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Review of devices used in neuromuscular

electrical stimulation for stroke rehabilitation

This article was published in the following Dove Press journal:

Medical Devices: Evidence and Research
24 August 2017
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Kotaro Takeda 1 Abstract: Neuromuscular electrical stimulation (NMES), specifically functional electrical
Genichi Tanino 2 stimulation (FES) that compensates for voluntary motion, and therapeutic electrical stimulation
Hiroyuki Miyasaka 1,3 (TES) aimed at muscle strengthening and recovery from paralysis are widely used in stroke
rehabilitation. The electrical stimulation of muscle contraction should be synchronized with
1
Faculty of Rehabilitation, School
of Health Sciences, 2Joint Research intended motion to restore paralysis. Therefore, NMES devices, which monitor electromyogram
Support Promotion Facility, Center (EMG) or electroencephalogram (EEG) changes with motor intention and use them as a trig-
for Research Promotion and Support,
ger, have been developed. Devices that modify the current intensity of NMES, based on EMG
Fujita Health University, Toyoake,
Aichi, 3Department of Rehabilitation, or EEG, have also been proposed. Given the diversity in devices and stimulation methods of
Fujita Health University Nanakuri NMES, the aim of the current review was to introduce some commercial FES and TES devices
Memorial Hospital, Tsu, Mie, Japan
and application methods, which depend on the condition of the patient with stroke, including
the degree of paralysis.
Keywords: functional electrical stimulation, therapeutic electrical stimulation, EMG-triggered
stimulation, brain–machine interface, brain–computer interface

Introduction
The clinical application of electrical stimulation is historical, with live torpedo fish
being used to deliver electric current for pain treatment ~2,000 years ago. In more recent
years, several implanted and non-implanted electrical stimulation devices have been
widely used in a clinical setting. Examples of implanted devices include the following:
artificial cardiac pacemakers, which are placed under the skin in the chest or belly to
electrically stimulate cardiac muscle to control heart rhythms;1 cochlear implants placed
in the inner ear, which electrically stimulate the auditory nerve corresponding to the
frequency of the sound;2 deep brain stimulation, which delivers electrical impulses to
specific brain areas to reduce tremor in Parkinson’s or other movement disorders;3,4
spinal cord stimulators, which send a mild electric current to nerves in the spinal cord
to mask a pain signal;5 and non-implanted devices, including transcutaneous electrical
nerve stimulation (TENS) and transcranial direct current stimulation (tDCS), which
deliver electrical stimulation via electrode pads on the skin and scalp, respectively. For
Correspondence: Kotaro Takeda TENS, electrodes are often placed on the area of skin where the pain is present, and
Faculty of Rehabilitation, School of a low-voltage electrical current is delivered to treat a variety of painful conditions.6,7
Health Sciences, Fujita Health University,
98-1 Dengakugakubo, Kutsukake-cho, tDCS is a noninvasive brain stimulation technique in which a weak direct current
Toyoake, Aichi 470-1192, Japan (1–2 mA) is applied from electrodes to the scalp,8 which excites or inhibits cortical
Tel +81 562 93 9000
Fax +81 562 93 6817
excitability,9 depending on the polarity of electrode. In recent years, tDCS has been
Email ktakeda@fujita-hu.ac.jp extensively studied in clinical neuropsychiatry and rehabilitation.10,11

