|
 
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| REVIEW |
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| Year : 2023 | Volume
: 2
| Issue : 1 | Page : 1-12 |
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Effectiveness of repetitive transcranial magnetic stimulation on post-stroke unilateral spatial neglect: a systematic review and meta-analysis
Xiao-Lin Li1, Xiao-Dan Liu1, Bo Chen2, Zhi-Xing Zhou3, Chunlei Shan1
1 School of Rehabilitation Science, Shanghai University of Traditional Chinese Medicine, Shanghai, China
2 Department of Rehabilitation, The Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan Province, China
3 The Faculty of Health and Social Sciences, The Hong Kong Polytechnic University, Hong Kong Special Administrative Region, China
| Date of Submission | 19-Oct-2021 |
| Date of Decision | 16-Dec-2022 |
| Date of Acceptance | 13-Mar-2023 |
| Date of Web Publication | 28-Mar-2023 |
Correspondence Address:
Xiao-Dan Liu
School of Rehabilitation Science, Shanghai University of Traditional Chinese Medicine, Shanghai
China
 Source of Support: None, Conflict of Interest: None
DOI: 10.4103/2773-2398.372306
Post-stroke cognitive impairment refers to the cognitive impairment caused by stroke. Unilateral spatial neglect is the main symptom and results in remarkably lower independence in activities of daily living and participation. Recent studies suggested that repetitive transcranial magnetic stimulation (rTMS) may have a positive effect on post-stroke cognitive impairment, but no relevant systematic review has been conducted on post-stroke cognitive impairment, especially unilateral spatial neglect. Therefore, relevant studies on rTMS in the treatment of post-stroke were collected and analyzed by systematic review and meta-analysis to determine whether rTMS can improve the cognitive function of patients, especially post-stroke unilateral spatial neglect, to provide reliable evidence for rTMS intervention. PubMed, Cochrane Central Register of Controlled Trials, Embase, PsycINFO databases, Web of Science and CINAHL were searched up to February 3, 2021. Three authors screened the reviews and independently assessed their methodological quality using the Jadad scale. The number of studies finally pooled was 28, and the sample size was 819. In the overall cognition function, the efficacy of the intervention group was superior to that of the control group. This meta-analysis result indicated that rTMS influences unilateral spatial neglect. rTMS was effective in improving patients’ activities of daily living. Subgroup analysis showed the preferred items in selecting frequency pulses and session. Furthermore, rTMS could not improve unilateral spatial neglect with an onset time of less than 1 month and over 1 month. This meta-analysis shows that rTMS intervention may be a promising way to treat post-stroke cognitive impairment.
Keywords: cognitive function; rTMS; stroke; unilateral neglect
How to cite this article:
Li XL, Liu XD, Chen B, Zhou ZX, Shan C. Effectiveness of repetitive transcranial magnetic stimulation on post-stroke unilateral spatial neglect: a systematic review and meta-analysis. Brain Netw Modulation 2023;2:1-12 |
How to cite this URL:
Li XL, Liu XD, Chen B, Zhou ZX, Shan C. Effectiveness of repetitive transcranial magnetic stimulation on post-stroke unilateral spatial neglect: a systematic review and meta-analysis. Brain Netw Modulation [serial online] 2023 [cited 2023 Jun 4];2:1-12. Available from: http://www.bnmjournal.com/text.asp?2023/2/1/1/372306 |
| Introduction | |  |
Stroke is the leading cause of neurological disability, which has a long-term effect on patients. Approximately 30–40% of stroke survivors have cognitive impairment (Leys et al., 2005; Hu and Chen, 2017). Unilateral spatial neglect is one of the most common behavioral cognitive impairments that occur immediately after stroke. It is characterized by the loss of sensory perception of the injured contralateral limb and the neglect of any abnormalities in contralateral visual, auditory, tactile, spatial positioning, and other behavioral abilities. Its incidence ranges from 13% to 82% (Karnath et al., 2011). Unilateral spatial neglect increases the risk of falls and results in tremendous restrictions in activity participation and activities of daily living (ADLs) (Campbell and Matthews, 2010). The main treatment interventions focus on visual scanning and sensory stimulation (Le et al., 2014). However, there is less evidence on the persistence of the benefits of the intervention (Bowen and Lincoln, 2007).
