SCI Nursing Journal

Graham H. Creasey, MD, FRCSEd; Chester H. Ho, MD; Ronald J. Triolo, PhD; David R. Gater, MD, PhD; Anthony F. DiMarco, MD; Kath M. Bogie, DPhil; Michael W. Keith, MD, FACS

This article first appeared in the Journal of Spinal Cord Medicine, Volume 27, Number 4, and is reprinted with permission.

ABSTRACT

Summary: During the last one-half century, electrical stimulation has become clinically significant for improving health and restoring useful function after spinal cord injury. Short-term stimulation can be provided by electrodes on the skin or percutaneous fine wires, but implanted systems are preferable for long-term use. Electrical stimulation of intact lower motor neurons can exercise paralyzed muscles and reverse wasting; improve strength, endurance, and cardiovascular fitness; and may reduce the progression of osteoporosis. Other potential therapeutic uses being investigated include reduction of spasticity, prevention of deep vein thrombosis, and improvement of tissue health. Pacing of intact phrenic nerves in high tetraplegia can produce effective respiration without mechanical ventilation, allowing improved speech, increased mobility, and increased sense of well-being. Improvement of cough has also been demonstrated. Stimulation of intact sacral nerves can produce effective micturition and reduce urinary tract infection; it can also improve bowel function and erection. It is usually combined with posterior sacral rhizotomy to improve continence and bladder capacity, and the combination has been shown to reduce costs of care. Electroejaculation can now produce semen in most men with spinal cord injury. Significant achievements have also been made in restoring limb function. Useful hand grasp can be provided in C5 and C6 tetraplegia, reducing dependence on adapted equipment and assistants. Standing, assistance with transfers, and walking for short distances can be provided to selected persons with paraplegia, improving their access to objects, places, and opportunities that are inaccessible from a wheelchair. This review summarizes the current state of therapeutic and neuroprosthetic applications of electrical stimulation after spinal cord injury and identifies some future directions of research and clinical and commercial development.

Key Words: electrical stimulation; spinal cord injuries; neuroprosthesis; paraplegia; tetraplegia; ventilation; bladder, neurogenic; activities of daily living; spasticity; pain; pressure ulcer

Introduction

Since ancient times, there have been observations of some of the effects of electricity on the body, but understanding these effects depended on the growing knowledge of electricity and electrophysiology in the 19th and 20th centuries. In the last 50 years, the microelectronic industry has made a significant number of clinically useful applications possible. Diagnostic electrical stimulation is widely used to distinguish innervated from denervated muscle and to test for the integrity of neural pathways. Therapeutic benefits persisting after electrical stimulation have been claimed in a great variety of conditions and are now being investigated more systematically. Functional electrical stimulation (FES) indicates the restoration of useful movement or sensation during electrical stimulation of excitable was the first clinically useful application of functional stimulation applied to muscle, while defibrillation of the heart might be considered an example of therapeutic stimulation. Following spinal cord injury (SCI), there are usually many muscles and peripheral nerves below the level of the lesion that can be activated for therapeutic and functional purposes.

Physiologic Principles

Muscle and nerve cells, like other cells, have electrical properties; their interior is usually electrically negative relative to the extracellular environment. When this polarization is reversed in one area of the cell membrane by application of an electrical stimulus, the depolarization can spread over the rest of the membrane, resulting in conduction of an action potential along a nerve and contraction of the muscle cells that it innervates. Denervated muscle cells undergo progressive atrophy that probably can not be prevented by electrical stimulation. Innervated muscle cells may undergo disuse atrophy but remain responsive to electrical stimulation applied directly to the muscle cell or to the motor nerve, the latter usually having a lower threshold. This is the basis of diagnostic tests of muscle innervation and neuromuscular stimulation that can be used for many years after damage to upper motor neurons, provided the lower motor neurons are intact.

Stimulation can also be applied to sensory neurons to produce action potentials propagating toward the central nervous system to affect sensation or reflexes or to modify activity in the central nervous system. Sensory function has been restored by implants that stimulate the hair cells of the cochlea to improve the sense of hearing; these have been implanted in over 50,000 people during the last 30 years. Pain can sometimes be modified by sensory stimulation, using transcutaneous electrical nerve stimulation or electrodes implanted near the spinal cord, and reflexes in the bladder or lower limbs can be inhibited by similar sensory stimulation. Stimulation of the vagus nerve can reduce the frequency of seizures by mechanisms that are still not fully understood.

Deep brain stimulation is also gaining acceptance for reduction of pain or abnormal movements such as tremor, chorea, and athetosis. It is also being investigated for treatment of psychiatric conditions such as obsessive- compulsive disorders.

