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32 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 12, NO. 1, MARCH 2004
Epidural Spinal-Cord Stimulation FacilitatesRecovery of Functional Walking Following
Incomplete Spinal-Cord InjuryMichael R. Carhart, Member, IEEE, Jiping He, Senior Member, IEEE, Richard Herman, S. D’Luzansky, and
Wayne T. Willis
Abstract—We investigated a novel treatment paradigm fordeveloping functional ambulation in wheelchair-dependentindividuals with chronic, incomplete spinal-cord injury. Bycoordinating epidural stimulation of the dorsal structures ofthe spinal cord with partial weight bearing treadmill therapy,we observed improvement in treadmill and over-ground am-bulation in an individual with chronic incomplete tetraplegia.The application of partial weight-bearing therapy alone was notsufficient to achieve functional ambulation over ground, thoughtreadmill ambulation improved significantly. Combining epiduralspinal-cord stimulation (ESCS, 10– 12 vertebral levels) withpartial weight-bearing therapy resulted in further improvementduring treadmill ambulation. Moreover, the combination oftherapies facilitated the transfer of the learned gait into overground ambulation. Performance improvements were elicited byapplying continuous, charge-balanced, monophasic pulse trainsat a frequency of 40–60 Hz, a pulse duration of 800 s, and anamplitude determined by the midpoint (50%) between the sensoryand motor threshold values. The participant initially reported areduction in sense of effort for over ground walking from 8/10to 3/10 (Borg scale), and was able to double his walking speed.After several weeks of over ground training, he reached maximumwalking speeds of 0.35 m/s, and was able to ambulate over 325m. We propose that ESCS facilitated locomotor recovery in thispatient by augmenting the use-dependent plasticity created bypartial weight bearing therapy. Confirmation of these promisingresults in a controlled study of groups of spinal-cord-injuredsubjects is warranted.
Index Terms—Electrical stimulation, gait rehabilitation, musclecoordination, spinal-cord injury.
I. INTRODUCTION
OVER the past decade, treadmill training with partialbody weight support has emerged as a promising tech-
nique for improving locomotor function in individuals with
Manuscript received December 6, 2002; revised May 23, 2003. This work wassupported in part by the U.S. National Science Foundation under Grant DGE-9987619 and in part by joint funding from Arizona State University (throughthe AZ Biodesign Institute) and Banner Health Systems.
M. R. Carhart was with the Harrington Department of Bioengineering, Ari-zona State University, Tempe, AZ 85287 USA. He is now with Exponent, Inc.,Phoenix, AZ 85027 USA.
J. He is with the Harrington Department of Bioengineering and ArizonaBiodesign Institute, Arizona State University, Tempe, AZ 85287 USA and alsowith Control Science and Engineering, Huazhong University of Science andTechnology, Wuhan 400032, China (e-mail: [email protected]).
R. Herman and S. D’Luzansky are with the Banner Good Samaritan MedicalCenter, Phoenix, AZ 85006 USA.
W. T. Willis is with the Kinesiology Department, Arizona State University,Tempe, AZ 85287 USA.
Digital Object Identifier 10.1109/TNSRE.2003.822763
incomplete spinal-cord injury (ISCI) [1]–[9]. Termed partialweight-bearing therapy (PWBT), this technique has evolvedfrom observations that moving treadmill belts can initiateand sustain locomotion in chronic spinal animals when thebody is supported [10]. The mechanism of this approach hasbeen attributed to plastic changes in the spinal-cord circuitryassociated with locomotion rhythm generation through thereintroduction of appropriate afferent input [11]. De Leonet al. demonstrated in animal studies that such spinal motorlearning is task—or training—specific [12], and dependentupon repetitive activation of the appropriate pathways throughpersistent training [13].
PWBT, applied alone [2], [4], [14] and in combinationwith functional electrical stimulation [15] and pharmaco-logical agents [16], has been shown to facilitate locomotorfunction in individuals with ISCI, improving coordination,speed, endurance, and the reliance on assistive devices. Moreimportantly, these benefits have not been limited to treadmillambulation, but have been shown to be transferable to overground walking and continue beyond the period of treadmilltraining [17].
An additional approach that holds promise for facilitatinglocomotor recovery is that offered by epidural spinal-cordstimulation (ESCS). Iwahara et al. demonstrated that active andfictive hindlimb locomotion could be induced in decerebratecats using nonpatterned surface stimulation of the dorsallumbar spinal cord [18]. Although nonweight bearing, theresulting locomotor patterns were well organized and expressedin the absence of afferent input. Promising results have alsobeen reported in human studies by Dimitrijevic et al. [19],[20]. These investigators have shown that tonic stimulation ofthe posterior lumbar spinal cord can induce “locomotor-like”muscle activity and rhythmic limb movement in supine indi-viduals with chronic, motor complete SCI. Finally, ESCS hasshown potential for improving locomotion among AmericanSpinal Injury Association (ASIA) D [21] and multiple sclerosis(MS) patients [21]–[24].
Since the use of spinal-cord stimulation was first reportedby Shealy et al. 35 years ago [25], neuromodulation systemshave been widely adopted for the treatment of chronic pain.Epidural stimulation systems have evolved substantially in thepast two decades, with current systems featuring multiple-elec-trodes having multiple contacts [26]. Such electrode configura-tions were developed in an effort to improve stimulus recruit-ment of dorsal columns in pain control applications [26], and
1534-4320/04$20.00 © 2004 IEEE
CARHART et al.: ESCS FACILITATES RECOVERY OF FUNCTIONAL WALKING 33
have been demonstrated to improve long-term device reliability[27], reduce the need for surgical repositioning [26], and im-prove paresthesia coverage in chronic pain applications [28].Moreover, these multicontact–multichannel systems are appro-priate for locomotion applications, where the programmable de-livery of focused stimulation to an extended region of the pos-terior lumbar cord is desirable.
