Perspectives on Modern Orthopaedics

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1 Perspectives on Modern Orthopaedics Implanted Neuroprostheses for Restoration of Hand Function in Tetraplegic Patients Roger Cornwall, MD, and Michael R. Hausman, MD Abstract Restoration of hand function through functional electrical stimulation allows tetraplegic patients to use existing abilities to control paralyzed muscles. In patients with C5 or C6 spinal cord injuries, implanted upper extremity neuroprostheses use functional electrical stimulation technology to power hand and arm muscles. A variety of devices, often using contralateral shoulder motion, sends signals via a small external controller and transmitting coil to an implanted stimulator. The stimulator powers designated upper extremity muscles via implanted electrodes. The surgical procedure is minimally invasive and easily reversed. Palmar and lateral grasp, among other functions, can be reliably restored, leading to significant improvements in functional capacity. High user satisfaction, low complication rates, and recent advances in technology and control systems contribute to the success of this technology in the treatment of devastating spinal cord injuries. J Am Acad Orthop Surg 2004;12:72-79 Spinal cord injury can be devastating, particularly in the cervical spine, where loss of hand function can reduce a patient to near-total dependency. However, damage to the upper motor neurons potentially preserves the lower motor neuron arc, thus maintaining the viability of the muscles. Functional electrical stimulation (FES) is controlled stimulation of muscles to achieve function in patients with upper motor neuron lesions. FES has been available for several decades; early external neuroprostheses used either surface or percutaneous electrodes. 1-3 Although percutaneous electrodes allow the entire device to be external and easily serviceable, frequent skin problems around the wires have precluded long-term use. Percutaneous electrodes have been used in prototypes of hand FES devices ultimately intended to be implantable. They are still being used in this way for the development of FES in other areas, such as the shoulder. 2,3 External neuroprostheses include the Handmaster 4 (Neuromuscular Electrical Stimulator Systems, Ra anana, Israel), which is FDA approved for stroke patients, and the Bionic Glove, 5 which remains in development. However, problems with donning and maintaining these devices have precluded widespread clinical application. The Freehand system (NeuroControl, Cleveland, OH), an implantable neuroprosthesis, can stimulate eight different muscles to produce useful grip and key pinch in tetraplegic patients. The Implantable Neuroprosthetic System The Freehand System is the only FDA-approved, implantable upper extremity neuroprosthesis. It is indicated for the restoration of grasp and pinch in patients with high-level (C5- C6) cervical spine injuries. First implanted in 1986, 6,7 the system consists of a surgically implanted receiver/ stimulator unit and electrodes with an external controller and power supply/microprocessor (Fig. 1). The development of durable, biocompatible electrodes with stable impedence was challenging. Initially, epimysial electrodes were used to stimulate the surface of the muscle near its motor point. 8 The electrodes were insulated from the surrounding tissue by a Silastic backing, which was used to help suture the electrode to the epimysium. These electrodes worked well in thinner muscles, such Dr. Cornwall is Orthopaedic Hand Surgeon, Children s Hospital of Philadelphia, and Assistant Professor of Orthopaedic Surgery, University of Pennsylvania School of Medicine, Philadelphia, PA. Dr. Hausman is Professor and Chief of Hand and Elbow Surgery, Leni and Peter W. May Department of Orthopaedics, Mount Sinai Hospital, Mount Sinai School of Medicine, New York, NY. None of the following authors or the departments with which they are affiliated has received anything of value from or owns stock in a commercial company or institution related directly or indirectly to the subject of this article: Dr. Cornwall and Dr. Hausman. Reprint requests: Dr. Hausman, Mount Sinai Hospital, Box 1188, 5 East 98th Street, New York, NY Copyright 2004 by the American Academy of Orthopaedic Surgeons. 72 Journal of the American Academy of Orthopaedic Surgeons

