Novel Patterns of Functional Electrical Stimulation Have an Immediate Effect on Dorsiflexor Muscle Function During Gait for People

Poststroke Trisha M. Kesar, Ramu Perumal, Angela Jancosko, Darcy S. Reisman, Katherine S. Rudolph, Jill S. Higginson and Stuart A. Binder-Macleod PHYS THER. 2010; 90:55-66. Originally published online November 19, 2009 doi: 10.2522/ptj.20090140

The online version of this article, along with updated information and services, can be found online at: [Link] Collections This article, along with others on similar topics, appears in the following collection(s): Electrotherapy Gait Disorders Injuries and Conditions: Ankle Injuries and Conditions: Foot Kinesiology/Biomechanics Stroke (Geriatrics) Stroke (Neurology) To submit an e-Letter on this article, click here or click on "Submit a response" in the right-hand menu under "Responses" in the online version of this article. Sign up here to receive free e-mail alerts

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Research Report
Novel Patterns of Functional Electrical Stimulation Have an Immediate Effect on Dorsiexor Muscle Function During Gait for People Poststroke
Trisha M. Kesar, Ramu Perumal, Angela Jancosko, Darcy S. Reisman, Katherine S. Rudolph, Jill S. Higginson, Stuart A. Binder-Macleod

Background. Foot drop is a common gait impairment after stroke. Functional electrical stimulation (FES) of the ankle dorsiexor muscles during the swing phase of gait can help correct foot drop. Compared with constant-frequency trains (CFTs), which typically are used during FES, novel stimulation patterns called variablefrequency trains (VFTs) have been shown to enhance isometric and nonisometric muscle performance. However, VFTs have never been used for FES during gait. Objective. The purpose of this study was to compare knee and ankle kinematics
during the swing phase of gait when FES was delivered to the ankle dorsiexor muscles using VFTs versus CFTs.

T.M. Kesar, PT, PhD, is PostDoctoral Researcher, Department of Physical Therapy, University of Delaware, Newark, Delaware. She was a doctoral student in the Biomechanics and Movement Science Program, University of Delaware, during the completion of this study. R. Perumal, PhD, is Research Scientist, Department of Physical Therapy, University of Delaware. A. Jancosko, PT, NCS, is Physical Therapist, Magee Rehabilitation Hospital, Philadelphia, Pennsylvania. D.S. Reisman, PT, PhD, is Assistant Professor, Department of Physical Therapy, University of Delaware. K.S. Rudolph, PT, PhD, is Associate Professor, Department of Physical Therapy, University of Delaware. J.S. Higginson, PhD, is Assistant Professor, Department of Mechanical Engineering, University of Delaware. S.A. Binder-Macleod, PT, PhD, FAPTA, is Edward L. Ratledge Professor and Chair, Department of Physical Therapy, University of Delaware, Newark, DE 19716 (USA). Address all correspondence to Dr Binder-Macleod at: sbinder@[Link]. [Kesar KM, Perumal R, Jancosko A, et al. Novel patterns of functional electrical stimulation have an immediate effect on dorsiexor muscle function during gait for people poststroke. Phys Ther. 2010; 90:55 66.] 2010 American Physical Therapy Association

Design. A repeated-measures design was used in this study. Participants. Thirteen individuals with hemiparesis following stroke (9 men, 4
women; age 46 72 years) participated in the study.

Methods. Participants completed 20- to 40-second bouts of walking at their

self-selected walking speeds. Three walking conditions were compared: walking without FES, walking with dorsiexor muscle FES using CFTs, and walking with dorsiexor FES using VFTs.

Results. Functional electrical stimulation using both CFTs and VFTs improved
ankle dorsiexion angles during the swing phase of gait compared with walking without FES (X SE 2.9 1.2). Greater ankle dorsiexion in the swing phase was generated during walking with FES using VFTs (X SE 2.1 1.5) versus CFTs (X SE 0.3 1.3). Surprisingly, dorsiexor FES resulted in reduced knee exion during the swing phase and reduced ankle plantar exion at toe-off.

