Effectiveness of Repetitive Transcranial Magnetic Stimulation in Stroke Patients with Motor Dysfunction: A Systematic Review_Chinese Journal of Evidence-Based Medicine

Authors：

WANG Juan ¹ , ZHU Fen ¹ , WANG Pu ² ,  LIAO Weijing ¹ , GUO Yi ³ , LI Huagang ⁴

1. Department of Rehabilitation Medicine, Zhongnan Hospital, Wuhan University, Wuhan 430071, China;2. Department of Rehabilitation Medicine, West China Hospital, Sichuan University, Chengdu 610041, China;3. Department of Epidemiology, Public Health College, Wuhan University, Wuhan 430071, China;4. Department of Neurology, Zhongnan Hospital, Wuhan University, Wuhan 430071, China;

Corresponding author：

LIAO Weijing, Email: weijingliao@sina.com

Keywords：

Repetitive transcranial magnetic stimulation; Stroke; Motor function; Systematic review; Meta-analysis; Randomized controlled trial

DOI：

10.7507/1672-2531.20120228

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective 　To evaluate the effectiveness of repetitive transcranial magnetic stimulation (rTMS) in treating stroke patients with motor dysfunction.
Methods 　The Cochrane Library, MEDLINE, EMbase, CBM, CNKI and WanFang Data were searched from inception to January 2012, and the references of the included studies were also retrieved to collect the randomized controlled trials (RCTs) on rTMS in treating stroke patients with motor dysfunction. Two reviewers independently screened articles according to the inclusion and exclusion criteria, extracted data and evaluated the quality of the included studies. Then meta-analysis was performed using RevMan 5.0.2 software, and evidence quality and recommendation level were assessed using the GRADE system.
Results 　A total of 11 RCTs involving 376 patients were included. The results of meta-analysis (including 3 RCTs, low quality) showed that, compared with the routine rehabilitation treatment, 2 to 4 weeks of rTMS was much beneficial to stroke patients with motor dysfunction, with significant differences (WMD=11.02, 95%CI 2.56 to 19.47). The other 8 studies only adopted descriptive analysis accordingly.
Conclusion 　It is still uncertain of the effectiveness of rTMS in improving motor dysfunction of stroke patients, so rTMS should be applied with caution in clinic.

Citation： WANG Juan,ZHU Fen,WANG Pu,LIAO Weijing,GUO Yi,LI Huagang. Effectiveness of Repetitive Transcranial Magnetic Stimulation in Stroke Patients with Motor Dysfunction: A Systematic Review. Chinese Journal of Evidence-Based Medicine, 2012, 12(12): 1478-1488. doi: 10.7507/1672-2531.20120228 Copy

