Neuromuscular Electrical Stimulation Applications

43  Neuromuscular Electrical Stimulation Applications Jayme S. Knutson, Nathaniel S. Makowski, Kevin L. Kilgore, John Chae

KEY POINTS • Neuromuscular electrical stimulation (NMES) systems can be used to rehabilitate patients who have upper or lower extremity paralysis caused by damage to motor neurons in the central nervous system, such as stroke and spinal cord injury. • Short-term regimens with external NMES systems can help stroke patients recover better volitional upper and lower extremity function.

• External and implanted NMES systems can be used as effective long-term assistive devices for walking in stroke patients and for standing, stepping, and grasp-release function in spinal cord injury.

Neuromuscular electrical stimulation (NMES) is the use of an electrical current to produce muscle contractions for the purpose of restoring motor function in individuals who have muscle weakness or paralysis. NMES works by creating an electrical field near motor axons of peripheral nerves that is of sufficient strength to depolarize the axonal membranes, eliciting action potentials and, consequently, muscle contractions. Therefore, despite commonly being referred to as “muscle stimulation,” NMES systems operate by depolarizing motor axons rather than muscle fibers directly. It follows, then, that for NMES to be effective, the peripheral nerves to the target muscles must be intact and the muscle physiology must be healthy. This typically excludes individuals who have muscle weakness or paralysis related to peripheral nerve injuries or muscular dystrophies. The patients for whom NMES can be used as a therapeutic or assistive device are those whose muscle paresis or paralysis is caused by injury or disease to the upper motor neurons (i.e., central nervous system injuries). Thus most clinical NMES applications are designed for spinal cord injury (SCI) or stroke patients, and they may also be applicable to individuals with cerebral palsy, traumatic brain injury, or multiple sclerosis. NMES can be applied with noninvasive surface (i.e., transcutaneous) electrodes positioned on the skin over the target muscle(s) or nerves or with implanted electrodes placed intramuscularly, epimysially, or around peripheral nerves innervating target muscles. Intramuscular electrodes may be percutaneous and interface with an external stimulator, or like other implanted electrodes can be completely subcutaneous and interface with an implanted stimulator. NMES stimulators range from being capable of delivering a single channel of electrical current to delivering multiple independent channels of stimulation. NMES current waveforms are typically characterized by a train of monophasic or biphasic current pulses. The frequency, amplitude, and duration of the pulses determine the strength of the muscle contractions elicited. Stimulators are equipped with controllers that allow the patient or clinician to set or select some of these stimulation parameters and the duration and coordination of muscle contractions. More sophisticated NMES systems have controllers that receive real-time input from patients,

which enables them to control the stimulation and subsequent muscle contractions and movements produced. User interfaces with such controllers range from buttons and switches to external or implanted sensors or biopotential recording electrodes (e.g., electromyographic [EMG] or cortical recordings). This chapter describes NMES systems that have been designed for and used primarily in patients with upper and lower limb weakness or paralysis caused by a stroke or SCI. There are two purposes for NMES systems in these populations. First, NMES may be used as a therapy to restore volitional movement and function after a stroke. A therapeutic effect is a change in voluntary movement or function as a result of a period of treatment with NMES (i.e., a before–after effect). Some studies have shown that NMES, especially if it is delivered in a way that assists the stroke patient in performing tasks (e.g., walking or activities of daily living [ADLs]), can improve the recovery of volitional function,26 possibly by promoting adaptive neuroplastic changes in the central nervous system.41,76,81 Therapeutic applications of NMES are intended to be temporary and therefore noninvasive. Second, NMES may be used long-term in the form of a neuroprosthesis, which is an assistive device that enables the patient to perform the function that was lost. A neuroprosthetic effect is the change in movement or function produced when the neuroprosthesis is being used (i.e., an on–off effect). Such devices may be external or implanted and may be beneficial for both stroke and SCI patients. This chapter describes upper and lower limb therapeutic and neuroprosthetic NMES applications for stroke and SCI.

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UPPER LIMB APPLICATIONS Stroke Loss of arm and hand movement on one side of the body is very common after stroke. Paretic upper limb extensors, hypertonic flexors, and loss of coordination make it very difficult for many stroke survivors to perform tasks that require reaching and hand opening with the affected limb. For approximately half of stroke patients, the loss of arm and/or hand function persists beyond 6 months and may become permanent.51

CHAPTER 43  Neuromuscular Electrical Stimulation Applications Abstract Neuromuscular electrical stimulation (NMES) of paralyzed muscles can be used to restore or replace motor function in individuals who have upper motor neuron damage from causes such as stroke or spinal cord injury (SCI). In some conditions, such as stroke or incomplete SCI, NMES may be part of a therapy regimen that helps restore volitional movement and function. In other conditions, such as severe stroke or complete SCI, permanent NMES applications are needed to replace the lost neuromuscular function. This chapter describes NMES devices for upper and lower extremity therapeutic and neuroprosthetic applications.

Keywords neuromuscular electrical stimulation neuroprosthesis functional electrical stimulation stroke spinal cord injury rehabilitation medicine medical device

432.e1

CHAPTER 43  Neuromuscular Electrical Stimulation Applications As a result, quality of life is diminished for many individuals who are forced to limit their preferences and participation to items and activities that do not require their paretic upper limb.20 The primary purpose of most upper limb NMES applications after stroke is therapeutic, to improve the extent of arm and hand recovery so that the upper limb can, at a minimum, be useful in performing bimanual tasks. For stroke patients who have exhausted therapeutic strategies, NMES devices are being developed for permanent use as neuroprostheses, assistive devices that help stroke survivors perform ADLs.44 This section of the chapter describes and summarizes the efficacy of several types of electrical stimulation devices that are in clinical use or are being developed for poststroke upper limb rehabilitation or function. Three categories of NMES, distinguished by the method in which the stimulation is controlled, are described: cyclic NMES, triggered NMES, and proportionally controlled NMES. Cyclic NMES is simple, widely available, and perhaps the most used method of administering NMES.61,75 Electrodes are placed on the skin over muscles that are targeted for activation, typically the wrist, finger, and thumb extensors. Elbow extensors or shoulder muscles may also be targeted in some patients. A single pair of electrodes may be adequate to produce wrist extension and hand opening. Commercially available cyclic NMES units (e.g., Intelect NMES, DJO Global, Inc.) often have two channels. A therapist adjusts the intensity of stimulation delivered from each channel to a level that produces comfortable muscle contractions and the desired movement (e.g., hand opening). Stimulation is delivered according to an on–off cycle, with the timing of the cycle, the number of repetitions, and the maximum intensity of stimulation preset by a therapist. When the device is turned on, stimulation elicits repeated muscle contractions, and therefore arm or hand movement, lasting several seconds at a time. Cyclic NMES requires no input from the patient. The patient can simply relax and let the stimulator activate the muscles, although therapists sometimes instruct patients to attempt to move the arm or hand in synchrony with the stimulation. Research studies of cyclic NMES have used regimens ranging from 1.5 to 10 hours per week for 6 to 12 weeks.45,61 Triggered NMES is another NMES modality that elicits repetitive muscle contractions, but it requires input from the patient or therapist for stimulation to be delivered. EMG-triggered stimulators (e.g., Neuromove, Zynex Medical, Inc.) prompt the patient to attempt to make the desired arm or hand movement while measuring the EMG signal from the target arm or hand muscle. If and when the amplitude of the EMG signal exceeds a preset threshold, the stimulator turns on, delivering a preset intensity of stimulation to the target muscle for a preset duration.58 After the stimulation turns off, the cycle repeats. This EMG-triggered NMES may be more effective in promoting neurologic changes leading to better recovery, because the stimulated movement coincides with the patient’s own effort to produce the movement.21 Sensors worn on the body can provide alternative methods of triggering stimulation. For example, an accelerometer on the arm has been used to trigger NMES to the triceps, wrist, and finger extensors when the patient achieves some threshold degree of shoulder flexion while attempting to reach forward.55 Switch-triggered NMES systems (e.g., NESS H200, Bioness, Inc.) use push buttons to trigger stimulation (Fig. 43.1). The push buttons may be operated by a therapist89 or by the patient.2 Push buttons give the therapist or patient control of the initiation and duration of stimulation, which makes it more feasible to incorporate NMES into task practice. Goal-oriented task practice is a hallmark of effective therapy42; using NMES to assist task practice may lead to better outcomes than might be achieved with NMES modalities like cyclic NMES or EMG-triggered NMES, which can be challenging to use to assist task practice because the timing of the stimulation pattern is preprogrammed.26

