As common sequelae in patients with stroke, mobility deficits associated with balance dysfunctions seriously affect patients' functional independence and quality of life.1,2 Each year, an estimated 700,000 individuals experience a stroke,3 and approximately 30% of patients cannot walk independently at 6 mos after stroke.4 Most patients adopt compensatory strategies such as hip hiking and circumduction coupled with a reduced walking speed. The inability to walk independently is a predictor for discharge to nursing homes after stroke5 and is associated with an increased risk of death.6 In addition, walking ability may have a positive impact on preventing secondary complications, such as cardiopulmonary disease and osteoporosis. Therefore, restoration of independent walking to allow patients to become active in their communities again is considered a top priority for rehabilitation in most patients. However, both drug therapies7,8 and traditional rehabilitation programs (e.g., neurodevelopmental therapy,9 proprioceptive neuromuscular facilitation,10 transcutaneous electrical nerve stimulation,11 and electromyography biofeedback12) seem to have little effect. Therefore, a more efficient therapeutic regimen is needed.
In recent years, repetitive transcranial magnetic stimulation (rTMS) has been introduced to the field of stroke rehabilitation. Using short-lasting, strong electrical currents through a copper wire coil, transcranial magnetic stimulation generates a rapidly changing, high-intensity magnetic field. By placing the coil over the target area of the cortex, this magnetic field induces perpendicular currents. At the right strength, it can depolarize the targeted neurons and influence cortical excitability, which may facilitate motor function after stroke. rTMS is simply the repeated application of transcranial magnetic stimulation. In general, low-frequency rTMS (LF-rTMS; ≤1 Hz) decreases cortical excitability, whereas high-frequency rTMS (HF-rTMS; >1 Hz) exerts an opposite effect. Moreover, the neuromodulatory effects of rTMS can outlast the stimulation period by several minutes to hours.13 Studies have demonstrated that rTMS could induce brain plasticity through the mechanisms of long-term potentiation and long-term depression. Other mechanisms underlying the neurophysiologic effects of rTMS include the change of voltage-gated channels and sodium and calcium flow velocity,14 alteration of neurotransmitters,15 and activation of neurotrophic factors.16
According to the interhemispheric competition model, increasing excitability in the affected hemisphere or decreasing the excitability in the unaffected hemisphere may enhance functional recovery in patients who have had a stroke.17 Although this model was initially proposed for the upper limb motor cortex, it might also be applicable to the lower limb motor cortex. To date, several small studies have investigated whether rTMS could be used as a treatment for post-stroke mobility deficiency, but the evidence is still inconclusive. Recently, two representative reviews have described the application of rTMS to the lower limbs after stroke.18,19 However, both reviews were narratives and lacked a meta-analysis. In addition, the most recent study included in the review was published in 2015; since then, several randomized controlled trials (RCTs) have been published.20 Therefore, a meta-analysis of RCTs was performed to investigate the effects of rTMS on walking and balance function in patients with stroke to more precisely evaluate the effects of rTMS on the recovery of lower extremity function using up-to-date information.
Data Sources and Search Strategy
In accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines (see Checklist, Supplemental Digital Content 1, http://links.lww.com/PHM/A604), a systematic search for studies published through March 2017 was conducted in the following databases: MEDLINE (via Ovid), EMBASE (via Ovid), CINAHL (via Ovid), PsycINFO (via Ovid), Web of Science, CENTRAL (via The Cochrane Library), and the Physiotherapy Evidence Database (via the PEDro Website). Key words and medical subject heading (MESH) terms regarding the intervention and condition included the following: (“transcranial magnetic stimulation, repetitive” OR “rTMS” OR “low-frequency transcranial magnetic stimulation” OR “high-frequency transcranial magnetic stimulation” OR “LF-rTMS” OR “HF-rTMS”) AND (“cerebrovascular disorders” OR “brain ischemia” OR “intracranial hemorrhages” OR “stroke” OR “brain infarction” OR “hemi*” OR “pare*”) AND (“randomized controlled trials” OR “RCT” or “controlled clinical trial” OR “randomization” OR “crossover” OR “placebo$” OR “sham” OR “controls”). Reference lists of the relevant studies were manually screened to identify additional studies for inclusion. All analyses were based on previously published studies; thus, no ethical approval or patient consent was required.
