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Open Access 01-12-2020 | Repetitive Transcranial Magnetic Stimulation | Research article

Effect of rTMS on Parkinson’s cognitive function: a systematic review and meta-analysis

Authors: Yi Jiang, Zhiwei Guo, Morgan A. McClure, Lin He, Qiwen Mu

Published in: BMC Neurology | Issue 1/2020

Abstract

Background

To evaluate the effects and optimal parameters of repetitive transcranial magnetic stimulation (rTMS) on cognition function of patients with Parkinson’s disease (PD) and to estimate which cognitive function may obtain more benefits from rTMS.

Method

The articles dealing with rTMS on cognitive function of PD patients were retrieved from the databases until April 2019. Outcomes of global cognitive function and different cognitive domains were extracted. The standardized mean differences (SMDs) with 95% confidence interval (CI) of cognitive outcome for different parameters, scales, and cognitive functions were estimated.

Results

Fourteen studies involving 173 subjects were included in this meta-analysis. A significant effect size was observed with the mini-mental state examination (MMSE) for the global cognitive outcome based on the evidence of four published articles. Further subtests for different cognitive domains demonstrated prominent effect for the executive function. The significant effect sizes for executive function were found with multiple sessions of high-frequency rTMS over frontal cortex; especially over dorsolateral prefrontal cortex (DLPFC). All of the other cognitive domains, which included memory, attention, and language ability, did not obtain significant effects.

Conclusions

Multiple sessions of high-frequency rTMS over the DLPFC may have positive effect on executive function in PD patients. Further well designed studies with large sample sizes are needed to verify our results and ascertain the long-term effects of rTMS.

Khoo TK, Yarnall AJ, Duncan GW, et al. The spectrum of non-motor symptoms in early Parkinson disease. Neurology. 2013;80(3):276–81. https://doi.org/10.1212/WNL.0b013e31827deb74 Epub 2013/01/16. PubMed PMID: 23319473; PubMed Central PMCID: PMCPmc3589180.CrossRefPubMedPubMedCentral

Chaudhuri KR, Schapira AH. Non-motor symptoms of Parkinson’s disease: dopaminergic pathophysiology and treatment. Lancet Neurol. 2009;8(5):464–74. https://doi.org/10.1016/s1474-4422(09)70068-7 Epub 2009/04/21. PubMed PMID: 19375664.CrossRefPubMed

Verbaan D, Marinus J, Visser M, et al. Cognitive impairment in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2007;78(11):1182–7. https://doi.org/10.1136/jnnp.2006.112367 Epub 2007/04/20. PubMed PMID: 17442759; PubMed Central PMCID: PMCPmc2117586.CrossRefPubMedPubMedCentral

Caviness JN, Driver-Dunckley E, Connor DJ, et al. Defining mild cognitive impairment in Parkinson’s disease. Mov Disord. 2007;22(9):1272–7. https://doi.org/10.1002/mds.21453 Epub 2007/04/07. PubMed PMID: 17415797.CrossRefPubMed

Aarsland D, Zaccai J, Brayne C. A systematic review of prevalence studies of dementia in Parkinson’s disease. Mov Disord. 2005;20(10):1255–63. https://doi.org/10.1002/mds.20527 Epub 2005/07/26. PubMed PMID: 16041803.CrossRefPubMed

Forsaa EB, Larsen JP, Wentzel-Larsen T, et al. What predicts mortality in Parkinson disease? A prospective population-based long-term study. Neurology. 2010;75:1270–6.CrossRef

Aarsland D, Bronnick K, Williams-Gray C, et al. Mild cognitive impairment in Parkinson disease: a multicenter pooled analysis. Neurology. 2010;75(12):1062–9. https://doi.org/10.1212/WNL.0b013e3181f39d0e Epub 2010/09/22. PubMed PMID: 20855849; PubMed Central PMCID: PMCPmc2942065.CrossRefPubMedPubMedCentral

