Journal of

Clinical Medicine

Systematic Review
Effects of Peripheral Electromagnetic Fields on Spasticity:
A Systematic Review
Maria Jesus Vinolo-Gil 1,2,3 , Manuel Rodríguez-Huguet 1,2, * , Cristina García-Muñoz 1 ,
Gloria Gonzalez-Medina 1,3,4 , Francisco Javier Martin-Vega 1 and Rocío Martín-Valero 5

1 Department of Nursing and Physiotherapy, University of Cadiz, 11009 Cadiz, Spain;

mariajesus.vinolo@gm.uca.es (M.J.V.-G.); cristina.garciamunoz@uca.es (C.G.-M.);
gloriagonzalez.medina@uca.es (G.G.-M.); javier.martin@uca.es (F.J.M.-V.)
2 Rehabilitation Clinical Management Unit, Interlevels-Intercenters Hospital Puerta del Mar, Hospital Puerto
Real, Cadiz Bay-La Janda Health District, 11006 Cadiz, Spain
3 Biomedical Research and Innovation Institute of Cadiz (INiBICA), Research Unit, Puerta del Mar University
Hospital, University of Cadiz, 11009 Cadiz, Spain
4 CTS-986 Physical Therapy and Health (FISA), University Institute of Research in Social Sustainable
Development (INDESS), 11009 Cadiz, Spain
5 Department of Physiotherapy, Faculty of Health Science, Ampliacion de Campus de Teatinos, University of
Malaga, C/Arquitecto Francisco Peñalosa 3, 29071 Malaga, Spain; rovalemas@uma.es
* Correspondence: manuel.rodriguez@uca.es

Abstract: Electromagnetic fields are emerging as a therapeutic option for patients with spasticity.
They have been applied at brain or peripheral level. The effects of electromagnetic fields applied to the
brain have been extensively studied for years in spasticity, but not so at the peripheral level. Therefore,
the purpose of our work is to analyze the effects of electromagnetic fields, applied peripherally to
spasticity. A systematic review was conducted resulting in 10 clinical trials. The frequency ranged
Citation: Vinolo-Gil, M.J.; from 1 Hz to 150 Hz, with 25 Hz being the most commonly used and the intensity it was gradually
Rodríguez-Huguet, M.; increased but there was low homogeneity in how it was increased. Positive results on spasticity
García-Muñoz, C.; Gonzalez-Medina, were found in 80% of the studies: improvements in stretch reflex threshold, self questionnaire about
G.; Martin-Vega, F.J.; Martín-Valero, difficulties related to spasticity, clinical spasticity score, performance scale, Ashworth scale, spastic
R. Effects of Peripheral
tone, Hmax/Mmax Ratio and active and passive dorsal flexion. However, results must be taken with
Electromagnetic Fields on Spasticity:
caution due to the large heterogeneity and the small number of articles. In future studies, it would
A Systematic Review. J. Clin. Med.
be interesting to agree on the parameters to be used, as well as the way of assessing spasticity, to be
2022, 11, 3739. https://doi.org/
more objective in the study of their effectiveness.
10.3390/jcm11133739

Academic Editor: Umberto Aguglia Keywords: electromagnetics; electromagnetic field; electromagnetic therapy; magnetic field therapies;
Received: 12 May 2022
spasticity
Accepted: 23 June 2022
Published: 28 June 2022

Publisher’s Note: MDPI stays neutral

1. Introduction
with regard to jurisdictional claims in
published maps and institutional affil-
The Spasticity is described as a speed-dependent increase in muscle tone and repetitive,
iations. uncontrolled involuntary contractions of skeletal muscles [1] and it arises from upper motor
neuron lesions due to a lesion in the pyramidal tracts [2].
The most common symptoms of spasticity are: increased muscle tone, pain and
decreased functional abilities with severe consequences are in lessen joint mobility and
Copyright: © 2022 by the authors. diminished muscle flexibility [3].
Licensee MDPI, Basel, Switzerland. This sensory-motor disorder is observed in patients of all ages [4] affecting about 85%
This article is an open access article of patients with multiple sclerosis, 65–78% with spinal cord injury and 30% with stroke [5],
distributed under the terms and among other neurological pathologies [6], such as cerebral palsy [7].
conditions of the Creative Commons Electromagnetic fields are emerging as a therapeutic option for these patients [8]. This
Attribution (CC BY) license (https:// therapy can produce electromagnetic biological effects such as regenerative effects on the
creativecommons.org/licenses/by/
peripheral nervous system [9] with the possibility of penetrating deep into the tissues [10].
4.0/).

J. Clin. Med. 2022, 11, 3739. https://doi.org/10.3390/jcm11133739 https://www.mdpi.com/journal/jcm

J. Clin. Med. 2022, 11, 3739 2 of 19

Moreover, it a safe and painless tool that may help in restoring motor control through
activation of sensory proprioceptive fibers [11].
They have been applied at brain or peripheral level, using different frequencies and
amplitudes. The following can be applied: Repetitive peripheral magnetic stimulation
(RPMS), Pulsed electromagnetic field therapy (PEMF) and Transcranial magnetic stimula-
tion (TMS).
RPMS is a system that produces eddy currents through electromagnetic induction
activating peripheral nerves and muscles without stimulating skin nociceptors [12]. These
electromagnetic fields target neuromuscular tissue and induce electrical currents that
depolarize neurons and cause concentric muscle contractions. They have a deep penetration
with an anti-spastic effect. As well, electromagnetic field increases blood perfusion of the
exposed region, leading to circulatory and trophic improvement [13].
On the other hand, PEMF uses electromagnetic fields, creating small electric fields in
the tissues, with a pulsing effect to produce athermal effects that promote tissue healing,
relieve pain and inflammation [14,15].
And finally, TMS is a neurostimulation and neuromodulation technique that has
provided over two decades of data in focal and non-invasive brain stimulation based on the
principles of electromagnetic induction with minimal risk and excellent tolerability [16].
The effects of electromagnetic fields applied to the brain using TMS have been exten-
sively studied for years in spasticity [17–22], but not so at the peripheral level, where most
research has focused on the effect of electromagnetic fields on bone regeneration [23–26].
Therefore, the purpose of our work is to analyze the effects of electromagnetic fields,
applied peripherally, on spasticity.

2. Materials and Methods

2.1. Search Strategy
The PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) [27]
guidelines were followed to perform this systematic review (Appendix A). The search
protocol was registered in the PROSPERO database of prospectively registered systematic
reviews (CRD 42022301773). The literature search was performed between December 2021
to February 2022 in the following electronic databases: Web of Science (WoS), Scopus,
PubMed, Cumulative Index to Nursing and Allied Health Literature (CINAHL), Cochrane
Central Register of Controlled Trials, SciELO, Physiotherapy Evidence Database (PEDro),
LILACs and ScienceDirect. Medical Subjects Headings (MeSH) descriptors and other
keywords combined with Boolean operators were used. The terms were: “spasticity”,
“muscle spasticity”, “electromagnetic stimulation”, “electromagnetic therapy”, “pulsed
electromagnetics”, “electromagnetics fields” and “magnetic field therapies”.
The search was filtered to full-text clinical trials papers. No date and language filters
were applied. Table 1 shows the different search combinations.

Table 1. Search combinations.

Databases Search Strategy

Cochrane Plus (field electromagnetic) AND spasticity in title abstract keyword
(muscle spasticity OR musc* tone OR spastic*OR (musc* stiffness) AND
PubMed (electromagnetic OR pulsed electromagnetic*OR c OR electromagnetic
field* OR electromagnetic radiation OR magnetic field therapy)
TITLE-ABS-KEY (((musc* AND tone) OR spastic* OR (musc* AND
stiffness)) AND (eletromagnetic AND field*) OR (electro-magnetic
AND therapy) OR (pulsed AND electromagnetics) OR
WOS (electromagnetics AND fields) OR (electromagnetic AND wave) OR
(magnetic AND field AND therapies)) AND (LIMIT-TO (DOCTYPE,
“ar”)) AND (LIMIT-TO (EXACTKEYWORD, “Human”) OR LIMIT-TO
(EXACTKEYWORD, “Humans”))
J. Clin. Med. 2022, 11, 3739 3 of 19

Table 1. Cont.

