Implantable functional neuromuscularstimulation in the tetraplegic hand

Functional neuromuscular stimulation of the upper extremity provides manipulative capacity topersons with high level tetraplegia who have insufficient voluntary muscles available for tendontransfer surgery. We report an enhancement of the technique to include surgical implantationof a multichannel receiver-stimulator, sensory feedback stimulation, and tendon transfers. Ten­don transfers were done with spastic, rather than voluntary motors employing standard surgicaltechniques. The system described has been operational for more than 1% years. (J HAND SURG

1989;14A:524-30.)

Michael W. Keith, MD, P. Hunter Peckham, PhD, Geoffrey B. Thrope, BS,Kathy C. Stroh, OT, Brian Smith, BSc (Hons), James R. Buckett, MS,Kevin L. Kilgore, MS, and James W. Jatich, Cleveland, Ohio

Provision of hand function for the personwith high level tetraplegia who has no voluntary mus­cles for tendon transfer has heretofore been impossibleexcept by splinting and primitive tenodesis grip. Al­though the grasp may be functional, it is weak andmanipulation is limited. Previous functional neuromus­cular stimulation (FNS) systems have been imple­mented using percutaneous electrodes to excite para­lyzed muscles with intact peripheral innervation. !-4 Thetechnique and experimental basis of FNS have beenpreviously described.': 2. 5. 6

We report the case study of one subject with a newmethod of powering spastic muscle using functionalneuromuscular stimulation employing an implantablestimulator and surgical procedures as part of the neu­roprosthesis. The system diagram is shown schemati­cally in Fig. 1. Control motions of the contralateral

From the Department of Orthopaedic Surgery and Biomedical En­gineering, Case Western Reserve University, Cleveland Metro­politan General/Highland View Hospital; and the Veterans Ad­ministration Medical Center, Cleveland, Ohio.

Supported in part by NIH-NINCDS Contract No. N01-NS-6-2303,and the Veterans Administration Research and DevelopmentService.

Received for publication Feb. 17, 1988; accepted in revised formJuly 29, 1988.

No benefits in any form have been received or will be received froma commercial form related directly or.indirectly to the subject ofthis article.

Reprint requests: P. Hunter Peckham, PhD, Rehabilitation Engi­neering Center, Department of Orthopaedics, 3395 Scranton Rd.,Cleveland, OH 44109.

524 THE JOURNAL OF HAND SURGERY

shoulder are related to hand position; shoulder elevationand depression control "hold or lock" functions. Fingerand thumb position and force are proportional to shoul­der protraction and retraction.' Tendon transfers usingelectrically stimulated spastic muscle are used to pro­vide power and motion to finger joints otherwise un­stable or uncontrolled. Surgical technique and rationalefor this implant technology is detailed; microprocessorbased controller and processor hardware is described.

Methods

Subject. The subject is a 37-year-old right-handedmale engineer who has tetraplegia resulting from a spi­nal cord injury in a swimming accident in August 1977.His functional level of injury was C6 and he retainedshoulder girdle control, elbow flexion, and wrist ex­tension provided by extensor carpi radialis longus(ECRL) only. All other forearm muscles were para­lyzed. Table I indicates the state of some pertinent mus­cles in this subject's case. He retained some sensibilityinto the C6 dermatome, but two-point discrimination(2PD) was greater than 10 mm over the thumb andindex finger. He was not a candidate for tendon transfersaccording to the criteria practiced in our Spinal InjuryCenter." No previous rehabilitation to independent handfunction enabled him to perform some activities ofdaily living with the assistance of an attendant and weakC6 tenodesis grip. He had been a participant inthe research program of the Case Western ReserveUniversity-Veterans Administration Rehabilitation En­gineering Center since 1978 and met all inclusion cri­teria for the study. These included medical stability,

Vol. 14A, No.3May 1989

TransmittinQAntenna

EiQht ChannelImplantable -+--_>AY'l­Stimulator

ElectrodeTerminations

Functional neuromuscular stimulation in tetraplegic hand 525

Fig. l. Line drawing representation of implantable system. The shoulder sensor. control electronics,and transmitting antenna are external, and the receiver-stimulator and leads are surgically implanted.