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Figure 43.1  NESS H200 (Bioness, Inc., Valencia, California), a switchtriggered neuromuscular electrical stimulation system. (From Knutson JS, Chae J. Functional electrical stimulation (FES) for upper limb function after stroke, p. 307–329. In: Kilgore K, Ed. Implantable Neuroprostheses for Restoring Function. Waltham, MA: Elsevier, 2015.)

CCFES stimulator

Normal

Weak

Figure 43.2  Contralaterally controlled functional electrical stimulation system (CCFES, Cleveland FES Center). Bend sensors in the glove worn on the unaffected hand proportionally control the intensity of stimulation to the paretic finger and thumb extensors. (Illustration by Erika Woodrum, courtesy of Cleveland FES Center.)

Proportionally controlled NMES is distinguished from cyclic and triggered NMES methods in that the intensity of the NMES is not preset but regulated in real time by the patient via a control strategy that translates the patient’s desired movement into stimulation intensities. Contralaterally controlled functional electrical stimulation (CCFES), developed at the Cleveland Functional Electrical Stimulation (FES) Center, is a proportionally controlled NMES approach in which the intensity of stimulation to the paretic finger and thumb extensors is proportionally controlled by an instrumented glove worn on the opposite (contralateral) hand (Fig. 43.2). With the glove, the patient is able to control the degree of opening of the affected hand and can practice using it in task-oriented therapy.45,46 Other researchers are using EMG signals from the impaired upper limb to deliver proportionally controlled NMES in accordance with the patient’s motor intention.88 Proportionally controlled NMES may be more efficacious than other NMES methods, because the approach capitalizes on the principle of intention-driven movement, linking the patient’s motor commands to the stimulated movement and the resulting proprioceptive feedback to the brain. This artificial reinstatement of the motor-sensory circuit (sensorimotor integration) may promote Hebbian-type neuroplasticity (i.e., connections between neurons that are simultaneously active are strengthened), which may lead to better motor recovery.76 A recent review of 31 randomized controlled trials concluded that there is strong evidence that NMES applied in the context of task practice

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SECTION 6  Assistive Devices

(also called functional electrical stimulation, or FES) improves upper extremity function in subacute and chronic stroke.19 This is corroborated by a recent systematic review with metaanalysis of 18 randomized controlled trials (9 were upper limb studies) that concluded that FES improves activity compared with training alone.26 The most recent guidelines published by the American Heart Association recommend NMES in combination with task-specific training for stroke rehabilitation.95 The type of motor improvements that have been reported with NMES include reductions in motor impairment (e.g., improvements in grip and extension strength, volitional EMG activity, Fugl-Meyer scores, active range of motion of wrist and fingers, spasticity) and improvements in motor function (e.g., Box and Blocks Test scores, Action Research Arm Test scores, Arm Motor Abilities Test scores, timed tasks). The persistence and magnitude of effects are variable and depend on the severity of impairment before NMES treatment and time since the stroke, with benefits being greatest in patients who have moderate to mild impairment and who are less than 2 years poststroke.25,27,45,71 Only a few studies have directly compared electrical stimulation modalities. One such study of 122 subacute (6 months or less) stroke survivors found no significant differences among cyclic NMES, EMGtriggered NMES, and sub–motor threshold sensory stimulation in relation to their effect on upper limb function,94 a finding that confirmed previous smaller studies.8,14 A recent study of 80 chronic (longer than 6 months) patients found that CCFES improved hand dexterity more than cyclic NMES,45 which agrees with earlier CCFES studies in subacute patients.47,80 This finding suggests that the method by which NMES is delivered can affect the effectiveness of the treatment. A clinically viable upper extremity neuroprosthesis for daily long-term use as an assistive device is not currently available. Implantable microstimulator12,92 or multichannel implantable pulse generator44 approaches may be suitable for stroke patients who have been carefully screened for prohibitive flexor hypertonia. However, most patients may not be able to realize a robust neuroprosthetic effect unless a means of suppressing flexor hypertonia is incorporated. Emerging technology that uses implanted nerve cuff electrodes to deliver high-frequency stimulus waveforms to block action potentials in nerves may prove capable of suppressing hypertonia.35 Adding such spasticity-suppressing stimulation to an NMES neuroprosthesis could conceivably improve its effect and widen its applicability. Providing an intuitive method by which patients control stimulation to their affected arm and hand without interfering with the task being attempted is another major challenge to implementing upper limb neuroprostheses in stroke. For the neuroprosthesis to be successful, the patient has to find that using it is easier and more effective than any compensatory strategy already attempted.

to wear braces or other orthotic devices, and reduce the time it takes to perform tasks. Although upper extremity neuroprosthetic systems based on externally applied surface electrodes have been tested in SCI,1,70,73,84 these systems have not been used for long-term function. Unlike stroke applications, recovery of volitional function is typically not achieved with electrical stimulation in SCI (with a possible exception being lower extremity function in incomplete SCI81), and therefore implanted neuroprostheses are used for long-term functional use. Two generations of implanted systems for hand function have been evaluated in SCI, the eight-channel implanted receiver-stimulator (IRS-8), which was marketed as the Freehand System (NeuroControl Corporation), and the implanted stimulator-telemeter (IST) system. The IRS-8 was a first generation upper extremity neuroprosthesis for control of hand grasp and release (Fig. 43.3) developed by the Cleveland FES Center.38,66 It was first implemented in a human volunteer in 1986.32,33,82 Eight electrodes were surgically placed on or in the paralyzed muscles of the forearm and hand, and a radiofrequency (RF) inductive link provided the communication and power to the implanted receiverstimulator. The external components of the neuroprosthesis were an external control unit, a transmitting coil, and an external shoulder position transducer.10 Two grasp patterns were provided for functional activities: lateral pinch and palmar prehension.39,68 Graded elevation of the user’s contralateral shoulder resulted in graded grasp closure.28 A multicenter clinical trial was performed to assess the safety, effectiveness, and clinical utility of the Freehand neuroprosthesis in persons with SCI at the C5 or C6 level and resulted in premarket approval (PMA) from the U.S. Food and Drug Administration (FDA) in August 1997. The results showed that the Freehand neuroprosthesis produced increased pinch force in every recipient and significantly increased the ability to move objects of different sizes and weight.66,96 When using the neuroprosthesis, 100% (n = 28) of participants improved in independence in at least one task, and 78% were more independent using the neuroprosthesis in at least three tasks tested. All (100%) participants preferred to use the neuroprosthesis for at least one task, and 96% preferred to use the neuroprosthesis for at least three tasks tested. More than 90% of the participants were satisfied with the neuroprosthesis, and most used it regularly.87 Subsequent follow-up surveys have indicated that usage patterns were maintained for at least Functional electrical stimulation hand grasp system Implanted components