2 Roger Cornwall, MD, and Michael R. Hausman, MD Figure 1 Schematic of the Freehand implanted upper extremity neuroprosthesis. (Adapted with permission, NeuroControl, Cleveland, OH.) as the wrist and finger extensors. However, obtaining uniform, strong contraction of thicker muscles, especially the flexor digitorum profundus, proved to be difficult. Intramuscular electrodes, developed to address this issue, are anchored with small polypropylene barbs that obviate the need for sutures (Fig. 2). This design has facilitated implantation using a percutaneous, minimally invasive technique. 9 Nerve cuffs, intraneural electrodes, and multiple ( hydraheaded ) electrodes also have been developed. Multiheaded electrodes allow stimulation of groups of muscles to approximate normal hand function more closely. The electrodes are connected to the receiver/stimulator with flexible leads of high fatigue strength 8,10 and with connectors in the subcutaneous tissue of the arm. The long leads attached to the electrodes and the short leads from the receiver/stimulator are joined with spring connectors that allow revision or modification of one component without removal of the entire lead-electrode system. 11 The receiver/stimulator provides eight independent channels of programmable electrical stimulation (Fig. 2). The current and pulse width can be programmed for each of the channels, thus controlling the strength of the target muscle s contraction. Combinations of muscle activity also can be programmed to optimize function for example, a combination of extensor digitorum communis, abductor pollicis brevis, and intrinsic muscle contraction to open the hand to grasp large objects. Any combination of contraction of the eight stimulated muscles is possible and can be changed and tuned throughout the patient s rehabilitation to individualize and optimize the grasp and pinch. Programming is done with a laptop computer attached to the external controller. The receiver/stimulator resides in a subcutaneous pocket on the chest wall and receives radiofrequency signals from the external control computer. Control signals and energy are Figure 2 The Freehand receiver/stimulator (A) and an intramuscular electrode (B), with polypropylene barbs (arrows). Vol 12, No 2, March/April

3 Implanted Neuroprostheses for Restoration of Hand Function in Tetraplegic Patients transmitted to the receiver/stimulator via a transmitting coil taped to the chest over the implant. All the energy required for muscle stimulation and operation of the receiver/stimulator is stored from the transmitting coil; thus, there are no batteries to replace in the implant. The implant is designed to last without maintenance for the life of the patient. The external controller processes signals from the joystick motion sensor to send to the receiver/stimulator. The controller is about the size of a pager and has a rechargeable cellular phone battery. The software in the computer recognizes specific controller signals and translates them into complex functions involving the various target muscles. 12 For example, the patient can signal the command for lateral grasp, which is translated by the computer to finger flexion, followed by thumb adduction and flexion. Palmar grasp is similarly translated to thumb palmar abduction, followed by finger flexion. The patient provides signals for hand motion by the joystick attached to the chest with adhesive pads. The motion sensor (a series of rheostats in three planes of motion) is mounted in a fixed position on the chest. The mobile end of the joystick attaches to the shoulder with another adhesive pad and is moved by elevation/depression and retraction/protraction of the shoulder. Even very limited motion is adequate because the sensitivity or gain of the joystick is programmable. For example, patients learn to use the system with low sensitivity and somewhat exaggerated movements. As they achieve facility, the gain can be increased so that very subtle movements of the contralateral shoulder produce a full flexion/ extension arc of the fingers. Accomplished users can use the system with nearly imperceptible shoulder motions. 13 Speed of muscle stimulation is proportional to the speed of moving the joystick; the strength of grasp or pinch is proportional to the amplitude or excursion of the joystick. A rapid shrug of the shoulder locks or fixes the hand. For example, the patient may lock onto a fork or pen so that it can be used without having to move the joystick again to maintain the grip. A second quick shrug unlocks the position. Other controllers have been designed to amplify electromyographic signals from weakly innervated muscles in the affected forearm, 1 and these have been adapted for use in implantable neuroprostheses. 