotherapy Evidence Database scale. The outcome measure was walking performance, including walking time (short term and long term), Timed Up and Go (TUG) test, and so on.

      Data Synthesis

      Among 14 eligible studies, including 298 participants (mean age ± SD [y], 63.24±9.71; 191 [64%] men) were analyzed in this meta-analysis. Walking time was improved with rTMS compared with sham rTMS (standardized mean difference [SMD] -0.30; 95% confidence interval [CI], -0.57 to -0.03; P=.03). The score for the freezing of gait questionnaire did not differ significantly between rTMS and no intervention. Four studies compared TUG between the 2 treatment groups and no significant differences were found between the rTMS and control group (SMD -0.45; 95% CI, -1.32 to 0.41; P=.30). During the off-state, there were no significant differences in estimated effect sizes (SMD=-0.29; 95% CI, -0.79 to 0.21; P=.25), which is significantly different in on-state (SMD -0.98; 95% CI, -1.78 to -0.18; P=.02) evaluation.

      Conclusions

      The results of the meta-analysis propose the favorable effect of rTMS on walking performance in the short term but not over the long term in individuals with PD.

      Keywords

      List of abbreviations:

      CI (confidence interval), FOG (freezing of gait), FOG-Q (freezing of gait questionnaire), M1 (primary motor cortex), PD (Parkinson disease), PEDro (Physiotherapy Evidence Database scale), RCT (randomized controlled trial), rTMS (repetitive transcranial magnetic stimulation), SMD (standardized mean difference), TUG (timed Up and Go)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Archives of Physical Medicine and Rehabilitation
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Rubenis J.
        A rehabilitational approach to the management of Parkinson's disease.
        Parkinsonism Relat Disord. 2007; 13: S495-S497
        • Obeso J.A.
        • Stamelou M.
        • Goetz C.G.
        • et al.
        Past, present, and future of Parkinson's disease: a special essay on the 200th anniversary of the shaking palsy.
        Mov Disord. 2017; 32: 1264-1310
        • Tysnes O.B.
        • Storstein A.
        Epidemiology of Parkinson's disease.
        J Neural Transm (Vienna). 2017; 124: 901-905
        • Ascherio A.
        • Schwarzschild M.A.
        The epidemiology of Parkinson's disease: risk factors and prevention.
        Lancet Neurol. 2016; 15: 1257-1272
        • Cucca A.
        • Biagioni M.C.
        • Fleisher J.E.
        • et al.
        Freezing of gait in Parkinson's disease: from pathophysiology to emerging therapies.
        Neurodegener Dis Manag. 2016; 6: 431-446
        • Latt M.D.
        • Lord S.R.
        • Morris J.G.
        • Fung V.S.
        Clinical and physiological assessments for elucidating falls risk in Parkinson's disease.
        Mov Disord. 2009; 24: 1280-1289
        • Perez-Lloret S.
        • Negre-Pages L.
        • Damier P.
        • et al.
        Prevalence, determinants, and effect on quality of life of freezing of gait in Parkinson disease.
        JAMA Neurol. 2014; 71: 884-890
        • Giladi N.
        Medical treatment of freezing of gait.
        Mov Disord. 2008; 23: S482-S488
        • Giladi N.
        • Nieuwboer A.
        Understanding and treating freezing of gait in parkinsonism, proposed working definition, and setting the stage.
        Mov Disord. 2008; 23: S423-S425
        • Nonnekes J.
        • Snijders A.H.
        • Nutt J.G.
        • Deuschl G.
        • Giladi N.
        • Bloem B.R.
        Freezing of gait: a practical approach to management.
        Lancet Neurol. 2015; 14: 768-778
        • Rascol O.
        • Payoux P.
        • Ferreira J.
        • Brefel-Courbon C.
        The management of patients with early Parkinson's disease.
        Parkinsonism Relat Disord. 2002; 9: 61-67
        • Connolly B.S.
        • Lang A.E.
        Pharmacological treatment of Parkinson disease: a review.
        JAMA. 2014; 311: 1670-1683
        • Nijkrake M.J.
        • Keus S.H.
        • Kalf J.G.
        • et al.