The use of electrical stimulation to modify existing activity in the central nervous system is sometimes called neuromodulation; this can be distinguished from stimulating nerves to produce function directly, replacing the function of damaged nerve tissue by a neural prosthesis.

Neural prostheses have particular potential in conditions, such as SCI, that cause permanent damage to upper motor neurons but leave many lower motor neurons and muscles intact and responsive to stimulation. The main requirements have been to develop safe and effective patterns of stimulation that can be applied on a long-term and cost-effective basis, and such requirements have been met in several areas. Neuromodulation of pain or reflex activity such as spasticity and the production of useful function by stimulating sensory nerves is also undergoing increasing investigation in patients with SCI.

Techniques

The least invasive techniques of applying electrical stimulation use electrodes applied to the skin surface. These are suitable for diagnostic and therapeutic purposes but are not always sufficiently selective or reproducible for restoring useful function; managing the electrodes, wires, and stimulators can also become inconvenient for long-term use.

Fine wire electrodes inserted with a hypodermic needle are widely used for diagnostic purposes, and some such percutaneous electrodes have been developed that can be left in place safely for months or years for research purposes. These allow specific reproducible stimulation patterns to be developed and evaluated using stimulators outside the body, although some care is needed for maintaining the skin exit sites and external leads.

For long-term functional use, it is most convenient to have stimulators fully implanted within the body. These may be powered by implanted batteries, in which case, revision surgery is required every few years to replace the batteries. However, implantable rechargeable batteries are being developed. More commonly, the implant is powered by radio frequency transmission from a controller outside the body; this controller also provides the opportunity for programming and controlling the implant.

The components of a fully implanted system generally include:

(a) Electrodes applied to muscles or nerves. Those placed around nerves usually need less current but require more complexity if different muscles innervated by the same nerve trunk are to be selected. Electrodes inserted into the body of a muscle or sutured to its surface primarily activate contraction via terminal branches of the motor nerve within the muscle.

(b) Wires or leads are usually insulated with silicone rubber and designed to be highly flexible to withstand years of movement.

(c) Connectors allow systems to be assembled during implantation, simplifying surgery, and parts can be selectively replaced in case of faults or improvements.

(d) Receiver/stimulators generate the patterns of small electrical pulses required for producing action potentials in muscle or nerve cells using electronic circuits packaged in hermetically sealed containers to protect them from body fluids. They are often under the control of radio signals received from an external controller.

(e) Transmitter/controllers outside the body provide power to implants by radio frequency transmission and can be programmed to transmit various patterns of stimulation in response to signals from sensors; in some cases, they may receive signals transmitted from sensors inside the body.

(f) Sensors may be external to the body or internal; they allow the user to command the function desired; to provide the user with some indication of function, such as force or position; and to provide the device with feedback for more automatic “closed-loop” control.

All implanted components must be designed to cause no harm to the tissues, whether electrical, chemical, or mechanical, and to be resistant to damage by body fluids or movement. Ideally, the implant should have a lifetime longer than that of the user, but in case of faults or improvements, provision should be made for repair or replacement.

Therapeutic Effects

After SCI, the therapeutic uses of electrical stimulation that have been most studied are various forms of exercise training; other potential applications being investigated, which have yet to gain widespread clinical acceptance, include deep venous thrombosis (DVT) prevention, spasticity management, tissue health improvement, and pressure ulcer treatment and prevention.

Therapeutic Exercise Training

Electrical stimulation has been used in various ways for muscle exercise after SCI (1–6). Intermittent trains of stimuli can move limbs against weights or other resistance, and a coordinated stimulation pattern can elicit a lower extremity cycling pattern for leg cycle ergometry (LCE), using skin surface electrodes, as in several commercial products (see Appendix).

Electrical stimulation can increase strength in paralyzed lower limb muscles of people with SCI (7–9). The quadriceps femoris of persons with paraplegia who had undergone 8 months of lower extremity anaerobic electrical stimulation training showed increased cross-sectional area (CSA), determined by computerized tomography, accompanied by significant increases in type II (but not type I) fiber diameter (10). Similar changes in CSA were noted for persons with tetraplegia after 6 months of training with an FES leg cycle ergometry (11,12). Electrical stimulation can also improve muscle endurance for lower extremity muscles subject to prolonged aerobic exercise (13–16). Furthermore, there are indirect benefits from lower extremity electrical stimulation exercise programs in SCI. These include cardiovascular benefits (17–21), increased high-density lipoprotein levels (22), and improved insulin sensitivity (23, 24). Chronic electrical stimulation LCE may also increase lower extremity bone mineral density or at least slow the progression of lower extremity osteopenia by increasing bone remodeling caused by contraction of lower extremity musculature on its point of insertion (25–27). Once FES training has been discontinued, however, lower extremity bone mineral density reverts to its previous level, just above fracture threshold.