14,15 Contralateral or ipsilateral wrist motion also can be used as a control source for grasp commands. 15 Head movement 2 and respiration 16 also have been used to control the prosthesis. Because available sources vary, the choice of control source must be individualized for each patient. 15 Arecent advance in FES control involves the use of electroencephalographic (EEG) signals. Individuals can be trained to voluntarily control the amplitude of specific frequency components of the EEG. 17 These EEG signals, detected by intracortical electrodes, have been used by patients with amyotrophic lateral sclerosis to control computer cursors. 18 Lauer et al 19 trained a neuroprosthesis user to control the device with frontal beta rhythms recorded by an array of surface electrodes. Patient Selection The functional stimulation of muscles in the extremities requires the presence of an intact lower motor neuron, including the anterior horn cell. For this reason, only patients with upper motor neuron lesions are candidates for FES. Brachial plexus injuries involve disruption and subsequent degeneration of the lower motor neuron and therefore preclude the use of FES in the upper extremity. Although upper extremity FES has been used with success in patients following stroke, 20,21 its predominant use is in spinal cord injury patients. Gorman et al 22 have established guidelines for the selection of spinal cord injury patients who can be considered for implantable neuroprostheses. The selection process must consider anatomic, physiologic, medical, and psychosocial factors. Patients must have stable tetraplegia with a C5 or C6 motor level, with international classification motor scores of 0, 1, or 2 23 or an impairment scale level of A, B, or C, as defined by the American Spinal Injury Association and the International Medical Society of Paraplegia. 24 Patients with injuries at this level have few available options for restoring hand function 25 and are ideal candidates for FES; those with lower level injuries can have useful grip and pinch restored with conventional tendon transfers. Surgery for tetraplegia usually is delayed for at least 1 year after injury to assure a stable plateau of functional recovery. Gorman et al 22 recommend beginning the discussion of FES earlier in the course because many patients are more receptive then. 22 External FES has been shown to improve recovery of hand function in patients after spinal cord injury. 4 Early implantation of neuroprostheses is under study. Such use may speed rehabilitation by promptly restoring useful hand function, thus preventing both contractures and an attitude of dependency. Target muscles must be physiologically suitable for FES. Innervated muscle has a much lower stimulation threshold than denervated muscle does. 26 For this reason, patients must have a sufficient number and distribution of innervated muscles to provide hand function, either directly or through tendon transfers. Excitabilityoftargetmusclesistestedbytranscutaneous stimulation before consideration because some patients with spinal cord injuries have concomitant lower motor neuron damage. 22,27 The patients also must be free of joint contractures unless the contractures are 74 Journal of the American Academy of Orthopaedic Surgeons

4 Roger Cornwall, MD, and Michael R. Hausman, MD isolated and surgically correctable. Multiple, long-standing contractures that are not easily correctable preclude the use of FES. Contraindications to neuroprosthesis use include cardiac disease, arrhythmias, pacemakers, chronic systemic infections, diabetes, and immune disease. 28 Conditions such as decubiti that prevent the prolonged wheelchair sitting necessary for training and use of the neuroprosthesis should preclude its implantation. 22 Because of the usually concomitant sensory deficits, patients with spinal cord injuries also must possess sufficient vision to provide visual feedback during training and neuroprosthesis use. Patients being considered for FES must display the cognitive ability and motivation required for preimplantation conditioning, postimplantation training, and ultimate daily neuroprosthesis use. A series of questionnaires administered by a clinical psychologist to determine mental suitability has been used. 29 Gorman et al 22 excluded patients based on substance abuse, failure to comply with medical advice, and head injury. Adequate family or caregiver support is essential at each step, including the daily application of the joystick controller and transmitting coil (the external components of the prosthesis). 