External components

Spinal Cord Injury For individuals with midcervical level SCI, restoration of hand function is the top priority.3 The existing alternatives for providing hand function for these individuals are limited and include braces, orthotics, and adaptive equipment. Surgical interventions, such as tendon transfers, can be used to provide increased hand and arm function.15,31 However, neuroprostheses provide the most promising method for significant gain in hand and arm function for cervical-level SCI.64 With NMES, muscle contractions can be orchestrated to produce coordinated grasp opening and closing; thumb opening, closing, and positioning; wrist extension and flexion; forearm pronation; and elbow extension for individuals with fifth cervical (C5) and sixth cervical (C6) level SCI. The individual controls the coordinated muscle stimulation through movement of the voluntary musculature. Neuroprostheses can be coupled with tendon transfers to maximize function.32 The objectives of these neuroprostheses are to reduce the need of individuals to rely on assistance from others, reduce the need for adaptive equipment, reduce the need

Receiver stimulator

Transmitting coil

Electrodes

Shoulder position transducer

External control unit

Figure 43.3  Freehand neuroprosthesis. An implanted stimulator provides activation of eight muscles. The system is powered through a coil taped to the user’s chest. Control of grasp opening and closing is obtained through movement of the opposite shoulder.

CHAPTER 43  Neuromuscular Electrical Stimulation Applications 4 years after the implant, and usage has extended beyond 20 years.40 However, the company exited the SCI market in 2001.63 A second-generation platform technology was developed that allows stimulation through additional channels and control with implanted sensors, the IST platform.83 Clinical studies of two configurations of the system were initiated, including a system with 10 stimulus channels with an implanted joint angle sensor,29 known as the IST-10,67 and a system with 12 stimulus channels and two channels of myoelectrical signal acquisition, known as the IST-12.36,65 The key feature of the IST platform is the bidirectional telemetry that allows the use of implanted control signals, thus freeing the user of all externally donned components except for a single transmitting coil. The additional stimulation channels provide advanced function, including better hand and arm control. Five individuals with C6-level SCI were implanted with the IST-10 system and ten electrodes. Four received an implanted wrist angle sensor, and one used an external sensor. All subjects demonstrated increased grasp strength and range of motion, increased ability to grasp objects, and increased independence in the performance of ADLs. All individuals were regular users of the neuroprosthesis.67 A myoelectrically controlled version of the IST system, IST-12,36 has been implanted in ten C5/C6 SCI subjects, as shown in Fig. 43.4. Three subjects received bilateral IST-12 systems. All subjects had a cervical-level spinal cord injury and were between 1 and 21 years postinjury at the time of implantation. Myoelectrical control has many distinct advantages for neuroprosthetics.24,48,77 Subjects were able to successfully use the myoelectrical signal from their extensor carpi radialis longus (C6) or brachioradialis (C5) for proportional control of grasp opening and closing. Subjects demonstrated the ability to generate myoelectrical signals from the trapezius, platysma, deltoid, and biceps muscles. The use of myoelectrical control in neuroprostheses allows considerable flexibility in the control algorithms, enabling them to be tailored to each individual subject. The study results indicate that every subject improved significantly in pinch force strength over the presurgery pinch force that was achieved by passive finger and thumb tone augmented with wrist extension. For most subjects, the presurgery pinch force was only useful for acquiring light objects, such as a piece of paper. With the neuroprosthesis turned on, pinch force typically doubled or tripled and could be used to perform a variety of tasks such as holding a fork for eating or a pen for writing. Every subject demonstrated improvement in at least two activities, with one subject demonstrating improvement in 11 of 12 activities tested

and another subject demonstrating improvement in 9 of 9 activities tested. Subjects with bilateral systems are able to perform activities such as using a fork and knife to cut food, using two hands to screw and unscrew a lid on a jar, and brushing hair while blow-drying. Complication rates have been similar to the rates for pacemakers and include infection (approximately 2%) and lead failure (less than 1%).37,40 In summary, upper extremity neuroprostheses have been shown to provide increased function and independence for cervical-level SCI. This improvement in function cannot be gained through the use of orthotics or surgical intervention alone. The clinical results of the first- and second-generation implanted systems have been universally positive, as summarized by the combined study data shown in Table 43.1. Across all studies, 98.4% (61 of 62) of the subjects demonstrated success on the grasp-release test (GRT), as defined by improvement in the ability to manipulate at least one additional object using the neuroprosthesis. In the ADLs test,9 100% (61 of 61) of the subjects demonstrated improvement in the ability to perform ADLs. Taken together, the results show that all 62 subjects (100%) demonstrated improvement in either the GRT or ADL tests (or both). These results demonstrate the exceptional efficacy of implanted upper extremity neuroprosthetic systems.

LOWER LIMB APPLICATIONS NMES to assist lower extremity function has primarily focused on (1) eliminating footdrop during hemiplegic gait, (2) enabling standing after SCI, and (3) empowering walking after SCI. Devices include both surface and implanted NMES systems. Some of these approaches are being expanded to additional conditions, including multiple sclerosis (MS) and cerebral palsy. Device capabilities are also being improved to enhance benefits for users.

Stroke

Neuromuscular Electrical Stimulation for Footdrop Hemiparesis of the lower limb is one of the most common impairments resulting from stroke.52 By 6 months after suffering a stroke, approximately 40% of all stroke survivors are still either unable to walk or require personal assistance to walk even short distances.30 A major contributor to impaired ambulation is the inability to dorsiflex the ankle during the swing phase of gait, which causes the foot to drag and

EMG-controlled functional electrical stimulation hand grasp system Transmitting/receiving coil EMG-recording electrodes Implant stimulator-telemeter

Implanted External

EMG-recording electrodes

Stimulation electrodes

A

External control unit

435

B

Figure 43.4  (A) Implementation of the implanted stimulator-telemeter (IST) as a hand grasp and release neuroprosthesis (not to scale). (B) IST recipient using the neuroprosthetic system.

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SECTION 6  Assistive Devices

TABLE 43.1  Outcomes Summary of Implanted Upper Extremity Neuroprostheses System IRS-8/Freehand IST-10 IST-12 TOTAL

Subjects (Number)a

GRT Improvement

ADLs Abilities Improvement

ADLs Habitsb Improvement

Improvement in at Least One Functional Test

50 3 9 62

49/50 3/3 9/9 61/62

28/28 3/3c 9/9c 40/40

21/21 21/21

50/50 3/3 9/9 62/62

a

No subjects were counted twice. Two IRS-8 subjects upgraded to IST-10 systems and one IRS-8 subject upgraded to an IST-12 system. The Freehand study used a survey-based version of the ADL Abilities test called the ADL Habits (see Peckham PH, Keith MW, Kilgore KL, et al. Efficacy of an implanted neuroprosthesis for restoring hand grasp in tetraplegia: a multicenter study. Arch Phys Med Rehabil. 2001;82(10):1380–1388 for details). c Includes ADL related to both grasp and reach. ADLs, Activities of daily living; GRT, grasp-release test; IRS-8, 8-channel implanted receiver-telemeter system; IST-10, 10-channel implanted stimulator-telemeter system; IST-12, 12-channel implanted stimulator-telemeter system. b