Based upon these concepts and technological developments,we posited that the novel combination of PWBT and ESCScould be utilized to facilitate the recovery of functional overground ambulation in individuals with more severe ASIA CISCI. In this paper, we describe our methodology for the ap-plication of this combined therapy, and present results and dis-cussion of the improvement in ambulatory function that was ob-tained using this approach.
II. METHOD
A. Epidural Neuromodulation Systems
An externally powered ESCS system was used in this study.It consists of an implanted receiver (X-trel 3470), a pair of im-planted quadripolar electrode leads (PISCES-Quad Plus, Model3888), dual implanted lead extensions, an external transmitter(X-trel, Model 3425), and an external antenna (Model 3440).The X-trel external transmitter powers the implanted receivervia transcutaneous radio frequency (RF) telemetry. This systemis well suited to applications requiring higher stimulation en-ergy, and offers the ability to deliver long pulse durations (up to1000 s).
The PISCES-Quad Plus leads were chosen to provide stimu-lation coverage over a broad region of the lumbar spinal cord.Each lead has four cylindrical platinum iridium contacts 6 mmlong, 1.27 mm in diameter, and separated by a distance of 12 mm(Fig. 1). The target placement for each lead was approximately1 mm lateral to the anatomical midline, assuming this midlineconfiguration would maximize the potential for recruiting neu-rons in the dorsal spinal cord [29] versus the dorsal roots [30](see also [26]), and to ensure that the electrode pair could pro-vide symmetric bilateral stimulation. The leads were placed ina parallel nonstaggered configuration, and driven using contin-uous, nonpatterned stimulation. The pulse generator was used inthe SingleStim mode, with each quadripolar lead configured tothe same contact combination, pulse amplitude, pulse duration,and stimulation rate. The stimulator was configured to delivermonophasic pulses; however, it is noted that this mode actu-ally involves the delivery of an asymmetric biphasic stimulationwaveform consisting of a single dominant rectangular stimula-tion pulse followed by a low-amplitude, long-duration pulse ofopposite polarity to maintain charge balance and chemical re-versibility at the electrode–electrolyte interface.
B. Participant Selection
A 43 year old – ISCI wheelchair-dependent individualwith tetraplegia (3.5 years post-injury at the time of admissionto the study) served as the first of three subjects approved for thisinvestigation. The Institutional Review Boards at Banner Good
Fig. 1. Schematic illustration of the ESCS leads used in this study andtheir approximate position relative to the spinal column as determined byfluoroscopy.
Samaritan Medical Center (BGSMC) and Arizona State Univer-sity (ASU) approved the study, as did the Food and Drug Ad-ministration (FDA) under the investigational device exemptions(IDE) provision. The patient was screened for general medicaland psychological conditions, contractures, chemical abuse, anda recent history of pressure ulcers, and gave his informed con-sent.
Sensory and motor functions of the lower extremity were as-sessed in accordance with the ASIA impairment rating scale.Lower extremity motor score was 15/50 with muscle strengthgrades no greater than 2/5 in any one muscle. The subject wasfitted with bilateral ankle foot orthoses (AFO), and utilized thesefor treadmill and over ground ambulation throughout the courseof the study.
C. Training Program
Recognizing the task-specific nature of locomotor learningafter SCI [3], we utilized a training program that initiallyfocused on PWBT with a treadmill, and progressed to overground training with a front wheeled walker as the subject’sability to support his weight and generate coordinated steppingmovements improved. The protocol utilized the followingthree modes of locomotor training: 1) treadmill-PWBT; 2)treadmill-PWBT with/without ESCS; and 3) over groundtraining with/without ESCS.
1) Treadmill-PWBT: Physical therapists conducted PWBTon a treadmill using the LiteGait system (Mobility Research,Tempe, AZ) for partial body-weight support. Therapy wasprovided for up to 2 h/day (with appropriate rest intervals),5 days/week. Initial training was done at a treadmill speed of0.45 m/s with 40% static body weight support. The therapists
34 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 12, NO. 1, MARCH 2004
initially guided the subject’s leg movements and providedpelvic stabilization. As the subject’s endurance and ability togenerate coordinated stepping movements improved, steppingassistance and static body support were reduced while tread-mill speed was increased. Progressive increases in treadmilltraining intensity (i.e., weight supported and belt speed) wereapplied after the subject demonstrated new levels of ambulatoryfunction independent of arm support and assistance fromthe physical therapists. This was quantified as the ability tocomplete three daily sixty-second epochs of symmetrical,well-organized gait during three consecutive training sessions.
2) ESCS Device Implantation: The electrical stimulationsystem was implanted following stabilization in partial-supporttreadmill performance above the criterion level. This was pre-defined as the ability to walk independently on the treadmill ata minimum speed of 0.65 m/s with body weight support of 20%or less, while maintaining gait temporal symmetry of 50% orbetter. Each electrode lead was percutaneously introduced intothe dorsal epidural space via needle at the L2–L3 interspace.The electrode was advanced rostrally until the 0 contact wasapproximately 1 mm lateral to the anatomical midline at the
vertebral level (i.e., above the lumbar enlargement). Furtheradjustment of lead location was performed based on trial stim-ulation with various contact configurations. In this procedure,the lead was pulled caudally until stimulation (50 Hz, 500- spulse duration) produced sensory paresthesias into both legs,as well as contraction (by palpation) of the iliopsoas at higheramplitudes. The second lead was then introduced parallel andcontralateral to the first. Fluoroscopy was used to provideanterior/posterior, lateral, and oblique radiographic imagesto facilitate positioning and provide documentation of theelectrode position with respect to the spinal column. Trial stim-ulation was again performed to ensure bilateral paresthesia andhip flexor activation. Subsequently, the leads were anchored tothe paraspinal musculature and spinous process at the L3 level,and a subcutaneous tunnel was formed to route the leads to theX-trel receiver implant site in the right anterior abdomen. Thefinal position of the implant leads relative to the spinal column,as determined by fluoroscopy, is illustrated schematically inFig. 1.
