Efficacy of repetitive transcranial magnetic stimulation (rTMS) on rehabilitation of unilateral neglect in patients with stroke: a systematic review_Chinese Journal of Evidence-Based Medicine

Authors：

ZHANG Qing ^1,2 , XIAO Hongqi ^1,2 , YU Jiadan ^1,2 , XU Yang ^1,2 , YANG Yonghong ^1,2 ,  WANG Pu ³

1. Rehabilitation Medicine Center, West China Hospital of Sichuan University, Chengdu, 610041, P.R.China;
2. School of Rehabilitation Sciences, West China Medical School of Sichuan University, Chengdu, 610041, P.R.China;
3. Department of Rehabilitation Medicine, Ruijin Hospital Affiliated to Shanghai Jiaotong University School of Medicine, Shanghai, 200025, P.R.China;

Corresponding author：

WANG Pu, Email: wangpu_03@126.com

Keywords：

Transcranial magnetic stimulation; Unilateral neglect; Stroke; Systematic review; Meta-analysis; Randomized controlled trial

DOI：

10.7507/1672-2531.201705048

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ObjectivesTo systematically review the efficacy of repetitive transcranial magnetic stimulation (rTMS) on rehabilitation of unilateral neglect in stroke patients.MethodsPubMed, The Cochrane Library, PEDro, EMbase, CNKI, WanFang Data and VIP databases were searched online for randomized controlled trials (RCTs) of rTMS on rehabilitation of unilateral neglect in stroke patients from inception to March 2017. Two reviewers independently screened literature, extracted data and assessed the quality of included studies. Meta-analysis was then performed by using RevMan 5.3 software.ResultsA total of 12 RCTs involving 303 patients were included. The results of meta-analysis showed that: the stimulate group was superior to the control group in line bisection test (MD=–5.54, 95%CI –6.79 to –4.29, P<0.000 01), line cancellation test (MD=–3.75, 95%CI –4.60 to –2.90,P<0.000 1) and star cancellation test (MD=–22.94, 95%CI –26.52 to –19.35,P<0.000 01). However, there was no significant difference in the score of the modified Barthel index between two groups (MD=3.91, 95%CI–9.52 to 17.34,P=0.57).ConclusionsrTMS appears to improve the symptoms of unilateral neglect in stroke patients. Due to limited quality and quantity of the included studies, more high quality studies are needed to verify above conclusions.

Citation： ZHANG Qing, XIAO Hongqi, YU Jiadan, XU Yang, YANG Yonghong, WANG Pu. Efficacy of repetitive transcranial magnetic stimulation (rTMS) on rehabilitation of unilateral neglect in patients with stroke: a systematic review. Chinese Journal of Evidence-Based Medicine, 2018, 18(2): 163-171. doi: 10.7507/1672-2531.201705048 Copy