Databases Search Strategy

PEDro spasticity AND electromagnetic fields
SciELO Electromagnetic field in title
((Musc* AND Tone) OR spastic* OR (musc* and stiffness)) AND
(eletromagnetic field*) OR (Electro-magnetic therapy) OR (pulsed
SCOPUS
electromagnetics) OR (electromagnetics fields) OR (electromagnetic
wave) OR (magnetic field therapies)
CINAHL AB electromagnetic fields AND AB spastic*
LILACs (electromagnetic field) AND spast* in title, abstract, subject
spasticity AND (electromagnetic fields) NOT transcranial. Research
ScienceDirect
articles. Subject area: Nursing and Health Professions

The PICOS (Population, Intervention, Comparison, Outcomes and Study design)

model [28] was used to establish the inclusion criteria: (I) Population: humans with spas-
ticity; (II) Intervention: Treatment with electromagnetic fields administered to the lower
or upper limbs or spine; (III) Comparison: placebo, no treatment, a different electrother-
apy modality or any other intervention; (IV) Outcomes: related to spasticity; (V) Study
design: controlled clinical trials. Articles where participants were people with spasticity,
but the outcome data were not provided or those where transcranial therapy was used,
were excluded.

2.2. Study Selection Process and Data Extraction

First, a search was carried out by combining the keywords in the different databases.
Duplicate articles were then removed using the Rayyan tool (https://www.rayyan.ai/,
accessed on 27 February 2022). Subsequently, studies were selected or excluded. Two
reviewers (M.J.V.-G. and G.G.-M.) carried out the process of study selection, review and
systematic data extraction. A third reviewer (R.M.-V.) was involved in reaching consensus
in case of controversy.
The following information was extracted from each article included in the review:
authors, type of intervention, disease or pathology causing spasticity, number of subjects,
frequency of sessions per week, time of each session, total duration of the intervention,
outcome measures, measurement instrument, device used for the application of magnetic
fields, parameters used and results obtained.

2.3. Risk of Bias and Assessment of the Methodological Quality of the Included Studies
The risk of bias was calculated for each selected study using the Cochrane Collabora-
tion tool [29]. The following types of bias were assessed: selection bias, performance bias,
detection bias, attrition bias, reporting bias and other biases.
In order to assess the quality of the articles used for the systematic review, the PEDro
scale [30] was used. This scale consists of 10 items: randomization, concealed allocation,
comparability at baseline, blinding of subjects, blinding of therapists, blinding of assessors,
more than 85% follow-up for at least one key outcome, intention-to-treat analysis, statistical
comparison between groups, and point and variability measures for at least one key
outcome. Items are scored as yes (1) or no (0), and the maximum score is 10 points. An
additional criterion (item 1: selection criteria) that relates to external validity (applicability
of the test) is included to complete the Delphi list, but this criterion is not used for the
calculation of the scale score [31]. Taking into account the established criteria, a study with
a PEDro score of 6 or higher is considered as evidence level 1 (6–8: good; 9–10: excellent),
and a study with a score of 5 or lower is considered as evidence level 2 (4–5: acceptable;
<4: poor).
 J. Clin. Med. 2022, 11, x FOR PEER REVIEW

3. Results
J. Clin. Med. 2022, 11, 3739 4 of 19
3.1. Selection of Studies
Once the database searches were completed, by combining the different key w
3. Results a total of 521 documents were obtained, of which 10 studies were finally included
3.1. Selection of systematic
Studies review [32–41]. Figure 1 shows the flow chart of the search process.
A meta-analysis was attempted with the EPIDAT program of the four s
Once the database searches were completed, by combining the different key words,
[32,33,40,41] that provided numerical data for its performance; however, given the
a total of 521 documents were obtained, of which 10 studies were finally included in the
odological, clinical and statistical heterogeneity, it was not possible.
systematic review [32–41]. Figure 1 shows the flow chart of the search process.

Figure 1. PRISMA 2020

Figure flow diagram.
1. PRISMA From:
2020 flow Page From:
diagram. MJ, McKenzie
Page MJ,JE, BossuytJE,
McKenzie PM, Boutron
Bossuyt PM,I,Boutron I
Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting
mann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporti
systematic reviews. BMJreviews.
tematic 2021;372:BMJn 71. doi: 10.1136/bmj.n71.
2021;372: n 71. doi: 10.1136/bmj.n71.

A meta-analysis was attempted with the EPIDAT program of the four studies [32,33,40,41]
that provided numerical data for its performance; however, given the methodological,
clinical and statistical heterogeneity, it was not possible.
J. Clin. Med. 2022, 11, 3739 5 of 19

3.2. Data Extraction

3.2.1. Characteristics of the Subjects
There were a total of 460 participants with an age ranging from 32 [38] to 76 years [40],
out of which 40% were men.
The largest sample studied was that of Lappin et al. [34] with a total of 117 subjects
and the smallest was that of Serag et al. [37] with 26. In 70% of the studies the sample was
between 26 and 38 years of age [32,33,35–37,39,40] and 63% were women.
Regarding the pathology that had originated the spasticity, 50% of the studies were
multiple sclerosis [32–35,37], although in the study by Krause et al. other spinal diseases
were also included [35] and the other 50% of the trials dealt with stroke [36,38–41], although
in the article by Krewer, subjects with traumatic brain injury were also included [38].

3.2.2. Main Characteristics of the Studies

Table 2 shows the main characteristics of the interventions performed in the different
studies that make up the present review. We can highlight that 80% of the trials used sham
stimulation in the control group [32–39] and in the other 20% in the intervention group
RPMS was applied in the antagonists and agonists and in the intervention group only in the
antagonists. In two of the trials there was a control group with healthy individuals [35,39].
Concerning the way the electromagnetic field was falsely applied, sometimes the device
was used switched on but without applying any intensity [32–35,37–39] or it was applied
without intensity and in another location [36].
Table 2. Principal studies characteristics.

Study
Authors Measuring (Evaluation
Groups/Mean Intervention Parameters/Device Used Results
(Year)/Design Instruments)
(SD)/Gender
RPMS: biphasic waveform
with a pulse width of 240 Spasticity: IG improvement
µsec, a rise time of 60 µsec, 18% for the clinical score and
and a maximum magnetic 27% for the stretch reflex
- Self-Questionnaire: field of 1.2 Tesla, with threshold,
daily day activities repeated periods of 78% (14/18) of the treated
with one score only stimulation for 8 s at 25 Hz patients improved clinically
(0–10). Focus on followed by 22 s of repose, and 50% (9/18) improved
the particular 25 min. their stretch reflex threshold.
N = 38
difficulties related IG: RPMS - Self questionnaire: IG:
Nielsen et al. M = 44 - Relaxed supine
to spasticity. CG: sham improved 22%
[32]/1996 26 women position.
- spasticity: stimulation (p = 0.007) vs. CG 29%
Multiple 12 men - Intensity: was
Ashworth twice daily for 7 (p = 0.004).
sclerosis IG: 21 gradually increased
scale/EMG consecutive days - Clinical spasticity score
CG: 17 to 0.7 Tesla within a
- reflex activ- improved −3.3± 4.7 vs.
ity:conventional few minutes CG and 0.7± 2.5
clinical grading. Device: magnetic (p = 0.003).
stimulator with an - Stretch reflex threshold
Evaluation: before,1st oil-cooled coil. The coil has
day, 8th day, 16th day. increased IG: 4.3+ 7.5
an outer vs. CG −3.8 ± 9.7
winding diameter of 13.4 (p = 0.001).
cm consisting of a 16-turns
copper tube.
Improvement performance
scale improved combined
- Clinical rating rating for bladder control,
(EDSS). IG: PEMP cognitive function, fatigue
Richards et al. - Patient-reported CG: sham PEMP: frequency 4–13 Hz level, mobility, spasticity, and
N = 30 performance scales. vision (IG −3.83 ± 1.08,
[33]/1997/RCT stimulation range (50–100 milliGauss)
IG: 15 - Quantitative p < 0.005; CG −0.17 ± 1.07).
Multiple Between 10 and Device: magnetic pulsing
CG: 15 electroencephalog-
sclerosis 24 h a day, 2 device (Enermed) - spasticity (functional
raphy during a months scales disability)
language task. average change IG
−0.80 (0.23) (p < 0.005)
vs. CG −0.17 (0.24)
J. Clin. Med. 2022, 11, 3739 6 of 19

Table 2. Cont.

Study Measuring
Authors
Groups/Mean (Evaluation Intervention Parameters/Device Used Results
(Year)/Design
(SD)/Gender Instruments)
- Improvements in fatigue,
- PEMP: pulsed
quality of life on the
IG: PEMP:2 electromagnetic signals
active device.
- spasticity: weeks 1 to 25 times per
- Mixed results for
(MSQLI) IG: Sham second.
spasticity:
- fatigue: (MSQLI) stimulation: 2
Lappin et al. N = 117 weeks Duration of each pulse: 1
- bladder control: Enermed ss 0.24 (0.79) vs. Sham
[34]/2003/cross- (41–62) 10 weeks, with milisecond, input wave form
(MSQLI) ss 0.13 (0.69) (p = 0.04),
over IG: 117 2, 3 week is a square wave. 24 h/day.
- quality of live: - Over the brachial not difference in the treatment
Multiple 89 women (MSQLI) treatment effects on daily diary
plexus.
sclerosis 28 men sessions - muscle spasm/spasticity
Evaluation: after each - Device: Enermed,
separated by a measured using the
of the 2 treatment Energy Medicine
2-week MSQLI at the end of each
sessions. Developmentes, Inc.,
washout sessions: statistically
Vancouver, British
period. significant differences
Columbia.
(p = 0.04).