        Allied health care interventions and complementary therapies in Parkinson's disease.
        Parkinsonism Relat Disord. 2007; 13: S488-S494
        • LaHue S.C.
        • Comella C.L.
        • Tanner C.M.
        The best medicine? The influence of physical activity and inactivity on Parkinson's disease.
        Mov Disord. 2016; 31: 1444-1454
        • Schrag A.
        • Jahanshahi M.
        • Quinn N.
        How does Parkinson's disease affect quality of life? A comparison with quality of life in the general population.
        Mov Disord. 2000; 15: 1112-1118
        • Faggiani E.
        • Benazzouz A.
        Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: from history to the interaction with the monoaminergic systems.
        Prog Neurobiol. 2017; 151: 139-156
        • Morgante L.
        • Morgante F.
        • Moro E.
        • et al.
        How many parkinsonian patients are suitable candidates for deep brain stimulation of subthalamic nucleus? Results of a questionnaire.
        Parkinsonism Relat Disord. 2007; 13: 528-531
        • Elahi B.
        • Elahi B.
        • Chen R.
        Effect of transcranial magnetic stimulation on Parkinson motor function--systematic review of controlled clinical trials.
        Mov Disord. 2009; 24: 357-363
        • Chou Y.H.
        • Hickey P.T.
        • Sundman M.
        • Song A.W.
        • Chen N.K.
        Effects of repetitive transcranial magnetic stimulation on motor symptoms in Parkinson disease: a systematic review and meta-analysis.
        JAMA Neurol. 2015; 72: 432-440
        • Xie C.L.
        • Chen J.
        • Wang X.D.
        • et al.
        Repetitive transcranial magnetic stimulation (rTMS) for the treatment of depression in Parkinson disease: a meta-analysis of randomized controlled clinical trials.
        Neurol Sci. 2015; 36: 1751-1761
        • Zhu H.
        • Lu Z.
        • Jin Y.
        • Duan X.
        • Teng J.
        • Duan D.
        Low-frequency repetitive transcranial magnetic stimulation on Parkinson motor function: a meta-analysis of randomised controlled trials.
        Acta Neuropsychiatr. 2015; 27: 82-89
        • Chung C.L.
        • Mak M.K.
        Effect of repetitive transcranial magnetic stimulation on physical function and motor signs in Parkinson's disease: a systematic review and meta-analysis.
        Brain Stimul. 2016; 9: 475-487
        • Reithler J.
        • Peters J.C.
        • Sack A.T.
        Multimodal transcranial magnetic stimulation: using concurrent neuroimaging to reveal the neural network dynamics of noninvasive brain stimulation.
        Prog Neurobiol. 2011; 94: 149-165
        • Higgins J.P.
        • Green S.
        Cochrane handbook for systematic reviews of interventions. Version 5.1.0.
        Cochrane Collaboration, London, England2011
        • de Morton N.A.
        The PEDro scale is a valid measure of the methodological quality of clinical trials: a demographic study.
        Aust J Physiother. 2009; 55: 129-133
        • Maher C.G.
        • Sherrington C.
        • Herbert R.D.
        • Moseley A.M.
        • Elkins M.
        Reliability of the PEDro scale for rating quality of randomized controlled trials.
        Phys Ther. 2003; 83: 713-721
        • Cohen J.
        Statistical power analysis for the behavioral sciences.
        2nd ed. L. Erlbaum Associates, Mahwah1988
        • Cumming G.
        Understanding the new statistics: effect sizes, confidence intervals, and meta-analysis.
        Routledge Taylor & Francis Group, New York2012
        • Higgins J.P.
        • Thompson S.G.
        • Deeks J.J.
        • Altman D.G.
        Measuring inconsistency in meta-analyses.
        BMJ. 2003; 327: 557-560
        • Fleiss J.L.
        The statistical basis of meta-analysis.
        Stat Methods Med Res. 1993; 2: 121-145
        • Borenstein M.
        • Hedges L.V.
        • Higgins J.P.
        • Rothstein H.R.
        A basic introduction to fixed-effect and random-effects models for meta-analysis.
        Res Synth Methods. 2010; 1: 97-111
      1. Australasian Cochrane Centre. 2014. The Nordic Cochrane Centre, The Cochrane Collaboration, Copenhagen2014