Conclusions. The ndings suggest that novel FES systems capable of delivering
VFTs during gait can produce enhanced correction of foot drop compared with traditional FES systems that deliver CFTs. The results also suggest that the timing of delivery of FES during gait is critical and merits further investigation.

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Effects of Dorsiexor Muscle Functional Electrical Stimulation on Poststroke Gait

troke is a leading cause of longterm adult disability.1 Regaining walking function is one of the primary concerns for individuals who experience stroke.2 Even after rehabilitation, residual gait decits are prevalent in individuals with stroke.2 Foot drop is a common poststroke gait impairment estimated to affect 20% of survivors of stroke.3 Foot drop is caused by total or partial paresis of ankle dorsiexor muscles,4 makes ground clearance difcult during swing, and can lead to inefcient gait compensations such as circumduction and hip hiking (increased hip abduction in the unaffected limb during stance, with simultaneous elevation of the affected side of the pelvis during swing).5,6 Residual gait decits such as foot drop contribute to increased energy expenditure during gait, decreased endurance, and an increased incidence of falls.2,5 8 Ankle-foot orthoses (AFOs) are widely prescribed for the management of foot drop.9,10 Functional electrical stimulation (FES) is another intervention that is used to deliver electrical stimulation to the ankle dorsiexor muscles during the swing phase of gait to correct foot drop.1114 In contrast to AFOs, FES promotes active muscle contractions, can help improve muscle strength (force-generating capacity),1518 prevents disuse atrophy,19 21 reduces muscle tone (velocitydependent resistance to stretch) and spasms,22 produces a more energyefcient use of proximal limb muscles,23 and aids in motor relearning.24

Figure 1.
(A) Example of the ankle angle, footswitch, and vertical ground reaction force (GRF) data from the paretic lower extremity of one representative participant. Data shown are for one complete gait cycle (ie, rst initial contact [IC] to toe-off [TO] to second IC for the same leg, as determined using the vertical GRFs). Initial contact and toe-off, as determined by the footswitches, are depicted by FSwIC and FSwTO. Dorsiexor stimulation was delivered during the swing phase of the paretic limb (ie, from FSwTO to FswIC). (B) A schematic depicting the 2 types of stimulation train patterns used for functional electrical stimulation in this study: constant-frequency trains (CFTs) and variable-frequency trains (VFTs). The CFTs consisted of single pulses (300-microsecond pulse duration) separated by 33-millisecond interpulse intervals. The VFTs consisted of a 200-Hz high-frequency burst at the start of a CFT with 33-millisecond interpulse intervals.

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Audio Abstracts Podcast This article was published ahead of print on November 19, 2009, at [Link].

Functional electrical stimulation also has been shown to reduce the energy cost of walking poststroke.17 Although FES offers many advantages compared with AFOs, it has been well documented that stimulation parameters traditionally used during FES can contribute to limitations such as imprecise control of

