Application of repetitive peripheral magnetic stimulation for recovery of motor function after stroke based on neuromodulation: a narrative review

Jia-Xin Pan; Yan-Bing Jia; Hao Liu

doi:10.4103/2773-2398.340140

REVIEW

Year : 2022 | Volume : 1 | Issue : 1 | Page : 13-19

Application of repetitive peripheral magnetic stimulation for recovery of motor function after stroke based on neuromodulation: a narrative review

Jia-Xin Pan¹, Yan-Bing Jia², Hao Liu³
¹ Neuro-Rehabilitation Center, JORU Rehabilitation Hospital, Yixing, Jiangsu Province, China; College of Rehabilitation Medicine, Gannan Medical University, Ganzhou, Jiangxi Province, China
² Neuro-Rehabilitation Center, JORU Rehabilitation Hospital, Yixing, Jiangsu Province, China
³ Department of Rehabilitation, JORU Rehabilitation Hospital, Yixing, Jiangsu Province, China

Date of Submission	11-Jan-2022
Date of Decision	07-Mar-2022
Date of Acceptance	12-Mar-2022
Date of Web Publication	29-Mar-2022

Correspondence Address:
Hao Liu
Department of Rehabilitation, JORU Rehabilitation Hospital, Yixing, Jiangsu Province
China

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/2773-2398.340140

Abstract

Repetitive peripheral magnetic stimulation (rPMS) is a non-invasive and painless approach that can penetrate deeper structures to improve motor function in people with physical impairment due to stroke. A review of available literature was undertaken to discuss the potential mechanisms of rPMS-based neuromodulation and the application of rPMS in the recovery of motor function (e.g., muscle strength, spasticity, motor control and joint mobility, glenohumeral subluxation) after stroke. Issues of concern about parameters and safety of rPMS were also overviewed. Existing evidence has shown that suprathreshold rPMS can be a potential intervention for motor recovery in patients with stroke because of its neuromodulatory effects. However, the rPMS parameters employed by each research team are highly variable for specific lesions. Thus, more high-quality studies on the optimal rPMS protocols for different impairments are warranted in the future.

Keywords: motor function; neuromodulation; repetitive peripheral magnetic stimulation; stroke

How to cite this article:
Pan JX, Jia YB, Liu H. Application of repetitive peripheral magnetic stimulation for recovery of motor function after stroke based on neuromodulation: a narrative review. Brain Netw Modulation 2022;1:13-9

How to cite this URL:
Pan JX, Jia YB, Liu H. Application of repetitive peripheral magnetic stimulation for recovery of motor function after stroke based on neuromodulation: a narrative review. Brain Netw Modulation [serial online] 2022 [cited 2023 Sep 22];1:13-9. Available from: http://www.bnmjournal.com/text.asp?2022/1/1/13/340140

Jia-Xin Pan, Yan-Bing Jia,
Both authors contributed equally to this work.

Introduction

Stroke is the second-leading cause of death and a major cause of disability-adjusted life-years lost worldwide, and the primary cause of disability-adjusted life-years and death in China (Lin et al., 2021). Damage to motor function is the most common type of disability after stroke, and 80% of stroke survivors suffer temporary/permanent impaired control of arm and leg movements (de Vries and Mulder, 2007). Thus, recovery of motor function is important for stroke patients, but long-term rehabilitation is needed.

Repetitive magnetic stimulation applied to peripheral nerves or muscles is termed “repetitive peripheral magnetic stimulation” (rPMS). It is a non-invasive and painless approach developed for therapeutic intervention in movement disorders (Beaulieu and Schneider, 2013). In recent decades, some studies have demonstrated that applying rPMS can improve motor function, reduce spasticity and enhance the effects of motor training in stroke patients (Struppler et al., 2003; Flamand et al., 2012; Beaulieu and Schneider, 2013; Flamand and Schneider, 2014). The underlying mechanism of action has been suggested to activate sensorimotor nerve fibers and mechanoreceptors directly or indirectly to induce neuromodulatory effects on the neural system (Struppler et al., 2004; Momosaki et al., 2017; Jia et al., 2021).