A logical progression in the development of electrical stimulation lower extremity exercise training has been the combined use of concurrent arm cycle ergometry (ACE) and electrical stimulation LCE, termed HYBRID exercise (28,29), for enhanced cardiovascular benefits.

DVT Prevention

Current practice following acute SCI includes a combination of low molecular weight heparin or unfractionated heparin together with compression hose or sequential compression devices applied to the calf. However, there exists evidence that the combination of low- dose heparin and electrical stimulation with electrodes on the skin over the tibialis anterior and gastrocnemius muscles is effective for DVT prophylaxis in acute SCI (30–32). As with sequential compression devices, it is necessary to set up and maintain the electrical stimulation unit for almost 24 h/d.

Spasticity Management

Current management of spasticity often involves oral medications that have significant side effects. In severe cases, intrathecal baclofen is increasingly considered. Although it may work well, it necessitates an invasive procedure that carries potential risks. The possibility of an effective local physical treatment is therefore attractive.

Several researchers have noted that the use of an FES system or surface electrical stimulation in the extremities may reduce spasticity (33–38), whereas others have found inconsistent results (39). There have been reports of cutaneous stimulation leading to a reduction in spasticity (40,41). The use of epidural electrical stimulation of posterior structures of the lumbosacral spinal cord in subjects with SCI for the treatment of spasticity has also been reported (42).

Despite the largely encouraging clinical observations, very few studies specifically addressed the physiologic mechanisms by which electrical stimulation might have an effect on spasticity. There are hypotheses, such as fatigue of the stimulated muscles and reciprocal inhibition (43), but much more scientific work is needed in this area.

Tissue Health: Pressure Ulcer Treatment and Prevention

Pressure Ulcer Treatment. Surface electrical stimulation is one of only two adjunctive modalities for pressure ulcer treatment recommended by the Agency for Health Care Policy and Research (AHCPR; now the Agency for Health Care Research and Quality) (44). It has been recommended for stage III and IV pressure ulcers that are unresponsive to traditional therapies and recalcitrant stage II pressure ulcers. Despite scientific evidence from clinical trials (45–48), the exact mechanism(s) by which this modality works remain(s) unclear. Furthermore, there is no standard clinical guideline for its use in the treatment of pressure ulcers in SCI. Clinical guidelines will probably be necessary for this treatment modality to gain more widespread clinical acceptance.

Pressure Ulcer Prevention. Electrical stimulation is being investigated as a method of preventing pressure ulcers both by altering the intrinsic characteristics of paralyzed muscle and by reducing the effects of extrinsic applied pressure through enhanced pressure relief maneuvers.

The primary site of pressure ulcer development in wheelchair users is the ischial region. In the sitting posture, the gluteus maximus muscle may lay directly over the ischial tuberosity or be adjacent to it. A gluteal percutaneous electrical stimulation system currently being studied allows the user to receive preprogrammed electrical stimulation. Percutaneous fine wire electrodes are implanted bilaterally in the gluteus maximus, caudal to the sitting interface, and routed subcutaneously to exit the skin on the front of the thigh. An external pager-sized stimulator attached to these wires provides the stimulation. Preliminary results have demonstrated that gluteal muscle hypertrophy occurs after following a regular stimulation regimen for 3 months, leading to increased muscle thickness and decreased ischial region interface pressures (41). Weight shifting can also be produced by electrically stimulated gluteal muscle contractions on alternating sides. These findings suggest that long-term use of electrical stimulation can potentially improve the health of paralyzed muscle and reduce the risk of pressure ulcer development. However, paralyzed muscles will reatrophy after withdrawal from the stimulation regimen, and for clinical efficacy and user acceptance of long-term gluteal stimulation, an implanted system will therefore be necessary. Preliminary results with implanted systems indicate that improvements in tissue health can be reasonably expected (50).

Pain Relief
Other uses of therapeutic stimulation that are already established in the non-SCI population deserve to have more studies specifically for SCI. One notable example is the use of electrical stimulation for neuromodulation in the treatment of neuropathic or nociceptive pain, which is another prevalent and difficult clinical problem following SCI.

Restoration of Function

Particular interest has focused on stimulation of peripheral nerves below the level of injury to restore useful function that might otherwise have been permanently lost. Several first-generation systems have been developed and used clinically over the last 30 years, and research is now proceeding on second-generation systems.