22 Using these selection guidelines, Gorman et al 22 found that only 14 of 120 patients (11.7%) presenting to a rehabilitation hospital with newonset tetraplegia were suitable candidates for neuroprosthesis implantation. However, extrapolating these results to the population of tetraplegic patients in the United States in 1990, they estimated that more than 12,000 patients could have benefited from the device. Most studies have limited the use of an implantable upper extremity neuroprosthesis to adults and skeletally mature adolescents. Neuroprostheses with percutaneous electrodes have been used successfully in children. 30 Smith et al 31 reported the first use of an implanted upper extremity neuroprosthesis in a growing 10-yearold child with C5 tetraplegia. During the 16-month follow-up, limb growth was accompanied by unwinding of redundant lead length. Surgical Strategy Implantation of the system can be performed under general (nondepolarizing) or regional anesthesia. The procedure takes approximately 4 to 6 hours when done by experienced surgeons. A subcutaneous pocket is developed in the chest wall and a temporary grounding electrode is inserted. The order of insertion of the electrodes is arbitrary but usually proceeds distal to proximal. Muscle choice is dictated by the individual patient and by muscle stimulation. Muscles selected are likely to include the abductor pollicis brevis, abductor pollicis, finger flexors, extensor digitorum communis, and extensor pollicis longus. Variations include the wrist extensors, extensor carpi ulnaris, triceps and intrinsic reconstruction. The original, open surgical procedure is described below, but Hausman and Masters 9 have reported a minimally invasive technique that avoids large forearm incisions. An incision is made in the palm to expose the abductor pollicis and abductor pollicis brevis muscles. The abductor pollicis produces key or lateral pinch and therefore is a critically important muscle. Abattery-powered stimulator is used to probe the muscles to identify the point of optimal stimulation, and an intramuscular electrode is inserted or an epimysial electrode is sutured to the muscle. A palmar incision is then made in the forearm and the electrodes are threaded through the carpal canal. The flexor digitorum profundus muscle is mapped and the electrode inserted. Obtaining uniform and synchronized stimulation may be difficult given the dual innervation of this muscle. If necessary, a side-to-side tenodesis may be done to synchronize the digits. A reverse cascade, with the ulnar digits lagging the index and long fingers, is desirable in tetraplegics to prevent the ring and little fingers from limiting opening of the hand. The flexor pollicis longus muscle usually is not utilized and will not, in itself, produce acceptable pinch. At this point in the procedure, tourniquet palsy usually occurs, so reliable stimulation of the muscles cannot be obtained. The remaining tourniquet time therefore may be used to perform the split flexor pollicis longus transfer 32,33 or interphalangeal arthrodesis of the thumb and any intrinsic transfers deemed necessary. The tourniquet is then deflated, and a 15- to 20-minute reperfusion period is allowed to restore normal muscle contractility before inserting electrodes into the extensor muscles. The inserted flexor leads may be checked with the battery-powered stimulator. Hemostasis is carefully achieved, and the incisions are closed with meticulous subcuticular sutures. A similar procedure is performed on the dorsum of the forearm, with electrodes inserted into or on the extensor digitorum communis, extensor pollicis longus, and a wrist extensor. The radial wrist extensors frequently are denervated in C5-C6 level injuries. If these muscles are not functional, the extensor carpi ulnaris is implanted and transferred to the extensor carpi radialis brevis. 34 The brachioradialis also may be transferred to the extensor carpi radialis brevis so that the patient may remain bracefree even when the system is switched off. Wrist extension is a priority, and normal strength must be achieved by stimulation or transfer to stabilize against the powerful finger flexors. Two channels remain; there are many variations in their application. Some surgeons prefer stimulating the flexor digitorum superficialis muscles Vol 12, No 2, March/April