results in inefficient and unsafe ambulation or nonambulation. One of the first applications of NMES was for the correction of footdrop in stroke patients by stimulating the peroneal nerve during gait. Today, there are three FDA-cleared commercially available surface peroneal nerve stimulation (PNS) systems: the Odstock dropped-foot stimulator (ODFS, Odstock Medical, Ltd), the WalkAide (Innovative Neurotronics, Inc.), and the NESS L300 (Bioness, Inc). Each of these devices uses surface electrodes, with the active electrode placed over the common peroneal nerve just below the head of the fibula and the return electrode placed over the tibialis anterior. A cuff that wraps around the upper portion of the shank contains the surface electrodes and stimulator. Step initiation for the impaired limb is detected by a sensor, which triggers stimulation and thereby generates ankle dorsiflexion during swing. The ODFS and NESS L300 both use a wireless heel switch in the shoe of the paretic limb to trigger stimulation when the heel is lifted (i.e., at heel-off in the gait cycle). The WalkAide (Fig. 43.5) uses a tilt sensor built into the cuff to detect the shank tilting forward when the contralateral limb steps forward. Recently, four large random controlled trials evaluated the therapeutic and neuroprosthetic effects of these surface PNS devices compared with an ankle–foot orthosis (AFO), which is usual care. Three of these studies evaluated participants after the subacute phase and demonstrated that PNS had both therapeutic and neuroprosthetic improvements in gait that were comparable with an AFO.6,43,79 Another study focused on patients less than a year after stroke to capitalize on greater potential for early improvement.17 Again, PNS produced results similar to an AFO. Although PNS was not better than an AFO, these studies demonstrated noninferiority. When participants were asked about device preference, the majority preferred PNS to an AFO because they felt more confident, safer, and more comfortable and found PNS easier to don and doff and use long-term. In summary, using surface PNS for 6 to 30 weeks can have significant therapeutic effects on functional mobility and walking speed. Wearing a PNS device (neuroprosthetic effect) can further improve walking speed and walking endurance beyond the therapeutic effect. However, PNS devices are neither superior nor inferior to AFOs with respect to these outcomes, although some patients may prefer PNS to an AFO.72 Surface PNS devices have also been evaluated in adults with multiple sclerosis and children with cerebral palsy. In multiple sclerosis, surface PNS has been shown to provide modest positive neuroprosthetic effects on gait speed, energy cost of walking, knee flexion in swing, stride length, ankle dorsiflexion angle at initial contact, and stair performance.59,78,86,93 The positive effects may be dependent on the individual’s volitional walking speed, with slower walkers benefiting more.60 Therapeutic effects of PNS for multiple sclerosis were minimal if present. In

Figure 43.5  WalkAide (Innovative Neurotronics, Reno, Nevada), a peroneal nerve stimulator cuff with an integrated tilt sensor worn below the knee. (Courtesy of Innovative Neurotronics.)

cerebral palsy, 6 hours per week of surface PNS for 3 months was shown to have a greater therapeutic effect than conventional physical therapy on gait parameters, including stride length and gait speed.16 Another study showed that 24 hours per week of surface PNS for 2 months increased community mobility and balance and decreased gastrocnemius spasticity more than conventional therapy.69 Also, walking with PNS (i.e., the neuroprosthetic effect) improved ankle dorsiflexion at initial contact, dorsiflexion during swing, and step length more than conventional therapy. Implanted PNS systems have been developed to address issues some patients have with surface NMES systems, such as pain from stimulation or difficulty positioning electrodes on the skin. There are two commercially available implanted systems in Europe (CE Mark). The

CHAPTER 43  Neuromuscular Electrical Stimulation Applications STIMuSTEP (FineTech Medical, Ltd.) has two bipolar nerve cuff electrodes implanted around the deep and superficial branches of the common peroneal nerve. The ActiGait system (OttoBock) uses a single nerve cuff with four channels of tripolar electrodes. Both systems are triggered by an external heel switch. An external control unit (ECU) transmits power and stimulation commands to an implanted pulse generator (IPG) based on heel switch detection of swing and stance initiation. STIMuSTEP has been shown to provide a significantly greater neuroprosthetic effect than usual care (AFO, orthopedic shoes, or no device) but no significant therapeutic effect in chronic stroke survivors after 26 weeks of use.50 Walking with the ActiGait produced an average increase in gait speed of 0.4 m/s in a study of 27 chronic patients.56 A pilot study of ActiGait in multiple sclerosis showed positive effects on gait speed and endurance at 10 weeks after surgery that persisted at 1 year.57 Adverse events related to implanted components in these studies included a single nerve injury resulting from a cuff pulling on the nerve and an infection from neurodermatitis that led to device removal. The participant recovered completely from the nerve injury, which was corrected through surgery. Another participant was treated for a woundhealing disorder. One device failed, requiring removal. Overall, improvements from implanted PNS systems are similar to surface PNS systems, but the implanted systems may be easier to use in daily life and provide improved selectivity of stimulation.

Multijoint Neuromuscular Electrical Stimulation for Hemiparetic Gait In addition to loss of active ankle dorsiflexion, many stroke patients have muscle weakness and impaired motor control at the hip and knee; therefore multichannel NMES systems have been and are being developed. The NESS L300Plus (Bioness, Inc.) has two channels of stimulation, which include a PNS cuff and another cuff wrapped around the thigh with electrodes that can be positioned for either knee flexion or extension (Fig. 43.6). This may be useful if a patient cannot generate sufficient knee flexion for toe clearance during swing or knee extension for loading and stance. A study of the NESS L300 Plus in 45 patients found significant therapeutic and neuroprosthetic improvements in walking speed similar to the previously described PNS studies and that the addition of knee

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stimulation to PNS had a statistically significant, but not clinically relevant, additive neuroprosthetic effect on gait speed.85 In a case study of an 18-year-old boy with cerebral palsy, quadriceps stimulation with the NESS L300 Plus was shown to improve crouched gait by increasing knee extension at midstance and stance.34 Patients with greater impairments such as limited hip range of motion, insufficient knee flexion during swing, inadequate knee extension during stance, or limited push off may benefit from assistance at additional joints. An implanted multijoint stimulation system may provide ambulation assistance on a daily basis in a consistent manner with relative ease of use. A case study demonstrated initial feasibility of an implanted neuroprosthesis (Advanced Platform Technology Center and Cleveland FES Center of the Cleveland VA Medical Center) to improve poststroke gait.54 The previously described IRS-8 stimulator was implanted with intramuscular electrodes in hip, knee, and ankle muscles (Fig. 43.7). The participant underwent gait training and stimulation pattern development to coordinate stimulation with volitional walking. A heel switch triggered temporal sequences for swing and stance stimulation, which were initiated at heel-off and heel strike, respectively. Therapeutic improvements in gait speed and spatiotemporal characteristics were statistically significant but modest. However, walking with stimulation assistance (i.e., the neuroprosthetic effect) had a clinically relevant change in gait speed (more than 0.2 m/s) with associated improvements in spatiotemporal characteristics.

Spinal Cord Injury

Neuromuscular Electrical Stimulation for Standing One of the main goals for lower extremity NMES systems for patients with paraplegia related to SCI is to enable them to stand from a seated posture and transfer to another position. Standing enables people to reach high objects, have face-to-face interactions, perform tasks that require standing, and transfer to and from a wheelchair independently or with minimal assistance.

Figure 43.7  Implanted and external components of a multijoint neu-

Figure 43.6  NESS L300 Plus (Bioness Inc., Valencia, California), a dual-cuff system for peroneal nerve and knee extensor stimulation. (Courtesy of Bioness Inc.)

romuscular electrical stimulation system (Cleveland VA Medical Center and Case Western Reserve University). (From Knutson JS, Wilson RD, Makowski NS, Chae J. Stimulation for Return of Function after Stroke. In: Krames, E.S., Peckham, P.H., Rezai, A.R., editors. Neuromodulation, 2nd Edition. London: Academic Press. 2017. Illustration by Erika Woodrum, courtesy of the Cleveland FES Center.)