After surgical wound healing and retraining with PWBTto the presurgery performance level, a variety of bipolar andtripolar electrode configurations and electrical parameter setswere examined to test the efficacy of ESCS on promotinggait (Table I). After testing a wide range of parameters, pulsedurations above 500 s and frequencies between 40 and 60Hz were selected. At a given combination of pulse durationand frequency, the stimulation amplitude was set at the mid-point between the sensory and motor thresholds. The sensorythreshold was identified as the minimum voltage producinga sense of paresthesia (tingling), while the motor thresholdwas determined as the minimum amplitude that producedtonic muscle contraction as determined by palpation. For eachwalking session, these thresholds were determined with theparticipant in an upright position.
3) PWBT, ESCS, and Over Ground Training: ESCS was ap-plied in combination with PWBT following retraining to presur-gical levels after implantation of the stimulation system. This
TABLE IMATRIX OF STIMULATION PARAMETERS INVESTIGATED. FOR EACH CONTACT
CONFIGURATION WE TESTED THE SENSORY AND MOTOR THRESHOLDS FOR
GIVEN VALUES OF STIMULATION PULSE DURATION AND RATE. THE VOLTAGE
WAS INCREASED IN 0.1-V STEPS UNTIL REACHING THE MOTOR THRESHOLD.THE STIMULATION INTENSITY WAS MEASURED AS THE TRIPLE PRODUCT OF
STIMULATION VOLTAGE, FREQUENCY, AND PULSE DURATION (V�Hz��s)
mode of training continued until the subject could support 80%of his body weight and his stepping ability reached a perfor-mance level rated by the clinicians to have demonstrated con-sistent inter- and intralimb coordination at the established tread-mill rate. Subsequently, we applied ESCS in alternating tread-mill and over ground training sessions until the subject reacheda plateau in performance. Following a plateau in performancewith alternating treadmill and over ground training sessions, wefocused on over ground training with ESCS. Finally, we evalu-ated functional ambulation in community settings when the sub-ject performed over ground walking at home and in restaurants,supermarkets, parking lots and over sidewalks. Evaluations ofperformance in these home and community settings were re-stricted to time–distance measurements and subjective evalua-tions by clinical staff.
D. Data Collection for Gait Evaluations
Periodic gait evaluations were conducted to documentchanges in kinematics and electromyographic (EMG) activityduring 1) partial-support treadmill walking and 2) over groundambulation with a front wheeled-walker.
Kinematics: Two different motion capture systems wereutilized during the course of this study. Initial evaluationswere performed utilizing a four-camera, 120-Hz MacReflexmotion capture system. Post-implantation of the ESCS system,dual Visualeyez three-dimensional (3-D) motion capture units(PhoeniX Technologies Inc., Burnaby, BC, Canada) wereutilized. In both cases, a minimum of two markers per rigidbody segment were utilized to quantify the motion of thefeet, shanks, thighs, pelvis, and torso bilaterally. The 3-Dmarker coordinates were sampled at 120 (MacReflex) or 80(Visualeyez) frames/s, and lowpass filtered with a cutoff of6 Hz. Foot switches were utilized to facilitate the identificationof gait timing events (i.e., foot contact and toeoff).
CARHART et al.: ESCS FACILITATES RECOVERY OF FUNCTIONAL WALKING 35
Muscle Activity: Bilateral surface EMG activity of the vastusmedialis, rectus femoris, biceps femoris long head, and bicepsfemoris short head was collected using 1.0-cm circular pregelledAg–AgCl electrodes (Blue Sensor). Ankle muscles were notmonitored due to the use of the AFO. Prior to electrode place-ment, the skin was shaved, lightly abraded, and cleaned with analcohol pad. Electrode pairs were placed parallel to muscle fiberdirections with a center-to-center separation distance of 3 cm,over the anatomical locations described by Delagi and Perotto[31]. A Noraxon MyoSystem 2000 was used to collect the eightchannels of raw data. This system provides differential analogamplification with a passband gain of 1000, and high- and low-pass cutoffs of 10 and 500 Hz ( 3 dB), respectively. The systeminput impedance is 10 M , and common mode rejection ratiois 85 dB. Raw signals were digitally sampled at a rate of 1000Hz, and then digitally highpass filtered at 10 Hz ( 3 dB, But-terworth, second order) to remove offset potentials and motionartifact.
To facilitate time-domain analysis, digital post-processingwas performed to compute the time- and amplitude-normalizedlinear envelope for each channel of EMG. In this offlineprocedure, signals were: 1) digitally full-wave rectified; 2)zero-phase bidirectionally lowpass filtered at 15 Hz ( 3 dB,Butterworth); then 3) time-normalized using the ipsilateralfoot-contact-to-foot-contact interval. Each channel of data wassubsequently amplitude-normalized using the maximum valueof the linear envelope observed during the recording session.Finally, EMG patterns for each condition were quantified bycomputing the average and standard deviation of the time- andamplitude-normalized signal envelopes.
Stimulus-triggered averaging was performed to assess the ef-fects of ESCS on baseline EMG activity. In this procedure, ex-tended recordings were made with the subject lying supine, in arelaxed, motionless state. Trials were alternately performed withand without ESCS, with a minimum inter-recording interval of1 min. When ESCS was applied, a proximal electrode pair wasused to record stimulation artifact and facilitate the construc-tion of 50-ms post-stimulus windows of EMG activity. ESCSwas delivered using a pulse duration of 800 s, at stimulationrates ranging from 10 to 60 Hz, and various amplitudes rangingup to and above the motor threshold.
Sense of Effort: The modified Borg scale was utilized toquantify the subject’s sense of effort or rating of perceivedexertion during training and gait evaluation sessions [33]. Thisscale was developed as a category scale with ratio properties; itis anchored using simple verbal expressions, and quantifies thesubjective sense of effort using a 0–10 rating scale.