Table I. Status of innervation of major musclegroups of the forearm and hand and musclesstimulated in stages I and II of the procedure

Abbreviations: BR, Brachioradialis; ECRL, extensor carpi radialis longus;ECRB, extensor carpi radialis brevis; FOP. flexor digitorum profundus; FOS,flexor digitorum superficialis; EDC, extensor digitorum communis; ECU, ex­.ensor carpi ulnaris; EPL, extensor pollicis longus; FPL. flexor pollicis longus;AdP, adductor pollicis; MTI, median nerve innervated thenar intrinsics.

pharmacologically controlled spasticity, stable seatedposture in a wheelchair, freedom from systemic infec­tion, high motivation for hand function, absence ofcardiac arrhythmia, cutaneous disorders or metal al­lergy, emotional stability and family support, a non­pathologic Minnesota Multiphasic Personality Inven­tory, and demonstrated satisfactory performance witha percutaneously installed electrode system and facileuse of the controller." With regard to the latter, he hadbeen a regular user of the percutaneous system for 8years and was able to perform activities of daily livingproficiently with the system. 3.4 Thus he was completelyversed in system operation and capabilities. He wascompletely informed of the status of developmentthroughout the project and was knowledgeable aboutpotential complications.

Goals of the operations. The goals of the imple­mentation of this system are related to the two separatestages in which the implementation was performed. Thegoals of the first-stage hand procedures were to stabilizethe thumb interphalangeal (lP) joint, provide uniform

Muscle

BRECRLECRBPDPPDSEDCECD

EPLFPLAdPMTI

Voluntary Ielectricallyexcitable Denervated

(VIEID)

vVDEEEE

EEEE

Stage I Stage II

526 Keith et al.The Journal of

HAND SURGERY

Fig. 2. The complete implantable stimulator including the stimulator package , lead connectors,leads, and terminal electrodes.

movement of the digits and equal transmission of forceacross the digits during active flexion and extension ,and an intrinsic plus type of finger positioning duringstimulation of the flexor digitorum superficial is (FDS).The goal of the second stage was to substitute the im­planted stimulator, leads , and electrodes for the per­cutaneous leads, and to provide electrotactile sensoryfeedback, while providing motor function at least equiv­alent to that available with the percutaneous unit.

Implantable stimulator. The implantable stimulatorprovides eight stimulation channels and is radio fre­quency powered and controlled by an external, portablecomputer-based controller and proce ssor." 10 Fig. 2shows the complete implantable device. The titanium­packaged, hermetically-sealed circuitry is further em­bedded in medical grade epoxy and coated with sili­cone. A reinforced backing of Dacron /silicone allowssutures to initially stabilize and orient the device on thepectoralis fascia. Interlead connectors are designed toallow leads of varying lengths to be attached and ad­justed to the size and location of activated muscles ineach patient and adjust for variations in limb length andthe mapped position of the electode-muscle interface .They also provide a separate site for subsequent serviceand lead exchange without stimulator replacement inthe event of single lead or electrode failure. The con­nectors allow stimulator replacement without alter­ations to the terminal electrode array that is encapsu-

lated and adherent to the epimysial interface . The epi­mysial muscle electrodes are platinum disks stabilizedin a molded silicone frame .

The stimulator is powered and controlled by an ex­ternally worn device that transmits all power and controlinformation using a radio frequency carrier. Controlmotions of the contra-lateral shoulder are related tohand position by an externally worn shoulder positiontransducer. Shoulder elevation and depression control"hold or lock" functions. Thumb and finger position isproportional to shoulder protraction and retraction.

Surgical procedures and postoperative manage­ment. The procedure was done in two stages. At thefirst stage procedures were done to balance the handand to restore lost functions by use of tendon transfer.Left thumb interphalangeal joint arthrodesis was doneusing three percutaneous Kirschner wires. To providesynchronous finger flexion , the tendons of flexor dig­itorum profundus (FDP) of index , long, ring and smallfingers were sutured together side to side with No.2-0 Dacron-braided suture at equal balance and jointposition . Intraoperative testing using electrical stimu­lation indicated symmetrical finger flexion. Preopera­tive claw posturing and metacarpal-phalangeal joint hy­perextension caused by intrinsic weakness was cor­rected by transfer of the flexor digitorum superficialis(FDS) of each finger to the Al pulleys as a modificationof the lasso procedure described by Zancolli. II Finger

Vol. 14A, No.3May 1989

Table II. Functions provided by in each grasp mode

Muscle group implanted

Functional neuromuscular stimulation in tetraplegic hand 527

Motion provided

Thumb

Fingers

Thumb intrinsics (median innervated)Adductor pollicisFlexor pollicis longusExtensor pollicis longus