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SECTION 6  Assistive Devices

An implanted neuroprosthesis for standing and transfer (Cleveland FES Center of the Cleveland VA Medical Center) uses the IRS-8 stimulator. A case series study (n = 15) demonstrated that the implanted neuroprosthesis enabled participants with C6 to T9 SCI to stand.91 Muscles that were stimulated with epimysial or intramuscular electrodes included bilateral vastus lateralis (knee extension), gluteus maximus (hip extension), semimembranosus (hip extension), and erector spinae (trunk extension). An external control unit worn around the waist transmitted power and stimulation commands through an RF communication coil taped to the skin over the stimulator, which was implanted in the anterior lower abdominal region. The user triggered bilateral stimulation with the push of a button on the external control unit or via a finger switch module cabled to the external control unit. After 12 weeks of rehabilitation, the neuroprosthesis enabled all 15 participants to stand. Maximum standing time ranged from 1.3 to 120.3 minutes across the participants, with a median standing time of 4.3 minutes. Participants’ lower extremities supported most of their body weight, and some users were able to release a hand from their walker to perform tasks (Fig. 43.8). Tissue health was evaluated in some participants (n = 8), demonstrating that in addition to enabling stand and transfer function, use of the device improved blood flow and reduced peak pressure while seated.7 Survey results from nine of the participants demonstrated that the system reduced secondary conditions, such as spasticity, bedsores and ulcers, emotional stress, and the occurrence of urinary tract infections.74 Participants also noted improvements in muscle strength, cardiovascular function, and circulation. Use of the device improved participation and ability to work by increasing some participants’ ability to stand to reach high objects or to transfer, allowing access to places where a wheelchair would not reach otherwise. IPGs with more stimulation channels can activate more muscles or include electrodes with multiple contacts, such as nerve cuff electrodes.

Figure 43.8  An individual with T9 ASIA A SCI using an implanted neuromuscular electrical stimulation standing system (Cleveland VA Medical Center and Case Western Reserve University) to perform a functional task. (Reprinted from Ho CH, Triolo RJ, Elias AL, et al. Functional electrical stimulation and spinal cord injury. Phys Med Rehabil Clin N Am. 2014;25:631–654, with permission from Elsevier.)

One participant’s 8-channel system (IRS-8) was upgraded to a 16-channel system (IST-16) with two bilateral four-contact femoral nerve cuff electrodes. This allowed a direct comparison between the 8-channel and 16-channel systems.18 The 16-channel system produced greater knee extension torques, and standing times increased from 2.9 minutes with the 8-channel system to 12.8 minutes with the 16-channel system. Advances in controller design may offer greater functional capacity to participants. For example, with open-loop controllers, the stimulation patterns do not adapt if the individual is bumped while standing or leans forward to reach something. More sophisticated controllers have enabled the NMES system to automatically respond to such perturbations and ensure the individual maintains balance.62 Incorporating feedback control also reduced the amount of load required to be maintained by the upper extremity. Feedforward model–based approaches are also being developed to enable users to control stimulation based on their posture, facilitating postural adjustments and a greater range of movement and requiring less arm support.4 At present, this implanted system is not commercially available.

Neuromuscular Electrical Stimulation for Walking Another major focus has been walking after SCI. The Parastep system (Sigmedics, Inc.) is an FDA-approved multijoint NMES system to enable standing and walking with a walker in people with T4–12 paraplegia. The Parastep uses six pairs of surface electrodes to stimulate bilateral quadriceps, peroneal nerves, and the glutei. A stimulator is worn at the waist, and the user presses buttons on the left and right handles of a walker to trigger sequential left and right steps. A stride can be produced by activating the quadriceps of one leg while initiating a flexion withdrawal reflex in the opposite leg by stimulating the peroneal nerve. To complete the stride, the knee extensors on the swinging leg are activated while the reflex is still flexing the hip. When the stimulus producing the flexion withdrawal reflex is turned off, the user is one step forward in double limb support with bilateral quadriceps stimulation and ready for the next step. More than 1000 people with SCI have used the system, and most have been able to stand and walk at least 30 feet. Secondary improvements include increased lower extremity blood flow, increased muscle mass, and improved cardiac responses. Despite these benefits, the Parastep has limited usefulness for mobility in daily life because of the modest immediate benefit provided, lack of or habituation of adequate flexion withdrawal reflex, and the high metabolic cost of walking.98 Implanted NMES systems with a greater number of stimulation channels may be a more effective way of providing ambulation function. Rather than eliciting a reflex to produce stepping, an 8- or 16-channel neuroprosthesis (Cleveland VA Medical Center and Case Western Reserve University) attempts to stimulate multiple individual muscles with appropriate intensities and timing to create walking movements in response to the user pressing buttons to initiate stepping. A series of case reports evaluated multijoint implanted NMES applied to hip, knee, and ankle muscles. Participants completed a series of home exercises and laboratory-based gait training with the neuroprosthesis. One individual with T10 complete paraplegia received an implanted 16-channel stimulation system consisting of two IRS-8 stimulators.49 He was unable to stand before the implant; the NMES system enabled him to stand and walk short distances. Two individuals with incomplete SCI (C6 ASIA D and C6/7 ASIA C) received an implanted 8-channel stimulator.5,23 Before the intervention, one of them could not initiate steps, and the other could only walk short distances (less than 30 m). After the intervention, therapeutic effects enabled each of them to walk with a walker without stimulation, and the addition of stimulation provided substantial neuroprosthetic benefits to walking ability, including improvements in walking speed, endurance, and joint kinematics. Participants triggered stimulation with a finger switch.

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Although finger switches are an effective trigger, controllers that coordinate stimulation with movement intent as measured from EMG or accelerometers may improve ease of use. One participant (C6 ASIA D) was implanted with an IST-12 stimulator with two EMG-recording electrodes on the right gastrocnemius and quadriceps. The first left step was initiated by pressing a button; successive alternating steps were initiated by EMG control. Right step was initiated by gastrocnemius EMG surpassing a threshold during push-off. Successive left steps were initiated by the right quadriceps EMG surpassing a threshold in response to loading during right stance. EMG-triggered walking could be controlled to walk at a range of speeds and generated faster walking than a cyclic stimulation pattern.53 This participant experienced both therapeutic and neuroprosthetic effects. Two individuals with incomplete SCI (C5 ASIA C and C6 ASIA C) were implanted with IRS-8 stimulators controlled by accelerometer-based triggering of stimulation.97 One participant’s accelerometers detected walker placement, and the other participant’s accelerometers detected bilateral forearm crutch strike to trigger stimulation. Walking with NMES requires high energy expenditure, which limits the maximum walking distance. Combining NMES with passive or powered bracing may improve endurance, stability, and torque generation. For example, combining multijoint implanted NMES with a variableimpedance knee mechanism to provide stiffness in stance and freedom to move during swing reduced the intensity of stimulation needed for knee extension during stance.11 Likewise, a variable hip restraint reduced both forward lean and load on the upper limbs.90 Similarly, combining a hip and knee state-controlled brace with multijoint NMES improved the stand-to-sit transition in SCI participants over NMES alone. The exoskeleton produced bilateral hip and knee flexion coupling and knee damping to reduce knee angular velocity, upper limb support, and impact force.13 Other hybrid approaches combine motorized exoskeletons with surface NMES. Surface NMES applied to knee flexors and extensors reduced the necessary torque output from motors at the hip and knee relative to the motorized exoskeleton alone.22