- Ashworth scale a peak

reduction 4–24 h after
stimulation (ipsilateral
and contralateral,
p < 0.008). Contralateral
side also decreased.
- velocity of the first swing
of the lower leg increases
in both legs (ipsilateral:
3620 s−1 before to
- RPMS unilateral 4280 s−1 after 24 h,
stimulation nerve roots p < 0.008; contralateral:
L3/L4 of the more 3440 s−1 before to
spastic leg. 4240 s−1 after 24 h,
- RPMS each series of p < 0.008
stimulations was - Intensity for determining
applied 10 times, each the motor threshold
series of stimulations higher in IG tan in CG
lasting 10 s at a (43% of the maximal
Krause et al. frequency of 20 Hz. stimulator output
[35]/2004/RCT The interstimulus was compared with 32%,
N = 31
Spinal diseases 4 s. Altogether, 2000 p = 0.01
IG: 15 spinal Spasticity:
(multiple single magnetic stimuli - Spastic tone decrease
lesions MAS/Wartenberg’s
sclerosis, IG: RPMS were given on more seen as an increase in
(M: 34.2) pendulum test.
familial spastic CG: sham affected leg. swing velocity of the
CG: 16 Evaluation: 2, 4, 24, 48
spinal stimulation - Subjects seated. lower limbs (ipsilateral
healthy h
paralysis, - The intensity of the and contralateral). The
subjects (M: CG: only 3 times
transverse motor threshold was reduction of spastic tone
42.3)
mielitis, spinal increased by around tended to be more
vasculitis) 20% for the stimulation pronounced
series. contralaterally, lasted for
- Device: Magstim Rapid around 20 h.
with a maximum - IG motor threshold for
output of 1275 T with the paraspinal magnetic
circular coil with a stimulation higher
diameter of 90 mm tan CG.
positioned at the level
of vertebrae L3/L4. The spastic tone decreased
between 4 and 24 h after
stimulation. This effect was
slightly more pronounced in the
contralateral extremity.
Furthermore, the stimulation
motor threshold of the patients
was significantly raised.
RPMS decreases spasticity for
1 day not only on the ipsilateral
but also on the
contralateral side.
J. Clin. Med. 2022, 11, 3739 7 of 19

Table 2. Cont.

Study Measuring
Authors
Groups/Mean (Evaluation Intervention Parameters/Device Used Results
(Year)/Design
(SD)/Gender Instruments)
IG: PEMP+PT
Sham G: Sham+PT
CG: PT
PT: programm of
lower limb (warm
up for 10 min,
N = 30 (50) functional electrical
Spasticity and alpha Hmax/Mmax Ratio
Abdollahi et al. IG: n = 10 stimulation for IG: PEMP 20 min in
motoneuron decreased in IG, Sham G, CG
[36] 2013/RCT Sham G: n = dorsi flexor position lying on the spinal
excitability: after treatment but more in IG
Stroke 10 muscles 20 min, cord
(Hmax/Mmax Ratio) (p = 0.012).
CG: n = 10 mat exercise to
hypertonecity
inhibition, stepping
and weight bearing
on the affected side
20 min, treadmill
walking 10 min).
IG: 1 Hz, RPMS
- IG: Improved muscle
- Spasticity (MAS) at a fixed intensity of 45%
IG: active RPMS spasticity (MAS)
- self-reported applied
N = 26 CG: sham RPMS (p = 0.05) and spasm
Serag et al. [37] spasm frequency. bilaterally at L2-4 spinal
IG = 18 frequency and intensity
2014/RCT - Degree of pain - On alternate roots, 2 cm from
34.6 ± 9.2 (p < 0.0001).
Multiple - walking speed:25 days, 2 midline.
CG = 8 - IG/CG:No difference
sclerosis feet walking test. weeks. 6 ss Stimulation:Dantec-
32 ± 11.2 in duration to complete
Maglite magnetic
Evaluation: before, 25 feet test or body
stimulator
2nd/4th weeks. pain
with a figure of eight coil.
- RPMS: 5000
- stimuli at a frequency
25 Hz, a train
duration of 1 s/
intertrain interval of
2 s.
- Intensity was set at - Limited effect on
10% above the level Spasticity (Tardieu > 0)
IG: active RPMS + that evoked a wrist was present in 83% of
PT or elbow movement wrist flexors, 62% of
CG: sham RPMS + taken at rest. Stimuli elbow flexors, 44% of
PT were distributed elbow extensors, and
N = 66 2 weeks, 2 times a consistently among 10% of wrist extensors.
IG = 31 Spasticity: Modified day extensors and flexors - G vs. CG: short-term
55 ± 13 Tardieu PT: of the upper effects on spasticity for
Krewer et al.
12 women Scale/Fugl-Meyer self-administered wrist flexors (p < 0.048),
[38]/2014 and lower arm.
19 men Assessment (arm score) ROM and long-term effects
Stroke/traumatic 20 min.
CG: 32 Evaluation: before, 2nd exercises/slow for elbow extensors
brain injury - CG: 20 min sham
54 ± 13 treatment/4th weeks. passive stretches (p < 0.045). Limited
13 women Tardie scale: 3 ss executed 30 s and stimulation
effect on
19 men proprioceptive - Device: Signal
- No effect on motor
neuromuscular software (Signal for
function. Arm motor
facilitation Windowsa), and the
function IG Med: 5 vs.
movement digital outputs were
CG Med: 4.
30 s. fed through an
- Effect on sensory
analogue-digital converter function
(Micro 1401 mk IIa) into the
magnetic
stimulator (P-Stim 160b):
generated double cosine
pulses with a magnetic
induction of
maximally 1 tesla.
J. Clin. Med. 2022, 11, 3739 8 of 19

Table 2. Cont.

Study Measuring
Authors
Groups/Mean (Evaluation Intervention Parameters/Device Used Results
(Year)/Design
(SD)/Gender Instruments)
IG: ankle dorsiflexion
mobility and maximal
IG: RPMS, biphasic isometric strength increased
waveform, 400-ms pulse and resistance to plantar
width, rapid-rate magnetic flexor stretch decreased.
stimulator Rapid2 - Sham stimulation
Magstim) were delivered yielded no effect.
at a theta-burst frequency, - A significant group
N = 32 - Ankle i.e., 5-Hz bursts of three time interaction was
IG: 9 (51 ± 50-Hz pulses each, detected for
impairments on the
15) Intermittent theta-burst
paretic side (EMG plantar flexor resistance to
5 women stimulation of 2 s ON 8 s
recordings, ROM, stretch (F55.71; P50.03)
4 men IG: RPMS over the OFF (600 pulses) was
active and passive with and a trend only for active DF
Sham C: 9 paretic TA applied for 190 s.
goniometer, sometric ROM (F53.92;
Beaulieu et al. (55 ± 11) Using an air film cooled
muscle strength and - 1 session P50.065). Planned
[39] 2015/RCT 6 women figure-of-eight coil. The coil
resistance of plantar lasting comparisons determined that
Stroke 3 men was held tangentially on
flexors to after
CG: 14 2–3 h including rest the skin overlying the
stretch(dynamometer) RPMS plantar flexor
healthy breaks paretic TA muscle. Intensity
- Ipsilateral TA resistance to stretch was
subjects (50 was set at 42% of the
cortical motor reduced
± 7) maximal stimulator output.
representation (mean decrease of 2.4 + 2.0 kg;
8 women - Sham G/CG: = P50.0007)
6 men (TMS)
parameters with low with concomitant increases in
intensity (5% of active DF ROM (mean
maximal stimulator increase of 7.8 + 7.3u;
output) with the coil P50.0005), passive DF
positioned directly ROM (mean increase of 2.2 +
above the metatarsals 1.9u; P50.03)
and DF strength (mean
increase of 1.32 + 1.25 kg;
P50.05)
IG: RPMS; 10 ss, 9 min,
frequency 25–150 Hz
pulsed duration 280
microseconds, daily,
above the pathological area
(contactless delivery),
firstly, agonist muscle in the - MAS: IG improved
upper extremities was results up to 66%
stimulated to achieve decreasing spasticity
IG: RPMS on post-facilitatory from 2.33 ± 0.90 in the
agonist and inhibition; subsequently, beginning to 0.87 ± 0.64
N = 30; 66.93 antagonist + PT the weakened antagonist points vs. CG improved up to
± 9.31 - Spasticity (MAS) IC: RPMS on muscles
Prouza et al. - Activities daily 31% decreasing
25 women antagonist + PT were stimulated. The spasticity from 2.13 ± 0.74 in
[40]. 2018/RCT living: Barthel
5 men PT: Bobath intensity of the therapy was the beginning to 1.47 ± 0.74
stroke Score
IG: 30 approach, set at the points (1-month follow-up)
CG: 30 proprioceptive beginning and was
neuromuscular increased/ decreased by - Barthel Index, IG, 81%
facilitation (Kabat) patient’s tolerance level of improvement
CG: 10 ss, 8 min 50–100 Hz vs. CG 72% level of
Pulse duration 0.2–2.0 improvement (1-month
microseconds, 10 daily follow-up).
therapies on the antagonist
muscles of the upper
extremities
Device: BTL-6000 Super
Inductive System, BTL
Industries Ltd.).
J. Clin. Med. 2022, 11, 3739 9 of 19

Table 2. Cont.