Respiratory Function

Inspiratory Muscle Pacing. In individuals with high tetraplegia but preserved bilateral phrenic nerve function, as assessed by phrenic nerve conduction studies and fluoroscopy, the phrenic nerves can be stimulated electrically to induce diaphragm contraction and restore adequate inspiration so that these patients no longer require mechanical ventilation (51).

There are several techniques by which the phrenic nerves can be stimulated. In the conventional methods that are commercially available, the diaphragm is activated by electrodes positioned directly on both phrenic nerves in the thorax. Such systems have been implanted in 1000 patients over the last 3 decades, and there are now several commercially available devices (see Appendix).

Some of the advantages of electrical stimulation compared with mechanical ventilation include improved speech, increased mobility, reduced anxiety and embarrassment, elimination of fear of ventilator disconnection, and improved sense of well being (52,53).

Conventional phrenic nerve pacing requires a thoracotomy, which is a major surgical procedure with associated risk, in-patient hospital stay, and high cost. In addition, this procedure requires phrenic nerve dissection and placement of electrodes directly on the nerves, and therefore, carries some risk of phrenic nerve injury. These disadvantages have limited the number of individuals willing to undergo diaphragm pacing.

An alternative procedure, currently under investigation, involves placement of electrodes into the muscular portion of the diaphragm near the entrance points of the phrenic nerve into the diaphragm (54). This procedure is performed laparoscopically and can be done on an out-patient basis. The advantages of intramuscular placement of phrenic nerve electrodes include less risk of phrenic nerve injury because the electrodes are not in direct contact with the phrenic nerve. Moreover, there is a reduction in overall cost due to the reduction or elimination of the hospitalization needed for thoracotomy.

Successful diaphragm pacing by intramuscular electrodes requires that the electrodes be placed near the motor point, ie, the position at which the phrenic nerve enervates the diaphragm. When placed near the motor point, as determined by intraoperative testing, intramuscular diaphragm stimulation results in virtually the same inspired volume production as that resulting from direct phrenic nerve stimulation.

Intramuscular diaphragm pacing has been evaluated in 6 patients. A pair of specially designed stainless steel electrodes was placed in each hemidiaphragm within the phrenic nerve motor point region via laparoscopy, and their wires were brought through the skin for connection to an external stimulator. Four of these patients are completely independent of mechanical ventilation, whereas one is ventilator-free for 12 to16 h/d. One patient had no response to stimulation, probably secondary to unrecognized lack of phrenic nerve function. The implantation was performed either on an out-patient basis or with a single overnight stay in hospital for observation. These patients have experienced benefits very similar to those who have undergone successful phrenic nerve pacing, including improved speech, a sensation of more normal breathing, and increased mobility. These preliminary results suggest that intramuscular diaphragm pacing can provide benefits similar to those achieved with conventional phrenic nerve pacing without the need for an invasive surgical procedure and with less risk of phrenic nerve injury.

Activation of the intercostal muscles also results in significant inspired volume production. Inspiratory intercostal muscle activation can be achieved by placement of a single electrode on the ventral epidural surface of the spinal cord at the T2 level. In a clinical trial of individuals with ventilator-dependent tetraplegia, activation of the intercostal muscles alone resulted in inspired volumes ranging from 470 to 850 mL in 4 of 5 patients. However, the maximum duration that ventilation could be sustained ranged between 20 minutes and 2 3/4 hours (55). While intercostal muscle stimulation results in significant inspired volume production, this technique alone does not provide sufficient inspired volumes to maintain adequate ventilatory support for prolonged time periods. A subset of individuals with ventilator-dependent tetraplegia has only unilateral phrenic nerve function. Therefore, these patients are not candidates for conventional phrenic nerve pacing. In 4 subjects, the use of combined unilateral phrenic nerve stimulation and intercostal pacing was evaluated.

Combined stimulation of both muscle groups resulted in maximum inspired volumes ranging from 600 to 1300 mL. Two of the 4 patients were able to achieve full-time pacing, whereas each of the others was comfortably maintained off mechanical ventilation for 12 to 16 h/d. These patients experienced similar benefits to those reported with bilateral phrenic nerve pacing. Combined intercostal and unilateral diaphragm pacing may be a useful therapeutic modality capable of maintaining full-time ventilatory support in patients with partial phrenic nerve function.

Expiratory Muscles and Coughing. Normal expiration is passive, owing to the elasticity of the chest wall and lungs. Forced expiration and cough production involves lower intercostal and abdominal muscle activation for normal cough generation and prevention of respiratory complications. Electrical stimulation of abdominal muscles using electrodes on the skin has been found to produce cough comparable with that produced with the manual assistance of a therapist (56,57). Electrical stimulation of the expiratory muscles has also been investigated with electrodes implanted on the lower thoracic spinal cord (58).