In this review, we discuss the potential mechanisms of rPMS-based neuromodulation and the application of rPMS in the recovery of motor function in stroke patients. Understanding the effects of rPMS-based neuromodulation on motor function could allow a better appraisal of rPMS as evidence-based treatment in post-stroke rehabilitation.

Retrieval Strategy

The literature was searched in three databases (PubMed, CINAHL and Embase) with no time limit using the following strategy: (peripheral magnetic stimulation) OR (rPMS) NOT “transcranial stimulation.” Reference lists of the included papers were hand searched for other relevant studies. The studies were retained for review if they met the following conditions: full-text original or review articles written in English, focusing on the underlying mechanism or clinical application of rPMS. The timeline of selected studies is shown in [Figure 1].

Figure 1: Timeline of studies

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Repetitive Peripheral Magnetic Stimulation Mechanisms Based On Neuromodulation

The mechanisms potentially involved in the improvement of motor function following rPMS are based on cortical and subcortical effects.

Cortical plastic effects induced by rPMS

rPMS has been reported to induce activation of the frontal-parietal sensorimotor cortex and modulate corticomotor excitability. Gallasch et al. (2015) undertook a study based on transcranial magnetic stimulation and functional magnetic resonance imaging. They revealed a large increase in motor-evoked potential (MEP) recruitment curves when repetitive magnetic stimulation of 25 Hz was applied to flexor carpi radialis for 20 minutes in healthy volunteers. In the subsequent functional magnetic resonance imaging assessment, short-lasting focal activations within the sensorimotor cortex were found, which presented as a significant increase in the oxygen dependence in the blood of the contralateral sensorimotor cortex after stimulation. Similarly, Jia and colleagues (2021) found that the slope of the MEP recruitment curve and peak MEP amplitude increased immediately after the use of magnetic pulses at 20 Hz on the median nerve of the non-dominant hand, and the increase in corticomotor excitablity was associated with improvement in hand dexterity assessed using the Purdue pegboard in healthy volunteers. Nito and coworkers (2021) investigated the effects of rPMS over the wrist extensor muscles on the excitability of cortico-spinal networks and motor performance in healthy volunteers. An increased MEP amplitude and intracortical facilitation, as well as decreased short-interval intracortical inhibition following 15 minutes of rPMS (25 and 50 Hz), was documented. This upregulation of cortical motor excitability was accompanied by increased muscle force and electromyography during wrist extension.

Struppler and collaborators (2007) applied rPMS on paretic upper-arm extensor muscles with 5000 single magnetic-field impulses at a repetitive frequency of 20 Hz in patients with brain lesions. After one session of stimulation, significant activation within the superior posterior parietal lobe and premotor cortex areas was found using H2O15-positron emission tomography. Meanwhile, the kinematics of the paretic arm improved significantly. Beaulieu and coworkers (2017) applied rPMS (20 Hz) on a hemiplegic tibialis anterior muscle for 15 minutes in patients who had suffered chronic stroke. They reported reduced intracortical inhibition mediated by gamma-aminobutyric acid-A receptors in both hemispheres and the motor threshold of a contralesional hemisphere after rPMS. According to those studies, irrespective of whether they were conducted in healthy volunteers or stroke patients, the cortical plastic effects induced by rPMS could be confirmed and the mechanism of action could be hypothesized. If rPMS is delivered to peripheral limbs, the rhythmic contraction–relaxation and vibration of muscles would elicit activation of Ia, Ib and II fiber groups as well as sensorimotor nerve fibers to induce the proprioceptive input (Struppler et al., 2004). Such a proprioceptive afferent input to the primary sensory cortex (S1) along the ascending sensory pathway might then produce plastic adaption in the motor cortex (M1) through structural and functional connections between S1 and M1 (Jia et al., 2021) [Figure 2].

Figure 2: Potential mechanism of repetitive peripheral magnetic stimulation.
Note: M1: Motor cortex; S1: primary sensory cortex.