Flexor digitorum profundusExtensor carpi ulnaris /Extensor digitorum communisFlexor digitorum superficialis

Abduction in palmar graspAdduction in lateral graspFlexion in lateral graspExtension in both grasps

Finger flexion in both grasps

Finger extension in both graspsMep flexion in palmar prehension

extensors were balanced by side-to-side suture of ex­tensor digitorum communis (EDC) of index, long, ringand small fingers side to side with No. 2-0 Dacron andsynchrony confirmed by electrical stimulation. Multi­strand intramuscular electrodes were implanted at op­eration into each muscle group to be controlled by FNS.Table II shows muscles implanted at the first stage. Theleads were tunneled subcutaneously to the upper, outerarm distal to the deltoid insertion and brought throughthe skin surface. A molded silicone surface connec­tor / cover protected the leads and allowed cable con­nection to the external controller. The arm was im­mobilized for 6 weeks to allow healing and electrodestabilization in muscle. Healing of finger incisions wasslower than average in this subject and exceeded ouroriginal plan for 3 weeks of immobilization. The stim­ulation array performed well, with the exception of thetwo leads to the abductor pollicis longus (APL), whichfractured at 8 months in the upper arm. Cause of thefracture of these two leads has not been established.They were replaced with additional leads implanted byour customary percutaneous technique." More uniformgrasp patterns were achieved than were available withthe previous percutaneous system, and the subject ap­proved of the result. However, some loss of finger ex­tension resulted from adhesion of the EDC tendons tothe tendon bed and surrounding tissue. We believethis was due to the prolonged immobilization period(8 weeks) and slow onset of subsequent movement withstimulation. Therapy and stimulation reduced but didnot eliminate resulting adhesions. At the completion ofthis stage, the subject had improved grasp even in theabsence of stimulation. With stimulation added, thegrasp strength and hand opening further improved.

At stage two, the objectives were to implant the stim­ulator with its epimysial electrode array, a sensory elec­trode, and do tenolysis and transfer for finger extension.The operation was done 13 months after the stage-one

procedure. Finger extension weakness was treated bytransfer of extensor carpi ulnaris (ECU) to the conjoinedEDC. Terminal electrodes were applied to the surfaceof the epimysium of the same muscles as previouslyexercised and controlled by the percutaneous system.Major differences at this stage were that the electrodeswere on the muscle surface opposite motor nerve entrypoints, with the exception of the FDP, which was lo­cated on the inferior, deep muscle surface to increasespecificity of recruitment and the implantation of a sen­sory electrode. 12

Receiver-stimulator implantation. The stimulatorwas surgically implanted, with the patient under generalendotracheal anesthesia, in a subcutaneous pocket overthe fascia of the pectoralis major muscle on the side ofthe body to be controlled using a transverse incision insensory intact C5 dermatome skin. The stimulator back­ing was sutured to the fascia with four No. 4-0 Tevdek(tm) sutures.

Fig. 3 shows a xerogram of the entire implantedsystem with the stimulator package located on the chestwall, the inter-lead connectors at the upper humerusand the epimysial electrodes over individual muscles inthe forearm and hand. Xerograms show a large radiusof curvature without kinking in the two tandem helicallywound 15 strand wire leads and electrodes. Construc­tion of the leads in a silicone tube improve tissue bio­compatibility and reduces lead strain by allowing freelead translation within the tissue surrounding the tubeand prevents anchoring of the helical coils in subcu­taneous tissue. No failures of these leads have beennoted in 152 animal-months of implantation for as longas 21

/ 2 years and over a total of over 1000 lead-monthsof testing in 16 devices.

Electrodes were initially stabilized to the epimysialtissue using five No. 4-0 Dacron sutures. These suturestemporarily align the electrode in the optimum positionfor stimulation on the muscle surface. Later, thin fibrous

528 Keith et at.The Journal of

HAND SURGERY

.._______J:CU...al'..........::;;,,;,, ......