III. RESULTS
An overview of the gait improvements resulting from PWBTis provided in Fig. 2 and Table II. Prior to training, unassistedpartial-support treadmill walking was characterized by a“crouched gait,” with the torso angulated forward and the hipsand knees remaining in flexion throughout the gait cycle [seeFig. 2(a)]. Correspondingly, there was a heavy reliance onthe LiteGate apparatus for vertical support. The subject alsohad difficulty with foot placement (i.e., scissoring frequently
(a)
(b)
Fig. 2. Sagittal plane joint kinematics for unassisted partial-supporttreadmill walking at 0.45 m/s (a) before and (b) after 12 weeks of PWBT.Solid curves denote the mean, while the dashed curves indicate themean� 1 standard deviation. Right and left limb kinematics are shown in grayand black, respectively. Gait kinematics improved significantly with PWBT.Specifically, torso angulation and hip extension were markedly improved whilethe percentage of the gait cycle occupied by double stance was reduced.
occurred). As a result, step lengths, step speeds, and maximumtreadmill speed were all limited.
There was progressive improvement in stepping pattern overthe initial 12 weeks of PWBT (see Fig. 3 and Table II). Bilat-erally, step lengths, cycle times, swing times, and stance timesall exhibited statistically significant increases. Similarly, kneeand hip range of motion increased, and there was significantimprovement in hip extension during terminal stance. Thesechanges were associated with a more upright torso posture[Fig. 2(b)] and significantly improved weight bearing duringpartial-support treadmill walking. These improvements allowedtreadmill training intensity to be increased; treadmill speed wasincreased up to 0.68 m/s while static partial weight supportlevels were reduced to less than 20% of body weight.
Despite these improvements in treadmill performance,walker-assisted over ground ambulation remained limitedby a heavy reliance on the walker for body weight support,
36 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 12, NO. 1, MARCH 2004
TABLE IICOMPARISON OF GAIT PERFORMANCE AT THE BEGINNING AND FOLLOWING
THREE MONTHS OF PWBT. DATA ARE FOR PARTIAL-SUPPORT TREADMILL
WALKING AT A SPEED OF 0.45 M/S, AND THE VALUES PRESENTED ARE THE
MEAN AND STANDARD DEVIATION ACROSS GAIT CYCLES. STATISTICAL
SIGNIFICANCE WAS ASSESSED USING THE MANN–WHITNEY U TEST
Fig. 3. PWBT-induced improvements in: (a) gait cycle timing; (b) step length;(c) hip flexion, extension, and range of motion; and (d) average torso angleduring the initial 12 weeks of training. Data presented are for partial-supporttreadmill walking at 0.45 m/s. Symbols denote the mean across a minimum of4 cycles, and error bars indicate the mean� 1 standard deviation.
slow speeds ( 0.1 m s ), poor endurance (i.e., maximumambulation distance of approximately 15 m), and marked senseof effort (8/10).
Training was interrupted for approximately five and a halfweeks for implantation of the ESCS system and post surgical re-covery. Approximately two weeks of training sessions were nec-essary to retrain the subject to presurgical performance levels.Subsequent evaluation of the ESCS parameters revealed thatstimulation intensity (V Hz s) was a critical parameter. Stim-ulation intensities below the sensory threshold did not generateobservable changes in treadmill or over ground walking per-
Fig. 4. Stimulus-triggered window of EMG activity recorded with theparticipant lying supine and motionless. A proximal electrode pair was used torecord stimulation artifact and facilitate the construction of 50-ms post-stimuluswindows of EMG activity. Individual traces (n = 200) are shown in gray,and the group mean and standard deviation are denoted by the black solid anddotted traces. Representative results are shown comparing the post-stimulussurface EMG activity: (a) with ESCS applied above the motor threshold(10 Hz, 800 �s, 4.7 V); (b) with ESCS applied at the midpoint between thesensory and motor thresholds (10 Hz, 800 �s, 4.0 V); and (c) without ESCS.To facilitate comparison, an equal duration recording made without ESCS wassubsectioned into 0.1-s intervals, overlaid, and averaged. The vertical scaledenotes the amplified signal amplitude in volts, which corresponds to a rawdifferential signal amplitude in millivolts (i.e., amplifier gain = 1000). Noticethat ESCS above the motor threshold induces short latency multiunit actionpotentials. Close scrutiny of the rectus femoris traces indicates several distinctpatterns of surface EMG were elicited by the stimulation, indicating severaldistinct patterns of motor unit recruitment. In contrast, submotor ESCS didnot produce significant stimulus related muscle activity at rest, and recordingsmade with submotor ESCS are similar in amplitude to those recorded in theabsence of stimulation.
formance. In contrast, stimulation intensities above the motorthreshold induced muscle contraction. Since the stimulation wasnonpatterned, tightness in stimulated muscles adversely alteredthe coordination of the stepping pattern. Thus, we settled on pa-rameter sets that fell between the sensory and motor thresholds,and adjusted stimulus amplitude to the midpoint between thesevalues. As illustrated in Fig. 4, the stimulus amplitudes appliedfor gait augmentation did not induce significant muscle contrac-tion at rest.
One of the best indicators for evaluating the effect of stimu-lation was the subject’s sense of effort, as the changes in kine-matics were subtle and gradual (see the following). The subjectenjoyed a reduced sense of effort and the ability to ambulate athigher speeds with the appropriate combination of stimulus pa-rameters. Among the three adjustable stimulation parameters asystematic evaluation revealed that pulse duration had the mostsubstantial effect on walking performance. For example, whenthe pulse duration was less than 500 s, the effect of stimulationon walking performance was not noticeable even when the stim-ulation amplitude was high (i.e., close to the motor threshold).Walking performance was also influenced by stimulation fre-quency, though less significant than the pulse duration, with
CARHART et al.: ESCS FACILITATES RECOVERY OF FUNCTIONAL WALKING 37
Fig. 5. Modification of EMG patterns with ESCS. Same-day comparison ofEMG activity with ESCS (black curves, n = 32 cycles) and without (graycurves, n = 54 cycles) collected during partial-support treadmill walkingat 0.9 m/s. Solid curves denote the mean, while the dotted curves depictthe mean + 1 standard deviation. Time normalization for each muscle wasperformed using the ipsilateral heel-strike-to-heel strike interval. Verticallines denote the mean centroid times for each condition. The application ofESCS resulted in statistically significant alterations in the centroid time foreach muscle (Mann–Whitney U-test, p < 0.001 for all muscles). Shown forcomparison (overbars) are periods of normal activity as reported by Shiavi[43] (striped) and Winter (black) [44]. Notice that patterns of activity withand without ESCS are bilaterally symmetric. In addition, the patterns of EMGactivity associated with ESCS are generally in better agreement with activitypatterns of the able-bodied.
low-frequency stimulation (20 Hz and lower) producing deterio-ration in performance, and high-frequency (100 Hz) stimulationproducing discomfort. In this subject, we found that a pulse du-ration of 800- s applied with stimulation frequencies of 40–60Hz produced the greatest improvements in performance.