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Subcortical effects induced by rPMS

In a randomized controlled trial, Behrens and colleagues (2011) investigated the effects of rPMS on the excitability of spinal neurons and peripheral nerves. A total of 2000 magnetic pulses with a frequency at 15 Hz lasting 172 seconds were applied to the soleus muscle in healthy volunteers. The maximal H-reflex and peak torque of the muscle soleus barely changed, whereas the maximal M-wave declined rapidly and the ratio of the maximal H-reflex: maximal M-wave increased significantly. The authors suggested that rPMS affected only the excitability of the M-wave related to fast muscle fibers, not spinal neurons. Thus, rPMS was postulated to promote the integration of neuromuscular transmission. However, Nito and collaborators (2021) showed that the maximal M-wave and maximal H-reflex were unchanged upon rPMS application on wrist extensor muscles at different frequencies (50, 25, and 10 Hz) for 20 minutes, which might also indicate that rPMS did not alter the excitability of spinal circuits. Matsuda and coworkers (2018) discovered that rPMS application on the triceps surae muscle in 12 healthy volunteers at 40 Hz for 10 minutes could reduce M-wave latency markedly, but the effects on the amplitude and latency of the H-reflex as well as the amplitude of the M-wave were not significant. Thus, the authors postulated that rPMS mainly increased the excitability of motor nerves. The studies mentioned above are not completely consistent, but all of them showed that rPMS mainly influenced the excitability or conduction of motor nerves.

Clinical Application of Repetitive Peripheral Magnetic Stimulation For Recovery Of Motor Function Following Stroke

Based on the mechanism mentioned above, rPMS has been applied to enhance motor function after stroke. Using magnetic stimulation of paretic limb muscles or nerves to produce muscle contraction and induce proprioceptive ascending input, previous studies have demonstrated various effects of rPMS on motor-related impairment after stroke: muscle strength, motor control and dexterity, as well as spasticity and glenohumeral subluxation.

Muscle strength

Few scholars have investigated the effects of rPMS on muscle strength after stroke. Beaulieu and colleagues (2017) demonstrated significant improvement in the isometric eversion (but not dorsiflexion strength) of paretic lower limbs after one session of magnetic stimulation applied to the paretic dorsiflexor and evertor muscle bellies at a frequency of 20 Hz for a total of 2400 stimuli. In another study, using an intermittent “theta-burst” protocol (i.e., 600 pulses delivered at 5-Hz bursts of three 50-Hz pulses-each for 190 seconds to the tibialis anterior muscle of the paretic limb), Beaulieu and colleagues reported a significant increase in dorsiflexion-muscle strength immediately in chronic stroke (Beaulieu et al., 2015). They postulated that the inconsistent effects of rPMS between those two studies might have been due to the baseline strength of dorsiflexion muscles and different stimulation paradigms.

Motor control and joint mobility

Several studies have provided data on the after-effects of rPMS on motor control and joint mobility of paretic limbs after stroke. Beaulieu and coworkers reported a significant increase in dorsiflexion region of motion after rPMS using a conventional protocol and intermittent theta-burst stimulation applied to paretic tibialis anterior muscles compared with sham stimulation (Beaulieu et al., 2015) and volitional exercises (Beaulieu et al., 2017). Struppler and colleagues (2003, 2007) showed that if rPMS involving 4500–5000 magnetic pulses was applied to the extensors of the paretic forearm, a significant improvement in the kinematics of finger movements in the extension velocity and amplitude of the active finger were observed. They also demonstrated that motor recovery was associated with a significant increase of plasticity activation in the brain. Using a protocol comprising 5000 magnetic pulses in each session at a stimulation frequency of 25 Hz applied to the extensors and flexors of the upper and lower arm, Krewer and coworkers (2014) adopted the Fugl–Meyer Assessment (FMA) as an outcome measure to investigate the rPMS effects on motor control of the paretic upper limb in hemiparetic patients (stroke, 60 of 63; traumatic brain injury, 3 of 63). They discovered that rPMS combined with rehabilitation did not increase the FMA score of the paretic upper limb compared with that obtained with rehabilitation only after 20 sessions of intervention for 2 weeks. However, they noted that the stimulation was delivered to the agonists and antagonists of the paretic upper limb. Whether the brain-modulatory effects induced by rPMS in the coupled muscles could be offset by antagonism and lead to non-significant improvement in function is not known.