In summary, there are new management options on the horizon for individuals with ventilator-dependent tetraplegia. In addition to conventional phrenic nerve pacing, less invasive techniques for electrode implantation will be available for individuals with bilateral phrenic nerve function. In patients with only unilateral diaphragm function, combined intercostal and diaphragm pacing can provide benefits similar to that achieved with bilateral diaphragm pacing.

Bladder, Bowel, and Sexual Function

In patients with preserved conus medullaris and sacral nerves, improved bladder, bowel, and sexual function can be achieved by electrical stimulation of the sacral nerves or roots. These supply somatic motor axons to the external urethral and anal sphincters, pelvic floor, and parasympathetic preganglionic efferents to the smooth muscle in the bladder, lower bowel, sphincters, and erectile tissue, in addition to conveying sensation from these regions back to the cord.

Voiding. Electrical stimulation of the sacral motor roots causes contraction of the external sphincters, in addition to the bladder and lower bowel, which might be expected to be ineffective for voiding and even harmful. However, intermittent bursts of stimulation for a few seconds separated by intervals of a few seconds can produce sustained contraction of the smooth muscle of the bladder while allowing the sphincter to relax during the intervals and permit urine to pass. Longer bursts and intervals can produce defecation in some patients. Such stimulation can be applied to motor roots by electrodes implanted intradurally. It can also be applied to mixed sacral nerves by electrodes placed extradurally; these also activate sensory axons that would cause reflex contraction of the sphincters and possibly rises in blood pressure or pain unless the sensory axons were divided proximally by a rhizotomy, which is usually performed in conjunction with electrode implantation.

Continence. Reflex incontinence can be reduced dramatically by surgical division of the sensory roots in the sacral segments as described above. It also reduces the risk of kidney damage from hyper-reflexia of the bladder and sphincter. However, it also abolishes desirable functions such as reflex erection and reflex ejaculation and reduces reflex defecation, and would abolish sacral sensation if present. Detrusor contractions can be inhibited by stimulation of sensory axons in sacral nerves, although this has not yet been established to be a viable way of reducing incontinence after SCI.

Stress incontinence is often associated with damaged peripheral nerves or muscles, which are less amenable to electrical treatment.

Erection. Stimulation of intact parasympathetic efferent axons in S2 can produce erection for as long as stimulation is maintained. Electrodes are usually implanted at the same time as electrodes for restoring bladder and bowel function as described above.

Ejaculation. This can be produced by electrodes implanted on the presacral sympathetic plexus (59), but such systems are not commercially available because it is preferable to obtain semen by applying stimulation via an electrode inserted temporarily into the rectum, sometimes called “electroejaculation” (60).

Clinical Results. An implantable stimulator capable of improving bladder, bowel, and erectile function was developed by Brindley at the Medical Research Council of Great Britain (61). It was first used successfully in SCI in 1978 and became available commercially in Britain in 1982. It has been implanted in over 2000 patients since that time. It was approved by the Food and Drug Administration (FDA) in the United States in 1998 as a Humanitarian Use Device, and about 100 patients have received it in the United States. This device usually produces voiding with residual volumes of 50 mL, resulting in a significant reduction in urinary tract infections (62,63). The rhizotomy, which is usually performed at the time of implantation, abolishes detrusor hyper-reflexia, greatly reducing incontinence and the need for urine collection devices (64,65). It also increases bladder capacity and compliance, reducing the risk of ureteric reflux and hydronephrosis (66,67). Reduced need for antibiotic and anticholinergic medication, appliances, and hospital visits results in reduced annual costs for bladder and bowel care; studies in Europe and the United States have indicated that, within 5 to 8 years, these savings could cover the cost of implanting and using the device (68,69).

Current research is addressing alternatives to surgical rhizotomy for reducing hyper-reflexia of the detrusor and sphincters and includes electrical block and inhibition of muscle contraction. Next generations of implantable stimulators may incorporate the ability to produce micturition and defecation, continence, and erection without surgical rhizotomy. However, such research and development typically takes many years, and at present, considerable clinical benefit can be achieved with existing technology.