Rajput AH, Voll A, Rajput ML, Robinson CA, Rajput A. Course in Parkinson disease subtypes: a 39-year clinicopathologic study. Neurology. 2009;73(3):206–12. https://doi.org/10.1212/WNL.0b013e3181ae7af1 Epub 2009/07/22. PubMed PMID: 19620608.CrossRefPubMed

Zuo LJ, Piao YS, Li LX, et al. Phenotype of postural instability/gait difficulty in Parkinson disease: relevance to cognitive impairment and mechanism relating pathological proteins and neurotransmitters. Sci Rep. 2017;7:44872.CrossRef

10.

Uitvlugt MG, Pleskac TJ, Ravizza SM. The nature of working memory gating in Parkinson’s disease: A multi-domain signal detection examination. Cogn Affect Behav Neurosci. 2016;16(2):289–301.CrossRef

11.

Safarpour D, Willis AW. Clinical epidemiology, evaluation, and management of dementia in Parkinson disease. Am J Alzheimers Dis Other Dement. 2016;31(7):585–94. https://doi.org/10.1177/1533317516653823 Epub 2016/06/15. PubMed PMID: 27295974.CrossRef

12.

Lefaucheur JP, Aleman A, Baeken C, et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS): an update (2014-2018). Clin Neurophysiol. 2020;131:474–528.CrossRef

13.

Wagle Shukla A, Vaillancourt DE. Treatment and physiology in Parkinson’s disease and dystonia: Using transcranial magnetic stimulation to uncover the mechanisms of action. Curr Neurol Neurosci Rep. 2014;14:449 [PubMed: 2477110.CrossRef

14.

Pell GS, Roth Y, Zangen A. Modulation of cortical excitability induced by repetitive transcranial magnetic stimulation: influence of timing and geometrical parameters and underlying mechanisms. Prog Neurobiol. 2011;93:59–98.CrossRef

15.

Ridding MC, Rothwell JC. Is there a future for therapeutic use of transcranial magnetic stimulation? Nat Rev Neurosci. 2007;8(7):559–67. https://doi.org/10.1038/nrn2169 Epub 2007/06/15. PubMed PMID: 17565358.CrossRefPubMed

16.

Guse B, Falkai P, Wobrock T. Cognitive effects of high-frequency repetitive transcranial magnetic stimulation: a systematic review. J Neural Transm (Vienna). 2010;117(1):105–22. https://doi.org/10.1007/s00702-009-0333-7 Epub 2009/10/28. PubMed PMID: 19859782; PubMed Central PMCID: PMCPmc3085788.CrossRef

17.

Jahanshahi M. Other cognitive functions. Magnetic stimulation in clinical (2005). Neurophysiology. 2005:281–302. https://doi.org/10.1016/B978-0-7506-7373-0.50022-5.

18.

Srovnalova H, Marecek R, Rektorova I. The role of the inferior frontal gyri in cognitive processing of patients with Parkinson’s disease: a pilot rTMS study. Mov Disord. 2011;26(8):1545–8. https://doi.org/10.1002/mds.23663 Epub 2011/04/12. PubMed PMID: 21480374.CrossRefPubMed

19.

Rektorova I, Megova S, Bares M, Rektor I. Cognitive functioning after repetitive transcranial magnetic stimulation in patients with cerebrovascular disease without dementia: a pilot study of seven patients. J Neurol Sci. 2005;229-230:157–61. https://doi.org/10.1016/j.jns.2004.11.021 Epub 2005/03/12. PubMed PMID: 15760635.CrossRefPubMed

20.

Pascual-Leone A, Valls-Sol J, Wassermann EM, et al. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain. 1994;(4):847–58. https://doi.org/10.1093/brain/117.4.847.

21.