5 Implanted Neuroprostheses for Restoration of Hand Function in Tetraplegic Patients of the index and long fingers to increase flexion power. Others prioritize intrinsic reconstruction by inserting an electrode either into the third intermetacarpal space or into the index and long finger flexor digitorum superficialis muscles, then transferring the split flexor digitorum superficialis tendons through the lumbrical canals to the lateral bands or extensor tendon, depending on the strength of interphalangeal extension needed. The last electrode may be used in the triceps, although deltoidto-triceps transfer is another effective strategy for restoring important elbow extension. Once the electrodes have been inserted and tested, a vascular graft tunneling device is used to pass the electrodes to a proximal incision near the axilla. The flexor and extensor electrode leads are passed in two separate groups as close as possible to the intermuscular septae and the axis of motion; doing so minimizes excursion, bending, and change of length with flexion and extension of the elbow. The axillary incision can be made anterior to the axilla, thus placing the leads in a more anterior position. This avoids stress on the leads if the patient hooks the arm over the wheelchair for balance; it also avoids pressure and trauma to the incision over the junction of the leads and connectors. The axilla is most vulnerable to wound breakdown and infection problems, perhaps relating to the volume of foreign material beneath the thin, mobile skin. Subfascial placement of the leads in two separate groups minimizes their volume and may reduce the risk of infection or wound problems. After passing the forearm leads, the triceps electrode, if used, is inserted through the axillary incision. The chest incision is reopened and the temporary grounding electrode is replaced with the receiver/stimulator implant. Maintaining absolute hemostasis is essential. The implant s eight leads are tunneled to the axillary incision, and the Silastic flange of the implant is sutured to the pectoralis fascia to prevent rotation. This incision is then closed. The implant leads are connected to the electrode leads in the axillary incision and a careful, two-layer closure is performed. The entire system is tested with a radiofrequency transmitter and transmitting coil enclosed in a sterile bag and placed over the implant. This step assures that coupling of the implant and the external controller occur and that all electrodes are functioning as intended. Sterile dressings and a long arm cast are applied. The position depends on whether a deltoid-to-triceps transfer has been done. Transfers must be protected for the appropriate interval, about 6 weeks, except for the deltoid transfer, which must be protected for 8 to 10 weeks. The electrodes are encapsulated at 1 to 2 weeks, so if transfers are not performed, the cast may be removed and rehabilitation begun at that time. Rehabilitation involves training in the use of the joystick controller and strengthening the muscles. Marked improvement in motion and strength can be expected. The system is programmed to automatically exercise at night and between periods of voluntary use, thereby facilitating rapid recovery. Use as tolerated is dictated solely by the patient s facility with the device and any period of protection required by tendon transfers. Outcomes Mechanical Results The Freehand system provides improvements in grasp force equivalent to those provided by surface-stimulation neuroprostheses. 5 In 1997, Kilgore et al 35 reported the results of a 3- to 9-year follow-up on the first five patients provided with the Freehand system. All five obtained functional lateral and palmar grasp patterns, with pinch forces ranging from 8 to 25 newtons (N). Twenty-three of the 25 muscle groups stimulated (five groups per patient) achieved a force of 4 of 5; both exceptions were finger extensors. In the five patients, all but one of the 41 epimysial electrodes implanted remained functioning throughout follow-up. One electrode failed at the lead-electrode junction, but all electrode-muscle interfaces remained stable over time. Carroll et al 36 described similar results in the first six patients implanted in Australia. All obtained palmar grasp and lateral pinch forces ranging from 5 to 15 N, with significant differences for both (P = 0.003) from presurgery and postsurgery device-off pinch forces. A large, multicenter trial of 50 patients implanted with the Freehand device reported similar results. 