force and rapid muscle fatigue and prevent FES from gaining widespread clinical application.2530 Stimulation frequency (number of pulses per second) and intensity (amplitude or duration of individual pulses) are the 2 primary parameters that are modulated to control movements during FES. The stimulation pattern, or the arrangement of pulses within
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Effects of Dorsiexor Muscle Functional Electrical Stimulation on Poststroke Gait a stimulation train, is another parameter that can be varied during FES27,31 (Fig. 1). However, typically, FES applications use only one type of stimulation pattern: stimulation trains consisting of stimulation pulses separated by constant interpulse intervals (constant-frequency trains [CFTs]).32,33 Our laboratory27,28,31,34 and others3537 have shown that novel stimulation patterns known as variable-frequency trains (VFTs) have several advantages compared with traditional CFTs.31 Variable-frequency trains can take advantage of the catchlike property of human muscles.38 The catchlike property of skeletal muscle, rst discovered in 1970 in mammalian motor units, is the force augmentation produced when an initial, brief, highfrequency burst of 2 to 4 pulses is included at the onset of a subtetanic low-frequency stimulation train.31,38 Variable-frequency trains have been shown to enhance isometric31,34 and nonisometric39 41 muscle performance in healthy human quadriceps femoris muscles compared with CFTs of similar frequency, especially when muscles are fatigued. Variablefrequency trains also have been shown to produce greater knee joint excursions using fewer pulses than CFTs in healthy human quadriceps femoris muscles.41 In addition to providing enhanced skeletal muscle performance, VFTs are a more physiologically based stimulation pattern compared with CFTs.42 Highfrequency doublets and triplets, such as those included at the onset of VFTs, have been reported to occur during animal and human muscle contractions.38,42 Interestingly, no previous study has systematically compared the effects of delivering VFTs versus CFTs during FES to correct foot drop in individuals poststroke. Global measures of walking performance, such as walking speed and
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physiological cost, typically are used as outcome measures in FES studies.3,13,43 45 Although important to justify inclusion of FES in rehabilitation protocols, such measures do not provide a detailed biomechanical understanding of how specic aspects of gait are modied during walking with FES. There is a dearth of data in the literature about the immediate effects of FES on gait kinematics, kinetics, and gait compensations.4,46 We posit that using instrumented gait analysis to study the immediate effects of FES on poststroke gait patterns can help develop better FES strategies to maximize the immediate (orthotic) effects of FES, which can enable the design of better neuroprostheses and potentially help to increase therapeutic benets to patients. Thus, the purpose of this study was to compare the immediate effects of dorsiexor FES using CFTs versus VFTs on gait kinematics in individuals who display gait impairments as a result of stroke.

sure outside of the range of 90/60 to 170/90 mm Hg, substantial cognitive decits (Mini-Mental State Exam score 22), inability to communicate with the investigators (severe aphasia), orthopedic conditions or pain in lower limbs or spine, cerebellar involvement (eg, ataxic hemiparesis), neglect (as assessed with the Star Cancellation Test), hemianopia, and absence of sensation on the skin of the calf or leg of the paretic limb. Participants completed an initial clinical evaluation conducted by a licensed physical therapist comprising clinical tests for characterizing decits following a stroke, including the lower-extremity portion of the Fugl-Meyer Assessment of Motor Recovery47 (Table). Each participants self-selected overground walking speeds was determined using the 6-meter walk test. All subjects signed informed consent forms approved by the Human Subjects Review Board of the University of Delaware. Design Overview Electrical stimulation. Surface electrical stimulation electrodes (5.08 5.08 cm [2 2 in])* were attached to the ankle dorsiexor muscles. A Grass S8800 stimulator in combination with a Grass Model SIU8TB stimulus isolation unit was used to deliver electrical stimulation. With participants seated and the foot hanging freely in a plantar-exed position, the stimulation amplitude was set by gradually increasing the amplitude of a 300-millisecond-long, 30-Hz train with a pulse duration of 300 microseconds until a neutral ankle joint position (0), or at least to 5 degrees of plantar exion in participants with decits of range of motion, was achieved. Electrode placement was adjusted to minimize ankle

Method
Setting and Participants Thirteen individuals (9 men, 4 women; age 46 72 years) with poststroke hemiparesis participated in this study (Table). All participants had experienced a stroke involving cerebral cortical regions more than 6 months previously, were able to walk continuously for 5 minutes at their self-selected speed, and had sufcient passive ankle dorsiexion range of motion to enable their paretic ankle joint to reach at least 5 degrees of plantar exion with the knee exed. Exclusion criteria included evidence of moderate to severe chronic white matter disease on magnetic resonance imaging, more than one previous stroke, congestive heart failure, peripheral artery disease with claudication, uncontrolled diabetes, shortness of breath without exertion, unstable angina, resting heart rate outside of the range of 40 to 100 bpm, resting blood pres-

* TENS Products Inc, PO Box 2089, Grand Lake, CO 80447. Grass Technologies, Div of Astro-Med Inc, 600 E Greenwich Ave, Warwick, RI 02893.

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Effects of Dorsiexor Muscle Functional Electrical Stimulation on Poststroke Gait Table.