1.	Warlow C, Van Gijn J, Sandercock P, et al. Stroke: practical management. 3Ed. UK: Blackwell Publishing, 2008: 5-76.
2.	吴兆苏, 姚崇华, 赵冬. 我国人群脑卒中发病率、死亡率的流行病学研究. 中华流行病学杂志, 2003, 24(3): 236-239.
3.	World Health Organization.International classification of functioning, isability and health: ICF. Geneva: World Health Organization, 2001.
4.	Wade DT. Measurement in neurological rehabilitation. Curr Opin Neurol Neurosurg, 1992, 5(5): 682-686.
5.	Duncan PW, Zorowitz R, Bates B, et al. Management of Adult Stroke Rehabilitation Care: a clinical practice guideline. Stroke, 2005, 36(9): 100-143.
6.	Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulotion of human motor cortex. Lancet, 1985,1(8437): 1106-1107.
7.	Khedr EM, Ahmed MA, Fathy N, et al. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology, 2005, 65(3): 466-468.
8.	World Health Organisation. Cerebrovascular Disorders(Offset Publications). Geneva:World Health Organization, 1978.
9.	中华医学会全国第4次脑血管病学术会议. 各类脑血管疾病诊断要点. 中华神经科杂志, 1996, 29(6): 379-381.
10.	Fugl-Meyer AR, Jaasko L, Leyman I, et al. The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. Scand J Rehabil Med, 1975, 7(1): 13-31.
11.	Wolf SL, Thompson PA, Morris DA, et al. The EXCITE trial: attributes of the Wolf Motor Function Test in patients with subacute stroke. Neurorehabil Neural Repair, 2005, 19(3): 194-205.
12.	Uswatte G, Taub E, Morris D, et al. Reliability and validity of the upper-extremity motor activity log-14 for measuring real-world arm use. Stroke, 2005, 36(11): 2493-2496.
13.	Wade DT. Measuring arm impairment and disability after stroke. Int Disabil Stud, 1989, 11(2): 89-92.
14.	Lindmark B, Hamrin E. Evaluation of functional capacity after stroke as a basis for active intervention. Validation of a modified chart for motor capacity assessment. Scand J Rehabil Med, 1988, 20(3): 111-115.
15.	Boissy P, Bourbonnais D, Carlotti MM, et al. Maximal grip force in chronic stroke subjects and its relationship to global upper extremity function. Clin Rehabil, 1999, 13(4): 354-362.
16.	Jebsen RH, Taylor N, Trieschmann RB, et al. An objective and standardized test of hand function. Arch Phys Med Rehabil, 1969, 50(6): 311-319.
17.	Bohannon RW, Melissa MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther, 1987, 67(2): 206-207.
18.	de Caneda MA, Fernandes JG, de Almeida AG, et al. Reliability of neurological assessment scales in patients with stroke. Arq Neuropsiquiatr, 2006, 64(3A): 690-697.
19.	Mansur CG, Fregni F, Boggio PS, et al. A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology, 2005, 64(10): 1802-1804.
20.	Fregni F, Boggio PS, Mansur CG, et al. Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. Neuroreport, 2005, 16(14): 1551-1555.
21.	Hamrin E, Wohlin AI. Evaluation of the functional capacity of stroke patients through an activity index. Scand J Rehabil Med, 1982, 14(3): 93-100.
22.	Atkins D, Best D, Briss PA, et al. Grading quality of evidence and strength of recommendations. BMJ (Clinical research ed.), 2004, 328(7454): 1490.
23.	Higgins JPT, Green S. Cochrance Handbook for Systematic Reviews of Interventions 4.2.6 2006: The Cochrane Collaboration.
24.	Fregni F, Boggio PS, Valle AC, et al. A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients. Stroke, 2006, 37(8): 2115-2122.
25.	Malcolm MP, Triggs WJ, Light KE, et al. Repetitive transcranial magnetic stimulation as an adjunct to constraint-induced therapy: an exploratory randomized controlled trial. Am J Phys Med Rehabil, 2007, 86(9): 707-715.
26.	Takeuchi N, Tada T, Toshima M, et al. Inhibition of the unaffected motor cortex by 1 HZ repetitive transcranial magnetiv stimulation enhances motor performance and training effect paretic hand in patients with chronic stroke. J Rehabil Med, 2008, 40(4): 298-303.
27.	Khedr EM, Abedl-Fadeil MR, Farghali A, et al. Role of 1 and 3 Hz repetitive transcranial magnetic stimulation on motor function recovery after acute ischaemic stroke. Eur J Neurol, 2009, 16(12): 1323-1330.
28.	Khedr EM, Etraby AE, Hemeda M, et al. Long-term effect of repetitive transcranial magnetic stimulation on motor function recovery after acute ischemic stroke. Acta Neurol Scand, 2010, 121(1): 30-37.