1.	Mesulam MM. Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philos Trans R Soc Lond B Biol Sci, 1999, 354(1387): 1325-1346.
2.	Heilman KM, Watson RT, Valenstein E. Neglect and related disorders. Clin Neuropsychol (4th Edition). Oxford University Press, 2003: 296-346.
3.	Stone SP, Halligan PW, Greenwood RJ. The incidence of neglect phenomena and related disorders in patients with an acute right or left hemisphere stroke. Age Ageing, 1993, 22(1): 46-52.
4.	Ringman JM, Saver JL, Woolson RF, et al. Frequency, risk factors, anatomy, and course of unilateral neglect in an acute stroke cohort. Neurology, 2004, 63(3): 468-474.
5.	Karnath HO, Rennig J, Johannsen L, et al. The anatomy underlying acute versus chronic spatial neglect: a longitudinal study. Brain, 2011, 134(Pt 3): 903-912.
6.	Yang NY, Zhou D, Chung RC, et al. Rehabilitation Interventions for Unilateral Neglect after Stroke: A Systematic Review from 1997 through 2012. Front Hum Neurosci, 2013, 7: 187.
7.	Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol, 2003, 2(3): 145-156.
8.	Huang YZ, Rothwell JC. The effect of short-duration bursts of high-frequency, low-intensity transcranial magnetic stimulation on the human motor cortex. Clin Neurophysiol, 2004, 115(5): 1069-1075.
9.	Cárdenas-Morales L, Nowak DA, Kammer T, et al. Mechanisms and applications of theta-burst rTMS on the human motor cortex. Brain Topogr, 2010, 22(4): 294-306.
10.	Lefaucheur JP, André-Obadia N, Antal A, et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol, 2014, 125(11): 2150-2206.
11.	杨雨洁, 朱毅, 程洁, 等. 重复经颅磁刺激治疗卒中后单侧空间忽略的Meta分析. 中国康复理论与实践, 2017, 23(3): 363-369.
12.	Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions version 5.1.0. Cochrane Collaboration, 2011. Available at: www.cochrane-handbook.org.
13.	Song W, Du B, Xu Q, et al. Low-frequency transcranial magnetic stimulation for visual spatial neglect: a pilot study. J Rehabil Med, 2009, 41(3): 162-165.
14.	胡洁, 杜博琪, 岳月红, 等. 重复经颅磁刺激的累积效应在治疗偏侧忽略中的作用研究. 中国康复医学杂志, 2010, 25(4): 311-314.
15.	Koch G, Bonnì S, Giacobbe V, et al. θ-burst stimulation of the left hemisphere accelerates recovery of hemispatial neglect. Neurology, 2012, 78(1): 24-30.
16.	Cazzoli D, Müri RM, Schumacher R, et al. Theta burst stimulation reduces disability during the activities of daily living in spatial neglect. Brain, 2012, 135(Pt 11): 3426-3439.
17.	张艳明, 付伟, 胡洁, 等. 行为学疗法联合重复经颅磁刺激治疗脑卒中后偏侧空间忽略的疗效观察. 中华物理医学与康复杂志, 2012, 34(12): 915-917.
18.	Kim BR, Chun MH, Kim DY, et al. Effect of high- and low-frequency repetitive transcranial magnetic stimulation on visuospatial neglect in patients with acute stroke: a double-blind, sham-controlled trial. Arch Phys Med Rehabil, 2013, 94(5): 803-807.
19.	Cha HG, Kim MK. The effects of repetitive transcranial magnetic stimulation on unilateral neglect of acute stroke patients: A randomized controlled trial. Hong Kong Physiother J, 2015, 33(2): 53-58.
20.	Fu W, Song W, Zhang Y, et al. Long-term effects of continuous theta-burst stimulation in visuospatial neglect. J Int Med Res, 2015, 43(2): 196-203.
21.	Yang W, Liu TT, Song XB, et al. Comparison of different stimulation parameters of repetitive transcranial magnetic stimulation for unilateral spatial neglect in stroke patients. J Neurol Sci, 2015, 359(1-2): 219-225.
22.	Cha HG, Kim MK. Effects of repetitive transcranial magnetic stimulation on arm function and decreasing unilateral spatial neglect in subacute stroke: a randomized controlled trial. Clin Rehabil, 2016, 30(7): 649-656.
23.	杨初燕, 张锡泉, 陈正威, 等. 高频重复经颅磁刺激治疗脑卒中患者单侧空间忽略的功能磁共振研究. 中国康复医学杂志, 2016, 31(10): 1088-1093.
24.	Yang NY, Fong KN, Li-Tsang CW, et al. Effects of repetitive transcranial magnetic stimulation combined with sensory cueing on unilateral neglect in subacute patients with right hemispheric stroke: a randomized controlled study. Clin Rehabil, 2016, 31(9): 1154-1163.
25.	Cermak SA, Hausser J. The behavioral inattention test for unilateral visual neglect. Phys Occup Ther Geriatr, 1989, 7(3): 43-53.
26.	Chen P, Hreha K, Fortis P, et al. Functional assessment of spatial neglect: a review of the Catherine Bergego scale and an introduction of the Kessler foundation neglect assessment process. Top Stroke Rehabil, 2012, 19(5): 423-435.
27.	Albert ML. A simple test of visual neglect. Neurology, 1973, 23(6): 658-664.
28.	Menon A, Korner-Bitensky N. Evaluating unilateral spatial neglect post stroke: working your way through the maze of assessment choices. Top Stroke Rehabil, 2004, 11(3): 41-66.
29.	Azouvi P. The ecological assessment of unilateral neglect. Ann Phys Rehabil Med, 2017, 60(3): 186-190.
30.	Wassermann EM, Lisanby SH. Therapeutic application of repetitive transcranial magnetic stimulation: a review. Clin Neurophysiol, 2001, 112(8): 1367-1377.
31.	Cazzoli D, Müri RM, Hess CW, et al. Treatment of hemispatial neglect by means of rTMS--a review. Restor Neurol Neurosci, 2010, 28(4): 499-510.
32.	Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. Electroencephalogr Clin Neurophysiol, 1998, 108(1): 1-16.