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Takeda et al Dovepress

Artificially controlling human muscles or muscle nerves 800

by neuromuscular electrical stimulation (NMES) is widely 700

used in clinical rehabilitation for spinal cord injury and 600

Number of entries
stroke, which often impair upper motor neurons and/or their 500
neuronal pathways to lower motor neurons, consequently 400
leading to paralysis of upper and/or lower limbs. Unilateral 300
paralysis (ie, hemiparesis or hemiplegia) is particularly 200
seen in many patients who survive a stroke. Recovery from 100
the motor impairments may occur over weeks and months. 0
The poststroke motor recovery is complex due to genetic, 1960 1970 1980 1990 2000 2010
Year
pathophysiologic, sociodemographic, and clinical factors.12
Figure 1 Results of a PubMed (service of the US National Library of Medicine
NMES is one of the therapeutic interventions that has been [https://www.ncbi.nlm.nih.gov/pubmed/]) search for (“electrical stimulation” OR
developed to try to induce the motor recovery.13 NMES can “electrical muscle stimulation” OR “electrical nerve stimulation” OR FES OR NMES)
AND (stroke OR “cerebrovascular disease” OR hemiplegic OR hemiparetic OR
be used to stimulate the neuromuscular activity of the paretic hemiparesis OR paralysis OR rehabilitation).
limbs after stroke because normal electrical excitability Abbreviations: FES, functional electrical stimulation; NMES, neuromuscular
electrical stimulation.
often remains in lower motor neurons and their innervated
muscles. Research on the use of NMES for rehabilitation has Wave forms for NMES
been increasing (Figure 1) since 1961, when Liberson et al14 In NMES therapy, various stimulation parameters are used
stimulated the tibialis anterior to dorsiflex the ankle joint of in the devices. Generally, as shown in Figure 2A, the wave-
patients with hemiplegia. form of the stimulation pulse may be monophasic, biphasic,
The purpose of NMES can be broadly classified into and burst (polyphasic) waves. The pulse width is usually
the following categories in general: functional electrical 150–300  ms, while the current intensity is dozens of mil-
stimulation (FES), which, in a narrow sense, compensates liampere. The pulse waveforms can be subdivided into rect-
for voluntary motion, and therapeutic electrical stimulation15 angular waves, sine waves, etc. Biphasic waves, in contrast,
(TES), with the aim of muscle strengthening or recovery can be further distinguished as symmetrical/asymmetrical or
from paralysis. Although there are both implanted16–18 and balanced/imbalanced (Figure 2B).
non-implanted19 NMES devices, this review mainly focused Muscle torque, fatigue, or pain induced by NMES
on the non-implanted type that uses surface electrodes for depends on the wave parameters. Pain depends on the total
stimulation and is often applied for stroke rehabilitation. amount of electrical charge delivered to the tissue.20 Petrofsky

A B
Stimulus train Wave forms
Interval T, pulse (burst) frequency = 1/T
Pulse width Half-cycle sine Exponentially climbing

Monophasic

Time
Sine Asymmetrical rectangular

Biphasic

t Sine

Burst
(polyphasic)

Burst duration Inter-burst duration

(carrier frequency = 1/t)

Figure 2 Parameters of NMES.

Notes: (A) Monophasic, biphasic, and polyphasic stimulus train. (B) Examples of wave forms. A specific stimulus, burst sine wave of carrier frequency of 2,500 Hz and burst
and inter-burst duration of 10 ms is called a Russian current.
Abbreviation: NMES, neuromuscular electrical stimulation.

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Dovepress NMES for stroke rehabilitation

et al21 showed that sine wave stimulation produced greater A

muscle strength, with less pain, in comparison with rectan-
gular or polyphasic waves. Laufer et al22 also reported that
monophasic and biphasic waveforms are more advantageous
than burst waveforms and argued that the electrically induced
fatigue is affected by the number of cycles per second, rather
than the number of bursts per second.23 Therefore, mono-
phasic or biphasic waveforms, rather than burst waveforms,
may be more suitable for the clinical use of NMES. In fact,
many NMES devices for stroke rehabilitation use the former. B

Functional electrical stimulation

Although FES is a method that compensates for voluntary
motion in a narrow sense, it cannot strictly be distinguished
from TES. Many studies have demonstrated that rehabilitation
training with FES improves activity of patients with stroke.24
The WalkAide system (Innovative Neurotronics, Inc.,
Figure 4 Commercial FES devices.
Austin, TX, USA)25 and NESS L300 (Bioness Inc., Valen- Notes: (A) NESS L300 and wireless foot switch for gait and (B) NESS H200, which
is worn over the paralyzed arm and hand. Image courtesy of Bioness Inc., Valencia,
cia, CA, USA)26 are examples of typical commercial FES CA, USA.
devices that are available for paralyzed lower limbs after Abbreviation: FES, functional electrical stimulation.

stroke (Figures 3 and 4A, respectively). These devices are

swing phase of gait, producing ankle dorsiflexion to keep
commonly used against forefoot dropping, which is a gait
leg clearance. The heel contact and off (stance and swing
abnormality that occurs due to paralysis of the muscles of
phases) are detected by a tilt sensor placed with the knee
the lower leg (decreased ankle dorsiflexion). The drop foot
cuff (WalkAide) or by a pressure sensor placed under the
during the swing phase (non-weight-bearing phase) of gait
insole of shoe to determine stimulation periods (WalkAide
is one of the risk factors for a fall.27 In these devices, sur-
and NESS L300).
face electrodes for stimulation are fixed by a cuff to the leg
Since NESS H200 (Bioness Inc.)28,29 is the only com-
below the knee. Electrical stimulation is delivered during the
mercially available FES device for the upper limb and hand
(Figure 4B), more robust and versatile devices are required
for a wider group of people.30 Since hand or upper limb
Electrode pads
motion is more diverse in comparison to lower limb motion,
the electrical stimulation system associated with stimulating
the former is also complicated. The NESS H200 has five
electrodes, which stimulate the five muscle groups of fore-
arm and hand (ie, the extensor digitorum, extensor pollicis
brevis, flexor digitorum superficialis, flexor pollicis longus,
and thenar muscles) and implement both key gripping and
palmar grasping.