29.	Emara TH, Moustafa RR, ElNahas NM, et al. Repetitive transcranial magnetic stimulation at 1Hz and 5Hz produces sustained improvement in motor function and disability after ischaemic stroke. Eur J Neurol, 2010, 17(9): 1203-1209.
30.	Chang WH, Kim YH, Bang OY, et al. Long-term effects of rTMS on motor recovery in patients after Subacute Storke. J Rehabit Med, 2010, 42(8): 758-764.
31.	Conforto AB, Anjos SM, Saposnik G, et al. Transcranial magnetic stimulation in mild to severe hemiparesis early after stroke: a proof of principle and novel approach to improve motor function. J Neurol, 2012, 259(7): 1399-1405.
32.	池登科, 吴爱玲, 龚凌云, 等. 重复经颅磁刺激在卒中后运动功能康复中的作用. 中西医结合心脑血管病杂志, 2008, 6(6): 743-744.
33.	饶江, 由丽, 邵伟波, 等. 重复经颅磁刺激对卒中后运动功能康复的临床观察. 中国民康医学, 2010, 22(21): 2712-2713.
34.	吴小丽, 吴宏胜, 谢德丰, 等. 重复经颅磁刺激在脑梗塞运动功能康复中的作用. 海南医学院学报, 2010, 16(6): 799-801.
35.	曾宪涛, 冷卫东, 李胜, 等. 如何正确理解及使用GRADE系统. 中国循证医学杂志, 2011, 11(9): 985-990.
36.	Ziemann U. Improving disability in stroke with RTMS. Lancet Neurol, 2005, 4(8): 454-455.
37.	Nowak DA, Grefkes C, Dafotakis M, et al. Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. Arch Neurol, 2008, 65(6): 741-747.
38.	Takeuchi N, Chuma T, Matsuo Y, et al. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke, 2005, 36(12): 2681-2686.
39.	Ward NS, Brown MM, Thompson AJ, et al. Neural correlates of outcome after stroke：across-sectional fMRI study. Brain, 2003, 126(Pt6): 1430-1448.
40.	Gorsler A, Bäumer T, Weiller C, et al. Interhemispheric effects of high and low frequency rTMS in healthy humans. Clin Neurophysiol, 2003, 114(10): 1800-1807.
41.	Gangitano M, Valero-Cabré A, Tormos JM, et al. Modulation of input-output curves by low and high frequency repetitive transcranial magnetic stimulation of the motor cortex. Clin Neurophysiol, 2002, 113(8): 1249-1257.
42.	Fitzgerald PB, Fountain S, Daskalakis ZJ. A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol, 2006, 117(12): 2584-2596.
43.	Wassermann EM, Lisanby SH. Therapeutic application of repetitive transeranial magnetic stimulation: a review. Clin Neurophysiol, 2001, 112(8): 1367-1377.
44.	Lazzaro VD, Dileone M, Profice P, et al. Direct demonstration that repetitive transcranial tmagnetic stimulation can enhance corticospinal excitability in stroke. Stroke, 2006, 37(11): 2850-2853.
45.	Huang YZ, Edwards MJ, Rounis E, et al. Theta burst stimulation of the human motor cortex. Neuron, 2005, 45(2): 201-206.
46.	Pascual-Leone A, Vails-Sole J, Wassermann EM, et al. Response to rapid-rate transcranial magnetite stimulation of the human motor cortex. Brain, 1994, 117(Pt4): 847-858.
47.	Chen R, Classen J, Gerloff C, et al. Depression of motor cortex excitability by low frequency transcranial magnetic stimulation. Neurology, 1997, 48(5): 1398-1403.
48.	Helmieh RC, Siebner HR, Bakker M, et al. Repetitive transcranial magnetic stimulation to improve mood and motor function in Parkinson’s disease. Neurol Sci, 2006, 248(2): 84-96.
49.	庄立. 重复经颅磁刺激改善缺血性脑卒中动功能的作用机制. 中国神经免疫学和神经病学杂志, 2009, 16(3): 213-216.
50.	Murase N, Duque J, Mazzocchio R, et al. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol, 2004, 55(3): 400-409.
51.	Khedr EM, Ahmed MA, Fathy N, et al. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology, 2005, 65(3): 466-468.
52.	Pal PK, Hanajirna R, Gmraj CA, et al. Effect of low-frequency repetitive transcranial magnetic stimulation on interhemispheric inhibition. J Neurophysiol, 2005, 94(3): 1668-1675.
53.	Jung SH, Shin JE, Jeong YS, et al. Changes in motor cortical excitability induced by high-frequency repetitive transcranial magnetic stimulation of different stimulation durations. Clin Neurophysiol, 2008, 119(1): 71-79.
54.	Küçükdeveci AA, Tennant A, Grimby G, et al. Strategies for assessment and outcome measurement in physical and rehabilitation medicine: an educational review. J Rehabil Med, 2011, 43(8): 661-672.
55.	Barak S, Duncan PW. Issues in Selecting Outcome Measures to Assess Functional Recovery After Stroke. NeuroRx, 2006, 3(4): 505-524.