Spasticity

“Spasticity” can be defined as velocity-dependent increased muscle tone and resistance to stretch following damage to upper motor neurons, as observed in stroke (Koh and Park, 2017). Numerous studies have revealed the positive effects of rPMS for spasticity treatment after stroke. Using the simple clinical quantification of the modified Ashworth scale and modified Tardieu scale, single session (Struppler et al., 2003; Werner et al., 2016; Chen et al., 2020) and multiple sessions (Krewer et al., 2014) of rPMS given alone (Struppler et al., 2003; Chen et al., 2020) or with rehabilitation therapy (Krewer et al., 2014; Werner et al., 2016) have been reported to reduce spasticity significantly in patients with central paresis. Concerning chronic stroke, Beaulieu and collaborators (2015) demonstrated that one session of rPMS to the tibialis anterior muscle of a paretic lower limb reduced the resistance to plantar-flexor stretch significantly. Struppler and colleagues (2003, 2007) adopted surface electromyography to measure the activity of the flexors and extensors of fingers during voluntary intended extension tasks with maximum effort. Significantly decreased electromyography of the flexors and extensors of the finger after one session of rPMS was documented, and was associated with improvement in motor mobility. Grozoiu and colleagues (2017) applied 10 sessions of rPMS to the spinal nerve roots innervating the quadriceps muscle of the thigh with the coil placed 2-cm paravertebrally at the level of vertebra L3 and ipsilateral to L4 at the paretic side. They reported that the knee-flexion deficit of the paretic lower limb decreased significantly. The effects of rPMS on spasticity after stroke demonstrated in those studies spanned spasms from mild to severe (Struppler et al., 2003, 2007; Krewer et al., 2014; Grozoiu et al., 2017; Chen et al., 2020).

Glenohumeral subluxation

Glenohumeral subluxation is a common complication after stroke. It causes shoulder pain and influences upper-limb function greatly (Paci et al., 2007). rPMS has been attempted to treat the shoulder subluxation induced by stroke in addition to conventional rehabilitation. Using a prospective case-control study design, Yang and colleagues (2018) applied rPMS at 5-Hz frequency with a resting motor threshold of 100% to stimulate the deltoid and supraspinatus muscles of the paretic side for 20 min/day in addition to conventional rehabilitation in acute stroke patients. Compared with electrical stimulation with matched parameters, rPMS for 4 weeks showed a significantly decreased difference in shoulder joint space between the bilateral side measured by musculoskeletal ultrasonography and greater improvement in the FMA score. Fujimura and collaborators (2020) demonstrated that rPMS to shoulder muscles for 4 weeks could reduce the acromiohumeral interval (according to radiography), release shoulder pain (according to a numerical rating scale) and increase FMA score and active shoulder range of the paretic upper limb. Those studies might indicate rPMS as a newer and efficacious treatment for stroke-induced subluxation, or improve the motor dysfunction associated with subluxation.

Parameters of a Repetitive Peripheral Magnetic Stimulation Protocol For Motor Function After Stroke

If rPMS is applied to promote recovery of motor function, then several parameters involved in the protocol (coil type, pulse frequency, stimulation intensity, number of pulses), should be selected carefully to ensure safety and treatment effects. Beaulieu and Schneider (2015) conducted a systematic review on the parameters of rPMS protocols for improving somatosensory or motor disorders. They discovered that the rPMS protocol adopted by each research team was different and that the parameters they adopted had wide variability. Therefore, the optimal parameters for specific treatment purposes have to be studied further. Nevertheless, some basic principles for selecting rPMS parameters can be recommended based on the literature.

Coil

Different types of coils have different characteristics, which can determine their clinical application. The most commonly used coils in clinical practice of rPMS for motor recovery after stroke are the “figure-of-eight” and circular. Thanks to its good focusability, the figure-of-eight coil is usually adopted to stimulate relatively superficial nerves or muscles (Struppler et al., 2003, 2007), or for a protocol to intensively stimulate a precise location, such as the trigger point (Smania et al., 2003, 2005) or motor points (Yang et al., 2018). The circular coil is employed more commonly to stimulate deeper tissues or large areas of muscles, such as spinal roots (Krause et al., 2004) or the spinal trunk (Lim et al., 2018), because of its greater range of stimulation coverage and depth. Some special-shaped coils have been used for rPMS in specific locations in stroke patients. For example, a U-shaped coil has been reported to stimulate the jaw of stroke patients to promote the motor function of swallowing-related muscles (Momosaki et al., 2014, 2015).