Anderkova L, Rektorova I. Cognitive effects of repetitive transcranial magnetic stimulation in patients with neurodegenerative diseases – clinician’s perspective. J Neurol Sci. 2014;339(1–2):15–25. https://doi.org/10.1016/j.jns.2014.01.037 Epub 2014/02/18. PubMed PMID: 24530170.CrossRefPubMed

22.

Rektorova I, Anderkova L. Non-invasive brain stimulation and implications for non-motor symptoms in Parkinson’s disease. Int Rev Neurobiol. 2017;134:1091–110. https://doi.org/10.1016/bs.irn.2017.05.009 Epub 2017/08/15. PubMed PMID: 28805565.CrossRefPubMed

23.

Dinkelbach L, Brambilla M, Manenti R, Brem AK. Non-invasive brain stimulation in Parkinson’s disease: exploiting crossroads of cognition and mood. Neurosci Biobehav Rev. 2017;75:407–18. https://doi.org/10.1016/j.neubiorev.2017.01.021 Epub 2017/01/26. PubMed PMID: 28119070.CrossRefPubMed

24.

Randver R. Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex to alleviate depression and cognitive impairment associated with Parkinson’s disease: a review and clinical implications. J Neurol Sci. 2018;393:88–99. https://doi.org/10.1016/j.jns.2018.08.014.CrossRefPubMed

25.

Lawrence BJ, Gasson N, Bucks RS, Troeung L, Loftus AM. Cognitive training and non-invasive brain stimulation for cognition in Parkinson's disease: a meta-analysis. Neurorehabil Neural Repair. 2017;31(7):597–608. https://doi.org/10.1177/1545968317712468 Epub 2017/06/07. PubMed PMID: 28583011.CrossRefPubMed

26.

Goodwill AM, Lum Jarrad AG, Hendy AM, et al. Using non-invasive transcranial stimulation to improve motor and cognitive function in Parkinson's disease: a systematic review and meta-analysis. Sci Rep. 2017;7:14840.CrossRef

27.

Cohen OS, Rigbi A, Yahalom G, et al. Repetitive deep TMS for Parkinson disease: a 3-month double-blind, randomized sham-controlled study. J Clinical Neurophysiol. 2018;35(2):159–65. https://doi.org/10.1097/wnp.0000000000000455 Epub 2018/01/27. PubMed PMID: 29373395.CrossRef

28.

Buard I, Sciacca DM, Martin CS, et al. Transcranial magnetic stimulation does not improve mild cognitive impairment in Parkinson’s disease. Mov Disord. 2018;33(3):489–91. https://doi.org/10.1002/mds.27246 Epub 2017/11/28. PubMed PMID: 29178298; PubMed Central PMCID: PMCPmc5839956.CrossRefPubMed

29.

Moher D, Schulz KF, Altman DG. The CONSORT statement: revised recommendations for improving the quality of reports of parallel group randomized trials. BMC Med Res Methodol. 2001;1:2. https://doi.org/10.1186/1471-2288-1-2.CrossRefPubMedPubMedCentral

30.

Boggio PS, Fregni F, Bermpohl F, et al. Effect of repetitive TMS and fluoxetine on cognitive function in patients with Parkinson’s disease and concurrent depression. Mov Disord. 2005;20(9):1178–84. https://doi.org/10.1002/mds.20508.CrossRefPubMed

31.

Cardoso EF, Fregni F, Martins MF, et al. rTMS treatment for depression in Parkinson’s disease increases BOLD responses in the left prefrontal cortex. Int J Neuropsychopharmacol. 2008;11(2):173–83. https://doi.org/10.1017/S1461145707007961.CrossRefPubMed

32.

Epstein CM, Evatt ML, Agnes F, et al. An open study of repetitive transcranial magnetic stimulation in treatment-resistant depression with Parkinson’s disease. Clin Neurophysiol. 2007;118(10):2189–94. https://doi.org/10.1016/j.clinph.2007.07.010.CrossRefPubMedPubMedCentral

33.