Study Selection and Eligibility Criteria
Two independent reviewers performed the literature search. Any discrepancy was resolved by discussion or by achieving a consensus with a third independent reviewer. Studies were eligible if they met the following inclusion criteria: (1) RCTs or randomized controlled crossover trials; (2) adults with a clinical diagnosis of stroke; (3) recruitment of more than 5 patients; (4) same interventions between the experimental and control groups, with the exception of rTMS treatment in the experimental group; (5) clinical trials that investigated the effects of rTMS on walking speed, balance function, motor function, and cortical excitability in patients with stroke; and (6) studies published in English. Excluded were quasi-randomized trials (e.g., by order of entry or date of birth), duplicate publications, and poor-quality studies (PEDro score <6, see quality assessment). Also excluded were studies using rTMS in the acute stage of stroke (<1 mo) for the sake of safety and elimination of various potential confounding factors. Moreover, abstracts from meeting proceedings with no corresponding full article published in a peer-reviewed journal or with no specific data provided even after contacting the author were excluded. In the event of duplicate publications, the data derived from only the study with the most up-to-date information were extracted.
Data Extraction and Quality Assessment
Two researchers independently extracted data from the included trials and conducted the quality assessment. A third arbitrator resolved any disagreements that occurred. Information on the demographic and clinical characteristics of patients, study design, intervention, coil type, site, treatment parameters, and outcomes from each study was extracted. If the results were merely presented in figures and a reply was not received in response to a data request from the authors, values were extracted using a plot digitizer program.21
The primary outcomes were defined as measures of walking speed (e.g., 10-meter walk test [10MWT] and quantitative gait analysis) and balance function (e.g., the Berg Balance Scale [BBS], time up and go tests, the balance subscale of any scale, and a balance measurement system). The secondary outcomes were defined as measures of motor function (lower limb subscale of the Fugl-Meyer Assessment [FMA-L]) and cortical excitability (amplitudes of motor-evoked potentials [MEPs] in bilateral lower limb muscles elicited by transcranial magnetic stimulation]. When multiple optional scales were used concurrently in a single study, only the most representative scale was included in the analysis. In the category of walking speed, the quantitative gait analysis received the highest priority, followed by the 10MWT. In terms of balance function, the BBS was chosen as the cardinal balance test, followed by quantitative evaluations of balance.
Quality assessments were performed with the PEDro scale,22 which is based on the Delphi List criteria23 and is considered valid and reliable.22,24 The scale contains 11 items. Item 1 refers to external validity and is not included in the total PEDro score.25 One point was assigned to each criterion that was satisfied. Therefore, a score of 0 to 10 was allocated to each study (9–10: excellent; 6–8: good; 4–5: fair; and ≤3: poor).
Statistical analyses were conducted with Review Manager 5.3 software (Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, 2014) and STATA version 12.0 (Stata Corp LP, College Station, TX). The summary effect size was estimated by calculating the mean difference (MD) and 95% confidence interval (CI) derived from the mean and standard deviation (SD) of each postintervention value. If studies used different methods or scales to measure the same outcome, standardized MDs (SMDs) were calculated instead of MDs. When different scales measuring the same outcome had opposite changes in scores, the corresponding values were multiplied by −1 to ensure an identical directional change. Statistical heterogeneity was assessed using the Cochrane Q statistic and was quantified by determining the estimated I2 value.26 A random-effects model was applied if severe heterogeneity was observed (P < 0.05 or I2 > 50%). Otherwise, a fixed-effects model was chosen. It was attempted to use a paired analysis to analyze crossover studies. However, if these studies lacked sufficient presented or acquirable data, they were treated as though they were derived from a parallel group, resulting in a conservative estimate of the effect.27 The subgroup analysis was performed based on the stimulation site (ipsilesional stimulation vs. contralesional stimulation vs. bilateral stimulation). The sensitivity analysis was conducted by deleting each study individually to evaluate the quality and consistency of the results. Both the Begg test and the Egger test were used to identify publication bias. For all outcome variables, two-tailed P values <0.05 were considered statistically significant.