Combining PWBT and ESCS, we observed substantial im-provement in treadmill gait performance. Notably, the subjectexhibited well-organized and smoother stepping patterns athigher treadmill rates (up to 0.9 m/s), and with greater self-sup-port of his body weight (e.g., 10 body weight support).This permitted training intensity to be further increased.
Same-day comparisons were utilized to evaluate the effectof ESCS on gait kinematics and EMG patterns during partial-support treadmill walking (0.9 m/s). Evaluation of the sagittalplane joint kinematics revealed only subtle differences in jointangle curves. Still, the ESCS condition was associated with astatistically significant increase in mean step length of 2.4 cm(Mann–Whitney U-test, ). In addition, the steppingmotions were more consistent as indicated by a lower variabilityin sagittal plane joint kinematics.
As shown in Fig. 5, ESCS had a more pronounced effecton EMG activity, producing statistically significant alterations
Fig. 6. Influence of ESCS on walker assisted over ground. (a) Ambulationspeed. (b) Sense of effort. ESCS was associated with improved speed andreduced sense of effort during short walks. Initially, ESCS doubled the overground speed while reducing the subject’s sense of effort by more than60%. With additional ESCS and NOESCS (ESCS off) conditions lessened.Statistically significant differences (Mann–Whitney U test, p < 0.05) at eachtraining interval are denoted by **. *1: Training was interrupted for five and ahalf weeks for implantation of the ESCS device and to allow surgical woundhealing and follow-up. Performance declined markedly during this period, andtraining was required to retrain the subject to preimplantation performancelevels. *2: At 90 sessions post-implantation, the subject reported a transientknee pain (unrelated to his participation in this study) and training wasdiscontinued for two and a half weeks. Subsequent training was also hamperedby a bladder infection.
in the timing of the EMG patterns toward that associated withnormal subjects. Across all channels monitored, activity was en-hanced during those periods when muscles are typically activein normal subjects, and reduced during periods of normal inac-tivity, i.e., a phase shift in muscle activation patterns occurreddue to the submotor, nonpatterned and continuous ESCS.
Analysis of over ground walking (Fig. 6) revealed that ESCSinitially had a dramatic effect on performance, doubling speedand reducing the subject’s sense of effort by more than six scales(from 8/10 to 2/10 on the Borg scale). ESCS also appears to havefacilitated learning of a functional over ground walking pattern,as speed improved both with and without the acute applica-tion of stimulation after continued, uninterrupted over groundtraining with ESCS. In addition, the differences in speed andsense of effort between the conditions decreased; however, ter-minal evaluations indicated that walking with ESCS was asso-ciated with a significantly higher speed and lower sense effort.The participant also enjoyed improved endurance with ESCS,particularly over longer distances (Fig. 7). After four months ofover ground training with ESCS, the subject demonstrated theability to ambulate more than 325 m. Moreover, over ground
38 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 12, NO. 1, MARCH 2004
Fig. 7. Over ground ambulation endurance with and without ESCS. In general,the subject was able to walk greater distances with ESCS. In a result similar tothat for walking speed, endurance improved for both the ESCS and NOESCSconditions over the post-implantation training period. However, the regressionlines suggest that the improvement in endurance with ESCS increased overthe training period. With ESCS and extended training, the subject was able toambulate in excess of 325 m.
Fig. 8. (a) Joint kinematics and (b) muscle activity during walker-assistedover ground ambulation with ESCS. Right- and left-limb joint angles arenormalized with respect to right heel strike for consistency with the stick figure.EMG data, on the other hand, are normalized with respect to the ipsilateralfoot-contact-to-foot-contact interval to permit comparison of side-to-sidesymmetry. Over ground ambulation with ESCS was characterized by bilaterallysymmetric patterns of joint angles and muscle activity. Although the subjectleaned forward over the walker for balance, full extension of the knee wasachieved during stance and reliance on the walker for body weight support wasmodest.
ambulation was characterized by consistent and bilaterally sym-metric patterns of joint kinematics and electromyographic ac-tivity (Fig. 8).
Reevaluation of lower extremity muscle strength at the cessa-tion of the study period did not reveal any discernable changes inisometric muscle strength. Despite the remarkable improvementin walking performance, lower extremity motor score remainedat 15/50. These observations are of considerable interest given
the ability of the subject to perform community and homeboundfunctional walking (see Herman et al. [34]).
IV. DISCUSSION
A. PWBT Improves Gait Pattern and Physical Condition
In normal gait, the step cycle is modulated by descendinginput and sensory information from various sensory organs inmuscles, joints, skin, and connective tissues [35], [36]. In part,this modulation is through pathways connecting dorsal to ven-tral circuits, driving locomotor rhythm and/or reflex activity.In individuals with severe, but incomplete spinal-cord lesions(ASIA C), descending input to locomotor circuits in the spinalcord is weak and almost always nonfunctional. The applica-tion of PWBT in this group reintroduces gait-related phasic af-ferent input to spinal-cord locomotor circuitry. Through repeti-tive training, spinal-cord circuits exhibit plastic changes [11] or“learn” [3], [12], [13], in a manner that is task specific and ren-ders them more sensitive to step cycle related sensory signals.