Upper Limb Function

In patients with tetraplegia and preserved lower motor neurons to some upper limb muscles, useful function can be restored by electrical stimulation. The primary approach has been to restore hand function in people with C5 and C6 SCI using implantable systems, and a device of this type has received FDA approval, but systems employing surface and percutaneous electrodes have also been tested clinically (70,71). Percutaneous wire electrodes have proven to be a valuable tool during research because they allow selective and reproducible activation of the many small muscles of the forearm and hand. Long-term function generally requires electrodes to be permanently implanted in or on muscles in the forearm and hand and to be connected to an implanted stimulator, avoiding problems of wire breakage and skin level infection. Implanted systems are usually enhanced by tendon transfers, as described below, and stimulation of paralyzed but innervated muscles can increase the number of potential tendon transfers.

Stimulation of flexors and extensors of the fingers and thumb, the adductor and opponens pollicis muscles, and sometimes wrist balancing muscles can produce palmar grasp and release for large objects and key-pinch grasp for smaller items. Tendon transfers are used to stabilize the thumb, synchronize finger movement, and compensate for some denervated muscle groups

A first-generation implant of this type using 8 electrodes (known commercially as Freehand) has been implanted in more than 200 patients with C5 or C6 tetraplegia by 35 centers in at least 8 countries. In a variety of activities of daily living, such as eating and drinking, brushing teeth, writing, and using the telephone, users showed improved function and less need for assistance and expressed a preference for using the system. A user satisfaction survey at least 6 months after completing training with the device confirmed that they needed less adaptive equipment and less assistance from others; on average, they used it 5 d/wk, and nearly one-half used it every day. The majority of patients were very satisfied with the system, and 80% said they would recommend it to others.

Second-generation devices with 12 active stimulation channels and 2 myoelectric signal sensing channels (Implantable Stimulator Telemeters, IST-12) are being investigated for improved control of the intrinsic muscles of the hand, wrist balance, forearm pronation and supination, and elbow and shoulder position (72). The triceps muscle is controlled to produce elbow extension and allow reaching above the head. The first-generation device was controlled by an external joystick following the movements of the contralateral clavicle, but alternatives have also been used, such as an implanted wrist- angle sensor and the EMG of voluntarily controlled muscles such as the trapezius or wrist extensors, on which recording electrodes have been implanted (73,74). This system is currently in clinical trials and has been tested by 7 subjects: 2 with the myoelectric control, 4 with the implanted joint angle sensor,and 1 with the external controller and IST implant. These systems areall in regular use, with the exception of one deceased patient; usage and satisfaction are high.

New research is also in progress on control of the paralyzed shoulder for people with high tetraplegia (75). Such control is complex because of its many potential movements; it needs more channels and other sensors for arm orientation. There are limited voluntary movements available to a person with high tetraplegia to control a stimulator, and direct electrical connections with the cerebral cortex are being investigated as a control interface.

The FES clinical and research community has shown a tenacious resolve to overcome the problems of tetraplegia using implantable electronic technology and strives to improve the quality of life for persons with physical limitations due to neurologic diseases.

Lower Limb Function

Surface and Percutaneous Systems. Functional electrical stimulation can provide individuals paralyzed by thoracic or low cervical SCIs with the ability to exercise, stand, transfer, and perform simple stepping (76–78). Standing up and stepping have been achieved with relatively simple systems using 2 to 6 channels of stimulation via electrodes on the skin surface (79–83). Standing can be achieved by activating both quadriceps muscles, whereas a stride can be produced by activating the quadriceps of one leg while initiating a flexion withdrawal in the other. Stimulation of a sensory nerve (peroneal, sural, or saphenous) triggers a spinal reflex arc that causes hip, knee, and ankle flexion; to complete the stride, the knee extensors on the swinging leg are activated. Some paralyzed individuals have been reported to walk at speeds approaching one quarter of normal and ascend a curb or step with surface stimulation (84,85). Selected individuals with neurologically incomplete SCI and some preserved motor and sensory function can regain household or community mobility.

Combining FES with conventional bracing has certain advantages (86–89). For walking in conventional braces, FES is effective at introducing large forces through activation of large lower extremity muscles, which reduces the upper extremity exertion required. Hybrid systems employing various brace and stimulation components have been fitted to patients with complete or incomplete thoracic or low-level cervical injuries (90). One design combines a Louisiana State University Reciprocating Gait Orthosis (LSU-RGO) with 4 channels of surface stimulation. With the knees locked in the brace, stimulating the hamstrings on one side extends the stance hip and flexes the contralateral hip through the action of the reciprocating mechanism. The rectus femoris actively flexes the swing hip and through the reciprocating mechanism assists with stance hip extension. The energy required to operate these hybrid systems is less than braces alone, but increases rapidly with walking velocity due to an increased reliance on the arms and trunk muscles to move the body forward.