Study Measuring
Authors
Groups/Mean (Evaluation Intervention Parameters/Device Used Results
(Year)/Design
(SD)/Gender Instruments)
- MAS increased
- 10th–30th: IG (−0.28 ±
0.53, p = 0.001 vs. CG
(−0.52 ± 0.51,
IG: RPMS, Super inductive
- Upper extremity p < 0.001.
system, 10 ss 9 min. On the
N = 60 (62) functional index: IG: RPMS - Barthel increased
agonist muscles (flexors
IG: 29 (MAS) agonists+antagonists 1st–30th: IG/CG (−1.93
forearm), 1 min +
Ciortea et al. 15 women - Activities daily muscles + PT ± 1.60, p < 0.001 vs.
antagonist (extensors
[41] 2022/RCT 14 men living: Barthel CG: RPMS −1.87 ± 1.09, p < 0.001)
forearm) 8 min + PT
Stroke CG: 31 Score antagonists and decreased
CG: RPMS, Super inductive
15 women muscles + PT 10th–30th IG/CG (0.35
Evaluation: system, antagonist
16 men 10 ss ± 0.94, p = 0.064 vs.
Before/10th day/30th (extensors forearm) 8 min +
0.55 ± 0.96, p = 0.005.
day PT
- % participants
improved MAS in GI
100% vs. GC 67,%,
p = 0.004.
PEMP: pulsed electromagnetic field; RPMS: Repetitive peripheral magnetic stimulation; IG: experimental group;
Sham G: sham group; CG: control group; PT: physiotherapy; min: minutes; h: hours; Hmax/Mmax Ratio: Hmax-
to-Mmax ratio, electromyographic ratio; ss: sessions; MAS: Modified Ashworth Scale; NRS: numerical rating scale;
ROM: active range of motion; FMA-UE: Fugl Meyer Assessment scale (subscale A; shoulder/elbow/forearm, B;
wrist, C; hand, D; coordination/speed); M: mean; SD: deviation standard; TA: tibialis anterior; TMS: transcranial
magnetic stimulation; RCT: randomized clinical trials; ROM: range of movement; DF: dorsal flexion; EMG:
electromyogram; MSQLI: Multiple Sclerosis Quality of Life Inventory; EDSS: Expanded Disability Status Scale.

In 3 articles [36,38,40], both the intervention and control groups also had a comple-
mentary physiotherapy program.
In 3 of the 10 trials the electromagnetic fields were administered in the form of
PEMP [33,34,36] and in the other 7 the therapy was RPMS [32,35,37–41].
There was much heterogeneity in terms of the device used, in two of the articles
it was portable [33,34]. The oldest trial (1997) used an oil-cooled coil [32] and the most
recent [40,41] (2018 and 2022) used an inductive system. There were articles in which the
brand of the device was mentioned: Enermed [33,34], Magstim Rapid [35,39], BTL-6000 [40],
Dantec-Maglite [37], P-Stim 160 b [38].
Some were placed on the spine [32,35–37] and others on the upper limbs [38–41]. In
one trial, the device was placed on an empirically determined acupuncture point on the
spine, shoulder or hip [33].
Some articles specified that they were placed directly on the skin [33,34] and in other
cases, there was no contact [35,37,40].
In terms of frequency, the most commonly used frequency was 25 Hz [32,34,38]. In
addition, 1 Hz [37], 4–13 Hz [33], 20 Hz [35], 50 Hz [39] and 25–150 Hz [40] were used.
The time of application ranged from 8 min [39,40] to 24 h a day [33,34], although
9 min [41], 20 min [36,38] or 25 min were also applied [32].
The intensity was gradually increased up to 0.7 Tesla [32], increased by around 20%
for the stimulation series [35], was increased or decreased by patient’s tolerance [40] or was
set at 10% above the level that evoked a movement [38].
The sessions were performed once a day but sometimes twice a day [32,38] or during
24 h [33] and the total number ranged from 1 session [39] to 10 sessions [40]. Concerning
the treatment time it was very variable: 1 day [39], 7 days [32], 10 days [40], 14 days [37,38],
56 days [33] or 70 days [34].
As for how to assess spasticity, the Asworth scale [32,35,37,40,41] was most com-
monly used, followed by electromyographic parameters [32,36,39]. Among them, the
Hmax/Mmax ratio [36] was recorded. The Watenberg’s pendulum test [35] and other
scales such as the Modified Tardie Scale [38] were also used.
J. Clin. Med. 2022, 11, 3739 10 of 19

There were also self-reported questionnaires on difficulties encountered in activities

of daily live [32] or on performance [33] due to spasticity and a self-reported spasm
frequency [37]. The Barthel Index [40,41] and other more specific multiple sclerosis scales
such as the Expanded Disability Status Scale (EDSS) [33] and the Multiple Sclerosis Quality
of Life Inventory (MSQLI) [34] were also used for the same purpose.
Other variables measured were upper limb functionality measured by the Fugl-Meyer
Assessment [38] and ankle functionality through passive and active range of motion mea-
sured with a goniometer, sometric muscle strength and resistance of plantar flexors to
stretch with a dynamometer [39] or walking speed through the 25 feet walking test [37].
In addition, a quantitative electroencephalografic during a language task [33] and a
TMS were used to see the ipsilateral cortical motor representation [39].
Regarding the results obtained in terms of spasticity, in 80% of the studies were positive.
Improvements were found in stretch reflex threshold [32,35,39], self questionnaire about
difficulties related to spasticity [32], clinical spasticity score [32], performance scale [33],
Ashworth scale [32,35,37,40,41], spastic tone [35], Hmax/Mmax Ratio [36] and active and
passive dorsal flexion [39].
Only 2 articles found mixed results [34] or a limited effect [38] for spasticity.
Regarding other measured variables, there was improvement in Barthel index [40,41],
fatigue [33,34], quality of life [34] and sensory function [38] but not gait speed [37].

3.3. Methodological Quality Assessment

80% of the studies were of good quality [32–34,36–39,41] and the other 20% [35,40]
were of acceptable quality. Table 3 shows the score for each study.

Table 3. Methodological quality assessment (PEDro Scale).

Nielsen Richards Lappin Krause Abdollahi Serag Krewer Beaulieu Prouza Ciortea
Criteria et al. et al. et al. et al. et al. et al. et al. et al. et al. et al.
[32] [33] [34] [35] [36] [37] [38] [39] [40] [41]
Eligibility criteria Y Y Y N N Y Y Y Y Y
Randomization Y Y Y N Y Y Y Y Y Y
Allocation concealed N N N N Y Y Y Y N N
Baseline comparability Y Y Y N N Y Y Y Y Y
Subject blinding Y Y Y Y Y Y Y Y N N
Therapist blinding N N N N N N N N N N
Evaluator blinding Y Y Y N N Y Y Y N N
Appropriate continuation Y Y Y Y Y Y Y Y Y Y
Intention to treat Y Y N Y Y Y Y Y Y Y
Comparison between
N Y Y Y Y Y Y Y Y Y
groups
Specific measurements and
Y Y Y Y N N Y Y Y Y
variability
Total PEDro Score 7 8 7 5 6 8 8 8 8 6
“N” indicates those items that not scoring; “Y“ indicates those items score.

3.4. Risk of Bias Assessment

The results of the risk of bias can be observed in Figure 2. It should be noted that the
risk of bias is low in relation with selection bias referring to random sequence generation
as in only one article it was not fulfilled [35] and another had uncertain risk [33]. Only
one article specified allocation concealment [37]. 80% of the articles had a low risk of bias
in relation with performance bias [32–39]. With respect to reporting bias all of them were
unclear risk because none of the articles specified whether they had registered the clinical
trial in a database before (Figure 3).
J. Clin. Med.
J. Clin. 2022,
Med. 11,11,
2022, 3739
x FOR PEER REVIEW 14 of 11
22of 19
J. Clin. Med. 2022, 11, x FOR PEER REVIEW 14 of 22

Figure2.
Figure 2. Risk
Risk of
of bias
bias summary
summary[32–41].
[32–41].
Figure 2. Risk of bias summary [32–41].