Benninger DH, Lomarev M, Wassermann EM, et al. Safety study of 50 Hz repetitive transcranial magnetic stimulation in patients with Parkinson's disease. Clin Neurophysiol. 2009;120(4):809–15. https://doi.org/10.1016/j.clinph.2009.01.012.CrossRefPubMedPubMedCentral

34.

Furukawa T, Izumi SI, Toyokura M, Masakado Y. Effects of low-frequency repetitive transcranial magnetic stimulation in Parkinson’s disease. Tokai J Exp Clin Med. 2009;34(3):63–71.PubMed

35.

Sedlackova S, Rektorova I, Srovnalova H, Rektor I. Effect of high frequency repetitive transcranial magnetic stimulation on reaction time, clinical features and cognitive functions in patients with Parkinson's disease. J Neural Transm (Vienna). 2009;116(9):1093–101. https://doi.org/10.1007/s00702-009-0259-0.CrossRef

36.

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(14):2311–7. https://doi.org/10.1002/mds.23270.CrossRefPubMed

37.

Kimura H, Kurimura M, Kurokawa K, et al. A comprehensive study of repetitive transcranial magnetic stimulation in Parkinson’s disease. ISRN Neurol. 2011:845453. https://doi.org/10.5402/2011/845453.

38.

Srovnalova H, Marecek R, Kubikova R, Rektorova I. The role of the right dorsolateral prefrontal cortex in the tower of London task performance: repetitive transcranial magnetic stimulation study in patients with Parkinson’s disease. Exp Brain Res. 2012;223(2):251–7. https://doi.org/10.1007/s00221-012-3255-9.CrossRefPubMed

39.

Chang WH, Kim MS, Park E, et al. Effect of dual-mode and dual-site non-invasive brain stimulation on freezing of gait in patients with Parkinson disease. Arch Phys Med Rehabil. 2017;98(7):1283–90. https://doi.org/10.1016/j.apmr.2017.01.011.CrossRefPubMed

40.

Dagan M, Herman T, Mirelman A, Giladi N, Hausdorff JM. 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(8):2463–72. https://doi.org/10.1007/s00221-017-4981-9.CrossRefPubMed

41.

Duchek J, Cheney M, Ferraro F, Storandt M. Paired associate learning in senile dementia of the Alzheimer type. Arch Neurol. 1991;48:1038–40. https://doi.org/10.1001/archneur.1991.00530220054019.CrossRefPubMed

42.

Cicerone K, Dahlberg C, Kalmar K, et al. Evidence-based cognitive rehabilitation: recommendations for clinical practice. Arch Phys Med Rehabil. 2000;81:1596–615. https://doi.org/10.1053/apmr.2000.19240.CrossRefPubMed

43.

Cicerone K, Dahlberg C, Malec J, et al. Evidence-based cognitive rehabilitation: updated review of the literature from 1998 through 2002. Arch Phys Med Rehabil. 2005;86:1681–92. https://doi.org/10.1016/j.apmr.2005.03.024.CrossRefPubMed

44.

Forbes CE, Poore JC, Krueger F, et al. The role of executive function and the dorsolateral prefrontal cortex in the expression of neuroticism and conscientiousness. Soc Neurosci. 2014;9(2):139–51. https://doi.org/10.1080/17470919.2013.871333.CrossRefPubMed

45.

Liao X, Li G, Wang A, et al. Repetitive transcranial magnetic stimulation as an alternative therapy for cognitive impairment in Alzheimer's disease: a meta-analysis. J Alzheimers Dis. 2015;48(2):463–72. https://doi.org/10.3233/jad-150346 Epub 2015/09/25. PubMed PMID: 26402010.CrossRefPubMed

46.

Monsch AU, Bondi MW, Salmon DP, et al. Clinical validity of the Mattis dementia rating scale in detecting dementia of the Alzheimer type. A double cross-validation and application to a community-dwelling sample. Arch Neurol. 1995;52(9):899–904 Epub 1995/09/01. PubMed PMID: 7661728.CrossRef

47.