In agreement with other investigations involving PWBT [2],[4]–[6], [14], we found that our ASIA C subject enjoyed signif-icant improvement in his ability to generate coordinated step-ping movements with treadmill training. However, followingthree months of intensive training (up to two hours per dayand five days per week), his performance reached a steady statethat still required extensive body weight support. In addition,he was unable to perform treadmill walking at speeds greaterthan 0.68 m/s. Finally, over ground ambulation in this “low-level” ASIA C subject (i.e., muscle strength grades no greaterthan 2/5) was still hampered by slow speeds, near maximal ef-fort, and rapid exhaustion while traversing short distances. Thus,the appearance of a coordinated, rhythmic gait pattern inducedby PWBT remained nonfunctional as the attempt to transferthe learned movements to efficient and functional over groundwalking failed.
B. ESCS Enhances PWBT and Facilitates Functional OverGround Ambulation
When submotor ESCS was applied in conjunction withPWBT, the electrical current appeared to provide the mod-ulation/amplification of the neural circuits responsible forlocomotion rhythm generation. Evaluation of muscle activityduring treadmill walking revealed that ESCS produced bilateralalterations in the timing and distribution of activity in legmuscles. Although the associated changes in joint kinematicswere subtle, step execution was improved. Collectively, theseeffects were manifested as an ability to train on the treadmill atgreater intensities (0.9 m/s), with lower exertion, and for longerdurations. In this sense, it appears that ESCS facilitated PWBTand enhanced the training effects provided by this therapy.
With continued PWBT and ESCS, the participant was ableto transfer the learned coordinated movements into functionalover-ground ambulation. The application of ESCS significantlyimproved speed and reduced sense of effort during over-groundwalking. Correspondingly, the participant’s walking speed im-proved up to 0.35 m/s and his maximum endurance increased toa level that enabled sustained walking over a distance in excessof 325 m. Although the adopted speed is approximately 25%
CARHART et al.: ESCS FACILITATES RECOVERY OF FUNCTIONAL WALKING 39
of that exhibited by an able-bodied person, it is neverthelessa functional one as it enabled our subject to perform commu-nity and homebound ambulation using a walker [34]. Interest-ingly, improvements in speed and effort were also demonstratedwithout ESCS after months of continuous over ground trainingwith ESCS. However, performance levels remained higher whenstimulation was delivered during walking (Figs. 6 and 7)
The reduced sense of effort perceived by our subject whenusing ESCS is further supported by metabolic analysis con-ducted early in the transition from treadmill to over ground am-bulation (see Herman et al. [34]). Analysis of gas exchangedata indicated that ESCS reduced the energy cost of walkingin this subject by roughly 20% to 30%. Moreover, analysis ofCO production implied: 1) a large increase in fat oxidation withESCS and/or 2) less accumulation of blood lactate. Both find-ings imply that ESCS reduced dependence of exercising muscleon glycolysis, and hence, accounted for the marked improve-ment in muscle endurance observed in the ESCS condition. Weconclude that ESCS may elicit greater activation of oxidativemotor unit pools, thereby reducing the energetic cost of walking,reducing sense of effort, and expanding physical work capacity.
C. Neural Structures Recruited by ESCS
The underlying neural mechanisms for the effects of ESCSfor functional improvement observed in our investigation arenot clear, though several possible mechanisms have been sug-gested. Experiments conducted in supine subjects undergoingepidural stimulation for the control of pain [29] and spasticity[37] have demonstrated both sensory and motor effects ofESCS. Hunter and Ashby showed that the application ofESCS at amplitudes producing sensory paresthesias inducedvolleys of activity in sensory, motor, and mixed nerves in thelower extremity [29]. These observations were attributed toantidromic activation of cutaneous and muscle afferents nearthe stimulating cathode. By examining the effects of ESCS onsingle unit muscle activity during light volitional contractions,these investigators also demonstrated that ESCS facilitatesmotoneuron recruitment. Specifically, they found that ESCS atamplitudes typically used for pain control induced low-latencyand short duration increases in the probability of motor unitfiring. On the basis of latency, variability, and the duration ofthe period of increased firing probability, they concluded thatthe facilitation in motor output was not direct, but rather theresult of monosynaptic facilitation. Similar observations wererecently reported by Murg et al., who showed that low-fre-quency stimulation of the lumbosacral cord at amplitudes abovethe motor threshold (delivered using a single, widely spacedbipolar electrode) generated muscle twitches at fixed, shortlatencies compatible with the half-reflex time of the respectivemuscle [37].
Although similar motor effects were observed in these studies[37], [29], there is no consensus as to what neural structures arerecruited by ESCS, or at what location. Hunter and Ashby [29]attributed the sensory and motor effects of ESCS to recruitmentand antidromic activation of Ia afferents in the dorsal columns.Murg et al. [37], on the other hand, attributed their observa-tion of multiunit action potentials to the orthodromic recruit-ment of large-diameter primary afferents at the dorsal root entry
zone, and activation of motor neurons via segmental spinal re-flex pathways [37], [38]. Comparing motor response latenciesbetween these studies reveals a significant difference in latency(approximately 6–9 ms), a finding that suggests that differentneural recruitment patterns may indeed have been responsiblefor these independent findings.
While it is generally accepted that the therapeutic benefits ofESCS when used for pain control are due to a combination ofdorsal root and dorsal column recruitment [26], Rattay et al. [30]recently concluded that bipolar stimulation of the lumbosacralcord will not produce activation of dorsal column fibers for stim-ulus voltages within the clinical range (i.e., up to 10 V), in-stead generating dorsal root recruitment at threshold, followedby the ventral roots at higher stimulus amplitudes. Additionalcomputer modeling studies have demonstrated that dorsal rootfibers, under many conditions, may have a lower threshold thandorsal column fibers [26], [39], [40], [38], but these relation-ships are highly dependent upon the thickness of the dorsal cere-brospinal fluid layer, the local geometry of the spinal cord anddorsal root fibers with respect to the stimulation electrodes, theelectrode configuration, and stimulation parameters utilized.