Figure 3. Risk of bias graph.

J. Clin. Med. 2022, 11, 3739 12 of 19

4. Discussion
A systematic review has been carried out to synthesize the scientific evidence regarding
the use of electromagnetic fields, applied peripherally, in the treatment of the spasticity.
With regard to the characteristics of the sample, it was homogeneous in terms of the
pathologies studied, as half were in sclerosis and the other half in stroke. It should be
borne in mind that, although the incidence and prevalence figures for spasticity vary [42],
multiple sclerosis and stroke are two of the most prevalent pathologies, with an estimated
80% [43] and 42.6% [44], respectively.
It would be advisable to study the effect of magnetic fields in other diseases where
prevalence is also high, such as spinal cord injuries where it is estimated that between
40 and 78% have spasticity [45] or in cerebral palsy where the percentage is even higher
(72–91%) [46].
Studies have been carried out on rats with induced spinal cord injuries with good
results demonstrating the viability and efficacy of this therapeutic strategy for spasticity;
however their results have not yet been demonstrated in humans [47].
Regarding the type of electromagnetic fields used in the treatment of spasticity, the
most investigated therapy has been transcranial [17–22]. In our extensive literature search
on peripherally delivered electromagnetic fields, only three of the articles [33,34,36] stud-
ied the efficacy of PEMF in spasticity. This type of therapy has been most studied in
osteogenesis stimulation [48] and in muscleskeleton disorders such as osteoarthritis [49],
fibromyalgia [50], rotator cuff tendinitis [51] and lateral epycondilitis [52].In neurology its
use has focused on diabetic peripheral neuropathy [53]. The rationale for this therapy is
that it has a stimulating effect on biological processes [54].
The other 7 articles [32,35,37–41] used RPMS. This system activates peripheral nerves
and muscles without stimulating skin nociceptors while limiting pain [12].
When compared to other types of electrotherapy that have been shown to be effective
in improving spasticity such as neuromuscular electrical stimulation NMES [55,56], RPMS-
induced pain is significantly less than NMES-induced pain, even when using the same
stimulation intensity [57]. Therefore, RPMS simultaneously provides stronger stimulation
than NMES and limits pain [58]. A review of non-pharmacological interventions used for
the treatment of spasticity in people with multiple sclerosis, there was no evidence for
the use of NMES. Furthermore, its depth of stimulation is very shallow and it has some
adverse effects including skin burns, dermatitis and pain [59]. However the authors found
that magnetic stimulation and electromagnetic therapies were beneficial although with a
‘low level’ of evidence [60].
Therefore, an important aspect of this type of therapy is that there are no known
adverse effects; only one of the articles mentions [32] that magnetic stimulation evoked
contraction of the mid-thoracic paravertebral and intercostal muscles, causing a sensation
of tension around the chest but without cardiac involvement, recommending for future
studies a more careful placement of the magnetic coil.
With respect to the number and duration of sessions, device used, doses, intensity and
place of therapy administration, there is no clear pattern. All these parameters have been
inhomogeneous.
Concerning the measuring instruments, they were very heterogeneous, but it must
be taken into account that the term “spasticity” is multifactorial, which makes it difficult
to evaluate, and there are different measurement methods that can be divided into non-
instrumental and instrumental methods, based on neurophysiological studies of spinal
reflexes [61]. In the articles of our review, the most commonly used method was the mod-
ified Ashowrth scale [32,35,37,40,41], which is in agreement with the scientific literature,
as it does not require any tools and is easy to apply [42], but it is not sensitive enough for
measuring the characteristics that distinguish spasticity from other tone alterations [62].
The Tardie scale is considered a better option as it compares muscle reaction to passive
movement at different speeds [63], although it was only used in one of the articles in our
review to measure spasticity in stroke [38]; however it is most reliable in cerebral palsy [64].
J. Clin. Med. 2022, 11, 3739 13 of 19

Other indirect clinical assessment methods would be those aimed at measuring the impact
of spasticity on the individual. The articles in our review used the Fugl-Meyer scale to
measure limb functionality [38], the Barthel Index [40,41] to assess functionality in daily
living, and gait scales such as the 25 feet walking test [33] to assess walking speed. There
were also more specific multiple sclerosis questionnaires such as the Expanded Disability
Status Scale (EDSS) [33] and the Multiple Sclerosis Quality of Life Inventory (MSQLI) [34].
As for quantitative or instrumental methods, the most accurate would be electromyog-
raphy and the pendulum test [42]. In our study, only two studies used these more objective
methods, in one of the articles the pendulum test [36] and the other the Hmax/Mmax
ratio [35]. Given the wide heterogeneity in the measurement of spasticity, it would be
advisable to be more specific in its measurement, using more objective instrumental meth-
ods that could be supported by more specific, reliable and validated non-instrumental
methods according to the pathology studied. Gómez-Soriano et al. recommended a combi-
nation of the different assessment tools such as the scales, neurophysiological measures,
biomechanical methods to know the degree of spasticity present in the patient [6].
Regarding the results, in most of the articles there is an improvement of spasticity,
in agreement with what has been found in the scientific literature where there have been
trials in rats [47], observational studies [65] or clinical case studies [66–68]. What is not
clear are the mechanisms of action and the maintenance time of the antispasticity effect.
In relation to the mechanisms of action, it would be useful to acquire more knowledge in
order to be able to be more specific in the treatment [48]. According to the maintenance
time of the anti-spasticity effect, it is stated that it did not outlast 24 h; however, in the
articles reviewed in this study, this effect lasted longer, up to 30 days [41].
The present study has several strengths, including the broad and easily reproducible
search strategy applied to nine major medical databases. In addition, studies have a good
or acceptable quality. It should be noted that in physiotherapy studies it is difficult to blind
subjects but with this type of therapy this has been achieved in most studies.
However, some limitations need to be addressed before drawing conclusions from the
results of the present analysis. Despite the extensive literature search was carried out, with
no date limit, only a few articles were found. The first one in 1996 and the last one in 2021.
The scientific evidence of electromagnetic fields on spasticity has been written about for
more than two decades, and there are few randomized clinical trials.
Another limitation was related to the great heterogeneity among the different studies.
It was so extensive that a meta-analysis could not be performed. There was little uniformity
in device used, time of application, duration, frequency, intensity and how and where it
was applied. Furthermore, different pathologies and types of electromagnetic fields applied
in the periphery were analyzed. In addition, the measurement instruments were not very
objective and very heterogeneous.
Large, multi-center, double-blind, controlled studies are needed to draw conclusions
for the therapeutic management of spastic patients, as well as comparative studies of
treatment protocols with standardized methodology should be carried out.

5. Conclusions
Based on the studies included in this review, it appears that the peripheral application
of electromagnetic fields is beneficial in spasticity. Improvements have been found in stretch
reflex threshold, self-questionnaire about difficulties related to spasticity, clinical spasticity
score, performance scale, Ashworth scale, spastic tone, Hmax/Mmax Ratio and active and
passive dorsal flexion. However, results must be taken with caution due the small number
of articles and to the large heterogeneity in terms of the device used, application site,
treatment time, intensity, number of sessions and duration of therapy. The most commonly
used form of application was RPMS and the frequency was 25 Hz. In future studies, it
would be interesting to define and agree on the parameters to be used, as well as the way of
assessing spasticity, in order to be able to make a more objective comparison of its efficacy
compared to other therapeutic alternatives.
J. Clin. Med. 2022, 11, 3739 14 of 19

Author Contributions: Conceptualization, M.J.V.-G., M.R.-H. and R.M.-V.; methodology, M.J.V.-G.,

R.M.-V. and G.G.-M.; software, R.M.-V.; validation, F.J.M.-V.; formal analysis, M.J.V.-G., G.G.-M. and
R.M.-V.; investigation, F.J.M.-V. and M.R.-H.; resources, C.G.-M.; data curation, C.G.-M.; writing—
original draft preparation, M.J.V.-G.; writing—review and editing, M.R.-H. and M.J.V.-G.; visualiza-
tion, M.J.V.-G. and C.G.-M.; supervision, M.J.V.-G. and R.M.-V.; project administration, M.J.V.-G. All
authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest.

Appendix A

Table A1. PRISMA 2020 Checklist.