Therapeutic electrical stimulation

Although some parameters of electrical stimulation (ie,
stimulus position, stimulus intensity, pulse width, etc.) are
Figure 3 WalkAide system. adjusted according to the motion or condition of patient
Notes: Surface electrode pads (red arrows) are fixed by a cuff to the leg below
the knee. The stimulator is also tied to the cuff. Initially, a clinician connects a hand during FES, the stimulation methods for TES are even more
switch device (black arrow head) to the stimulator to dorsiflex the ankle manually varied.
during the swing phase of the patient’s gait. The specific stimulation timing is
then programmed, so that the electrical stimulation can be accurately performed Patients who have survived a stroke sometimes undergo
consequently with the stimulator alone. A heel sensor under the insole of shoe or
a tilt sensor built in the stimulator is used as a measure of the patient’s gait. Image
electrical stimulation for muscle strengthening, although its
courtesy of Innovative Neurotronics, Inc., Austin, TX, USA. use is not particular to stroke rehabilitation. In general, NMES

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often stimulates specific muscles, but in the case of muscle A

strengthening in stroke rehabilitation, multiple muscles,
including those on the non-paralyzed side, are stimulated to
enhance muscle strength. The reason for muscle strengthening
in the non-paralyzed limb is to improve muscle weakness due
to hospitalization (for example, knee extension force of the
unaffected side decreases by ~30% on the seventh day after
the onset of stroke)31 or to acquire the compensatory strate-
gies using the non-paralyzed limb. The belt electrode skeletal
muscle electrical stimulation (B-SES) was also recently
B C
developed (Auto Tens Pro; Hormer Ion Co. Ltd., Tokyo,
Japan) for muscle strengthening (Figure 5). For the B-SES,
belt-like electrodes are wrapped around the waist, both knees,
and both ankles to contract all lower limb skeletal muscles
simultaneously.32 Since it is desirable to induce stronger
muscle contraction to obtain sufficient muscle strengthening
effect, the stimulus intensity is set to the limit that patients can
endure. Therefore, B-SES adopts the exponentially climbing
wave form shown in Figure 2B, which can produce greater Figure 6 Robotic training for affected upper limb using MIT-Manus/InMotion2
system (Interactive Motion Technologies, Inc., Cambridge, MA, USA) (A) combined
muscle strength with less pain.33 with NMES at sub-motor threshold intensity.37 NMES was delivered to the anterior
deltoid and triceps muscles (B) using the Trio300 system (Ito Co. Ltd., Tokyo,
In contrast, weak current NMES, which is approximately Japan). (C) These devices are currently used in Fujita Health University Nanakuri
at sensory threshold or below motor threshold, has also been Memorial Hospital.
Abbreviation: NMES, neuromuscular electrical stimulation.
proposed as a possible supplemental therapy to facilitate
motor function in patients with stroke.34 This is based on
reports that somatosensory input enhances corticomoto- for the motor recovery of paretic limbs after stroke, it is more
neuronal excitability to the stimulated body parts.35,36 In common to perform NMES to encourage muscle contrac-
this approach, rather than being used in isolation, NMES tion for an intended motion or to perform reciprocal NMES
is applied in combination with rehabilitation training. The with agonists and antagonists. Rosewilliam et al38 recruited
advantages of this approach are high safety, low pain, and patients with stroke with no upper limb function and dem-
high usability for various types of rehabilitation, including onstrated that repetitive NMES for 30 minutes (on and off
robot training (Figure 6).37 periods = 15 s), which was applied twice in a working day
In the abovementioned TES approaches, the electrical for 6 weeks, to produce repetitive wrist extension, improved
stimulation is applied continuously and passively. However, the wrist function of patients. Wu et al39 developed bilateral
arm training combined with NMES for the triceps brachii
Belt-like electrode muscle and anterior deltoid muscle in the affected arm. Dur-
ing the training, patients were required to move both their
paralyzed and non-paralyzed arms simultaneously in the
same way, and the NMES was triggered by the difference in
movement of both arms to assist the motion. Osu et al40 used
a surface electromyogram (EMG) of the unaffected hand as
a clue for electrical stimulation of the paralyzed hand in a
bilateral simultaneous motion. The EMG recorded by surface
electrodes on the skin above skeletal muscle tissue is a com-
mon noninvasive method to assess the electrical activity that
Figure 5 B-SES by Auto Tens Pro (Hormer Ion Co. Ltd.). initiates muscle contraction and produces a physical force.41,42
Notes: Using the belt-like electrodes, B-SES can be used to stimulate all the
muscles in the lower extremities, including the quadriceps femoris, hamstring, tibialis For reciprocal NMES, alternate stimulation of dorsiflexors
anterior, and triceps surae muscles. This device is currently used in Fujita Health
University Nanakuri Memorial Hospital.
and plantarflexors according to the timing of gait improved
Abbreviation: B-SES, belt electrode skeletal muscle electrical stimulation. the walking ability of patients with stroke.43,44 This therapeutic