A flowchart of the search process is shown in Figure 1. A total of 3980 studies were identified in the initial search. After duplicates were removed and abstracts screened, 26 studies remained for further assessment. After reviewing the full papers to obtain additional details and excluding articles for various reasons (no relevant outcomes reported, intervention or control group not coherent with inclusion criteria, nonrandomized studies, non-English publications, or studies using rTMS in the acute stage of stroke), nine studies including 220 patients fulfilled the inclusion criteria and were included in the final analysis.20,28–35
The PEDro scores of the included studies ranged from 6 to 8, with a mean score of 7. All included studies were of good quality. Concealed allocation was mentioned in four studies, five studies did not blind the assessors, and seven studies did not perform an intention-to-treat analysis. A detailed evaluation of the methodologic quality is provided in Table 1.
Characteristics of the Included Studies
Among all included studies, five studies were RCTs, and the others were randomized crossover trials. These studies were published from 2012 to 2017. The mean time after stroke ranged from several months to several years. All studies included patients with both ischemic and hemorrhagic stroke. The frequency of rTMS ranged from 1 to 20 Hz. Seven studies adopted HF-rTMS and the others adopted LF-rTMS.20,35 High-frequency stimulation was delivered to the primary motor area (M1) of the affected brain hemisphere in four studies, the bilateral leg motor area in two studies,28,29 and the trunk motor spot in one study,33 whereas low-frequency stimulation was delivered to M1 of the unaffected brain hemisphere in the other two studies. In terms of coils, one study used an H coil,29 another used a double-cone coil,28 and the others used a regular figure-of-eight coil. Control group interventions included sham rTMS, rehabilitation therapy, motor imagery, task-oriented training, and strengthening exercises. Table 2 summarizes the main characteristics of the included studies.
Among the included studies, six studies (n = 139) provided complete data about walking speed. The 10MWT and quantitative gait analysis were used for the evaluations. Significant heterogeneity was not observed (I2 = 0%, P = 0.85); therefore, a fixed-effects model was chosen. The analysis revealed a significant treatment effect on walking speed (SMD, 0.64; 95% CI, 0.32– 0.95; P < 0.0001; Fig. 2). According to the results of the subgroup analysis, ipsilesional stimulation (SMD, 0.80; 95% CI, 0.36–1.24; P = 0.0003), but not contralesional stimulation (SMD, 0.74; 95% CI, −0.09 to 1.58; P = 0.08) or bilateral stimulation (SMD, 0.35; 95% CI, −0.19 to 0.88; P = 0.21; Fig. 2), improved the walking speed of patients with stroke. No evident publication bias for walking speed was detected using the Begg and Egger tests (Begg test: P = 0.851; Egger test: P = 0.471).
Among the included studies, three studies (n = 77) provided complete data related to balance function. The BBS, timzed up and go test, and results from balance measurement systems were used for the evaluations. Significant heterogeneity was not observed (I2 = 0, P = 0.97); therefore, a fixed-effects model was chosen. No significant improvement in balance function was noted after the treatment (SMD, 0.10; 95% CI: −0.26 to 0.45; P = 0.59; Fig. 3).
Among the included studies, three (n = 76) provided complete data pertaining to motor function. The FMA-L was used for the evaluations. Significant heterogeneity was not observed (I2 = 0, P = 0.44); therefore, a fixed-effects model was chosen. No significant improvement in motor function was noted after treatment (MD, 0.50; 95% CI, −0.68 to 1.68; P = 0.41; Fig. 4).
Among the included studies, two studies (n = 44) provided complete data describing cortical excitability. The amplitude of MEPs in the hemiplegic soleus muscle and bilateral rectus femoris elicited by transcranial magnetic stimulation were used for the evaluations. Significant heterogeneity was observed (I2 = 90%, P = 0.002); therefore, a random-effects model was chosen. Although rTMS decreased the MEP amplitude in the unaffected hemisphere (MD, 0.09 mV; 95% CI. −0.16 to −0.02; P = 0.01), no significant effect on the MEP amplitude in the affected hemisphere was observed (MD, 0.21 mV; 95% CI, −0.11 to 0.54; P = 0.19; Figure 5a in the Supplementary Material, Supplemental Digital Content 2, http://links.lww.com/PHM/A605).