Fig. 3. A, Xerogram mosaic of stimulator, leads, connectors and sensory stimulation electrode.B, Electrode installations on forearm and intrinsic muscles of the left upper extremity. The trans­mitting antenna is applied on the skin surface over the distal end of the stimulator package.

tissue encapsulation of the electrode binds it to themuscle surface. The site on the muscle surface for stim­ulation was selected for desirable length-tension prop­erties of muscle, selective muscle recruitment, and cou­pling of the electrode to intramuscular nerve branches. 12

Suboptimal placement may lead to excessive nerve re­cruitment such that muscle force is difficult to gradeby spatial summation of motor units (increasing currentapplication), or that the force of contraction changesdue to coupling change between the nerve and elec­trodes. The technique of intraoperative determinationof length-tension properties was performed using thetechnique of a buckle transduction over the intact ten­don." The intrinsic muscle electrodes were placed onthe superficial aspect of the adductor pollicis and ab­ductor pollicis brevis muscles, The leads pass throughthe carpal tunnel and then proximally on the flexorsurface of the forearm fascia.

A sensory feedback electrode was sutured to sub­cutaneous tissue within a pocket made beneath the skinover the clavicle in the C-4 sensory distribution. Theexposed platinum electrode is oriented toward the skin

surface. The electrode was used to provide cognitiveand machine state feedback. Specifically, a frequencycode indicated the on/off/hold condition of the stim­ulator, and the position of the shoulder. Sensory stimuliwere perceived as a comfortable "buzz," "vibration,"or "tone. "14 Care was taken to avoid too superficialplacement such that erosion is unlikely and yet not toodeep such that muscle stimulation occurs or high cur­rents are needed to elicit skin responses.

The leads were tunneled subcutaneously using a tro­char and aluminum tube. The lead connectors wereassembled between stimulator and leads by a separateincision at the lateral upper arm and,the metal coveredby a silicone sheath held in place with sutures." Theelbow, forearm, and wrist were immobilized after im­plantation to prevent lead migration and facilitate en­capsulation.

Postoperative exercise was started after 3 weeks ofarm immobilization. The patient used a 12-hour pernight exercise program, which allowed finger flexionand extension and thumb adduction. The stimulus wasadjusted to provide full active range of motion (with

Vol. 14A, No.3May 1989

9

8

7

6

3

o

Functional neuromuscular stimulation in tetraplegic hand 529

STIMULATION THRESHOLDSRTMC& SUBJECT JHJ

-ITHRESIIOLDS NORMALIZED TO POST 100 DAY MEAN

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Fig. 4. Threshold responses for each of the electrodes. Threshold responses are shown normalizedto this average value obtained over the first 100 days after implantation for each of the eightelectrodes. The threshold of all electrodes have remained essential stable since implantation, withthe exception of channel 3 (FPL), which transiently increased during a period of extensive elec­trically induced exercise. This recovered to a stable level when the exercise was moderated.

stimulation) of thumb abduction and finger flexion andmaximum finger extension. Dynamic splinting wasused to assist the passive flexion forces of the fingersduring finger extension, with the objecti ve of protectingthe tendon transfer. The patient was allowed to do lightADL tasks with adaptive equipment, but used a pro­tective splint for the rest of the day. Four weeks afterthe operation, thumb extension was included into theexercise program, and active exercise increased. Thepatient began functional use with the neuroprosthesis 2months after operation.

Results

The device and electrode array functioned as de­signed. There have been no surgical or technical com­plications, infection, lead erosion, or lead failure at I Yzyears follow-up. However, the transmitted power nec­essary to activate the implant circuitry has increased.This has not changed the stimulus output, which ex­ternal measurements show to be stable over the implantperiod. No sensibility or motor function was lost.

Threshold responses (Fig. 4) have essentially been sta­ble, except for one channel (No.3) during the earlypostimplantation period when excessive exercise wasused. This recovered after reducing exercise, and isbelieved to be due to a movement-induced compartmentsyndrome.

The subject was able to perform activities of dailyliving such as eating, brushing teeth, grooming, wash­ing, operation of computer and electronic equipment,telephoning, and manipulate objects without a prehen­sion splint and without the necessity of an attendantprepositioning the object or adapting objects for grasp.Some tasks that could not be accomplished before op­eration and without stimulation could now be accom­plished without stimulation as a result of better teno­desis function from the tendon transfers. Preoperativeobject grasp was limited to small light objects held inweak tenodesis grasp, whereas after operation largerand heavier objects could be held. Preoperative passiveforce was 0.5 N and increased to 1.8 N after surgery.Lateral prehension force with stimulation increased

530 Keith et al .

from 8 N preoperatively to 14 N postoperatively. Pal­mar prehension force with stimulation was asymmetricpreoperatively and forces were not measured, they were12 N postoperatively. Hand opening after operation was7 cm with passive wrist flexion due to tenodesis openingand increased to 11 cm with stimulation. For lateralprehension/release, the hand opening (thumb to lateralsurface of index finger) was 2.5 em. Lateral prehensionpermitted strong grip of small objects such as a com­puter floppy disk or paper. Palmar prehension of largerobjects such as cups and bottles was possible. Aftertraining in use of the system for functional activities,the use of the prosthesis is selected for manipulationtasks in which the remaining voluntary strength is in­sufficient. We believe this represents a level of inte­gration of the system into identified needs.