Litvan I, Goldman JG, Tröster AI, et al. Diagnostic criteria for mild cognitive impairment in Parkinson's disease: Movement Disorder Society task force guidelines. Mov Disord. 2012;27:349–56.CrossRef

48.

Moser DJ, Jorge RE, Manes F, Paradiso S, Benjamin ML, Robinson RG. Improved executive functioning following repetitive transcranial magnetic stimulation. Neurology. 2002;58(8):1288–90 Epub 2002/04/24. PubMed PMID: 11971103.CrossRef

49.

Dalrymple-Alford JC, Livingston L, MacAskill MR, et al. Characterizing mild cognitive impairment in Parkinson’s disease. Mov Disord. 2011;26(4):629–36. https://doi.org/10.1002/mds.23592 Epub 2011/02/03. PubMed PMID: 21287603.CrossRefPubMed

50.

Mamikonyan E, Moberg PJ, Siderowf A, et al. Mild cognitive impairment is common in Parkinson’s disease patients with normal Mini-Mental State Examination (MMSE) scores. Parkinsonism Relat Disord. 2009;15(3):226–31. https://doi.org/10.1016/j.parkreldis.2008.05.006 Epub 2008/07/04. PubMed PMID: 18595765; PubMed Central PMCID: PMCPmc2668811.CrossRefPubMed

51.

Sollinger AB, Goldstein FC, Lah JJ, Levey AI, Factor SA. Mild cognitive impairment in Parkinson’s disease: subtypes and motor characteristics. Parkinsonism Relat Disord. 2010;16(3):177–80. https://doi.org/10.1016/j.parkreldis.2009.11.002 Epub 2009/11/27. PubMed PMID: 19939721; PubMed Central PMCID: PMCPmc3622717.CrossRefPubMed

52.

Helmich RC, Siebner HR, Bakker M, Munchau A, Bloem BR. Repetitive transcranial magnetic stimulation to improve mood and motor function in Parkinson’s disease. J Neurol Sci. 2006;248(1–2):84–96. https://doi.org/10.1016/j.jns.2006.05.009 Epub 2006/06/24. PubMed PMID: 16793065.CrossRefPubMed

53.

Strafella AP, Paus T, Barrett J, Dagher A. Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. Neuroimage. 2001;13(6):1008.CrossRef

54.

Siebner HR, Rothwell J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res. 2003;148(1):1–16. https://doi.org/10.1007/s00221-002-1234-2 Epub 2002/12/13. PubMed PMID: 12478392.CrossRefPubMed

55.

Conca A, Peschina W, Konig P, Fritzsche H, Hausmann A. Effect of chronic repetitive transcranial magnetic stimulation on regional cerebral blood flow and regional cerebral glucose uptake in drug treatment-resistant depressives. A brief report. Neuropsychobiology. 2002;45(1):27–31. https://doi.org/10.1159/000048669 Epub 2002/01/23. PubMed PMID: 11803238.CrossRefPubMed

56.

Xie J, Chen J, Wei Q. Repetitive transcranial magnetic stimulation versus electroconvulsive therapy for major depression: a meta-analysis of stimulus parameter effects. Neurol Res. 2013;35(10):1084–91. https://doi.org/10.1179/1743132813Y.0000000245.CrossRefPubMed

57.

Teng S, Guo Z, Peng H, et al. High-frequency repetitive transcranial magnetic stimulation over the left DLPFC for major depression: session-dependent efficacy: a meta-analysis. Eur Psychiatry. 2017;41:75–84. https://doi.org/10.1016/j.eurpsy.2016.11.002.CrossRefPubMed

58.

Petersen RC, Roberts RO, Knopman DS, et al. Mild cognitive impairment: ten years later. Archives Neurol. 2009;66(12):1447–55. https://doi.org/10.1001/archneurol.2009.266 Epub 2009/12/17. PubMed PMID: 20008648; PubMed Central PMCID: PMCPmc3081688.CrossRef

59.