Repetitive transcranial magnetic stimulation (rTMS) is a noninvasive, safe, and easy-to-use neurophysiological technique. It can induce a current in the brain by rapidly changing the magnetic field, which can depolarize neurons and directly regulate cortical excitability. The effect of rTMS on the nervous system involves many aspects. It affects the release of neurotransmitters and neurotrophic factors (Cho and Strafella, 2009), changes the functional connections between brain regions (Fox et al., 2012) and maintains its effect for a long time by regulating synaptic plasticity (Hoogendam et al., 2010). Recent studies have shown that rTMS has a positive effect on motor and cognitive functions (Dionísio et al., 2018; Salazar et al., 2018). However, the reviews vary in scopes, methods, and qualities. Although some systematic reviews with meta-analysis have assessed the efficacy of noninvasive brain stimulation on unilateral neglect (Moher et al., 2009; Graef et al., 2016), the lack of rTMS has not been discussed separately. The therapeutic value associated with rTMS, including benefits and hazards, effective methods, timing, and intensity, needs to be determined.
This study aimed to conduct a systematic review and meta-analysis to evaluate pieces of evidence from published clinical trials to determine the effectiveness of rTMS in post-stroke unilateral spatial neglect and optimize the parameters to guide clinical practice. This systematic review and meta-analysis used the Participants, Interventions, Comparisons, and Outcomes (PICO) component to define a specific research question. The PICO question was: “In post-stroke cognitive impairment, how does rTMS affect unilateral neglect compared with sham rTMS, sham rTMS+conventional therapy, and other interventions?”
| Data and methods | | |
Search strategy
This systematic review and meta-analysis were conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) statement (Page et al., 2021). PubMed, Cochrane Central Register of Controlled Trials, Embase, PsycINFO databases, Web of Science and CINAHL were searched up to February 3, 2021. The keywords used to search are listed in Additional Table 1 [Additional file 1]. The search plan was registered on PROSPERO (https://www.crd.york.ac.uk/PROSPERO/) in advance with registration number CRD42021238701 on March 24, 2021.
Inclusion and exclusion criteria
Based on the PICO component, this systematic review and meta-analysis only considered randomized controlled trials which focus on adult patients with post-stroke unilateral neglect. The detailed inclusion and exclusion criteria are as follows. Inclusion criteria: Participants: (1) patients diagnosed with ischemic or hemorrhagic stroke by magnetic resonance imaging or computed tomography, (2) age ≥ 18 years; Intervention and comparison: (3) the intervention was rTMS alone or rTMS combined with other treatments, (4) studies are randomized controlled trials; Outcomes: (5) behavioral inattention test for the assessment of unilateral spatial neglect. Exclusion criteria: (1) non-human studies; (2) rTMS studies that only reported motor, language, and perception outcomes; (3) interventions were not designed for ischemic or hemorrhagic stroke; (4) cognitive impairment was not caused by stroke; (5) case reports; (6) studies from grey literature.
Data extraction
Two investigators independently evaluated, primarily selected, and reviewed the literature data according to a uniform standard method to determine whether the literature should be included. Any disagreements were resolved by the third investigator through discussion. Information was then extracted according to the Cochrane Reviewer Handbook (Sterne et al., 2001). The basic information extracted is shown in Additional Table 2 (Fregni and Pascual-Leone, 2007; Song et al., 2009; Kim et al., 2010, 2013, 2015, 2018; Barwood et al., 2011; Koch et al., 2012; Waldowski et al., 2012; Heiss et al., 2013; Seniów et al., 2013; Thiel et al., 2013; Khedr et al., 2014; Tsai et al., 2014, 2020; Wang et al., 2014; Cha and Kim, 2015; Fu et al., 2015; Lu et al., 2015; Rubi-Fessen et al., 2015; Yang et al., 2015, 2017; Cao et al., 2016; Haghighi et al., 2017; Nyffeler et al., 2019; Ren et al., 2019; Vatanparasti et al., 2019; Iwański et al., 2020; Li et al., 2020; Liu et al., 2020; Tsai et al., 2020; Yin et al., 2020). The extracted data included sample size, age, study design, rTMS protocol, and the outcomes of unilateral spatial neglect and other cognition domains.
Study quality
The Jadad scale (Corbetta and Shulman, 2011) was used by two investigators independently to assess the quality of the included studies. The Jadad scale score includes three items: (1) description of the randomization method, (2) blinding method, and (3) loss to follow-up. The Jadad scores of > 3 and 0–2 indicate high and low quality, respectively. Any disagreements were resolved by discussion with the third investigator. The Jadad scale score of each study is shown in Additional Table 3.