First-Generation Implanted Systems. Activating a larger number of muscles individually with implanted electrodes has allowed functions such as transfers, standing, stepping, and stair ascent and descent. Fine wire electrodes inserted percutaneously via a hypodermic needle permit sophisticated lower extremity motions with up to 48 separate muscles (91–93). Some well-trained subjects are able to walk 300 m repeatedly at 0.5 m/s with this system (94).

For long-term clinical application, implanted systems offer major advantages over surface and percutaneous stimulation including improved convenience, cosmesis, and reliability (95). Exercise and standing have been reported with a cochlear implant modified to deliver 22 channels of stimulation (96), and a 12-channel system for activation of the L2-S2 motor roots has been applied to several volunteers (97).

An 8-channel implanted stimulator with electrodes implanted in or on muscles has undergone clinical testing in 13 subjects (98–103). For standing, the system activates the hip (gluteus maximus and semimembranosus), knee (vastus lateralis), and trunk (lumbar erector spinae) extensor muscles. A molded AFO protects the ankle and midfoot during weight-bearing, pivot transfers, and swing-to gait. On average, subjects were able to stand for more than 10 minutes with 85% of their body weight on their legs. Eight individuals with lower level (C7–T9) injuries were able to release one hand from a support device and perform reaching tasks above shoulder height while standing. The system also successfully facilitated standing transfers for the users with cervical level injuries and their assistants. Of the 9 volunteers with lower-level injuries and good upper extremity strength who completed rehabilitation, 7 were able to achieve short distance mobility with a swing-to gait. Reciprocal stepping can be achieved with 16 channels of stimulation through the addition of a second implant to activate hip flexors and ankle dorsiflexors (104,105).

These first-generation systems are sufficient for basic function but are unresponsive to unexpected disturbances. All standing and walking neuroprostheses, whether they are implanted, still require assistive devices such as crutches, walkers, or additional bracing, and this restricts the activities and environments in which the neuroprosthesis can be used. The true value of current lower extremity FES systems lies in their ability to facilitate brief mobility-related tasks, allowing people with paraplegia to overcome physical obstacles (106), negotiate architectural barriers (107), and reach and manipulate objects that are otherwise inaccessible from the wheelchair (108,109). They can also facilitate standing transfers by eliminating the heavy lifting and lowering required by an assistant. FES can augment and extend the function of the wheelchair and may prove to be a valuable option to enhance the well-being and independence of persons with disabilities.

Future Trends

Clinical

The effects of activity on the nervous system below a SCI are being investigated in partial-weight—supported treadmill training in the hope that function in the central nervous system may be beneficially affected by processes such as activity-dependent plasticity or motor relearning; such activity is often provided by therapists or robots but may be provided more cost-effectively by electrical stimulation. Electrically stimulated exercise of the lower limbs has recently been shown to enhance new neural cell birth and survival following chronic SCI in rats (110). This demonstrates that FES can enhance cellular regeneration in the injured adult CNS and raises the possibility of using controlled electrical activation of the nervous system for optimizing spontaneous regeneration and functional recovery in neurologic injuries.

Technical

The trend in surgery to less invasive techniques also affects the design and implantation of neural prostheses. Many electrodes and cables can now be implanted with minimally invasive surgery and tunneled under the skin to connect to a stimulator placed like a pacemaker through a small incision. Miniature single-channel stimulators (2.4 mm diameter, 16.7 mm long; BION) with electrodes on each end that can be inserted through a trocar are undergoing FDA trials. They still require external transmitter coils to provide power and control, and these coils can be large or numerous for multiple stimulation targets requiring access to deep muscles. Another version of these devices that is being developed will contain a battery that can be recharged from an external coil; this may reduce the dependence on external equipment, although there is a limit to how many times the battery can be recharged. Other developments include the development of standards that will allow many components to be interconnected in wired and wireless networks within the body. This will allow systems to be assembled and upgraded as needed with minimal surgery; it also will allow compatible components to be made by different manufacturers, permitting larger-scale production and reduced costs and increasing the flexibility with which systems can be assembled. This is likely to further improve the balance between restored function and the investment of time, energy, and money required.

Ultimately the provision of improved care to SCI patients depends, not primarily on development of new techniques, but on their delivery by clinicians and funding agencies. The last one-half century has seen SCI care move from survival to treatment and prevention of complications to an awareness of quality of life. With collaboration, communication, and investment, the next one-half century may see increasing restoration of function that, in the past, was lost for life.

Acknowledgments

Vision, leadership, and mentoring have been given generously over many years by Prof. P. Hunter Peckham, Professor of Biomedical Engineering and Orthopaedics at Case Western Reserve University and Director of the Functional Electrical Stimulation Center, Louis Stokes Veterans Affairs Medical Center, Cleveland, Ohio.