Item Location Where

Section and Topic Checklist Item
# Item Is Reported
TITLE
Title 1 Identify the report as a systematic review. Pag. 1
ABSTRACT
Abstract 2 See the PRISMA 2020 for Abstracts checklist. Pag. 1
INTRODUCTION
Rationale 3 Describe the rationale for the review in the context of existing knowledge. Pag. 1–2
Provide an explicit statement of the objective(s) or question(s) the review
Objectives 4 Pag. 2
addresses.
METHODS
Specify the inclusion and exclusion criteria for the review and how studies
Eligibility criteria 5 2–3
were grouped for the syntheses.
Specify all databases, registers, websites, organizations, reference lists and
Information sources 6 other sources searched or consulted to identify studies. Specify the date 3
when each source was last searched or consulted.
Present the full search strategies for all databases, registers and websites,
Search strategy 7 3
including any filters and limits used.
Specify the methods used to decide whether a study met the inclusion
criteria of the review, including how many reviewers screened each record
Selection process 8 4
and each report retrieved, whether they worked independently, and if
applicable, details of automation tools used in the process.
Specify the methods used to collect data from reports, including how many
reviewers collected data from each report, whether they worked
Data collection
9 independently, any processes for obtaining or confirming data from study 4
process
investigators, and if applicable, details of automation tools used in the
process.
List and define all outcomes for which data were sought. Specify whether all
results that were compatible with each outcome domain in each study were
10a 4
sought (e.g., for all measures, time points, analyses), and if not, the methods
Data items used to decide which results to collect.
List and define all other variables for which data were sought (e.g.,
10b participant and intervention characteristics, funding sources). Describe any
assumptions made about any missing or unclear information.
Specify the methods used to assess risk of bias in the included studies,
Study risk of bias including details of the tool(s) used, how many reviewers assessed each
11 4
assessment study and whether they worked independently, and if applicable, details of
automation tools used in the process.
J. Clin. Med. 2022, 11, 3739 15 of 19

Table A1. Cont.

Item Location Where

Section and Topic Checklist Item
# Item Is Reported
Specify for each outcome the effect measure(s) (e.g., risk ratio, mean
Effect measures 12
difference) used in the synthesis or presentation of results.
Describe the processes used to decide which studies were eligible for each
13a synthesis (e.g., tabulating the study intervention characteristics and 4
comparing against the planned groups for each synthesis (item #5)).
Describe any methods required to prepare the data for presentation or
13b synthesis, such as handling of missing summary statistics, or data
conversions.
Describe any methods used to tabulate or visually display results of
13c
individual studies and syntheses.
Synthesis methods
Describe any methods used to synthesize results and provide a rationale for
the choice(s). If meta-analysis was performed, describe the model(s),
13d
method(s) to identify the presence and extent of statistical heterogeneity, and
software package(s) used.
Describe any methods used to explore possible causes of heterogeneity
13e
among study results (e.g., subgroup analysis, meta-regression).
Describe any sensitivity analyses conducted to assess robustness of the
13f
synthesized results.
Reporting bias Describe any methods used to assess risk of bias due to missing results in a
14 4
assessment synthesis (arising from reporting biases).
Describe any methods used to assess certainty (or confidence) in the body of
Certainty assessment 15
evidence for an outcome.
RESULTS
Describe the results of the search and selection process, from the number of
16a records identified in the search to the number of studies included in the Figure 1
Study selection review, ideally using a flow diagram.
Cite studies that might appear to meet the inclusion criteria, but which were
16b
excluded, and explain why they were excluded.
Study characteristics 17 Cite each included study and present its characteristics. Table 2
Risk of bias in
18 Present assessments of risk of bias for each included study. Figures 2 and 3
studies
For all outcomes, present, for each study: (a) summary statistics for each
Results of individual
19 group (where appropriate) and (b) an effect estimate and its precision (e.g., Table 2
studies
confidence/credible interval), ideally using structured tables or plots.
For each synthesis, briefly summarize the characteristics and risk of bias Table 3, Figures 2
20a
among contributing studies. and 3
Present results of all statistical syntheses conducted. If meta-analysis was
carried out, present for each the summary estimate and its precision (e.g.,
20b
confidence/credible interval) and measures of statistical heterogeneity. If
Results of syntheses comparing groups, describe the direction of the effect.
Present results of all investigations of possible causes of heterogeneity
20c
among study results.
Present results of all sensitivity analyses conducted to assess the robustness
20d
of the synthesized results.
Present assessments of risk of bias due to missing results (arising from Figures 2 and 3.
Reporting biases 21
reporting biases) for each synthesis assessed. Pag. 15
Certainty of Present assessments of certainty (or confidence) in the body of evidence for
22
evidence each outcome assessed.
J. Clin. Med. 2022, 11, 3739 16 of 19

Table A1. Cont.

Item Location Where

Section and Topic Checklist Item
# Item Is Reported
DISCUSSION
Provide a general interpretation of the results in the context of other
23a 14
evidence.
23b Discuss any limitations of the evidence included in the review. 16
Discussion
23c Discuss any limitations of the review processes used. 16
23d Discuss implications of the results for practice, policy, and future research. 16
OTHER INFORMATION
Provide registration information for the review, including register name and
24a Pag. 2
registration number, or state that the review was not registered.
Registration and Indicate where the review protocol can be accessed, or state that a protocol
24b
protocol was not prepared.
Describe and explain any amendments to information provided at
24c
registration or in the protocol.
Describe sources of financial or non-financial support for the review, and the
Support 25
role of the funders or sponsors in the review.
Competing interests 26 Declare any competing interests of review authors. Pag. 1
Report which of the following are publicly available and where they can be
Availability of data,
found: template data collection forms; data extracted from included studies;
code and other 27
data used for all analyses; analytic code; any other materials used in the
materials
review.
From: Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020
statement: an updated guideline for reporting systematic reviews. BMJ 2021;372, n71. doi: 10.1136/bmj.n71.

References
1. Chang, E.; Ghosh, N.; Yanni, D.; Lee, S.; Alexandru, D.; Mozaffar, T. A Review of Spasticity Treatments: Pharmacological and
Interventional Approaches. Crit. Rev. Phys. Rehabil. Med. 2013, 25, 11–22. [CrossRef] [PubMed]
2. Ozcakir, S.; Sivrioglu, K. Botulinum Toxin in Poststroke Spasticity. Clin. Med. Res. 2007, 5, 132–138. [CrossRef] [PubMed]
3. Taricco, M.; Adone, R.; Pagliacci, C.; Telaro, E. Pharmacological Interventions for Spasticity Following Spinal Cord Injury. Cochrane
Database Syst. Rev. 2000, 2, CD001131. [CrossRef] [PubMed]
4. Awaad, Y.; Rizk, T.; Siddiqui, I.; Roosen, N.; Mcintosh, K.; Waines, G.M. Complications of Intrathecal Baclofen Pump: Prevention
and Cure. ISRN Neurol. 2012, 2012, 575168. [CrossRef]
5. Thibaut, A.; Chatelle, C.; Ziegler, E.; Bruno, M.A.; Laureys, S.; Gosseries, O. Spasticity after Stroke: Physiology, Assessment and
Treatment. Brain Inj. 2013, 27, 1093–1105. [CrossRef]
6. Gómez-Soriano, J.; Cano-de la Cuerda, R.; Munóz-Hellin, E.; Ortiz-Gutierrez, R.; Taylor, J.S. Valoración y Cuantificación de La
Espasticidad: Revisión de Los Métodos Clínicos, Biomecánicos y Neurofisiológicos. Rev. Neurol. 2012, 55, 217–226. [CrossRef]
7. Shamsoddini, A.; Amirsalari, S.; Hollisaz, M.T.; Rahimniya, A.; Khatibi-Aghda, A. Management of Spasticity in Children with
Cerebral Palsy. Iran. J. Pediatr. 2014, 24, 345–351. [CrossRef]
8. Oluigbo, C.O.; Rezai, A.R. Addressing Neurological Disorders with Neuromodulation. IEEE Trans. Biomed. Eng. 2011, 58,
1907–1917. [CrossRef]
9. Huang, P.; Xu, L.; Xie, Y. Biomedical Applications of Electromagnetic Detection: A Brief Review. Biosensors 2021, 11, 225.
[CrossRef]
10. Sakai, K.; Yasufuku, Y.; Kamo, T.; Ota, E.; Momosaki, R. Repetitive Peripheral Magnetic Stimulation for Patients after Stroke.
Stroke 2020, 51, E105–E106. [CrossRef]
11. Struppler, A.; Binkofski, F.; Angerer, B.; Bernhardt, M.; Spiegel, S.; Drzezga, A.; Bartenstein, P. A Fronto-Parietal Network
Is Mediating Improvement of Motor Function Related to Repetitive Peripheral Magnetic Stimulation: A PET-H2O15 Study.
Neuroimage 2007, 36, T174–T186. [CrossRef] [PubMed]
12. Barker, A.T. An Introduction to the Basic Principles of Magnetic Nerve Stimulation. J. Clin. Neurophysiol. 1991, 8, 26–37. [CrossRef]
[PubMed]
13. Zarkovic, D.; Kazalakova, K. Repetitive Peripheral Magnetic Stimulation as Pain Management Solution in Musculoskeletal and
Neurological Disorders—A Pilot Study. Int. J. Physiother. 2016, 3, 671–675. [CrossRef]
14. Özgüçlü, E.; Çetin, A.; Çetin, M.; Calp, E. Additional Effect of Pulsed Electromagnetic Field Therapy on Knee Osteoarthritis
Treatment: A Randomized, Placebo-Controlled Study. Clin. Rheumatol. 2010, 29, 927–931. [CrossRef] [PubMed]
J. Clin. Med. 2022, 11, 3739 17 of 19