        • Arias P.
        • Vivas J.
        • Grieve K.L.
        • Cudeiro J.
        Controlled trial on the effect of 10 days low-frequency repetitive transcranial magnetic stimulation (rTMS) on motor signs in Parkinson's disease.
        Mov Disord. 2010; 25: 1830-1838
        • Benninger D.H.
        • Iseki K.
        • Kranick S.
        • Luckenbaugh D.A.
        • Houdayer E.
        • Hallett M.
        Controlled study of 50-Hz repetitive transcranial magnetic stimulation for the treatment of Parkinson disease.
        Neurorehabil Neural Repair. 2012; 26: 1096-1105
        • Benninger D.H.
        • Berman B.D.
        • Houdayer E.
        • et al.
        Intermittent theta-burst transcranial magnetic stimulation for treatment of Parkinson disease.
        Neurology. 2011; 76: 601-609
        • Cohen O.S.
        • Rigbi A.
        • Yahalom G.
        • et al.
        Repetitive deep TMS for Parkinson disease: a 3-month double-blind, randomized sham-controlled study.
        J Clin Neurophysiol. 2018; 35: 159-165
        • Dagan M.
        • Herman T.
        • Mirelman A.
        • Giladi N.
        • Hausdorff J.M.
        The role of the prefrontal cortex in freezing of gait in Parkinson's disease: insights from a deep repetitive transcranial magnetic stimulation exploratory study.
        Exp Brain Res. 2017; 235: 2463-2472
        • del Olmo M.F.
        • Bello O.
        • Cudeiro J.
        Transcranial magnetic stimulation over dorsolateral prefrontal cortex in Parkinson's disease.
        Clin Neurophysiol. 2007; 118: 131-139
        • El-Tamawy M.S.
        • Shehata H.S.
        • Shalaby N.M.
        • Nawito A.
        • Esmail E.H.
        Can repetitive transcranial magnetic stimulation help on-freezers with Parkinson's disease?.
        Egypt J Neurol Psychiatry Neurosurg. 2013; 50: 355-360
        • Khedr E.M.
        • Rothwell J.C.
        • Shawky O.A.
        • Ahmed M.A.
        • Hamdy A.
        Effect of daily repetitive transcranial magnetic stimulation on motor performance in Parkinson's disease.
        Mov Disord. 2006; 21: 2201-2205
        • Khedr E.M.
        • Farweez H.M.
        • Islam H.
        Therapeutic effect of repetitive transcranial magnetic stimulation on motor function in Parkinson's disease patients.
        Eur J Neurol. 2003; 10: 567-572
        • Kim M.S.
        • Chang W.H.
        • Cho J.W.
        • et al.
        Efficacy of cumulative high-frequency rTMS on freezing of gait in Parkinson's disease.
        Restor Neurol Neurosci. 2015; 33: 521-530
        • Lomarev M.P.
        • Kanchana S.
        • Bara-Jimenez W.
        • Iyer M.
        • Wassermann E.M.
        • Hallett M.
        Placebo-controlled study of rTMS for the treatment of Parkinson's disease.
        Mov Dis. 2006; 21: 325-331
        • Lefaucheur J.P.
        • Drouot X.
        • Von Raison F.
        • Menard-Lefaucheur I.
        • Cesaro P.
        • Nguyen J.P.
        Improvement of motor performance and modulation of cortical excitability by repetitive transcranial magnetic stimulation of the motor cortex in Parkinson's disease.
        Clin Neurophysiol. 2004; 115: 2530-2541
        • Maruo T.
        • Hosomi K.
        • Shimokawa T.
        • et al.
        High-frequency repetitive transcranial magnetic stimulation over the primary foot motor area in Parkinson's disease.
        Brain Stimul. 2013; 6: 884-891
        • Pal E.
        • Nagy F.
        • Aschermann Z.
        • Balazs E.
        • Kovacs N.
        The impact of left prefrontal repetitive transcranial magnetic stimulation on depression in Parkinson's disease: a randomized, double-blind, placebo-controlled study.
        Mov Disord. 2010; 25: 2311-2317
        • Yang Y.R.
        • Tseng C.Y.
        • Chiou S.Y.
        • et al.
        Combination of rTMS and treadmill training modulates corticomotor inhibition and improves walking in Parkinson disease: a randomized trial.
        Neurorehabil Neural Repair. 2013; 27: 79-86
        • Mak M.K.