Participant Demographic and Clinical Informationa
Participant No. 1 2 3 4 5 6 7 8 9 10 11 12 13 Average SD
a

Sex M M F F M M M M M M M F F

Age (y) 66 52 58 51 49 72 57 58 60 74 56 46 66 58.8 8.6

Time Since Stroke (y) 2.4 6.3 21.3 1.9 9.3 6.1 2.7 9.9 5.8 4.7 9.8 2.2 1.4 6.4 5.4

Side of Hemiparesis L L L L R R R R R R R L R

Gait Speed (m/s) 0.9 0.6 0.2 0.3 0.9 0.5 0.7 0.7 0.8 0.7 1.2 0.9 0.3 0.7 0.3

Fugl-Meyer Score (Maximum Score 34) 24 20 23 20 28 18 22 21 25 31 25 23 18 23 3.8

Data for participant 13 were not included in the results due to technical problems during data collection. M male, F female, L left, R right.

eversion and dorsiexion.

inversion

during

Two compression-closing footswitches (25-mm diameter MA-153) attached bilaterally to the soles of each shoe, one on the forefoot under the fth metatarsal head and the other on the hindfoot under the lateral portion of the heel, were used to control the timing of FES during gait. Timing of FES during gait. A customized, real-time FES system (CompactRIO) consisting of a real-time controller (NI cRIO-9004), analog input module (NI 9210), and digital input/output module (NI9401) was used to deliver stimulation during gait.48 The FES system delivered FES to the paretic ankle dorsiexor muscles during the swing phase of each gait cycle, as detected by the footswitches (ie, from the time when the forefoot footswitch was off the
Motion Lab Systems Inc, 15045 Old Hammond Hwy, Baton Rouge, LA 70816. National Instruments Inc, 11500 N Mopac Expwy, Austin, TX 78759.

ground to the time when the hindfoot footswitch contacted the ground) (Fig. 1). For FES using CFTs, a 30-Hz constant-frequency train was delivered. For FES using VFTs, a highfrequency (200-Hz) 3-pulse burst was delivered followed by a lowerfrequency (30-Hz) CFT (Fig. 1B). All stimulation parameters for the VFTs and CFTs were identical except that the 200-Hz 3-pulse burst was included at the onset of the VFTs. Marker placement. Retroreective markers (14-mm diameter) placed bilaterally over the iliac crests, greater trochanters, lateral and medial femoral condyles, lateral and medial malleoli, and fth metatarsal heads were used to dene the joint centers of the lower limb. Elastic bands (SuperWrap) were tightly wrapped around the bilateral thigh and shank segments. Four-marker clusters attached to rigid thermoplastic shells were afxed to the elastic
Fabrifoam, 900 Springdale Dr, Exton, PA 19341.

wraps and used to track the bilateral thigh and shank segments. A 3-marker cluster on the sacrum and 3 additional markers on the shoe were used to track pelvis and foot movements, respectively. Gait analysis. During gait analysis, participants walked on a split-belt treadmill# instrumented with two 6-degree-of-freedom force platforms. Participants held on to a handrail during walking. All participants wore a harness that was attached to an overhead support for safety. No body weight was supported by the harness. Marker data were collected using an 8-camera motion analysis system (Vicon 5.2).** Video data were sampled at 100 Hz, and analog data (force platforms, footswitches, and stimulation channel) were sampled at 2,000 Hz.

# Advanced Mechanical Technology Inc, 176 Waltham St, Watertown, MA 02472-4800. ** Vicon, 14 Minus Business Park, West Way, Oxford, United Kingdom OX2 OJB.