NMES, Neuromove, NESS H200) are commercially available for therapeutic use in stroke. Implanted 8- to 12-channel neuroprostheses have been highly successful in giving SCI patients with C5 and C6 level tetraplegia grasp-release hand function and greater independence in ADLs. However, there remains a need for neuroprostheses that can be used long-term for assisting stroke patients with severe upper limb impairment in performing ADLs. NMES can improve gait after stroke and enable standing and walking after SCI. Surface NMES systems that stimulate the peroneal nerve to prevent footdrop during hemiparetic gait (NESS L300, ODFS, and WalkAide) are available in the United States, and implanted systems (ActiGait and STIMuSTEP) are available in Europe. These systems can have both therapeutic and neuroprosthetic effects. Multijoint lower limb neuroprostheses to assist walking in stroke and standing and walking in SCI are in development and have shown positive results in case series studies. An external ankle–knee system for stroke (NESS L300 Plus) is commercially available in the United States, and a six-channel external system for SCI (Parastep) has limited availability through a foundation. Implanted systems with 8 to 16 channels are not yet available outside of research programs. Hybrid systems that combine NMES with exoskeletons are also being developed, as are more advanced stimulators and controllers, which may increase functional capabilities. Decades of research and development have led to NMES systems that can be used clinically. New ideas for improving existing devices and achieving greater return of function and quality of life continue to be explored. As engineers develop NMES systems that are more sophisticated and more capable of addressing more severe impairments, it is critical that they work with clinicians and patients to ensure that the technology can be practically implemented in clinical and home environments. Programs for training clinicians in the implementation of NMES systems are also critical to successfully disseminating NMES technology that can have a great impact on the quality of life of many individuals who have experienced a neurologic injury.

CONCLUSION

A complete reference list can be found online at ExpertConsult.com.

NMES therapies can improve volitional upper limb movement and hand function in stroke survivors. Several NMES devices (e.g., Intelect

CHAPTER 43  Neuromuscular Electrical Stimulation Applications

REFERENCES 1. Alon G, McBride K. Persons with C5 or C6 tetraplegia achieve selected functional gains using a neuroprosthesis. Arch Phys Med Rehabil. 2003;84(1):119–124. 2. Alon G, Levitt AF, McCarthy PA. Functional electrical stimulation enhancement of upper extremity functional recovery during stroke rehabilitation: a pilot study. Neurorehabil Neural Repair. 2007;21(3):207–215. 3. Anderson KD. Targeting recovery: Priorities of the spinal cord-injured population. J Neurotrauma. 2004;21(10):1371–1383. 4. Audu ML, Gartman SJ, Nataraj R, et al. Posture-dependent control of stimulation in standing neuroprosthesis: Simulation feasibility study. J Rehabil Res Dev. 2014;51(3):481–496. 5. Bailey SN, Hardin EC, Kobetic R, et al. Neurotherapeutic and neuroprosthetic effects of implanted functional electrical stimulation for ambulation after incomplete spinal cord injury. J Rehabil Res Dev. 2010;47(1):7–16. 6. Bethoux F, Rogers HL, Nolan KJ, et al. The effects of peroneal nerve functional electrical stimulation versus ankle-foot orthosis in patients with chronic stroke: A randomized controlled trial. Neurorehabil Neural Repair. 2014;28(7):688–697. 7. Bogie KM, Triolo RJ. Effects of regular use of neuromuscular electrical stimulation on tissue health. J Rehabil Res Dev. 2003;40(6):469–475. 8. Boyaci A, Topuz O, Alkan H, et al. Comparison of the effectiveness of active and passive neuromuscular electrical stimulation of hemiplegic upper extremities: A randomized, controlled trial. Int J Rehabil Res. 2013;36(4):315–322. 9. Bryden AM, Kilgore K, Keith MW, et al. Assessing activity of daily living performance after implantation of an upper extremity neuroprosthesis. Top Spinal Cord Inj Rehabil. 2008;13(4):37–53. 10. Buckett JR, Peckham PH, Thrope GB, et al. A flexible, portable system for neuromuscular stimulation in the paralyzed upper extremity. IEEE Trans Biomed Eng. 1988;35(11):897–904. 11. Bulea TC, Kobetic R, Audu ML, et al. Stance controlled knee flexion improves stimulation driven walking after spinal cord injury. J Neuroengineering Rehabil. 2013;10:68. 12. Burridge JH, Turk R, Merrill D, et al. A personalized sensor-controlled microstimulator system for arm rehabilitation poststroke. Part 2: Objective outcomes and patients’ perspectives. Neuromodulation. 2011;14(1):80–88, discussion 88. 13. Chang SR, Nandor MJ, Kobetic R, et al. Improving stand-to-sit maneuver for individuals with spinal cord injury. J Neuroengineering Rehabil. 2016;13:27. 14. de Kroon JR, Ijzerman MJ. Electrical stimulation of the upper extremity in stroke: Cyclic versus EMG-triggered stimulation. Clin Rehabil. 2008;22(8):690–697. 15. Ejeskar A, Hentz VR, Holst-Nielsen F, et al. Reconstructive hand surgery. Spinal Cord. 1999;37(7):475–479. 16. El-Shamy SM, Abdelaal AA. WalkAide efficacy on gait and energy expenditure in children with hemiplegic cerebral palsy: A randomized controlled trial. Am J Phys Med Rehabil. 2016;95(9):629–638. 17. Everaert DG, Stein RB, Abrams GM, et al. Effect of a foot-drop stimulator and ankle-foot orthosis on walking performance after stroke: A multicenter randomized controlled trial. Neurorehabil Neural Repair. 2013;27(7):579–591. 18. Fisher LE, Miller ME, Bailey SN, et al. Standing after spinal cord injury with four-contact nerve-cuff electrodes for quadriceps stimulation. IEEE Trans Neural Syst Rehabil Eng. 2008;16(5):473–478. 19. Foley N, Cotoi A, Serrato J, et al. Upper extremity interventions. In: Teasell R, ed. The Stroke Rehabilitation Evidence Based Review: 17th Edition. 17th ed. Canadian Partnership for Stroke Recovery; 2016. 20. Franceschini M, La Porta F, Agosti M, et al. Is health-related-quality of life of stroke patients influenced by neurological impairments at one year after stroke? Eur J Phys Rehabil Med. 2010;46(3):389–399. 21. Francisco G, Chae J, Chawla H, et al. Electromyogram-triggered neuromuscular stimulation for improving the arm function of acute