28 Median lateral pinch force was 12 N using the device and 1.5 N with the device switched off, with a significant improvement (P < 0.001) in all 50 patients. Median palmar pinch force was 6.6 N with the device and 0.4 N without it, with a significant improvement (P < 0.001) in 48 of the 50 patients. These improvements remained stable after at least 1 year in 19 of 26 patients available for follow-up. All 50 patients gained active finger motion using the neuroprosthesis, whereas none had active finger motion without it. Functional Results As has been shown with surfacestimulation neuroprostheses, 4,5 the Freehand system enables users to perform several manual tasks that are not possible without the device. A quantitative test of grasp-and-release function has been developed for the evaluation of neuroprosthesis function. 37 Of the first five patients implanted with the device in the United States, 35 all while using the neuroprosthesis were able to manipulate five of six objects that they could not manipulate without it. In the multicenter study,,28 49 of 50 patients (98%) were able to manipulate at least one 76 Journal of the American Academy of Orthopaedic Surgeons

6 Roger Cornwall, MD, and Michael R. Hausman, MD more object with the neuroprosthesis than without, and 37 patients (74%) could manipulate at least three more objects. The neuroprosthesis has shown substantial benefits in activities of daily living (ADL). All five patients reported by Kilgore et al 35 gained independence from others and from adaptive equipment in tasks such as eating with a fork and writing with a pen. These results are similar to those seen with an earlier external neuroprosthesis with percutaneous electrodes. 38 Similarly, all of the six patients implanted in Australia became independent of physical assistance or adaptive equipment in 97% of activities for which they were dependent without the neuroprosthesis. 36 Hobby et al 29 reported similar results in seven of nine patients in Great Britain. In their multicenter study, Peckham et al 28 reported an improvement in all 49 patients tested with Activities of Daily Living Abilities or Activities of Daily Living Assessment tests. Improvements in ageappropriate ADLs also have been demonstrated in five adolescents 39 and one 10-year-old child 31 implanted with the neuroprosthesis. Improvements in independence can be translated into savings in the costs of assistance. One calculation predicted that the cost of a hand neuroprosthesis could be recovered over the user s lifetime if attendant time were reduced by 2 hours per day. 40 However, in one series of nine users, no patient reported a reduction in use of care from outside agencies, although two reported a reduction in use of family-provided care. 41 Use and Satisfaction The percentage of patients that voluntarily uses the Freehand system after implantation compares favorably with that for surface-stimulation neuroprostheses, which ranges from 30% to 60%. 4,5 Kilgore et al 35 found that four of five patients implanted with the device used the neuroprosthesis for ADLs at least half the time. The fifth patient s use was limited by ipsilateral shoulder pain unrelated to the prosthesis. Seven of the nine patients provided with the neuroprosthesis in Great Britain used the prosthesis daily and preferred its use to dependence on others or assistive devices for 80% of ADLs. 29,41 (The remaining two patients in this series lost the use of the device because of complications.) Carroll et al 36 reported that six of six patients preferred to use the neuroprosthesis for 85% of ADLs. Peckham et al 28 surveyed the use of the neuroprosthesis in 40 patients; 34 (85%) used the device regularly for ADLs, 3 (7.5%) used it for ADLs and exercise, and 3 did not use the device. Commonly reported reasons for not using functioning neuroprostheses are difficulties donning the external equipment, shoulder pain, and lack of need. 42 In general, patients have been satisfied with the prosthesis. Stroh Wuolle et al 42 surveyed 34 patients from several centers; 97% said that they would recommend the prosthesis to others and 87%, that they would have the surgery again. Ninety percent were satisfied in general; 80% felt the neuroprosthesis met their expectations. Ninety percent of patients reported that the neuroprosthesis improved their quality of life, and 93% could perform ADLs more easily. Eighty-seven percent of patients felt more independent and reported that their appearance was unchanged or improved. Complications and Failures Mechanical and electrical failures have been infrequent. During the first 2 years of implantation, memory corruption in the external control unit was common, but this problem has been largely eliminated in newer models. 