Statistical analysis
This meta-analysis was conducted by RevMan 5.0 (Cochrane Collaboration) and Stata 16.0 (StataCorp LLC, College Station, TX, USA) software. The heterogeneity of the studies was predicted to be high due to the diversity of the evaluation methods for the specific content involved in the cognitive field. Standardized mean difference (SMD) and 95% confidence intervals (CIs) were used to display the results of the random effects meta-analysis. The SMD values of 0.2–0.5, 0.5–0.8, and > 0.8 were considered small, medium, and large effect sizes, respectively. Statistical heterogeneity was assessed by I2 statistics. A fixed-effects model was used if the value was lower than 50%, and a random-effects model was used if the value was greater than 50% (Corbetta et al., 2005). P < 0.05 was considered significant for heterogeneity. For sensitivity analysis, one-by-one exclusion method was used to assess the stability of the pooled SMD value. Contour enhancement funnel plot combined with the trim and fill method were used to assess publication bias. Egger’s test was used to quantitatively assess publication bias (P < 0.05 was considered significant).
| Results | | |
Characteristics of the included studies
A total of 3842 articles were retrieved from various databases. Thirty-one articles were included after screening the title and abstract and excluding the duplicate articles. The studies with a Jadad score of more than 3 points were included to obtain high-quality literature. Finally, 819 subjects from 28 studies were enrolled. The detail of literature screening is shown in [Figure 1]. The research areas of the study included overall cognitive function, unilateral spatial neglect, attention, memory, language ability, and information storage. Six studies were evaluated for overall cognitive function, 13 studies were evaluated for unilateral spatial neglect, and 10 studies were evaluated for different cognitive domains (e.g., executive function, attention, memory, and language ability). The included studies used different coil types, frequencies, durations, number of sessions, thresholds, and stimulation locations. Ten studies on unilateral spatial neglect used the left posterior parietal cortex as the stimulation location, and the only one study reported the left and right posterior parietal cortices. The detailed information of the included studies is shown in Additional Table 2. | Figure 1 : Selection process based on the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) flow diagram.
Note: RCT: Randomized controlled trial.
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Effect of rTMS on unilateral spatial neglect
The conventional subtest of the behavioral inattention test was used in the studies of Yang et al. (2015) and Iwanski et al. (2020). Eleven studies used line bisection test and star cancellation test. The meta-analysis results of unilateral spatial neglect after rTMS intervention (SMD = −0.92 [95% CI, −1.64 to −0.20], I2 = 87.57%, P = 0.01) indicated that rTMS was more effective than the control group [Figure 2]. The sensitivity analysis was performed by excluding studies one by one. | Figure 2: Forest plot of the meta-analysis of repetitive transcranial magnetic stimulation for unilateral spatial neglect.
Note: CI: confidence interval; SD: standard deviation; SMD: standardized mean difference.
Click here to view |
The pooled value did not deviate considerably, indicating that the above result is robust [Figure 3]. However, for the result after follow-up, the intervention group did not show better outcomes than the control group regardless of the follow-up length (SMD = −0.91 [95% CI, −2.40 to 0.57], I2 = 94.21%). To understand the effectiveness of rTMS for patients in acute phrase, a subgroup analysis was conducted. The results showed that rTMS could not improve unilateral spatial neglect in patients with an onset time of less than 1 month (SMD = −1.35 [95% CI, −3.74 to 1.05], I2 = 93.67%, P = 0.00), and over 1 month (SMD = 0.31 [95% CI, −0.74 to 0.11]; I2 = 0.00%, P = 0.89; [Figure 4]). | Figure 3: Sensitivity analysis of repetitive transcranial magnetic stimulation for unilateral spatial neglect.
Note: CI: confidence interval.
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 | Figure 4: Forest plot of the meta-analysis of repetitive transcranial magnetic stimulation for unilateral spatial neglect based on follow-up length.
Note: CI: confidence interval; SD: standard deviation; SMD: standardized mean difference.
Click here to view |
Parameters of rTMS in unilateral spatial neglect
A subgroup analysis was performed according to rTMS frequency (≤ 1 or > 10 Hz) and continuous theta burst stimulation. The result showed that a frequency of less than 1 Hz was better than other frequencies (SMD = −1.24 [95% CI, −1.93 to −0.56], I2 = 77.12%, P = 0.00; [Figure 5]). Moreover, ≥ 1200 pulses had a significant effect (SMD = −1.56 [95% CI, −2.87 to −0.26], I2 = 82.21%, P = 0.00; [Figure 6]), and > 10 sessions were beneficial in reducing the patient’s unilateral spatial neglect (SMD = −1.11 [95% CI, −2.04 to −0.19], I2 = 85.62%, P = 0.00; [Figure 7]). | Figure 5: Forest plot of the meta-analysis of repetitive transcranial magnetic stimulation for unilateral spatial neglect based on repetitive transcranial magnetic stimulation frequency.