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Effects of Dorsiexor Muscle Functional Electrical Stimulation on Poststroke Gait The data presented are a subset of the data collected during one testing session. The complete testing session comprised 18 trials, and each trial was 20 to 40 seconds in duration. Rest intervals of 5 to 10 minutes were provided between consecutive trials (Fig. 2). In this article, we report data for 3 walking trials or conditions: (1) walking without FES (noFES), (2) walking with dorsiexor muscle FES using CFTs (FES-CFT), and (3) walking with dorsiexor muscle FES using VFTs (FES-VFT). The noFES data presented in this article were collected during the beginning (1st trial), middle (8th trial), and end (17th trial) of the session (Fig. 2). Data for different types of walking trials with FES of the ankle muscles at 2 different gait speeds were collected either during the 2nd through 7th walking trials (rst block) or the 9th through 15th walking trials (second block) (Fig. 2). Within any one trial, the gait speed and the stimulation condition were kept constant. The 2 FES conditions presented in this study (ie, FES-CFT and FES-VFT) were randomly distributed across the rst and second blocks within the testing session. All 3 walking conditions presented in this study were tested at the participants self-selected overground walking speed, determined during a separate clinical testing session. Data Processing Marker trajectories and ground reaction force data were low-pass ltered (Butterworth fourth-order, phase lag) at 6 and 30 Hz, respectively, using commercial software (Visual 3D). Lower-limb kinematics were calculated using rigid-body analysis and Euler angles using Visual 3D software. Vertical GRFs were used to identify initial contact and toe-off for the gait data, using a force threshold

Figure 2.
Schematic showing the walking trials conducted as part of the experimental protocol. Each trial comprised 20 to 40 seconds of treadmill walking with a 5- to 10-minute rest provided between consecutive trials. The data for walking without functional electrical stimulation (noFES) used to compare with the data for walking with dorsiexor muscle functional electrical stimulation using constant-frequency trains (FES-CFT) and walking with dorsiexor muscle functional electrical stimulation using variable-frequency trains (FES-VFT) were obtained by averaging the noFES data obtained from the walking trials at the beginning, middle, and end of the session.

of 20 N. Strides were time normalized to 100% of the gait cycle and averaged across trials for each participant and walking condition. The noFES data were obtained by averaging the 3 noFES trials from the beginning, middle, and end of the session. For each of the 3 walking conditions, all outcome variables were computed using Visual 3D software for each stride and averaged across strides using a custom-written program. Outcome Variables The 2 primary outcome measures for the effectiveness of FES during gait were peak ankle dorsiexion angle during swing and ankle dorsiexion angle at initial contact. Three secondary outcome measures were computed: peak exion of the paretic knee during the swing phase, circumduction, and dorsiexion angle of the paretic ankle at toe-off. Circumduction refers to a compensatory strategy during the swing phase that involves hip abduction and lateral (external) rotation and often is accompanied by pelvic hiking on the paretic side during the swing

phase. Circumduction was dened as the maximum distance between the heel marker position during stance and the greatest lateral position of the heel marker during the subsequent swing phase.49,50 Based on an exploratory analysis of the data, we included ankle dorsiexion angle at toe-off as a secondary outcome variable to capture the interesting and surprising decrease in ankle plantar-exion angle observed at the stance-to-swing transition. Data Analysis One-way analyses of variance (ANOVAs) for repeated measures were performed for each dependent variable to test for overall differences across the 3 walking conditions tested (noFES, FES-CFT, and FESVFT). Post hoc pair-wise comparisons were performed to detect differences between noFES versus FESCFT, noFES versus FES-VFT, and FESCFT versus FES-VFT conditions. Based on our directional hypotheses, we planned to perform one-tailed paired t tests for ankle angle during swing and ankle angle at initial contact. Two-tailed paired t tests were
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C-Motion Inc, 15819 Crabbs Branch Way #A, Rockville, MD 20855.

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Effects of Dorsiexor Muscle Functional Electrical Stimulation on Poststroke Gait W911NF-05-1-0097. Part of the funding came from the University of Delaware Dissertation Fellowship awarded to Dr Kesar.