15. Rioja-Toro, J.; Estévez-Poy, P.J.; De Prada-Espinel, J.; González-Rebollo, A. Los Campos Magnéticos de Baja Amplitud y de
Frecuencia Extremadamente Baja Para El Tratamiento de La Gonalgia Crónica. Rehabilitacion 2008, 42, 127–136. [CrossRef]
16. Rajapakse, T.; Kirton, A. Non-Invasive Brain Stimulation in Children: Applications and Future Directions. Transl. Neurosci. 2013,
4, 217–233. [CrossRef]
17. Valle, A.C.; Dionisio, K.; Pitskel, N.B.; Pascual-Leone, A.; Orsati, F.; Ferreira, M.J.L.; Boggio, P.S.; Lima, M.C.; Rigonatti, S.P.;
Fregni, F. Low and High Frequency Repetitive Transcranial Magnetic Stimulation for the Treatment of Spasticity. Dev. Med. Child
Neurol. 2007, 49, 534–538. [CrossRef]
18. McIntyre, A.; Mirkowski, M.; Thompson, S.; Burhan, A.M.; Miller, T.; Teasell, R. A Systematic Review and Meta-Analysis on the
Use of Repetitive Transcranial Magnetic Stimulation for Spasticity Poststroke. PMR 2018, 10, 293–302. [CrossRef]
19. Kumru, H.; Murillo, N.; Vidal Samso, J.; Valls-Sole, J.; Edwards, D.; Pelayo, R.; Valero-Cabre, A.; Tormos, J.M.; Pascual-Leone,
A. Reduction of Spasticity with Repetitive Transcranial Magnetic Stimulation in Patients with Spinal Cord Injury. Neurorehabil.
Neural Repair 2010, 24, 435–441. [CrossRef]
20. Mori, F.; Ljoka, C.; Magni, E.; Codecà, C.; Kusayanagi, H.; Monteleone, F.; Sancesario, A.; Bernardi, G.; Koch, G.; Foti, C.; et al.
Transcranial Magnetic Stimulation Primes the Effects of Exercise Therapy in Multiple Sclerosis. J. Neurol. 2011, 258, 1281–1287.
[CrossRef]
21. Centonze, D.; Koch, G.; Versace, V.; Mori, F.; Rossi, S.; Brusa, L.; Grossi, K.; Torelli, F.; Prosperetti, C.; Cervellino, A.; et al.
Repetitive Transcranial Magnetic Stimulation of the Motor Cortex Ameliorates Spasticity in Multiple Sclerosis. Neurology 2007, 68,
1045–1050. [CrossRef] [PubMed]
22. Fisicaro, F.; Lanza, G.; Grasso, A.A.; Pennisi, G.; Bella, R.; Paulus, W.; Pennisi, M. Repetitive Transcranial Magnetic Stimulation
in Stroke Rehabilitation: Review of the Current Evidence and Pitfalls. Ther. Adv. Neurol. Disord. 2019, 12, 1756286419878317.
[CrossRef] [PubMed]
23. Griffin, X.L.; Costa, M.L.; Parsons, N.; Smith, N. Electromagnetic Field Stimulation for Treating Delayed Union or Non-Union of
Long Bone Fractures in Adults. Cochrane Database Syst. Rev. 2011, 4, CD008471. [CrossRef] [PubMed]
24. Handoll, H.H.G.; Elliott, J. Rehabilitation for Distal Radial Fractures in Adults. Cochrane Database Syst. Rev. 2015, 2015, CD003324.
[CrossRef] [PubMed]
25. Diniz, P.; Shomura, K.; Soejima, K.; Ito, G. Effects of Pulsed Electromagnetic Field (PEMF) Stimulation on Bone Tissue Like
Formation Are Dependent on the Maturation Stages of the Osteoblasts. Bioelectromagnetics 2002, 23, 398–405. [CrossRef]
26. Gossling, H.R.; Bernstein, R.A.; Abbott, J. Treatment of Ununited Tibial Fractures: A Comparison of Surgery and Pulsed
Electromagnetic Fields (PEMF). Orthopedics 1992, 15, 711–719. [CrossRef]
27. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.;
Brennan, S.E.; et al. The PRISMA 2020 Statement: An Updated Guideline for Reporting Systematic Reviews. BMJ 2021, 10, 89.
[CrossRef]
28. Brennan, S.E.; Cumpston, M.S.; McKenzie, J.E.; Thomas, J. The Use of ‘PICO for Synthesis’ and Methods for Synthesis without
Meta-Analysis: Protocol for a Survey of Current Practice in Systematic Reviews of Health Interventions. F1000Research 2021,
9, 678. [CrossRef]
29. Green, S.; Higgins, J.P.T. Cochrane Handbook for Systematic Reviews of Interventions—Version 5.0.2; John Wiley & Sons: Chichester,
UK, 2009.
30. Foley, N.C.; Bhogal, S.K.; Teasell, R.W.; Bureau, Y.; Speechley, M.R. Estimates of Quality and Reliability with the Physiother-
apy Evidence-Based Database Scale to Assess the Methodology of Randomized Controlled Trials of Pharmacological and
Nonpharmacological Interventions. Phys. Ther. 2006, 86, 817–824. [CrossRef]
31. Verhagen, A.P.; De Vet, H.C.W.; De Bie, R.A.; Kessels, A.G.H.; Boers, M.; Bouter, L.M.; Knipschild, P.G. The Delphi List: A Criteria
List for Quality Assessment of Randomized Clinical Trials for Conducting Systematic Reviews Developed by Delphi Consensus.
J. Clin. Epidemiol. 1998, 51, 1235–1241. [CrossRef]
32. Nielsen, J.F.; Sinkjaer, T.; Jakobsen, J. Treatment of Spasticity with Repetitive Magnetic Stimulation; a Double-Blind Placebo-
Controlled Study. Mult. Scler. 1996, 2, 227–232. [CrossRef] [PubMed]
33. Richards, T.L.; Lappin, M.S.; Acosta-Urquidi, J.; Kraft, G.H.; Heide, A.C.; Lawrie, F.W.; Merrill, T.E.; Melton, G.B.; Cunningham,
C.A. Double-Blind Study of Pulsing Magnetic Field Effects on Multiple Sclerosis. J. Altern. Complement. Med. 1997, 3, 21–29.
[CrossRef] [PubMed]
34. Lappin, M.S.; Lawrie, F.W.; Richards, T.L.; Kramer, E.D. Effects of a Pulsed Electromagnetic Therapy on Multiple Sclerosis Fatigue
and Quality of Life: A Double-Blind, Placebo Controlled Trial. Altern. Ther. Health Med. 2003, 9, 38–48. [PubMed]
35. Krause, P.; Edrich, T.; Straube, A. Lumbar Repetitive Magnetic Stimulation Reduces Spastic Tone Increase of the Lower Limbs.
Spinal Cord 2004, 42, 67–72. [CrossRef] [PubMed]
36. Abdollahi, M.; Bahrpeyma, F.; Forough, B. Investigation of the Effects of Spinal Pulsed Electromagnetic Field on Spasticity of
Lower Extremity and Alpha Motoneuron Excitability in Hemiplegic Patients Using Hmax/Mmax Ratio. Cerebrovasc. Dis. 2013,
36, 18–19.
37. Serag, H.; Abdelgawad, D.; Emara, T.; Moustafa, R.; El-Nahas, N.; Haroun, M. Effects of Para-Spinal Repetitive Magnetic
Stimulation on Multiple Sclerosis Related Spasticity. Int. J. Phys. Med. Rehabil. 2014, 2, 2. [CrossRef]
J. Clin. Med. 2022, 11, 3739 18 of 19