36 Kilgore et al 35 reported two instances (of five patients) in which the receiver/stimulator rotated on the chest wall, causing a lead fracture in one case. An additional receiver/ stimulator had to be replaced because of powering difficulties. A few users have reported problems associated with the external components, such as irritation from the adhesives or difficulty positioning the external components. In a series of 51 patients with a minimum follow-up of 3 years, no cases of neuroprosthesis failure were reported, although 3 of the 408 implanted electrodes failed and required replacement. 28 Only one lead failed because of mechanical fatigue. Infections have been uncommon. In the series of Peckham et al, 28 3of 51 patients (6%) had localized infections that required removal and subsequent reimplantation of an electrode. One patient allowed a localized infection to progress along the electrode leads before seeking medical attention, requiring removal of the entire system. Summary Advances in technology promise to increase the capabilities of and applications for implantable neuroprostheses. The first-generation Freehand System is no longer available from NeuroControl because of financially based business decisions by the company s management. Devices are still available on a selective basis in several centers. Further development work continues. The controller has already shrunk from a 7-lb device to a beeper-sized package powered by a cell phone battery. Twelve-channel systems have been implanted in several patients under experimental protocols. Networked systems are under development in the United States and Europe that use independent receiver/stimulators networked together by a central electronic spinal cord. Such systems can incorporate a large number of sensors as well as leads that make complex motions possible in both the upper and lower extremities. Improved motion, myoelectric, and EEG-based controllers Vol 12, No 2, March/April

7 Implanted Neuroprostheses for Restoration of Hand Function in Tetraplegic Patients also will permit more nearly natural, physiologic control. An EEG-controlled, 24-channel, bilateral implantable prosthesis is possible, thus realizing the potential of neuroprosthetics to bypass the injured spinal cord by providing a natural, closely physiological detour from the brain to the extremities. References 1. van Overeem Hansen G: EMGcontrolled functional electrical stimulation of the paretic hand. Scand J Rehabil Med 1979;11: Peckham PH, Mortimer JT, Marsolais EB: Controlled prehension and release in the C5 quadriplegic elicited by functional electrical stimulation of the paralyzed forearm musculature. Ann Biomed Eng 1980;8: Peckham PH, Marsolais EB, Mortimer JT: Restoration of key grip and release in the C6 tetraplegic patient through functional electrical stimulation. J Hand Surg [Am] 1980;5: Snoek GJ: I Jzerman MJ, in t Groen FA, Stoffers TS, Zilvold G: Use of the NESS handmaster to restore handfunction in tetraplegia: Clinical experiences in ten patients. Spinal Cord 2000;38: Prochazka A, Gauthier M, Wieler M, Kenwell Z: The bionic glove: An electrical stimulator garment that provides controlled grasp and hand opening in quadriplegia. Arch Phys Med Rehabil 1997;78: Keith MW, Peckham PH, Thrope GB, Buckett JR, Stroh KC, Menger V: Functional neuromuscular stimulation neuroprostheses for the tetraplegic hand. Clin Orthop 1988;233: Keith MW, Peckham PH, Thrope GB, et al: Implantable functional neuromuscular stimulation in the tetraplegic hand. J Hand Surg [Am] 1989;14: Smith B, Peckham PH, Keith MW, Roscoe DD: An externally powered, multichannel, implantable stimulator for versatile control of paralyzed muscle. IEEE Trans Biomed Eng 1987;34: Hausman MR, Masters JE: Percutaneous Freehand system intramuscular electrode placement. J Hand Surg [Br] 2002;27: 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: Letechipia JE, Peckham PH, Gazdik M, Smith B: In-line lead connector for use with implanted neuroprosthesis. IEEE Trans Biomed Eng 1991;38: Kilgore KL, Peckham PH, Thrope GB, Keith MW, Gallaher-Stone KA: Synthesis of hand grasp using functional neuromuscular stimulation. IEEE Trans Biomed Eng 1989;36: Johnson MW, Peckham PH: Evaluation of shoulder movement as a command control source. IEEE Trans Biomed Eng 1990;37: Rakoš M, Freudenschuss B, Girsch W, et al: Electromyogram-controlled functional