Results
Of the 13 participants tested in this study, one participants data (participant 13) were excluded from the analyses due to technical problems encountered during the testing session. Results are presented for the remaining 12 participants (Table). For each condition, data for each outcome variable represent the mean of the rst 6 consecutive gait cycles for which accurate forceplate data could be analyzed. A qualitative analysis of stride-bystride data showed that FES using VFTs consistently produced greater ankle dorsiexion during swing and at initial contact compared with FES using CFTs and that FES using CFTs produced greater ankle angles compared with noFES for each of the 6 gait strides included in the analyses (Fig. 3). The ensemble gait data for the 12 participants sagittal-plane ankle angles throughout the gait cycle showed that FES-CFT and FES-VFT shifted the ankle angle toward greater dorsiexion during swing, at initial contact, and at toe-off (Fig. 4A). The descriptive statistics presented in the text are means standard errors. Primary Outcome Variables Peak ankle angle during swing. Without FES, participants walked with their paretic ankle joints in a slightly plantar-exed position (ankle angle 2.9 1.2) during swing (Figs. 4A and 5A). The repeated-measures ANOVA detected signicant differences in swing phase ankle angles among the 3 walking conditions tested (F 14.73, P .01). Dorsiexor FES using either CFTs or VFTs produced signicant improvements in ankle dorsiexion during swing compared with noFES
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Figure 3.
Average (n 12) stride-by-stride values of the 2 primary outcome variables: (A) peak swing phase ankle angle and (B) ankle angle at initial contact for the 3 walking conditions tested (walking without functional electrical stimulation [noFES], walking with dorsiexor muscle functional electrical stimulation using constant-frequency trains [FES-CFT], and walking with dorsiexor muscle functional electrical stimulation using variable-frequency trains [FES-VFT]). Data shown are for the rst 6 consecutive strides. Positive standard error bars are shown. Positive angles represent dorsiexion. IC initial contact.

planned for circumduction, peak swing phase knee exion, and ankle angles at toe-off. In addition, we compared the peak ankle angles during swing and ankle angle at initial contact measured during the noFES walking condition at the beginning, middle, and end of the session using a one-way ANOVA for repeated measures to assess the presence of either muscle fatigue or potentiation. A decrease in ankle dorsiexion angles during swing or initial contact would signify the presence of fatigue within the testing session. A post hoc 2-tailed pair-wise comparison was performed to check for differences between noFES data at the beginning versus the end of
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the session. The alpha level was set at .05. The Shapiro-Wilk test was used to test for normal distribution of data for each of the outcome variables. All statistical analyses were performed using SPSS version 16.0. Role of the Funding Source This study was supported by National Institute of Nursing Research grant RO1 NR010786 awarded to Dr Binder-Macleod. This funding source did not bias the outcome of this investigation. Funding for the laboratory instrumentation was provided by NIH Shared Instrumentation grant S10 RR022396-01 and DOD grant

SPSS Inc, 233 S Wacker Dr, Chicago, IL 60606.

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Effects of Dorsiexor Muscle Functional Electrical Stimulation on Poststroke Gait (both P .01). Functional electrical stimulation using CFTs brought the paretic ankle joint to an approximately neutral position during swing (0.3 1.3), and FES using VFTs produced signicantly greater ankle dorsiexion (2.1 1.5) compared with FES using CFTs (P .05). The peak swing phase ankle angles for the nonparetic extremities were 5.2 2.0 degrees. Ankle angle at initial contact. Overall, there were differences in ankle angle at initial contact among the 3 walking conditions tested (F 16.92, P .01) (Figs. 4A and 5B). Our participants were in a markedly plantar-exed position at initial contact ( 8.5 1.6) when walking without FES. Functional electrical stimulation using either CFTs ( 3 1.4) or VFTs ( 1 1.7) signicantly reduced the amount of ankle plantar exion at initial contact compared with walking without FES (both P .01). The post hoc pair-wise comparison detected a trend toward signicantly improved dorsiexion using VFTs versus CFTs (P .07). The ankle angles at initial contact for the nonparetic extremities were 2.8 2.2 degrees. Secondary Outcome Variables Although FES was delivered only to the muscles crossing the paretic ankle joint, there were signicant differences in the peak knee exion attained by the paretic leg during the swing phase among the 3 walking conditions (F 13.9, P .01) (Figs. 4B and 6). Two-tailed pair-wise comparisons showed that participants demonstrated signicantly reduced knee exion during walking with FES using CFTs (42.6 4.3) or VFTs (40.8 4.2) compared with walking without FES (44.1 4.2) (both P .05) (Fig. 6A). In addition, FES using VFTs produced a greater decrease in knee exion compared with FES using CFTs (P .05). The peak swing phase knee exion anJanuary 2010