The most obvious benefits of the implant have beenthe elimination of the maintenance of the percutaneouswires and sensory feedback. Difficulties in external ca­ble reliability and continuity have been eliminated.These changes reflect significantly on the acceptabilityof the device to the user and his family. Sensory feed­back provided by electrocutaneous stimulation providesa clear and inconspicuous source of signaling the devicestate. We believe that this approach of restoration offersa great deal of increased potential to the patient with ahigh level spinal injury.

Conclusions

Functional neuromuscular stimulation with an im­plantable stimulator eliminates the percutaneous inter­face and simplifies donning the neuroprosthesis. Theaddition of FNS powered and controlled tendon trans­fers permits new functions to be added to the paralyzedhand beyond those not possible by percutaneous stim­ulation alone. The specificity of electrode-muscle cou­pling is improved by operative mapping and placement.The system provides grasp and manipulation unavail­able by conventional methods increasing the indepen­dence of the person with high level tetraplegia.

REFERENCES

1. Peckham PH, Mortimer JT, Marsolais EB. Controlledprehension and release in the C5 quadriplegic elicited byfunctional electrical stimulation of the paralyzed forearmmusculature. Ann Biomed Eng 1980;8:369-87.

The Journal ofHAND SURGERY

2. Peckham PH, Marsolais EB, Mortimer JT. Restorationof key grip and release in the C6 tetraplegic patientthrough functional electrical stimulation. J HAND SURG1980;5:462-69.

3. Peckham PH. Functional electrical stimulation : currentstatus and future prospects of applications to the neu­romuscular system in spinal cord injury. Paraplegia1987;25:274-88.

4. Peckham PH, Keith MW, Freehafer AA. Restoration offunctional control by electrical stimulation in the upperextremity of the quadriplegic patient. J Bone Joint Surg1988;70A:I44-8.

5. Peckham PH, Mortimer JT, Marsolais EB. Alteration inthe force and fatigability of skeletal muscle in quadri­plegic humans following exercise induced by chronicelectrical stimulation. Clin Orthop 1976;114:326-34 .

6. Peckham PH, Mortimer JT. Marsolais EB. Upper andlower motor neuron lesions in the upper extremity mus­cles of tetraplegics . Paraplegia 1976;14:115-21.

7. Freehafer AA. Kelly CM, Peckham PH. Tendon transferfor restoration of upper limb function after a cervicalspinal cord injury . J HAND SURG 1984;9A:887-93.

8. Keith MW, Peckham PH. Thrope GO, Buckett JR , StrohKC, Menger VL. Functional neuromuscular stimulationneuroprostheses for the tetraplegic hand . Clin Orthop1988;233:25-33.

9. Buckett JR, Peckham PH, Thrope GB, Braswell SD,Keith MW. A flexible , portable functional neuromuscularstimulation neuroprosthetic system. (Submitted for pub­lication.)

10. Smith B, Buckett J, Peckham PH, Keith MW, RoscoeDO. An externally powered, multichannel, implantablestimulator for versatile control of paralyzed muscle . IEEETrans Biomed Eng 1987;34:499-508.

II . ZancoJli E. Structural and dynamic basis of hand surgery.2nd ed. Philadelphia: Lippincott, 1979;117.

12. Grandjean PA, Mortimer JT. Recruitment propertiesof monopolar 'and bipolar epimysial electrodes. AnnBiomed Eng 1986;14:53-66 .

13. Mendelson LS, Peckham PH, Freehafer AA, Keith MW.Intraoperative assessment of wrist extensor muscle force .(Submitted for publication.)

14. Riso RR, Ignagni AR, Keith MW. Sensory augmentationfor enhanced control of FNS grasp restoration systems .In: Popovic 0 , ed . Advances in external control of humanextremities. Belgrade, Yugoslavia: 1987:215-31.

15. Letechipia 1£, Peckham PH, Gazdik M, Smith B. In­line Lead connector for use with implanted neuropros­thesis . (Submitted for publication.)