The data were reanalyzed by deleting each study individually. Most of the outcomes yielded consistent results. However, after excluding the study conducted by Wang et al. on cortical excitability of the affected hemisphere, the direction of the outcome changed (SMD, 0.39; 95% CI, 0.20–0.58; P < 0.0001; Figure 5b in the Supplementary Material, Supplemental Digital Content 2, http://links.lww.com/PHM/A605).
This study represents the first meta-analysis to examine the effects of rTMS on walking speed, balance function, motor function, and cortical excitability in patients with stroke. The data supported a significant effect size of rTMS on walking speed. Especially ipsilesional stimulation, but not contralesional stimulation or bilateral stimulation, improved patients' walking speeds. However, the changes in balance function, motor function and cortical excitability of the affected hemisphere were not significant. All included studies achieved PEDro scores greater than 6, which indicated the good methodologic quality of these trials.
Using walking speed as an outcome, a favorable effect of ipsilesional stimulation was observed in the present meta-analysis. For the nonsignificant effect of contralesional stimulation on walking speed, it is too early to make a conclusion because only one study was included. Intriguingly, two studies using bilateral stimulation had negative results. Limited numbers of participants and estimated data derived from the postintervention values using a plot digitizer program may have caused inaccurate results. Notably, both of these studies delivered rTMS with custom-designed coils, in contrast to the conventional figure-of-eight coil used in the other studies. Chieffo et al.29 used an H coil, and Kakuda et al.28 used a double-cone coil. The double-cone coil was composed of two wings connected at a fixed angle of approximately 90 degrees; it can be considered as a larger figure-of-eight coil and can stimulate areas at depths of 3 to 4 cm.36 A base portion and return portions constitute the essential parts of an H coil, which can stimulate regions at depths of 4 to 6 cm.37,38 In theory, these types of coils have a better ability to stimulate deeper leg-related cortical motor areas, which are located within the intercerebral fissure approximately 3 to 4 cm below the skull.39 Roth et al.40 tested the efficacy of the H coil and the figure-of-eight coil to stimulate both the upper and lower limb-related regions of the motor cortex. They measured the resting and active motor thresholds for the right hand abductor pollicis brevis and leg abductor hallucis brevis muscles in 10 healthy volunteers, and more efficient activation was found when using the H-coil than when using the figure-of-eight coil.40 However, the results were derived from healthy subjects, and more trials are needed to confirm the safety and applicability of this method for patients with stroke.
MEPs represent the activation of the motor neuron system, which occurs when rTMS is applied at intensities above the motor threshold, followed by excitement of the motor nerve pathway and the subsequent activation of alpha motor neurons in the spinal cord, which results in muscle responses.41 The MEP amplitude has been used to measure cortical excitability. According to the meta-analysis in this study, although rTMS decreases the MEP amplitude in the unaffected hemisphere, no significant effect on the MEP amplitude in the affected hemisphere was observed, and strong evidence for statistical heterogeneity was detected. Moreover, the results were unstable. In addition to the limited number of included studies and the small sample size of each study, the reliability and variability of paretic lower limb MEP amplitudes in patients with stroke cannot be ignored. Compared with most studies examining the MEPs obtained from hand and forearm muscles,42–44 only a few studies examined muscles in the lower limbs.45–47 However, the interclass correlation coefficient r values for the paretic soleus muscle and quadriceps were approximately 0.5, which demonstrated poor reliability. Apart from the biologic variability of MEPs, assessors and equipment factors (e.g., coil type and position, stimulated muscles, recording electrode placement, and data collection and processing procedures) also exerted a certain degree of influence on the variability of MEPs.48