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stroke survivors: A randomized pilot study. Arch Phys Med Rehabil. 1998;79(5):570–575. 22. Ha KH, Murray SA, Goldfarb M. An approach for the cooperative control of FES with a powered exoskeleton during level walking for persons with paraplegia. IEEE Trans Neural Syst Rehabil Eng. 2016;24(4):455–466. 23. Hardin E, Kobetic R, Murray L, et al. Walking after incomplete spinal cord injury using an implanted FES system: A case report. J Rehabil Res Dev. 2007;44(3):333–346. 24. Hart RL, Kilgore KL, Peckham PH. A comparison between control methods for implanted FES hand-grasp systems. IEEE Trans Rehabil Eng. 1998;6(2):208–218. 25. Hendricks HT, IJzerman MJ, de Kroon JR, et al. Functional electrical stimulation by means of the ‘Ness Handmaster Orthosis’ in chronic stroke patients: an exploratory study. Clin Rehabil. 2001;15(2):217–220. 26. Howlett OA, Lannin NA, Ada L, et al. Functional electrical stimulation improves activity after stroke: A systematic review with meta-analysis. Arch Phys Med Rehabil. 2015;96(5):934–943. 27. Hsu SS, Hu MH, Luh JJ, et al. Dosage of neuromuscular electrical stimulation: is it a determinant of upper limb functional improvement in stroke patients? J Rehabil Med. 2012;44(2):125–130. 28. Johnson MW, Peckham PH. Evaluation of shoulder movement as a command control source. IEEE Trans Biomed Eng. 1990;37(9):876–885. 29. Johnson MW, Peckham PH, Bhadra N, et al. Implantable transducer for two-degree of freedom joint angle sensing. IEEE Trans Rehabil Eng. 1999;7(3):349–359. 30. Jorgensen HS, Nakayama H, Raaschou HO, et al. Recovery of walking function in stroke patients: The Copenhagen Stroke Study. Arch Phys Med Rehabil. 1995;76(1):27–32. 31. Keith MW, Peljovich AE. Rehabilitation of the hand and upper extremity in tetraplegia. In: Hunter, MacKinnon, Callahan, et al, eds. Rehabilitation of the Hand and Upper Extremity. St. Louis, MO: Mosby, Inc; 2002. 32. Keith MW, Kilgore KL, Peckham PH, et al. Tendon transfers and functional electrical stimulation for restoration of hand function in spinal cord injury. J Hand Surg Am. 1996;21(1):89–99. 33. Keith MW, Peckham PH, Thrope GB, et al. Implantable functional neuromuscular stimulation in the tetraplegic hand. J Hand Surg Am. 1989;14(3):524–530. 34. Khamis S, Martikaro R, Wientroub S, et al. A functional electrical stimulation system improves knee control in crouch gait. J Child Orthop. 2015;9(2):137–143. 35. Kilgore KL, Bhadra N. Reversible nerve conduction block using kilohertz frequency alternating current. Neuromodulation. 2013. 36. Kilgore KL, Hoyen HA, Bryden AM, et al. An implanted upper-extremity neuroprosthesis using myoelectric control. J Hand Surg Am. 2008;33(4):539–550. 37. Kilgore KL, Peckham PH, Keith MW, et al. Durability of implanted electrodes and leads in an upper-limb neuroprosthesis. J Rehabil Res Dev. 2003;40(6):457–468. 38. Kilgore KL, Peckham PH, Keith MW, et al. An implanted upper-extremity neuroprosthesis. Follow-up of five patients. J Bone Joint Surg Am. 1997;79(4):533–541. 39. Kilgore KL, Peckham PH, Thrope GB, et al. Synthesis of hand grasp using functional neuromuscular stimulation. IEEE Trans Biomed Eng. 1989;36(7):761–770. 40. Kilgore KL, Peckham P, Keith MW. Twenty year experience with implanted neuroprostheses. Conf Proc IEEE Eng Med Biol Soc. 2009;2009:7212–7215. 41. Kimberley TJ, Lewis SM, Auerbach EJ, et al. Electrical stimulation driving functional improvements and cortical changes in subjects with stroke. Exp Brain Res. 2004;154(4):450–460. 42. Kleim JA, Jones TA. Principles of experience-dependent neural plasticity: Implications for rehabilitation after brain damage. J Speech Lang Hear Res. 2008;51(1):S225–S239. 43. Kluding PM, Dunning K, O’Dell MW, et al. Foot drop stimulation versus ankle foot orthosis after stroke: 30-week outcomes. Stroke. 2013;44(6):1660–1669.

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SECTION 6  Assistive Devices

44. Knutson JS, Chae J, Hart RL, et al. Implanted neuroprosthesis for assisting arm and hand function after stroke: A case study. J Rehabil Res Dev. 2012a;49(10):1505–1516. 45. Knutson JS, Gunzler DD, Wilson RD, et al. Contralaterally controlled functional electrical stimulation improves hand dexterity in chronic hemiparesis: A randomized trial. Stroke. 2016;47:2596–2602. 46. Knutson JS, Harley MY, Hisel TZ, et al. Improving hand function in stroke survivors: A pilot study of contralaterally controlled functional electric stimulation in chronic hemiplegia. Arch Phys Med Rehabil. 2007;88(4):513–520. 47. Knutson JS, Harley MY, Hisel TZ, et al. Contralaterally controlled functional electrical stimulation for upper extremity hemiplegia: An early-phase randomized clinical trial in subacute stroke patients. Neurorehabil Neural Repair. 2012b;26(3):239–246. 48. Knutson JS, Hoyen HA, Kilgore KL, et al. Simulated neuroprosthesis state activation and hand-position control using myoelectric signals from wrist muscles. J Rehabil Res Dev. 2004;41(3B):461–472. 49. Kobetic R, Triolo RJ, Uhlir JP, et al. Implanted functional electrical stimulation system for mobility in paraplegia: A follow-up case report. IEEE Trans Rehabil Eng. 1999;7(4):390–398. 50. Kottink AI, Hermens HJ, Nene AV, et al. A randomized controlled trial of an implantable 2-channel peroneal nerve stimulator on walking speed and activity in poststroke hemiplegia. Arch Phys Med Rehabil. 2007;88(8):971–978. 51. Kwakkel G, Kollen BJ, van der Grond J, et al. Probability of regaining dexterity in the flaccid upper limb: Impact of severity of paresis and time since onset in acute stroke. Stroke. 2003;34(9):2181–2186. 52. Lai SM, Studenski S, Duncan PW, et al. Persisting consequences of stroke measured by the Stroke Impact Scale. Stroke. 2002;33(7):1840–1844. 53. Lombardo LM, Bailey SN, Foglyano KM, et al. A preliminary comparison of myoelectric and cyclic control of an implanted neuroprosthesis to modulate gait speed in incomplete SCI. J Spinal Cord Med. 2015;38(1):115–122. 54. Makowski NS, Kobetic R, Lombardo LM, et al. Improving walking with an implanted neuroprosthesis for hip, knee, and ankle control after stroke. Am J Phys Med Rehabil. 2016. 55. Mann G, Taylor P, Lane R. Accelerometer-triggered electrical stimulation for reach and grasp in chronic stroke patients: A pilot study. Neurorehabil Neural Repair. 2011;25(8):774–780. 56. Martin KD, Polanski WH, Schulz AK, et al. Restoration of ankle movements with the ActiGait implantable drop foot stimulator: A safe and reliable treatment option for permanent central leg palsy. J Neurosurg. 2016a;124(1):70–76. 57. Martin KD, Polanski WH, Schulz AK, et al. ActiGait implantable drop foot stimulator in multiple sclerosis: A new indication. J Neurosurg. 2016b;1–6. 58. Meilink A, Hemmen B, Seelen HA, et al. Impact of EMG-triggered neuromuscular stimulation of the wrist and finger extensors of the paretic hand after stroke: A systematic review of the literature. Clin Rehabil. 2008;22(4):291–305. 59. Miller L, Rafferty D, Paul L, et al. A comparison of the orthotic effect of the Odstock Dropped Foot Stimulator and the Walkaide functional electrical stimulation systems on energy cost and speed of walking in Multiple Sclerosis. Disabil Rehabil Assist Technol. 2014. 60. Miller L, Rafferty D, Paul L, et al. The impact of walking speed on the effects of functional electrical stimulation for foot drop in people with multiple sclerosis. Disabil Rehabil Assist Technol. 2016;11(6):478–483. 61. Nascimento LR, Michaelsen SM, Ada L, et al. Cyclical electrical stimulation increases strength and improves activity after stroke: A systematic review. J Physiother. 2014;60(1):22–30. 62. Nataraj R, Audu ML, Triolo RJ. Center of mass acceleration feedback control of standing balance by functional neuromuscular stimulation against external postural perturbations. IEEE Trans Biomed Eng. 2013;60(1):10–19. 63. Pancrazio JJ, Chen D, Fertig SJ, et al. Toward Neurotechnology Innovation: Report from the 2005 Neural Interfaces Workshop. An NIH-Sponsored Event. Neuromodulation. 2006;9(1):1–7.