1. Mesulam MM. Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philos Trans R Soc Lond B Biol Sci, 1999, 354(1387): 1325-1346.
2. Heilman KM, Watson RT, Valenstein E. Neglect and related disorders. Clin Neuropsychol (4th Edition). Oxford University Press, 2003: 296-346.
3. Stone SP, Halligan PW, Greenwood RJ. The incidence of neglect phenomena and related disorders in patients with an acute right or left hemisphere stroke. Age Ageing, 1993, 22(1): 46-52.
4. Ringman JM, Saver JL, Woolson RF, et al. Frequency, risk factors, anatomy, and course of unilateral neglect in an acute stroke cohort. Neurology, 2004, 63(3): 468-474.
5. Karnath HO, Rennig J, Johannsen L, et al. The anatomy underlying acute versus chronic spatial neglect: a longitudinal study. Brain, 2011, 134(Pt 3): 903-912.
6. Yang NY, Zhou D, Chung RC, et al. Rehabilitation Interventions for Unilateral Neglect after Stroke: A Systematic Review from 1997 through 2012. Front Hum Neurosci, 2013, 7: 187.
7. Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol, 2003, 2(3): 145-156.
8. Huang YZ, Rothwell JC. The effect of short-duration bursts of high-frequency, low-intensity transcranial magnetic stimulation on the human motor cortex. Clin Neurophysiol, 2004, 115(5): 1069-1075.
9. Cárdenas-Morales L, Nowak DA, Kammer T, et al. Mechanisms and applications of theta-burst rTMS on the human motor cortex. Brain Topogr, 2010, 22(4): 294-306.
10. Lefaucheur JP, André-Obadia N, Antal A, et al. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol, 2014, 125(11): 2150-2206.
11. 杨雨洁, 朱毅, 程洁, 等. 重复经颅磁刺激治疗卒中后单侧空间忽略的Meta分析. 中国康复理论与实践, 2017, 23(3): 363-369.
12. Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions version 5.1.0. Cochrane Collaboration, 2011. Available at: www.cochrane-handbook.org.
13. Song W, Du B, Xu Q, et al. Low-frequency transcranial magnetic stimulation for visual spatial neglect: a pilot study. J Rehabil Med, 2009, 41(3): 162-165.
14. 胡洁, 杜博琪, 岳月红, 等. 重复经颅磁刺激的累积效应在治疗偏侧忽略中的作用研究. 中国康复医学杂志, 2010, 25(4): 311-314.
15. Koch G, Bonnì S, Giacobbe V, et al. θ-burst stimulation of the left hemisphere accelerates recovery of hemispatial neglect. Neurology, 2012, 78(1): 24-30.
16. Cazzoli D, Müri RM, Schumacher R, et al. Theta burst stimulation reduces disability during the activities of daily living in spatial neglect. Brain, 2012, 135(Pt 11): 3426-3439.
17. 张艳明, 付伟, 胡洁, 等. 行为学疗法联合重复经颅磁刺激治疗脑卒中后偏侧空间忽略的疗效观察. 中华物理医学与康复杂志, 2012, 34(12): 915-917.
18. Kim BR, Chun MH, Kim DY, et al. Effect of high- and low-frequency repetitive transcranial magnetic stimulation on visuospatial neglect in patients with acute stroke: a double-blind, sham-controlled trial. Arch Phys Med Rehabil, 2013, 94(5): 803-807.
19. Cha HG, Kim MK. The effects of repetitive transcranial magnetic stimulation on unilateral neglect of acute stroke patients: A randomized controlled trial. Hong Kong Physiother J, 2015, 33(2): 53-58.
20. Fu W, Song W, Zhang Y, et al. Long-term effects of continuous theta-burst stimulation in visuospatial neglect. J Int Med Res, 2015, 43(2): 196-203.
21. Yang W, Liu TT, Song XB, et al. Comparison of different stimulation parameters of repetitive transcranial magnetic stimulation for unilateral spatial neglect in stroke patients. J Neurol Sci, 2015, 359(1-2): 219-225.
22. Cha HG, Kim MK. Effects of repetitive transcranial magnetic stimulation on arm function and decreasing unilateral spatial neglect in subacute stroke: a randomized controlled trial. Clin Rehabil, 2016, 30(7): 649-656.
23. 杨初燕, 张锡泉, 陈正威, 等. 高频重复经颅磁刺激治疗脑卒中患者单侧空间忽略的功能磁共振研究. 中国康复医学杂志, 2016, 31(10): 1088-1093.
24. Yang NY, Fong KN, Li-Tsang CW, et al. Effects of repetitive transcranial magnetic stimulation combined with sensory cueing on unilateral neglect in subacute patients with right hemispheric stroke: a randomized controlled study. Clin Rehabil, 2016, 31(9): 1154-1163.
25. Cermak SA, Hausser J. The behavioral inattention test for unilateral visual neglect. Phys Occup Ther Geriatr, 1989, 7(3): 43-53.
26. Chen P, Hreha K, Fortis P, et al. Functional assessment of spatial neglect: a review of the Catherine Bergego scale and an introduction of the Kessler foundation neglect assessment process. Top Stroke Rehabil, 2012, 19(5): 423-435.
27. Albert ML. A simple test of visual neglect. Neurology, 1973, 23(6): 658-664.
28. Menon A, Korner-Bitensky N. Evaluating unilateral spatial neglect post stroke: working your way through the maze of assessment choices. Top Stroke Rehabil, 2004, 11(3): 41-66.
29. Azouvi P. The ecological assessment of unilateral neglect. Ann Phys Rehabil Med, 2017, 60(3): 186-190.
30. Wassermann EM, Lisanby SH. Therapeutic application of repetitive transcranial magnetic stimulation: a review. Clin Neurophysiol, 2001, 112(8): 1367-1377.
31. Cazzoli D, Müri RM, Hess CW, et al. Treatment of hemispatial neglect by means of rTMS--a review. Restor Neurol Neurosci, 2010, 28(4): 499-510.
32. Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. Electroencephalogr Clin Neurophysiol, 1998, 108(1): 1-16.

Chinese Journal of Evidence-Based Medicine

Efficacy of repetitive transcranial magnetic stimulation (rTMS) on rehabilitation of unilateral neglect in patients with stroke: a systematic review

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