Several investigators have reported nonpatterned, continuousstimulation of the dorsal spinal cord elicits locomotion-likeneurograms or EMG in transected cats and human subjects withcomplete SCI [18]–[20]. In humans, the appearance of phasicmuscle activity occurs in response to stimulus amplitudesabove those producing tonic muscle activity. In this investiga-tion involving an incomplete spinal-cord injured subject, wehave adopted an approach that utilizes stimulation amplitudesbetween the sensory and motor thresholds. Therefore, we didnot induce increased muscle contraction when the subjectwas at rest (Fig. 4). However, application of this submotorstimulation during locomotion produced significant alterationsin muscle activity toward desired patterns, improving walkingspeed and endurance, and reducing the subject’s sense of effort.In contrast, we found the application of stimulation above themotor threshold induced muscle twitches synchronized with thestimulation. Such high-intensity stimulation was detrimental toambulation training because of undesirable muscle tightness.
Another significant difference between the present study andprevious investigations of epidural stimulation in humans is thepulse duration used. Short duration pulses (e.g., 210 s) areoften used in pain control applications [41], and have been ap-plied to study the sensory and motor effects of ESCS in subjectslying supine [19], [29], [30], [37], [42]. In contrast, we foundthat: 1) short duration stimulation pulses (i.e., below 500 s) didnot provide a measurable improvement in ambulation and 2) pa-rameter sets using pulse durations of 800 s (but still submotor)offered the greatest acute improvements in locomotion. Interest-ingly, Iwahara et al. reported that similarly long pulse durations(500–1000 s) were optimal for eliciting stepping movements incats [18]. This requirement of a long pulse duration may be sig-nificant in our search for an understanding of the neural mech-anisms of ESCS for improved functional ambulation.
Among the three parameters determining the stimulation in-tensity (voltage, frequency, and pulse duration), pulse durationgenerated the most significant differences in performance. It isnoteworthy that such long duration stimulation pulses did not
40 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 12, NO. 1, MARCH 2004
produce significant motor activity at rest, yet altered patternsof EMG activity during walking. This is an interesting findinggiven the assertion put forth by Rattay et al. [31], i.e., that ESCSwill only recruit nerve fibers in the dorsal roots (and will recruitthe largest diameter fibers first). With this assumption, pulse du-rations in excess of a few hundred milliseconds should alter theeffects of ESCS very little, since chronaxie for large fibers inthe dorsal roots are substantially below 500 s. Our finding thatpulse durations of 800 s were required to generate the func-tional improvement suggests that the ESCS applied in this in-vestigation recruited much less excitable neural structures in thedorsal roots and/or dorsal spinal cord.
V. CONCLUSION
The quantitative results presented in this study demonstratethat ESCS can facilitate locomotor recovery in individuals withchronic ISCI. Additional, controlled studies of this approach ingroups of individuals with ISCI are needed to confirm the pos-itive effects of ESCS documented in this participant. In addi-tion, further investigation is required to understand the neuralmechanism(s) by which ESCS facilitated the effects of PWBTfor the recovery of functional ambulation. Electrophysiologicalparameters, such as reflex latency and sensitivity, conductionvelocity in corticospinal pathways, and EMG amplitude andmuscle force under isometric conditions, etc., need to be mea-sured and evaluated. Another important question is when andhow to apply the coordinated ESCS and PWBT to achieve thebest effect. In this investigation, we applied ESCS after monthsof PWBT training, in an effort to distinguish any further im-provement induced by ESCS. In real clinical application of thistherapy, this delay may not be necessary. It is intriguing to thinkthat early application of coordinated ESCS and PWBT may helpto elicit the necessary performance improvement for functionalambulation in a much shorter training period.
In our view, the patient’s “sensation of lightness” associatedwith a “low sense of effort” [22] was a significant feature in thedifference between the stimulation and nonstimulation condi-tions. Initially, the application of ESCS in this volunteer enabledhim to train at higher intensities and progress significantly be-yond the performance levels obtained with PWBT alone. In thissense, it appears that ESCS augmented the use-dependent plas-ticity created by PWBT. The application of ESCS also producedacute changes in EMG activity and improvements gait perfor-mance, even after extensive treadmill and over ground training.This was manifested as an ability to walk farther, faster, and witha lower sense of effort with the assistance of ESCS.
ACKNOWLEDGMENT
The authors recognize the assistance of the physical therapystaff at BGSMC, Q. Wang, G. Yamaguchi, and J. Sweeney tothis project. They also would like to thank A. Seif-Naraghi forhis valuable insight; Medtronic for contributing the stimulationdevice; J. Porter, M.D., for his clinical care of the patient and D.Herbert, M.D., for his surgical skills during implantation; Dr.G. Loeb and Dr. V. Dietz for their insights in our discussionof the project; and the anonymous reviewers for their valuablesuggestions to improve the manuscript.
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Michael R. Carhart (M’93) was born in LaCrosse,WI, in 1969. He received the B.S. degree in biomed-ical engineering from the Milwaukee School of En-gineering, Milwaukee, WI, in 1991 and the Ph.D. de-gree in bioengineering from Arizona State University(ASU), Tempe, in 2000.
He was an Assistant Research Scientist withthe Harrington Department of Bioengineering,ASU, from 2000 to 2003 and served as Presidentof Forensic Dynamics, LLC. He is currently aManaging Engineer with Exponent Failure Analysis
Associates, Phoenix, AZ, and an Adjunct Professor of Bioengineering at ASU.His research interests include the biomechanics of normal and pathologicalposture and gait; the development and use of dynamic models of the humanbody for the analysis of movement, internal forces, and injuries; and rehabilita-tion engineering approaches to the recovery of standing and walking followingSCI.
Dr. Carhart is member of the International Society of Biomechanics, the So-ciety of Automotive Engineers, Tau Beta Pi, Eta Kappa Nu, and Phi Kappa Phi.
Jiping He (S’86–M’89–SM’97) was born inShanghai, China. He received the B.S. degree incontrol engineering from Huazhong University ofScience and Technology, Wuhan, China, in 1982 andthe M.S. and Ph.D. degrees in electrical engineeringfrom University of Maryland, College Park, in 1984and 1988, respectively.