Note: CI: confidence interval; cTBS: continue theta burst stimulation; SD: standard deviation; SMD: standardized mean difference.
Click here to view |
 | Figure 6: Forest plot of the meta-analysis of repetitive transcranial magnetic stimulation for unilateral spatial neglect based on pulses.
Note: CI: confidence interval; SD: standard deviation; SMD: standardized mean difference.
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 | Figure 7: Forest plot of the meta-analysis of repetitive transcranial magnetic stimulation for unilateral spatial neglect based on the number of sessions.
Note: CI: confidence interval; SD: standard deviation; SMD: standardized mean difference.
Click here to view |
Publication bias
Funnel plots can be used to directly observe whether the estimation of the effect number of the original study is related to its sample size (Sterne et al., 2001). Therefore, publication bias was investigated using contour-enhanced funnel plots combined with the trim and fill method. Some smaller studies seemed to be missed in the funnel plot’s significant and nonsignificant areas [Figure 8]. Egger regression-based test was used to quantitatively detect publication bias. The quantitative test results showed the presence of publication bias (P = 0.0107). | Figure 8: Contour-enhanced funnel plots of studies on repetitive transcranial magnetic stimulation for unilateral spatial neglect.
Note: P = 0.0107. SMD: standardized mean difference.
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Effect of rTMS on overall cognitive function
Some studies used the Mini-mental State Examination, the Montreal Cognitive Assessment and the Loewenstein Occupational Therapy Cognitive Assessment to assess the overall cognitive function. The meta-analysis results of the overall cognitive function after rTMS intervention (SMD = 0.52 [95% CI, 0.22 to 0.82]; I2 = 76.46%, P = 0.00) indicates an improvement in overall cognitive function in the rTMS group compared with the control group [Figure 9]. | Figure 9: Forest plot of the meta-analysis of the effect of repetitive transcranial magnetic stimulation on overall cognitive function.
Note: CI: confidence interval; SMD: standardized mean difference.
Click here to view |
Effect of rTMS on ADL
rTMS can improve the ADL ability of patients with post-stroke cognitive impairment (SMD = 0.60 [95% CI, 0.15 to 1.05], I2 = 58.72%, P = 0.01; [Figure 10]). A subgroup analysis was further confirmed according to the time of onset to explore the differences in the effects of rTMS on the ADL ability of patients in the subacute (< 6 months) and chronic (> 6 months) stages. The results showed that rTMS had a positive effect on patients in the subacute and chronic stages with no significant differences between the two groups (P = 0.56, [Figure 11]). | Figure 10: Forest plot of the meta-analysis of the effect of repetitive transcranial magnetic stimulation on activity of daily living.
Note: CI: confidence interval; SD: standard deviation; SMD: standardized mean difference.
Click here to view |
 | Figure 11: Forest plot of the meta-analysis of the effect of repetitive transcranial magnetic stimulation on activity of daily living based on the onset time.
Note: CI: confidence interval; SD: standard deviation; SMD: standardized mean difference. P = 0.56.
Click here to view |
| Discussion | | |
This study quantitatively tested the efficacy of rTMS on post-stroke unilateral spatial neglect. The overall result of this meta-analysis indicated that rTMS intervention can improve post-stroke unilateral spatial neglect. The researchers believe that the excitability of the front parietal neural network is unbalanced between the cerebral hemispheres. The competition between cerebral hemispheres is the main pathophysiological mechanism of unilateral spatial neglect (He et al., 2007; Klomjai et al., 2015; Salazar et al., 2018). rTMS was used to rebalance this interhemispheric interaction and induce an electrical current sufficient to depolarize neurons. rTMS could reduce unilateral spatial neglect by normalizing and balancing asymmetrical brain activation (Salazar et al., 2018). In a meta-analysis, noninvasive brain stimulation improved hemispatial neglect after stroke and improved unilateral spatial neglect (Salazar et al., 2018). However, this meta-analysis included only four articles on rTMS (Albert, 1973). Another meta-analysis of rehabilitation interventions for unilateral spatial neglect based on the functional outcome measure showed that rTMS has a promising efficacy in the recovery of post-stroke unilateral spatial neglect, but had no treatment effect after follow-up (Meidian et al., 2022). The follow-up time of the included studies varied greatly from 2 weeks to 3 months. Since uniform setting of follow-up time is conducive to observing the treatment effect, 1 month was selected as the critical value. Currently, the main clinical assessment methods for unilateral neglect include paper-and-pencil tests, behavioral inattention test (Jiang et al., 2020) and Catherine Bergego Scale (Albert, 1973). Behavioral inattention test and Catherine Bergego Scale are more concerned with functional neglect. In addition to screening for unilateral neglect, the assessments are also concerned with possible impairment in ADL. They can be used as a reference for the patients to return the daily life.