1. Warlow C, Van Gijn J, Sandercock P, et al. Stroke: practical management. 3Ed. UK: Blackwell Publishing, 2008: 5-76.
2. 吴兆苏, 姚崇华, 赵冬. 我国人群脑卒中发病率、死亡率的流行病学研究. 中华流行病学杂志, 2003, 24(3): 236-239.
3. World Health Organization.International classification of functioning, isability and health: ICF. Geneva: World Health Organization, 2001.
4. Wade DT. Measurement in neurological rehabilitation. Curr Opin Neurol Neurosurg, 1992, 5(5): 682-686.
5. Duncan PW, Zorowitz R, Bates B, et al. Management of Adult Stroke Rehabilitation Care: a clinical practice guideline. Stroke, 2005, 36(9): 100-143.
6. Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulotion of human motor cortex. Lancet, 1985,1(8437): 1106-1107.
7. Khedr EM, Ahmed MA, Fathy N, et al. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology, 2005, 65(3): 466-468.
8. World Health Organisation. Cerebrovascular Disorders(Offset Publications). Geneva:World Health Organization, 1978.
9. 中华医学会全国第4次脑血管病学术会议. 各类脑血管疾病诊断要点. 中华神经科杂志, 1996, 29(6): 379-381.
10. Fugl-Meyer AR, Jaasko L, Leyman I, et al. The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. Scand J Rehabil Med, 1975, 7(1): 13-31.
11. Wolf SL, Thompson PA, Morris DA, et al. The EXCITE trial: attributes of the Wolf Motor Function Test in patients with subacute stroke. Neurorehabil Neural Repair, 2005, 19(3): 194-205.
12. Uswatte G, Taub E, Morris D, et al. Reliability and validity of the upper-extremity motor activity log-14 for measuring real-world arm use. Stroke, 2005, 36(11): 2493-2496.
13. Wade DT. Measuring arm impairment and disability after stroke. Int Disabil Stud, 1989, 11(2): 89-92.
14. Lindmark B, Hamrin E. Evaluation of functional capacity after stroke as a basis for active intervention. Validation of a modified chart for motor capacity assessment. Scand J Rehabil Med, 1988, 20(3): 111-115.
15. Boissy P, Bourbonnais D, Carlotti MM, et al. Maximal grip force in chronic stroke subjects and its relationship to global upper extremity function. Clin Rehabil, 1999, 13(4): 354-362.
16. Jebsen RH, Taylor N, Trieschmann RB, et al. An objective and standardized test of hand function. Arch Phys Med Rehabil, 1969, 50(6): 311-319.
17. Bohannon RW, Melissa MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther, 1987, 67(2): 206-207.
18. de Caneda MA, Fernandes JG, de Almeida AG, et al. Reliability of neurological assessment scales in patients with stroke. Arq Neuropsiquiatr, 2006, 64(3A): 690-697.
19. Mansur CG, Fregni F, Boggio PS, et al. A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology, 2005, 64(10): 1802-1804.
20. Fregni F, Boggio PS, Mansur CG, et al. Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. Neuroreport, 2005, 16(14): 1551-1555.
21. Hamrin E, Wohlin AI. Evaluation of the functional capacity of stroke patients through an activity index. Scand J Rehabil Med, 1982, 14(3): 93-100.
22. Atkins D, Best D, Briss PA, et al. Grading quality of evidence and strength of recommendations. BMJ (Clinical research ed.), 2004, 328(7454): 1490.
23. Higgins JPT, Green S. Cochrance Handbook for Systematic Reviews of Interventions 4.2.6 2006: The Cochrane Collaboration.
24. Fregni F, Boggio PS, Valle AC, et al. A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients. Stroke, 2006, 37(8): 2115-2122.
25. Malcolm MP, Triggs WJ, Light KE, et al. Repetitive transcranial magnetic stimulation as an adjunct to constraint-induced therapy: an exploratory randomized controlled trial. Am J Phys Med Rehabil, 2007, 86(9): 707-715.
26. Takeuchi N, Tada T, Toshima M, et al. Inhibition of the unaffected motor cortex by 1 HZ repetitive transcranial magnetiv stimulation enhances motor performance and training effect paretic hand in patients with chronic stroke. J Rehabil Med, 2008, 40(4): 298-303.
27. Khedr EM, Abedl-Fadeil MR, Farghali A, et al. Role of 1 and 3 Hz repetitive transcranial magnetic stimulation on motor function recovery after acute ischaemic stroke. Eur J Neurol, 2009, 16(12): 1323-1330.
28. Khedr EM, Etraby AE, Hemeda M, et al. Long-term effect of repetitive transcranial magnetic stimulation on motor function recovery after acute ischemic stroke. Acta Neurol Scand, 2010, 121(1): 30-37.