electrical stimulation for treatment of the paralyzed upper extremity. Artif Organs 1999;23: Hart RL, Kilgore KL, Peckham PH: A comparison between control methods for implanted FES hand-grasp systems. IEEE Trans Rehabil Eng 1998;6: Hoshimiya N, Naito A, Yajima M, Handa Y: A multichannel FES system for the restoration of motor functions in high spinal cord injury patients: A respiration-controlled system for multijoint upper extremity. IEEE Trans Biomed Eng 1989;36: Wolpaw JR, McFarland DJ: Multichannel EEG-based brain-computer communication. Electroencephalogr Clin Neurophysiol 1994;90: Kennedy PR, Bakay RA: Restoration of neural output from a paralyzed patient by a direct brain connection. Neuroreport 1998;9: Lauer RT, Peckham PH, Kilgore KL: EEG-based control of a hand grasp neuroprosthesis. Neuroreport 1999;10: Hummelsheim H, Maier-Loth ML, Eickhof C: The functional value of electrical muscle stimulation for the rehabilitation of the hand in stroke patients. Scand J Rehabil Med 1997;29: Chae J, Bethoux F, Bohine T, Dobos L, Davis T, Friedl A: Neuromuscular stimulation for upper extremity motor and functional recovery in acute hemiplegia. Stroke 1998;29: Gorman PH, Wuolle KS, Peckham PH, Heydrick D: Patient selection for an upper extremity neuroprosthesis in tetraplegic individuals. Spinal Cord 1997;35: Moberg E, McDowell CL, House JH: Third International Conference on Surgical Rehabilitation of the Upper Limb in Tetraplegia (quadriplegia). J Hand Surg [Am] 1989;14: Ditunno JF Jr, Young W, Donovan WH, Creasey G: The international standards booklet for neurological and functional classification of spinal cord injury: American Spinal Injury Association. Paraplegia 1994;32: Freehafer AA, Peckham PH, Keith MW: New concepts on treatment of the upper limb in the tetraplegic: Surgical restoration and functional neuromuscular stimulation. Hand Clin 1988;4: Crago PE, Peckham PH, Mortimer JT, Van der Meulen JP: The choice of pulse duration for chronic electrical stimulation via surface, nerve, and intramuscular electrodes. Ann Biomed Eng 1974;2: Mulcahey MJ, Smith BT, Betz RR: Evaluation of the lower motor neuron integrity of upper extremity muscles in high level spinal cord injury. Spinal Cord 1999;37: 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: Hobby J, Taylor PN, Esnouf J: Restoration of tetraplegic hand function by use of the neurocontrol freehand system. J Hand Surg [Br] 2001;26: Smith BT, Mulcahey MJ, Triolo RJ, Betz RR: The application of a modified neuroprosthetic hand system in a child with a C7 spinal cord injury: Case report. Paraplegia 1992;30: Smith BT, Mulcahey MJ, Betz RR: An implantable upper extremity neuroprosthesis in a growing child with a C5 spinal cord injury. Spinal Cord 2001;39: Mohammed KD, Rothwell AG, Sinclair SW, Willems SM, Bean AR: Upper-limb surgery for tetraplegia. J Bone Joint Surg Br 1992;74: Van Heest A, Hanson D, Lee J, Wentdorf F, House J: Split flexor pollicus longus tendon transfer for stabilization of the thumb interphalangeal joint: A cadaveric and clinical study. J Hand Surg [Am] 1999;24: Keith MW: Neuroprostheses for the upper extremity. Microsurgery 2001;21: Journal of the American Academy of Orthopaedic Surgeons

8 Roger Cornwall, MD, and Michael R. Hausman, MD 35. 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: Carroll S, Cooper C, Brown D, Sormann G, Flood S, Denison M: Australian experience with the Freehand System for restoring grasp in quadriplegia. Aust N Z J Surg 2000;70: Wuolle KS, Van Doren CL, Thrope GB, Keith MW, Peckham PH: Development of a quantitative hand grasp and release test for patients with tetraplegia using a hand neuroprosthesis. J Hand Surg [Am] 1994;19: Wijman CA, Stroh KC, Van Doren CL, Thrope GB, Peckham PH, Keith MW: Functional evaluation of quadriplegic patients using a hand neuroprosthesis. Arch Phys Med Rehabil 1990;71: Mulcahey MJ, Betz RR, Smith BT, Weiss AA, Davis SE: Implanted functional electrical stimulation hand system in adolescents with spinal injuries: An evaluation. Arch Phys Med Rehabil 1997; 78: Creasey GH, Kilgore KL, Brown-Triolo DL, Dahlberg JE, Peckham PH, Keith MW: Reduction of costs of disability using neuroprostheses. Assist Technol 2000;12: Taylor P, Esnouf J, Hobby J: Pattern of use and user satisfaction of Neuro Control Freehand system. Spinal Cord 2001; 39: Stroh Wuolle K, Van Doren CL, Bryden AM, et al: Satisfaction with and usage of a hand neuroprosthesis. Arch Phys Med Rehabil 1999;80: Vol 12, No 2, March/April

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