He then spent one and a half years as a Post-doctoral Fellow with the Center for BiologicalInformation Processing, Massachusetts Instituteof Technology, Cambridge. In 1990, he joined
the Functional Neurosurgery Division, Thomas Jefferson University (TJU),Philadelphia, PA, as a Research Assistant Professor and Adjunct Professor ofPhysical Therapy. He was a Visiting Scientist with the Human InformationProcessing Program, Princeton University, Princeton, NJ, during 1991 and1992. He joined Arizona State University (ASU), Tempe, as an AssociateProfessor in 1994 and is now a Professor of Bioengineering with the Director ofCenter for Neural Interfaces and Control, ASU. He is also actively involved inthe curriculum development of bio-control and neural engineering. His researchand teaching interests include the application of advanced control theory tothe analysis and control of neuromuscular systems for posture and movement,implantable neural interface technology, cortical and spinal cord recording andstimulation for sensorimotor adaptation and control, application of robotics,and virtual reality research to neuromotor rehabilitation and prosthetic devices.
Richard Herman was born in Brooklyn, NY. He re-ceived the B.S. degree in physical chemistry fromWestern Reserve University, Cleveland, OH, in 1948,a Certificate in Physical Therapy from the School ofEducation, New York University, New York, in 1951,and the Bachelor of Medicine degree in obstetrics andsurgery from Queens University, Belfast, N. Ireland,in 1959.
His internship was carried out at the Kings CountyHospital, Brooklyn, NY, from 1959 to 1960 and hisresidency in rehabilitation medicine was conducted
at the Bronx Municipal Hospital, Albert Einstein College of Medicine, Bronx,NY, from 1960 to 1963. He was awarded a postdoctoral Vocational Rehabilita-tion Administration Fellowship to support research on motor control and clin-ical activities in rehabilitation medicine from 1963 to 1965. From 1965 to 1969,he was an Assistant Professor of Rehabilitation Medicine at the Albert EinsteinCollege of Medicine. In 1969, he became a Professor with the Department ofRehabilitation Medicine, Temple University, Philadelphia, PA, and Director ofthe Krusen Center for Research and Engineering, Moss Rehabilitation Hospital,Philadelphia. In 1971, he became the Professor and Chairman of the Depart-ment of Rehabilitation Medicine, Temple University, and an Adjunct Professorof Biomedical Engineering at Drexel University, Philadelphia. In 1982, he be-came the Director of the Rehabilitation Medicine Unit, Catholic Medical Center,Manchester, NH and Research Professor of Surgery (neurosurgery) at the Dart-mouth Medical School, Hanover, NH. In 1987, he joined the Samaritan Rehabil-itation Institute, Phoenix, AZ, as its Medical Director and assumed the Director-ship of the Clinical Neurobiology and Bioengineering Research Laboratories.He currently maintains the Director position and is also Research Professor inthe Departments of Bioengineering and Kinesiology, Arizona State University,Tempe, and in the Department of Pharmacology, Health Sciences Center, Uni-versity of Arizona, Tuscon. He has also established laboratories dedicated toneural control of the microcirculation with emphasis on the role of small pri-mary sensory neurons in certain populations of obese and pre- and post-dia-betic subjects. His research interests include developing tools to better under-stand movement control, and testing contemporary as well as novel therapeuticinterventions for CNS-related dysfunctions. Currently, he is developing a physi-ological and functional models with emphasis on the interaction between neuraland metabolic (bioenergetics) systems.
Dr. Herman is a member of the Society of Neuroscience, American Phys-iology Society, American Academy of Physical Medicine and Rehabilitation,and the Association of Academic Physiatrists.
42 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 12, NO. 1, MARCH 2004
S. D’Luzansky was born in Cleveland, OH. Hereceived the B.S. degree in biomedical engineeringfrom Arizona State University (ASU), Tempe, in1987.
In 1987, while taking graduate classes at ASU,he was Vice President of DLY Inc., a technical con-sulting group in both Cambridge, MA, and Phoenix,AZ. He was a Consultant to Dr. R. Herman’sClinical Neurobiology and Bioengineering ResearchLaboratory, Banner Good Samaritan RehabilitationInstitute, Phoenix, AZ. He provided clinical diag-
nostic and scientific support for neurodegenerative disease patients and spinalcord injury populations. He joined Banner Good Samaritan RehabilitationInstitute as Research Associate and Clinical Research Coordinator for theClinical Neurobiology and Bioengineering Research Laboratory in 1990.He is currently a Senior Bioengineer at Banner Good Samaritan MedicalCenter in the Clinical Neurobiology and Bioengineering Research Laboratory.He has maintained a close relationship with the Harrington Department ofBioengineering, ASU, and he has facilitated the clinical internships for manygraduate and undergraduate students over 14 years. He is currently serving aspresident of the Industrial Advisory Board for ASU’s Bioengineering Program.His research interests include pathoneurophysiology, neuropharmacology, andapplications of central and peripheral electrical stimulation for recovery offunction.
Mr. D’Luzansky is a member of the Biomedical Engineering Society, Societyfor Neuroscience, and the Clinical Research Professional Society.
Wayne T. Willis received the Ph.D. degree in ex-ercise physiology from the University of California,Berkeley, in 1986.
For three years, he was a Postdoctoral Researcherwith the Department of Pediatrics, University of Cal-ifornia Medical Center, San Francisco. Since 1989,he has been a Faculty Member of the KinesiologyDepartment, Arizona State University, Tempe. Hisresearch interests include the cost-benefit tradeoffin mitochondrial design, particularly as it pertainsto the control of oxidative phosphorylation in
vertebrate skeletal muscle fast and slow myocytes. His recent collaborations areaimed at elucidating the neuromuscular basis, and in particular the contributionof skeletal muscle energy metabolism, to recently observed improvements inlocomotion in spinal cord injured individuals subjected to newly developedinterventions.
Dr. Willis is a Fellow of the American College of Sports Medicine.