        Reduced step length, not step length variability is central to gait hypokinesia in people with Parkinson's disease.
        Clin Neurol Neurosurg. 2013; 115: 587-590
        • Morris M.E.
        • Iansek R.
        • Matyas T.A.
        • Summers J.J.
        The pathogenesis of gait hypokinesia in Parkinson's disease.
        Brain. 1994; 117: 1169-1181
        • Nieuwboer A.
        • Kwakkel G.
        • Rochester L.
        • et al.
        Cueing training in the home improves gait-related mobility in Parkinson's disease: the RESCUE trial.
        J Neurol Neurosurg Psychiatry. 2007; 78: 134-140
        • Dubuis R.
        'On-off' phenomenon: description, incidence and management.
        Eur Neurol. 1987; 27: 3-8
        • Lees A.J.
        The on-off phenomenon.
        J Neurol Neurosurg Psychiatry. 1989; Suppl: 29-37
        • Kim Y.W.
        • Shin I.S.
        • Moon H.I.
        • Lee S.C.
        • Yoon S.Y.
        Effects of non-invasive brain stimulation on freezing of gait in parkinsonism: a systematic review with meta-analysis.
        Parkinsonism Relat Disord. 2019 Feb 27; ([Epub ahead of print])
        • Heremans E.
        • Nieuwboer A.
        • Vercruysse S.
        Freezing of gait in Parkinson's disease: where are we now?.
        Curr Neurol Neurosci Rep. 2013; 13: 350
        • Bartels A.L.
        • Leenders K.L.
        Brain imaging in patients with freezing of gait.
        Mov Disord. 2008; 23: S461-S467
        • Lewis S.J.
        • Shine J.M.
        The next step: a common neural mechanism for freezing of gait.
        Neuroscientist. 2016; 22: 72-82
        • Lenka A.
        • Naduthota R.M.
        • Jha M.
        • et al.
        Freezing of gait in Parkinson's disease is associated with altered functional brain connectivity.
        Parkinsonism Relat Disord. 2016; 24: 100-106
        • Yoo W.K.
        • You S.H.
        • Ko M.H.
        • et al.
        High frequency rTMS modulation of the sensorimotor networks: behavioral changes and fMRI correlates.
        Neuroimage. 2008; 39: 1886-1895
        • Chang W.H.
        • Kim Y.H.
        • Yoo W.K.
        • et al.
        rTMS with motor training modulates cortico-basal ganglia-thalamocortical circuits in stroke patients.
        Restor Neurol Neurosci. 2012; 30: 179-189
        • Bestmann S.
        • Baudewig J.
        • Siebner H.R.
        • Rothwell J.C.
        • Frahm J.
        Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits.
        Eur J Neurosci. 2004; 19: 1950-1962
        • Lee S.Y.
        • Kim M.S.
        • Chang W.H.
        • Cho J.W.
        • Youn J.Y.
        • Kim Y.H.
        Effects of repetitive transcranial magnetic stimulation on freezing of gait in patients with Parkinsonism.
        Restor Neurol Neurosci. 2014; 32: 743-753
        • Shirota Y.
        • Ohtsu H.
        • Hamada M.
        • Enomoto H.
        • Ugawa Y.
        Supplementary motor area stimulation for Parkinson disease: a randomized controlled study.
        Neurology. 2013; 80: 1400-1405
        • Yang C.
        • Guo Z.
        • Peng H.
        • et al.
        Repetitive transcranial magnetic stimulation therapy for motor recovery in Parkinson's disease: a meta-analysis.
        Brain Behav. 2018; 8e01132
        • Ueno S.
        • Tashiro T.
        • Harada K.
        Localized stimulation of neural tissues in the brain by means of a paired configuration of time-varying magnetic fields.
        J Appl Phys. 1988; 64: 5862-5864
        • Deng Z.D.
        • Lisanby S.H.
        • Peterchev A.V.
        Coil design considerations for deep transcranial magnetic stimulation.
        Clin Neurophysiol. 2014; 125: 1202-1212
        • Hao D.
        • Zhou Y.
        • Gao P.
        • Yang L.
        • Yang Y.
        • Chen F.
        Simulation study on coil design for transcranial magnetic stimulation.
        Conf Proc IEEE Eng Med Biol Soc. 2018; 2018: 2174-2177
        • Schulz K.F.
        • Altman D.G.
        • Moher D.
        • CONSORT Group
        CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials.
        BMJ. 2010; 340: c332