Litvan I, Aarsland D, Adler CH, et al. MDS Task Force on mild cognitive impairment in Parkinson’s disease: critical review of PD-MCI. Mov Disord. 2011;26(10):1814–24. https://doi.org/10.1002/mds.23823 Epub 2011/06/11. PubMed PMID: 21661055; PubMed Central PMCID: PMCPmc3181006.CrossRefPubMedPubMedCentral

60.

Bagherzadeh Y, Khorrami A, Zarrindast MR, Shariat SV, Pantazis D. Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex enhances working memory. Exp Brain Res. 2016;234(7):1807–18. https://doi.org/10.1007/s00221-016-4580-1.CrossRefPubMed

61.

Yang Z, Zhao X, Wang C, Chen H, Zhang Y. Neuroanatomic correlation of the post-stroke aphasias studied with imaging. Neurol Res. 2008;30(4):356–60. https://doi.org/10.1179/174313208X300332.CrossRefPubMed

62.

Ross E. Cerebral localization of functions and the neurology of language: fact versus fiction or is it something else? Neuroscientist. 2010;16(3):222–43. https://doi.org/10.1177/1073858409349899.CrossRefPubMed

63.

Zimmerer V, Watson S, Turkington D, Ferrier I, Hinzen W. Deictic and propositional meaning-new perspectives on language in schizophrenia. Front Psychiatry. 2017;8:17. https://doi.org/10.3389/fpsyt.2017.00017.CrossRefPubMedPubMedCentral

64.

Ikkai A, Curtis C. Common neural mechanisms supporting spatial working memory, attention and motor intention. Neuropsychologia. 2011;49(6):1428–34. https://doi.org/10.1016/j.neuropsychologia.2010.12.020.CrossRefPubMed

65.

Ipata A, Gee A, Bisley J, Goldberg M. Neurons in the lateral intraparietal area create a priority map by the combination of disparate signals. Exp Brain Res. 2009;192(3):479–88. https://doi.org/10.1007/s00221-008-1557-8.CrossRefPubMed

66.

Halligan P, Fink G, Marshall J, Vallar G. Spatial cognition: evidence from visual neglect. Trends Cogn Sci. 2003;7(3):125–33 PMID: 12639694.CrossRef

67.

Hilgetag CC, Kötter R, Théoret H, Claßen J, Wolters A, Pascual-Leone A. Bilateral competitive processing of visual spatial attention in the human brain. Neurocomputing. 2003;52(3):793–8. https://doi.org/10.1016/S0925-2312(02)00776-2.CrossRef

68.

Strafella AP, Ko JH, Monchi O. Therapeutic application of transcranial magnetic stimulation in Parkinson’s disease: the contribution of expectation. Neuroimage. 2006;31(4):1666–72. https://doi.org/10.1016/j.neuroimage.2006.02.005.CrossRefPubMedPubMedCentral

69.

Kim JY, Chung EJ, Lee WY, et al. Therapeutic effect of repetitive transcranial magnetic stimulation in Parkinson’s disease: analysis of [11C] raclopride PET study. Mov Disord. 2008;23(2):207–11. https://doi.org/10.1002/mds.21787.CrossRefPubMed

Title: Effect of rTMS on Parkinson’s cognitive function: a systematic review and meta-analysis
Authors: Yi Jiang
Zhiwei Guo
Morgan A. McClure
Lin He
Qiwen Mu
Publication date: 01-12-2020
Publisher: BioMed Central
Keywords: Repetitive Transcranial Magnetic Stimulation
Parkinson's Disease
Published in: BMC Neurology / Issue 1/2020
Electronic ISSN: 1471-2377
DOI: https://doi.org/10.1186/s12883-020-01953-4

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Effect of rTMS on Parkinson’s cognitive function: a systematic review and meta-analysis

Abstract

Background

Method

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Method

Results

Conclusions

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