29. Emara TH, Moustafa RR, ElNahas NM, et al. Repetitive transcranial magnetic stimulation at 1Hz and 5Hz produces sustained improvement in motor function and disability after ischaemic stroke. Eur J Neurol, 2010, 17(9): 1203-1209.
30. Chang WH, Kim YH, Bang OY, et al. Long-term effects of rTMS on motor recovery in patients after Subacute Storke. J Rehabit Med, 2010, 42(8): 758-764.
31. Conforto AB, Anjos SM, Saposnik G, et al. Transcranial magnetic stimulation in mild to severe hemiparesis early after stroke: a proof of principle and novel approach to improve motor function. J Neurol, 2012, 259(7): 1399-1405.
32. 池登科, 吴爱玲, 龚凌云, 等. 重复经颅磁刺激在卒中后运动功能康复中的作用. 中西医结合心脑血管病杂志, 2008, 6(6): 743-744.
33. 饶江, 由丽, 邵伟波, 等. 重复经颅磁刺激对卒中后运动功能康复的临床观察. 中国民康医学, 2010, 22(21): 2712-2713.
34. 吴小丽, 吴宏胜, 谢德丰, 等. 重复经颅磁刺激在脑梗塞运动功能康复中的作用. 海南医学院学报, 2010, 16(6): 799-801.
35. 曾宪涛, 冷卫东, 李胜, 等. 如何正确理解及使用GRADE系统. 中国循证医学杂志, 2011, 11(9): 985-990.
36. Ziemann U. Improving disability in stroke with RTMS. Lancet Neurol, 2005, 4(8): 454-455.
37. Nowak DA, Grefkes C, Dafotakis M, et al. Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. Arch Neurol, 2008, 65(6): 741-747.
38. Takeuchi N, Chuma T, Matsuo Y, et al. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke, 2005, 36(12): 2681-2686.
39. Ward NS, Brown MM, Thompson AJ, et al. Neural correlates of outcome after stroke：across-sectional fMRI study. Brain, 2003, 126(Pt6): 1430-1448.
40. Gorsler A, Bäumer T, Weiller C, et al. Interhemispheric effects of high and low frequency rTMS in healthy humans. Clin Neurophysiol, 2003, 114(10): 1800-1807.
41. Gangitano M, Valero-Cabré A, Tormos JM, et al. Modulation of input-output curves by low and high frequency repetitive transcranial magnetic stimulation of the motor cortex. Clin Neurophysiol, 2002, 113(8): 1249-1257.
42. Fitzgerald PB, Fountain S, Daskalakis ZJ. A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol, 2006, 117(12): 2584-2596.
43. Wassermann EM, Lisanby SH. Therapeutic application of repetitive transeranial magnetic stimulation: a review. Clin Neurophysiol, 2001, 112(8): 1367-1377.
44. Lazzaro VD, Dileone M, Profice P, et al. Direct demonstration that repetitive transcranial tmagnetic stimulation can enhance corticospinal excitability in stroke. Stroke, 2006, 37(11): 2850-2853.
45. Huang YZ, Edwards MJ, Rounis E, et al. Theta burst stimulation of the human motor cortex. Neuron, 2005, 45(2): 201-206.
46. Pascual-Leone A, Vails-Sole J, Wassermann EM, et al. Response to rapid-rate transcranial magnetite stimulation of the human motor cortex. Brain, 1994, 117(Pt4): 847-858.
47. Chen R, Classen J, Gerloff C, et al. Depression of motor cortex excitability by low frequency transcranial magnetic stimulation. Neurology, 1997, 48(5): 1398-1403.
48. Helmieh RC, Siebner HR, Bakker M, et al. Repetitive transcranial magnetic stimulation to improve mood and motor function in Parkinson’s disease. Neurol Sci, 2006, 248(2): 84-96.
49. 庄立. 重复经颅磁刺激改善缺血性脑卒中动功能的作用机制. 中国神经免疫学和神经病学杂志, 2009, 16(3): 213-216.
50. Murase N, Duque J, Mazzocchio R, et al. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol, 2004, 55(3): 400-409.
51. Khedr EM, Ahmed MA, Fathy N, et al. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology, 2005, 65(3): 466-468.
52. Pal PK, Hanajirna R, Gmraj CA, et al. Effect of low-frequency repetitive transcranial magnetic stimulation on interhemispheric inhibition. J Neurophysiol, 2005, 94(3): 1668-1675.
53. Jung SH, Shin JE, Jeong YS, et al. Changes in motor cortical excitability induced by high-frequency repetitive transcranial magnetic stimulation of different stimulation durations. Clin Neurophysiol, 2008, 119(1): 71-79.
54. Küçükdeveci AA, Tennant A, Grimby G, et al. Strategies for assessment and outcome measurement in physical and rehabilitation medicine: an educational review. J Rehabil Med, 2011, 43(8): 661-672.
55. Barak S, Duncan PW. Issues in Selecting Outcome Measures to Assess Functional Recovery After Stroke. NeuroRx, 2006, 3(4): 505-524.

Chinese Journal of Evidence-Based Medicine

Effectiveness of Repetitive Transcranial Magnetic Stimulation in Stroke Patients with Motor Dysfunction: A Systematic Review

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