Frequency is an important parameter of rTMS. High frequency can change the activity of local neurons and improve the excitability of the cerebral cortex. On the contrary, low-frequency stimulation can inhibit the activity of local neurons and reduce the excitability of the cerebral cortex (Jiang et al., 2020). Our results suggest that low-frequency stimulation is more effective on cognition, unilateral spatial neglect, and ADL function. Some studies reported using low frequency is a good rTMS strategy to treat unilateral spatial neglect (Fregni and Pascual-Leone, 2007; Kang et al., 2016). However, a study suggested that low- and high-frequency rTMS treatments are effective for the treatment of unilateral spatial neglect. In our study, we identified that > 10 sessions and ≥ 1200 pulses are the optimal parameters. Although the efficacy of rTMS is promising in the recovery of post-stroke unilateral spatial neglect, the best stimulation parameters are still controversial. In general, rTMS can stimulate local nerves and affect the function of multiple parts through the connection and interaction between neural networks. The effect of a single session is limited and hardly lasts. Multiple choices can bring cumulative and long-term benefits. However, excessive stimulation can lead to side effects, such as headaches (Cicerone et al., 2000). Identification of safe parameters is a priority, and further randomized controlled trials are required.
Our study showed that rTMS can improve the ADL in patients. Unilateral spatial neglect would lead to significant limitations in ADL and slow progress in rehabilitation (Katz et al., 1999; Cherney et al., 2001). ADL ability involves the simultaneous execution of multiple tasks. Only the studies that used MBI or FIM for ADL assessment were selected to merge studies with better homogeneity. Our results showed a correlation between treatment outcomes in these two domains for post-stroke cognitive impairment. However, this result cannot explain the effect on daily participation, because real daily life is more dynamic, demanding, and complex. Future studies may consider using assessment tools which are closer to real life. The Catherine Bergego Scale has been used for neglect evaluation (Kim et al., 2013; Yi et al., 2016).
Limitations and improvements
The heterogeneity of the included studies was very high because they had different intervention measures, research objects, and assessment methods. For example, general cognition measurements used in the included studies covered different cognitive domains, which may cause high heterogeneity between different studies. In addition, the heterogeneity of rTMS protocol is also high.
We classified the intervention effects in different domains, which can provide guidance for clinical practice. The quantitative results showed a publication bias amongst the included studies. The possible reason is the limited number of studies included. Some improvements need to be done to better compare the effects of different studies in the future. First, the clinical diagnosis, neuropsychological symptoms, neuroimaging, and other similar imaging methods need to be described in detail. Second, standardized assessments and tests should be used to promote homogeneity amongst different research studies. Third, objective detection methods, such as electroencephalogram, functional magnetic resonance imaging, and functional near-infrared spectroscopy, should be used.
Conclusion
This meta-analysis showed that rTMS intervention may be a promising treatment for poststroke unilateral spatial neglect. Unilateral spatial neglect may benefit from low-frequency rTMS (≤ 1 Hz, > 10 sessions, and ≥ 1200 pulses). Furthermore, rTMS had a positive effect on ADL activity during the follow-up.
Author contributions
XLL, XDL, BC, CS designed study and revised article; XLL, ZXZ collected data; XLL, BC, ZXZ analyzed data; XLL, BC, CS wrote article; XLL, XDL revised article. All authors wrote the manuscript and approved the final version of the manuscript.
Conflicts of interest
The authors declare that there are no conflicts of interest.
Editor note: CS is an Editorial Board member of Brain Network and Modulation. He was blinded from reviewing or making decisions on the manuscript. The article was subject to the journal’s standard procedures, with peer review handled independently of this Editorial Board member and his research group.
Data availability statement
All data relevant to the study are included in the article or uploaded as Additional files.
Open access statement
This is an open access journal, and articles are distributed under the terms of the Creative Commons AttributionNonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.[59]
Additional files
Additional Table 1: Search strategy.
Additional Table 2: Characteristics of the included studies.
Additional Table 3: Jadad score.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11]
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