The coil diameter should be selected according to the stimulation site to reduce undesirable neuromuscular co-activation (Beaulieu and Schneider, 2015). When magnetic pulses are delivered through the coil, a specific orientation of the coil might be needed to exploit the effects of rPMS. To simulate the motor nerve, Bischoff et al. (1995) demonstrated that the maximal compound muscle action potential was achieved if the direction of the current induced by magnetic stimulation was centrifugal (from proximal to distal). Of note, coil overheating has been reported as a major problem for rPMS, especially by using a former stimulation device (Beaulieu and Schneider, 2015). A solution could be to conduct rPMS by a coil-implemented cooling device (Struppler et al., 2003; Beaulieu et al., 2015, 2017; Yang et al., 2018; Chen et al., 2020; Fujimura et al., 2020) or by using two coils in alternation (Krause et al., 2004; Krause and Straube, 2005).

Frequency

Unlike repetitive transcranial magnetic stimulation, rPMS has nodiametrically opposite frequency-dependent neuromodulation effects to up- and down-regulate corticomotor excitability at high (> 5 Hz) and low frequency (≤ 1 Hz) respectively. Krause and Straube (2005) compared the effects of rPMS using three frequencies (20, 15, and 10 Hz) on spasticity when applied to the lower-limb muscles of a patient with spinal cord injury. They found similar spasticity reduced upon the use of these three frequencies, and speculated that the effect of rPMS in reducing spasticity was independent of frequency. In contrast, Gallasch and colleagues (2015) and Nito and coworkers (2021) found that rPMS using a pulse frequency of 25 Hz and 50 Hz applied to the forearm could activate the sensorimotor cortex significantly and/or enhance the excitability of the corticospinal conduction pathway, whereas the effect of 10 Hz was not obvious. Thus, the influence of frequency on the effects of rPMS merits further study. For recovery of motor function post-stroke, studies have adopted a pulse frequency of rPMS ranging from 5 Hz to 30 Hz (Struppler et al., 2003, 2007; Bernhardt et al., 2007; Krewer et al., 2014; Werner et al., 2016; Beaulieu et al., 2017; Yang et al., 2018; Chen et al., 2020; Fujimura et al., 2020), with 20 Hz being employed most often (Struppler et al., 2004, 2007; Bernhardt et al., 2007; Beaulieu et al., 2017; Chen et al., 2020). Thus, 20 Hz might be the reference frequency adopted in clinical practice for post-stroke rehabilitation.

Intensity

Intensity of stimulation appears to be a decisive parameter for the effects of rPMS (Beaulieu and Schneider, 2015). Nonetheless, there is currently no uniform method to express the stimulation intensity of rPMS. Some studies expressed rPMS intensity in percentage of muscle contraction or movement threshold (Krewer et al., 2014; Yang et al., 2018; Chen et al., 2020), and other expressed it using the visible feedback of the joint movement (Struppler et al., 2003, 2007; Beaulieu et al., 2017) or the participants’ tolerance (Fujimura et al., 2020). In several studies, the rPMS intensity was expressed in percentage of the maximal stimulator output of the magnetic machine (Beaulieu and Schneider, 2015; Werner et al., 2016). Whatever it is, as the modulation effects of rPMS are mainly induced by the proprioceptive afferent input, the suprathreshold stimulation has been usually selected to achieve muscle contraction or joint movement for the recovery of motor function after stroke (Struppler et al., 2003, 2007; Krewer et al., 2014; Werner et al., 2016; Beaulieu et al., 2017; Yang et al., 2018; Chen et al., 2020; Fujimura et al., 2020).

Duty cycle

Almost all studies involving rPMS have used an intermittent pattern of stimulation for post-stroke rehabilitation. In a meta-analysis, Beaulieu and Schneider (2015) demonstrated the average OFF/ON ratio of rPMS at 3.9 for sensorimotor impairments in their included studies. For post-stroke motor rehabilitation, the ON period of rPMS protocol has been employed at 1–3 seconds with the corresponding OFF period at 1–19 seconds (Struppler et al., 2003, 2007; Krewer et al., 2014; Werner et al., 2016; Beaulieu et al., 2017; Yang et al., 2018; Chen et al., 2020; Fujimura et al., 2020). To select a specific ON duration in these studies seems arbitrary. However, one factor that must be considered in clinical practice is that the prolonged contraction can result in muscle fatigue. In contrast, the longer OFF duration will avoid unnecessary fatigue of paretic muscles and coil overheating (Beaulieu and Schneider, 2015).