Over the past decade, rTMS has been widely used to investigate changes in cortical excitability and provides valuable information about mechanisms underlying the functional recovery of the upper extremities.49 Based on previous results, the interhemispheric competition model was proposed for the upper limb motor cortex; this model states that decreased excitability and increased inhibition of the affected hemisphere, coupled with hyperexcitability and disinhibition of the unaffected hemisphere, are related to poor functional recovery.50 According to the findings of this study, no conclusion can be made whether this model is applicable in the procedure of paretic lower limb rehabilitation in light of the aforementioned limitation. However, it must be noted that there was an evident difference between post-stroke lower and upper limb hemiparesis that involved the control of nerve fibers. In a healthy individual, approximately 90% or more of the motor functions of the upper limbs are governed by nerve fibers originating from the contralateral hemisphere. However, 70% to 80% of the motor functions of the lower limbs are governed by nerve fibers originating from the contralateral hemisphere, whereas the remaining 20% to 30% are governed by nerve fibers from the ipsilateral hemisphere.51 Consequently, simple transference of the model from the arm to the leg seems unreasonable. Some studies have reported that the unaffected hemisphere has an impact on the recovery of lower limb function after stroke with the help of functional neuroimaging techniques. As described by Enzinger et al., greater walking function is correlated with increased brain activation in the bilateral primary motor area, cingulate motor areas, and the caudate nuclei as well as in the thalamus of the affected hemisphere, as detected using functional magnetic resonance imaging.52 Another functional magnetic resonance imaging study indicated that different locations at the cortical layer, subcortical layer, and brainstem might have different contributions to gait control. Similar activation patterns were found in patients with subcortical stroke and controls, with recruitment of the contralateral primary motor cortex (M1), supplementary motor area contralateral to the paretic limb, and bilateral somatosensory area. Better walking was associated with less contralateral sensorimotor cortex activation in the brainstem, but stronger recruitment of the ipsilateral sensorimotor and bilateral somatosensory cortices was observed in patients with subcortical and cortical stroke, respectively.53 In summary, the unaffected motor system might adapt for the recovery of lower limb function, probably based on different lesion localizations.
No significant improvement in balance function was observed after treatment between the rTMS and control groups. It is possible that most of the patients recruited for rTMS showed a relatively mild to moderate balance impairment at baseline, which might have prevented the detection of further significant changes. Moreover, studies with the greatest impact33 on the results recruited patients in the chronic stage of stroke and used the BBS for the assessment. According to findings reported by Mao et al.,54 the BBS has a ceiling effect, particularly in later stages after stroke. Alternatively, several repeated assessments used in the experimental design of randomized crossover trials allowed patients to become familiar with the test. Notably, balance control involves several aspects, such as vision, proprioception, inner ear function, muscle strength, cerebellar function, cerebral cortex function, medication, and age. Further studies should verify the impacts of these aspects and determine whether rTMS and these aspects interact.
With regard to motor function, two studies using HF-rTMS in the acute stage of stroke were excluded for two main reasons.55,56 First, there is a potential risk of epileptic seizures associated with rTMS therapy during the acute period. Second, spontaneous recovery at this stage makes it difficult to detect the real effect of rTMS. The meta-analysis of rTMS in this study found no statistically significant improvement in motor function of the lower limb. The results may be explained in part by the fact that all patients had a relatively mild motor impairment at baseline that was sufficient for walking, because when proximal joints, like the hip and knee, recovered enough to resist gravity, the patients with stroke could basically walk.57 Furthermore, a significant carryover effect was observed up to the second baseline measurement for the real treatment in the study with the greatest weight,29 which might weaken its efficacy.
The present meta-analysis has the following limitations that must be considered: (1) because some authors did not reply to requests for data and the plot digitizer was used to extract the data from figures, the results may be biased. (2) Some studies published in languages other than English were excluded. (3) Both RCTs and randomized crossover trials were included. (4) The meta-analysis extracted postintervention data only; thus, the authors were not able to deduce long-term effects. (5) A relatively small number of studies were included. Therefore, caution is needed when interpreting these results.
This meta-analysis suggests that rTMS, particularly ipsilesional stimulation with HF-rTMS, has a significant effect on improving walking speed. Its effect on cortical excitability is still uncertain owing to the small number of RCTs and the significant heterogeneity between studies. Future studies with larger sample sizes and an adequate follow-up period are required to further investigate the effects of rTMS on lower limb function and its relationship with changes in cortical excitability with the help of functional neuroimaging techniques.
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