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Dovepress NMES for stroke rehabilitation

approach is similar to that of FES described earlier, which is motor attempt, motor imagery, or voluntary movement.56 A
triggered depending on the phase of gait. Essentially, there brain–computer interface (BCI) or brain–machine interface
is little distinction between “TES” and “FES” in stroke (BMI), a direct technological interface between the brain
rehabilitation. and a computer, based on the ERD and/or the ERS has
Since adjusting the NMES to the timing of motion recently been found to be a new tool to facilitate motor
means synchronizing it to motor intention, EMG-triggered recovery after stroke.57 Clinical reports of stroke rehabilita-
NMES has been developed.45–47 In this system, electrical tion using a BCI system to trigger NMES (EEG-triggered
stimulation is voluntarily triggered by EMG in the affected NMES) for finger function,58 upper59 and lower60 limb train-
limb (the residual muscle activity of the paralyzed muscle). ing, and gait rehabilitation61 have been published. Similar
In recent years, EMG-triggered NMES has been combined to the EMG-modulated NMES described earlier, an EEG-
with robot-aided rehabilitation, which has demonstrated modulated NMES system has also been reported, which
improved motor function in patients with stroke.48,49 Fur- controls the current intensity of the NMES in a stepwise
thermore, EMG-modulated NMES devices have also been manner according to the appearance or disappearance of
developed,50–52 which controls not only the timing but also ERD.62 Although some of these BCI-NMES studies showed
the intensity of electrical stimulation in direct proportion to an improvement in paretic limbs of patients with stroke,
the amount of residual voluntary EMG. Since Muraoka53 currently, almost all are case reports or feasibility/safety
developed the device, where a pair of surface electrodes studies. Thus, larger, controlled studies are warranted to
simultaneously records EMG from a muscle and stimulates validate the manufacture of commercial devices of EEG-
the same muscle, EMG-modulated NMES can be applied modified NMES.
even to a small muscle, in which it can be challenging to
apply separate stimulating and recording electrodes. This Conclusion
NMES device, which is known as the integrated volitional In stroke rehabilitation, NMES is used not only for muscle
control electrical stimulator (IVES), has been manufactured strengthening and motor recovery of paralyzed limbs as
in Japan since 2008.54 The commercial IVES devices (PAS introduced in this review but also for reducing spasticity63
System and IVES+ System, OG Wellness Technologies Co., and improving swallowing function.64 With the development
Ltd., Okayama, Japan) have two modes, ie, EMG-triggered of electronic engineering and clinical neuroscience, the
NMES and EMG-modulated NMES (Figure 7). devices and stimulation methods of NMES are diversifying.
In more recent years, there has also been an attempt to The application method of NMES differs depending on the
detect the motor intention using an electroencephalogram condition of the patient with stroke, including the degree
(EEG) instead of an EMG. Event-related desynchroniza- of paralysis. For patients with mild paralysis, weak NMES
tion (ERD) and event-related synchronization (ERS), at sensory threshold or below motor threshold, combined
which respectively decrease and increase EEG frequency with rehabilitation, may promote functional improvement.
band power, are used to interpret the dynamics of brain For moderate paralysis, EMG-triggered/modulated NMES
oscillations55 and are well known to be associated with may be a potential rehabilitative treatment option to restore

A B

EMG-triggered NMES

EMG-modulated NMES

Threshold

EMG

Figure 7 (A) The IVES+ system (OG Wellness Technologies Co., Ltd.) that is currently used in Fujita Health University Nanakuri Memorial Hospital. (B) EMG-triggered
and EMG-modulated modes can be used for this device. In the former mode, NMES is applied with a constant current intensity for a fixed time when an EMG that exceeds
a predefined threshold is detected. In the latter mode, the intensity of the stimulation current is proportional to the amplitude of EMG.
Abbreviations: IVES, integrated volitional control electrical stimulator; EMG, electromyogram; NMES, neuromuscular electrical stimulation.

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motor function and improve recovery. For severely affected 13. Langhorne P, Coupar F, Pollock A. Motor recovery after stroke: a
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