Total number of magnetic pulses

In the studies employing rPMS for post-stroke motor rehabilitation, the number of magnetic pulses has ranged from 600 (Beaulieu et al., 2015) to 6000 (Fujimura et al., 2020). It seems to have better effects on the sensorimotor system if more stimuli are delivered in rPMS (Beaulieu and Schneider, 2015). It is unknown how many stimuli of rPMS are minimally required to impact the recovery of motor function after stroke. Further studies are warranted to compare the efficiency of rPMS protocols with various amounts of stimuli at the fixed other parameters for motor recovery following stroke.

Comparison of Repetitive Peripheral Magnetic Stimulation With Peripheral Electrical Stimulation

rPMS is often compared with peripheral electrical stimulation (PES), and some advantages of rPMS have been noted. First, magnetic stimulation achieves a higher level of intensity than electrical stimulation without patient discomfort. Hence, rPMS is deemed to stimulate more deeply and induce substantial tissue modification than electrical stimulation (Smania et al., 2005; Beaulieu and Schneider, 2015; Gallasch et al., 2015). Second, rPMS is easier to administer than PES (Smania et al., 2005) because the magnetic field can penetrate uneven tissues. Hence, the clothes of the patient do not need to be removed when rPMS is delivered, whereas electrical stimulation requires the skin to adhere to electrodes. Thus, rPMS is more widely applicable. Third, rPMS has been shown to elicit superior effects for strengthening muscles and improving motor control (Beaulieu et al., 2017) and shoulder subluxation (Yang et al., 2018) in stroke patients. Despite these three main advantages of rPMS over PES, rPMS equipment is larger, more complex, and more expensive than that used for PES, which hinders its further application.

Safety of Repetitive Peripheral Magnetic Stimulation

Most studies that we have reviewed have reported an absence of the side-effects of rPMS, and that participants did not complain of discomfort during rPMS application. In two recent meta-analyses, Momosaki and colleagues (2017) and Sakai and coworkers (2019) adopted the prevalence of adverse events as an outcome to evaluate the effects of rPMS in stroke. All the included clinical trials reported an absence of adverse events (including death) associated with rPMS. The safety of rPMS has been demonstrated in animal models. Suzuki et al. (2015) investigated the safety of high-frequency rPMS of skeletal muscles through the histology of muscles and blood biochemical tests in male Wistar rats. In the rPMS group, periodic acid-Schiff staining showed glycogen depletion in muscle fibers after stimulation, but recovery 4 hours after stimulation. In comparison with rats in a control group taking absolute rest, the tissue level of lactate dehydrogenase was significantly lower in the rPMS group, and significant differences in histologic staining and serum levels of enzymes were not observed. Those data might indicate only fatigue after muscle contraction induced by rPMS. Thus, rPMS appears to be safe if it is applied with tolerable stimulation intensity that would not cause pain.

Conclusions

This paper reviews the literature on the potential mechanism of rPMS and its clinical effects in muscle strengthening, spasticity reduction, improvement of motor control and glenohumeral subluxation after stroke. Despite selection bias may occur due to the limited scope of authors’ knowledge, existing evidence indicates that suprathreshold rPMS to induce muscle contraction or joint movement could be a potential intervention for motor recovery in patients with stroke because of its neuromodulatory effects. However, inconsistent parameters (e.g., frequency, duty cycle, the total number of stimuli) have been employed in the rPMS protocol by different research groups for specific impairment. Thus, more high-quality studies are required to ascertain the optimal parameters for different motor-related impairments after stroke.

Author contributions

JXP, YBJ and HL searched and reviewed the literature, and drafted the manuscript; HL revised the final manuscript. All authors approved the final version of the manuscript.

Conflicts of interest

The authors declare that they have no conflicts of interest concerning this article.

Editor note: HL 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.

Open access statement

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