Appendix: Manufacturers

Exercise Cycles

Ergys, Regys: Therapeutic Alliances Inc., 333 North Broad Street, Fairborn, OH 45324; phone: 937.879.0734; fax: 937.879.5211; http://www.MusclePower.com

StimMaster: Electrologic of America, 2790 Indian Ripple Road, Beavercreek, OH 45440; http://www.electrologic.com

Phrenic Nerve Stimulators

Mark IVBreathing Pacemaker: Avery Laboratories, Inc., 61 Mall Drive, Commack, NY 11725-5703; phone: 631.864.1600; fax: 631.864.1610; http://www.breathingpacemakers.com

Atrostim Phrenic Nerve Stimulator V1.0: available in the United States under Investigational Device Exemption from Lifestream Medical Corp., LifeGroup International, LLC, PO Box 517, Windermere, FL 34786; phone: 407.529.9920; fax: 407.277.3935; http://www.lifegroupinternational.com

Atrostim Phrenic Nerve Stimulator V2.0: available only outside the United States from Atrotech, Ltd., Hermiankatu 6-8F, 33720 Tampere, Finland; phone: 358.3.3831300; fax: 358.3.3831324; http://www.atrotech.com

MEDimplant: available only outside the United States from MEDimplant Medizinsch-technische GmbH, Vienna, Austria

Sacral Nerve Stimulators

Finetech-Brindley (Vocare) Bladder System: Finetech Medical Ltd., 13 Tewin Court, Welwyn Garden City, Herts AL7 1AU, England; phone: 1707.330.942; fax: 1707.334.143; http://www. finetech-medical.co.uk. National distributors given on website. Distributed in the United States by NDI Medical, One Chagrin Highlands, 2000 Auburn Dr., Suite 320, Cleveland, OH 44122; phone: 216.378.9106; http://www.ndimedical.com

Upper Limb Surface Stimulation

Handmaster: NESS Ltd., 19 Ha-Haroshet St., PO Box 2500, Ra’anana 43654, Israel; phone: 972.9.7485738; fax:
972.9. 7485740; http://www.nessltd.com

Lower Limb Surface Stimulation

Parastep: Sigmedics, Inc., 335 North Broad St., Fairborn, OH 45324; phone: 937.439.9131; fax: 937.439.9272; http://www.sigmedics.com

Microstimulators

BION: BionTech, PO Box 905, Santa Clarita, CA 91380; phone: 661.775.3995; http://www.biontech.org

References

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Graham H. Creasey, MD, FRCSEd, is affiliated with the VA Center of Excellence in Functional Electrical Stimulation, Cleveland, Ohio; the Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland, Ohio; the MetroHealth Medical Center, Cleveland, Ohio; and Case Western Reserve University, Cleveland, Ohio.

Chester H. Ho, MD, is affiliated with the VA Center of Excellence in Functional Electrical Stimulation, Cleveland, Ohio; the Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland, Ohio; and Case Western Reserve University, Cleveland, Ohio.

Ronald J. Triolo, PhD, is affiliated with VA Center of Excellence in Functional Electrical Stimulation, Cleveland, Ohio; the Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland, Ohio; the MetroHealth Medical Center, Cleveland, Ohio; and Case Western Reserve University, Cleveland, Ohio.

David R. Gater, MD, PhD, is affiliated with the Ann Arbor VA Hospital System, Ann Arbor, Michigan; and the University of Michigan, AnnArbor, Michigan.

Anthony F. DeMarco, MD, is affiliated with the MetroHealth Medical Center, Cleveland, Ohio; and Case Western Reserve University, Cleveland, Ohio.

Kath M. Bogie, DPhil, is affiliated with the VA Center of Excellence in Functional Electrical Stimulation, Cleveland, Ohio; the Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland, Ohio; the MetroHealth Medical Center, Cleveland, Ohio; and Case Western Reserve University, Cleveland, Ohio.

Michael W. Keith, MD, FACS, is affiliated with the VA Center of Excellence in Functional Electrical Stimulation, Cleveland, Ohio; the MetroHealth Medical Center, Cleveland, Ohio; and Case Western Reserve University, Cleveland, Ohio.

Please address correspondence to Graham H. Creasey, MD, FRCSEd, 2500 Metro Health Drive, Cleveland, OH 44109; phone: 216.778. 8802; fax: 216.778.1653 (e-mail: ghc@po.cwru.edu).

Research funding has been provided principally by Rehabilitation Research & Development Service, Department of Veterans Affairs and National Institutes of Health FDA Orphan Products Program.

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