38. Krewer, C.; Hartl, S.; Müller, F.; Koenig, E. Effects of Repetitive Peripheral Magnetic Stimulation on Upper-Limb Spasticity and
Impairment in Patients with Spastic Hemiparesis: A Randomized, Double-Blind, Sham-Controlled Study. Arch. Phys. Med.
Rehabil. 2014, 95, 1039–1047. [CrossRef]
39. Beaulieu, L.D.; Massé-Alarie, H.; Brouwer, B.; Schneider, C. Noninvasive Neurostimulation in Chronic Stroke: A Double-Blind
Randomized Sham-Controlled Testing of Clinical and Corticomotor Effects. Top. Stroke Rehabil. 2015, 22, 8–17. [CrossRef]
40. Prouza, O.; Kouloulas, E.; Zarkovic, D. High-Intensity Electromagnetic Stimulation Can Reduce Spasticity in Post-Stroke Patients.
Int. J. Physiother. 2018, 5, 87–91. [CrossRef]
41. Ciortea, V.M.; Motoas, că, I.; Borda, I.M.; Ungur, R.A.; Bondor, C.I.; Iliescu, M.G.; Ciubean, A.D.; Lazăr, I.; Bendea, E.; Irsay, L.
Effects of High-Intensity Electromagnetic Stimulation on Reducing Upper Limb Spasticity in Post-Stroke Patients. Appl. Sci. 2022,
12, 2125. [CrossRef]
42. Sainz-Pelayo, M.P.; Albu, S.; Murillo, N.; Benito-Penalva, J. Spasticity in Neurological Pathologies. An Update on the Pathophysi-
ological Mechanisms, Advances in Diagnosis and Treatment. Rev. Neurol. 2020, 70, 453–460. [CrossRef] [PubMed]
43. Patejdl, R.; Zettl, U.K. Spasticity in Multiple Sclerosis: Contribution of Inflammation, Autoimmune Mediated Neuronal Damage
and Therapeutic Interventions. Autoimmun. Rev. 2017, 16, 925–936. [CrossRef] [PubMed]
44. Wissel, J.; Manack, A.; Brainin, M. Toward an Epidemiology of Poststroke Spasticity. Neurology 2013, 80, S13–S19. [CrossRef]
[PubMed]
45. Levi, R.; Seiger, S. The Stockholm Spinal Cord Injury Study: 1. Medical Problems in a Regional SCI Population. Paraplegia 1995,
33, 308–315. [CrossRef] [PubMed]
46. Odding, E.; Roebroeck, M.E.; Stam, H.J. The Epidemiology of Cerebral Palsy: Incidence, Impairments and Risk Factors. Disabil.
Rehabil. 2006, 28, 183–191. [CrossRef]
47. Hou, J.; Nelson, R.; Mohammad, N.; Mustafa, G.; Plant, D.; Thompson, F.J.; Bose, P. Effect of Simultaneous Combined Treadmill
Training and Magnetic Stimulation on Spasticity and Gait Impairments after Cervical Spinal Cord Injury. J. Neurotrauma 2020, 37,
1999–2013. [CrossRef]
48. Waldorff, E.I.; Zhang, N.; Ryaby, J.T. Pulsed Electromagnetic Field Applications: A Corporate Perspective. J. Orthop. Transl. 2017,
9, 60–68. [CrossRef]
49. Yang, X.; He, H.; Ye, W.; Perry, T.A.; He, C. Effects of Pulsed Electromagnetic Field Therapy on Pain, Stiffness, Physical Function,
and Quality of Life in Patients with Osteoarthritis: A Systematic Review and Meta-Analysis of Randomized Placebo-Controlled
Trials. Phys. Ther. 2020, 100, 1118–1131. [CrossRef]
50. Sutbeyaz, S.T.; Sezer, N.; Koseoglu, F.; Kibar, S. Low-Frequency Pulsed Electromagnetic Field Therapy in Fibromyalgia. Clin. J.
Pain 2009, 25, 722–728. [CrossRef]
51. Binder, A.; Parr, G.; Hazleman, B.; Fitton-Jackson, S. Pulsed Electromagnetic Field Therapy of Persistent Rotator Cuff Tendinitis.
A Double-Blind Assessment. Lancet 1984, 323, 695–698. [CrossRef]
52. Uzunca Murat Birtane Nurettin Taştekin, K. Effectiveness of Pulsed Electromagnetic Field Therapy in Lateral Epicondylitis. Clin.
Rheumatol. 2007, 26, 69–74. [CrossRef]
53. Pieber, K.; Herceg, M.; Paternostro-Sluga, T. Electrotherapy for the Treatment of Painful Diabetic Peripheral Neuropathy—A
Review. J. Rehabil. Med. 2010, 42, 289–295. [CrossRef] [PubMed]
54. Sadlonovas, J.; Korpas, J.; Vrabec, M.; Salat, D.; Buchancova, J.; Kudlicka, J. The Effect of the Pulsatile Electromagnetic Field in
Patients Suffering from Chronic Obstructive Pulmonary Disease and Bronchial Asthma. Bratisl. Lek. Listy 2002, 103, 260–265.
55. Cobo-Vicente, F.; San Juan, A.F.; Larumbe-Zabala, E.; Estévez-González, A.J.; Donadio, M.V.F.; Pérez-Ruiz, M. Neuromuscular
Electrical Stimulation Improves Muscle Strength, Biomechanics of Movement, and Functional Mobility in Children with Chronic
Neurological Disorders: A Systematic Review and Meta-Analysis. Phys. Ther. 2021, 101, pzab170. [CrossRef] [PubMed]
56. Stein, C.; Fritsch, C.G.; Robinson, C.; Sbruzzi, G.; Plentz, R.D.M. Effects of Electrical Stimulation in Spastic Muscles After Stroke:
Systematic Review and Meta-Analysis of Randomized Controlled Trials. Stroke 2015, 46, 2197–2205. [CrossRef]
57. Han, T.R.; Shin, H.I.; Kim, I.S. Magnetic Stimulation of the Quadriceps Femoris Muscle: Comparison of Pain with Electrical
Stimulation. Am. J. Phys. Med. Rehabil. 2006, 85, 593–599. [CrossRef]
58. Kagaya, H.; Ogawa, M.; Mori, S.; Aoyagi, Y.; Shibata, S.; Inamoto, Y.; Mori, H.; Saitoh, E. Hyoid Bone Movement at Rest by
Peripheral Magnetic Stimulation of Suprahyoid Muscles in Normal Individuals. Neuromodulation 2019, 22, 593–596. [CrossRef]
59. Kinoshita, S.; Ikeda, K.; Yasuno, S.; Takahashi, S.; Yamada, N.; Okuyama, Y.; Sasaki, N.; Hada, T.; Kuriyama, C.; Suzuki, S.; et al.
Dose-Response of RPMS for Upper Limb Hemiparesis after Stroke. Medicine 2020, 99, e20752. [CrossRef]
60. Amatya, B.; Khan, F.; La Mantia, L.; Demetrios, M.; Wade, D.T. Non Pharmacological Interventions for Spasticity in Multiple
Sclerosis. Cochrane Database Syst. Rev. 2013, 2013, CD009974. [CrossRef]
61. Aloraini, S.M.; Gäverth, J.; Yeung, E.; MacKay-Lyons, M. Assessment of Spasticity after Stroke Using Clinical Measures: A
Systematic Review. Disabil. Rehabil. 2015, 37, 2313–2323. [CrossRef]
62. Petek Balci, B. Spasticty Measurement. Arch. Neuropsychiatry 2018, 55, S49. [CrossRef] [PubMed]
63. Van Wijck, F.M.J.; Pandyan, A.D.; Johnson, G.R.; Barnes, M.P. Assessing Motor Deficits in Neurological Rehabilitation: Patterns of
Instrument Usage. Neurorehabil. Neural Repair 2001, 15, 23–30. [CrossRef] [PubMed]
64. Numanoǧlu, A.; Günel, M.K. Intraobserver Reliability of Modified Ashworth Scale and Modified Tardieu Scale in the Assessment
of Spasticity in Children with Cerebral Palsy. Acta Orthop. Traumatol. Turc. 2012, 46, 196–200. [CrossRef]
J. Clin. Med. 2022, 11, 3739 19 of 19

65. Kinoshita, S.; Ikeda, K.; Hama, M.; Suzuki, S.; Abo, M. Repetitive Peripheral Magnetic Stimulation Combined with Intensive
Physical Therapy for Gait Disturbance after Hemorrhagic Stroke: An Open-Label Case Series. Int. J. Rehabil. Res. 2020, 43, 235–239.
[CrossRef] [PubMed]
66. Havel, P.; Struppler, A. First Steps in Functional Magnetic Stimulation (FMS)-Movements of Forearm and Fingers Induced by
Closed-Loop Controlled FMS. Acta Physiol. Pharmacol. Bulg. 2001, 26, 185–188. [PubMed]
67. Flamand, V.H.; Schneider, C. Noninvasive and Painless Magnetic Stimulation of Nerves Improved Brain Motor Function and
Mobility in a Cerebral Palsy Case. Arch. Phys. Med. Rehabil. 2014, 95, 1984–1990. [CrossRef] [PubMed]
68. Bernhardt, M.; Angerer, B.; Buss, M.; Struppler, A. Neural Observer Based Spasticity Quantification during Therapeutic Muscle
Stimulation. In Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology, New York,
NY, USA, 30 August–3 September 2006; pp. 4897–4900.