64. Peckham PH, Kilgore KL. Challenges and opportunities in restoring function after paralysis. IEEE Trans Biomed Eng. 2013;60(3): 602–609. 65. Peckham PH, Knutson JS. Functional electrical stimulation for neuromuscular applications. Annu Rev Biomed Eng. 2005;7: 327–360. 66. Peckham PH, Keith MW, Kilgore KL, et al. Efficacy of an implanted neuroprosthesis for restoring hand grasp in tetraplegia: A multicenter study. Arch Phys Med Rehabil. 2001;82(10):1380–1388. 67. Peckham PH, Kilgore KL, Keith MW, et al. An advanced neuroprosthesis for restoration of hand and upper arm control using an implantable controller. J Hand Surg Am. 2002;27(2):265–276. 68. Peckham PH, Thrope GB, Buckett JR. Coordinated two mode grasp in the quadriplegic initiated by functional neuromuscular stimulation. In: Campbell RM, ed. IFAC Control Aspects of Prosthetics and Orthotics. Oxford: Pergamon Press; 1983. 69. Pool D, Valentine J, Bear N, et al. The orthotic and therapeutic effects following daily community applied functional electrical stimulation in children with unilateral spastic cerebral palsy: A randomised controlled trial. BMC Pediatr. 2015;15:154. 70. Popovic MR, Thrasher TA, Adams ME, et al. Functional electrical therapy: Retraining grasping in spinal cord injury. Spinal Cord. 2006;44(3):143–151. 71. Powell J, Pandyan AD, Granat M, et al. Electrical stimulation of wrist extensors in poststroke hemiplegia. Stroke. 1999;30(7):1384–1389. 72. Prenton S, Hollands KL, Kenney LP. Functional electrical stimulation versus ankle foot orthoses for foot-drop: A meta-analysis of orthotic effects. J Rehabil Med. 2016;48(8):646–656. 73. Prochazka A, Gauthier M, Wieler M, et al. The bionic glove: An electrical stimulator garment that provides controlled grasp and hand opening in quadriplegia. Arch Phys Med Rehabil. 1997;78(6):608–614. 74. Rohde LM, Bonder BR, Triolo RJ. Exploratory study of perceived quality of life with implanted standing neuroprostheses. J Rehabil Res Dev. 2012;49(2):265–278. 75. Rosewilliam S, Malhotra S, Roffe C, et al. Can surface neuromuscular electrical stimulation of the wrist and hand combined with routine therapy facilitate recovery of arm function in patients with stroke? Arch Phys Med Rehabil. 2012;93(10):1715–1721.e1711. 76. Rushton DN. Functional electrical stimulation and rehabilitation–an hypothesis. Med Eng Phys. 2003;25(1):75–78. 77. Scott TR, Peckham PH, Kilgore KL. Tri-state myoelectric control of bilateral upper extremity neuroprostheses for tetraplegic individuals. IEEE Trans Rehabil Eng. 1996;4(4):251–263. 78. Sheffler LR, Hennessey MT, Knutson JS, et al. Neuroprosthetic effect of peroneal nerve stimulation in multiple sclerosis: A preliminary study. Arch Phys Med Rehabil. 2009;90(2):362–365. 79. Sheffler LR, Taylor PN, Gunzler DD, et al. Randomized controlled trial of surface peroneal nerve stimulation for motor relearning in lower limb hemiparesis. Arch Phys Med Rehabil. 2013;94(6):1007–1014. 80. Shen Y, Yin Z, Fan Y, et al. Comparison of the effects of contralaterally controlled functional electrical stimulation and neuromuscular electrical stimulation on upper extremity functions in patients with stroke. CNS Neurol Disord Drug Targets. 2015;14(10):1260–1266. 81. Shin HK, Cho SH, Jeon HS, et al. Cortical effect and functional recovery by the electromyography-triggered neuromuscular stimulation in chronic stroke patients. Neurosci Lett. 2008;442(3):174–179. 82. Smith B, Peckham PH, Keith MW, et al. An externally powered, multichannel, implantable stimulator for versatile control of paralyzed muscle. IEEE Trans Biomed Eng. 1987;34(7):499–508. 83. Smith B, Tang Z, Johnson MW, et al. An externally powered, multichannel, implantable stimulator-telemeter for control of paralyzed muscle. IEEE Trans Biomed Eng. 1998;45(4):463–475. 84. Snoek GJ, IJzerman MJ, in ‘t Groen FA, et al. Use of the NESS handmaster to restore handfunction in tetraplegia: Clinical experiences in ten patients. Spinal Cord. 2000;38(4):244–249. 85. Springer S, Vatine JJ, Lipson R, et al. Effects of dual-channel functional electrical stimulation on gait performance in patients with hemiparesis. Scientific World Journal. 2012;2012:530906.

CHAPTER 43  Neuromuscular Electrical Stimulation Applications 86. Street T, Taylor P, Swain I. Effectiveness of functional electrical stimulation on walking speed, functional walking category, and clinically meaningful changes for people with multiple sclerosis. Arch Phys Med Rehabil. 2015;96(4):667–672. 87. Stroh Wuolle K, Van Doren CL, Bryden AM, et al. Satisfaction with and usage of a hand neuroprosthesis. Arch Phys Med Rehabil. 1999;80(2):206–213. 88. Thorsen R, Cortesi M, Jonsdottir J, et al. Myoelectrically driven functional electrical stimulation may increase motor recovery of upper limb in poststroke subjects: A randomized controlled pilot study. J Rehabil Res Dev. 2013;50(6):785–794. 89. Thrasher TA, Zivanovic V, McIlroy W, et al. Rehabilitation of reaching and grasping function in severe hemiplegic patients using functional electrical stimulation therapy. Neurorehabil Neural Repair. 2008;22(6):706–714. 90. To CS, Kobetic R, Bulea TC, et al. Sensor-based hip control with hybrid neuroprosthesis for walking in paraplegia. J Rehabil Res Dev. 2014;51(2):229–244. 91. Triolo RJ, Bailey SN, Miller ME, et al. Longitudinal performance of a surgically implanted neuroprosthesis for lower-extremity exercise, standing, and transfers after spinal cord injury. Arch Phys Med Rehabil. 2012;93(5):896–904.

439.e3

92. Turk R, Burridge JH, Davis R, et al. Therapeutic effectiveness of electric stimulation of the upper-limb poststroke using implanted microstimulators. Arch Phys Med Rehabil. 2008;89(10):1913–1922. 93. van der Linden ML, Scott SM, Hooper JE, et al. Gait kinematics of people with multiple sclerosis and the acute application of functional electrical stimulation. Gait Posture. 2014;39(4):1092–1096. 94. Wilson RD, Page SJ, Delahanty M, et al. Upper-limb recovery after stroke: A randomized controlled trial comparing EMG-triggered, cyclic, and sensory electrical stimulation. Neurorehabil Neural Repair. 2016. 95. Winstein CJ, Stein J, Arena R, et al. Guidelines for adult stroke rehabilitation and recovery: A guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2016;47(6):e98–e169. 96. Wuolle KS, Van Doren CL, Thrope GB, et al. Development of a quantitative hand grasp and release test for patients with tetraplegia using a hand neuroprosthesis. J Hand Surg Am. 1994;19(2):209–218. 97. Foglyano KM, Schnellenberger JR, Kobetic R, et al. Accelerometer-based step initiation control for gait-assist neuroprostheses. J Rehabil Res Dev. 2016;53(6):919–932. 98. Brissot R, Gallien P, Le Bot MP, et al. Clinical experience with functional electrical stimulation-assisted gait with Parastep in spinal-cord injured patients. Spine (Phila Pa 1976). 2000;25(4):501–508.