Figure 4.
Ensemble plots showing the average time normalized (0% to 100% initial contact to initial contact) ankle (A) and knee (B) angles for 12 participants. Ankle dorsiexion and knee exion are positive. The 3 lines in each graph denote the 3 walking conditions tested: walking without functional electrical stimulation (noFES), walking with dorsiexor muscle functional electrical stimulation using constant-frequency trains (FESCFT), and walking with dorsiexor muscle functional electrical stimulation using variable-frequency trains (FES-VFT). Vertical dashed line represents toe-off.

gles for the nonparetic extremity were 68.3 2.0 degrees. Participants demonstrated no differences in the amount of circumduction among the 3 walking conditions (F 0.473, P .63). Average circumduction was 4.0 0.8 cm for noFES, 3.8 0.8 cm for FES-CFT, and 3.7 0.7 cm for FES-VFT. The circumduction values for the nonparetic extremities were 1.62 0.39 cm.

There were signicant differences in the position of the paretic ankle angle at the stance-to-swing transition (F 16.92, P .01) among the 3 walking conditions (Fig. 6B). The position of the paretic ankle angle at toeoff changed from a more plantarexed position during walking without FES ( 9.1 1.2) to signicantly less plantar exion during walking with FES using CFTs ( 5.2 1.2; P .01) or VFTs

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Effects of Dorsiexor Muscle Functional Electrical Stimulation on Poststroke Gait CFTs. Surprisingly, we also found that dorsiexor FES decreased ankle plantar exion at toe-off and decreased knee exion during the swing phase, and these effects were enhanced by the use of VFTs versus CFTs. Although peak ankle dorsiexion during swing improved with FES, there were no changes in circumduction during walking with FES. Additionally, analysis of the noFES data suggested that despite the rest intervals provided to the participants and the short (20- to 40-second) durations of the walking trials, the ankle dorsiexor muscles may have experienced fatigue within one testing session. This was the rst study to compare the effects of using traditional (CFTs) versus novel (VFTs) stimulation patterns for dorsiexor FES on poststroke gait. Interestingly, dorsiexor FES using VFTs produced greater peak dorsiexion angles during the paretic swing phase compared with FES using CFTs. Previous dynamometric studies on human and animal muscles showed greater rates of rise of force in response to VFTs versus CFTs during isometric contractions in nonfatigued muscle.33,34,51 Furthermore, in fatigued muscles, VFTs have consistently been shown to generate greater rates of rise of force, peak forces, and force-time integrals during isometric contractions51 and greater joint excursions and power during dynamic contractions.31,40 Our testing session was designed with 5- to 10-minute rest breaks between brief (20- to 40-second) walking trials to minimize fatigue. Nevertheless, our noFES walking data showed a signicant decrement in ankle dorsiexor angles from the beginning to the end of the session. The presence of fatigue in the dorsiexor muscles could partly explain the enhanced ankle dorsiexion seen with VFTs versus CFTs,51 along
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Figure 5.
Graphs showing average values and standard error bars for (A) peak ankle angles during swing and (B) ankle angles at initial contact for the 12 participants tested in our study. Three walking conditions shown are: walking without functional electrical stimulation (noFES), walking with dorsiexor muscle functional electrical stimulation using constant-frequency trains (FES-CFT), and walking with dorsiexor muscle functional electrical stimulation using variable-frequency trains (FES-VFT). *Signicant difference from noFES (P .05). Signicant difference from FES-CFT (P .05). #Trend for difference from FES-CFT (P .07).

( 3.1 1.5; P .01). Functional electrical stimulation using VFTs produced lesser plantar exion at toe-off compared with FES using CFTs (P .01). The ankle angles at toe-off for the nonparetic extremities were 13.4 2.1 degrees. Analysis of No FES Data There were signicant differences in peak ankle angles during swing among the 3 noFES walking trials at the beginning, middle, and end of the testing session (F 5.13, P .05). Participants demonstrated signicantly reduced peak swing phase ankle angles (P .05) during the noFES walking trial at the end
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( 3.8 1.3) versus the beginning of the session ( 2.2 1.1). Similarly, there were signicant differences in ankle angles at initial contact among the noFES walk trials collected at the beginning, middle, and end of the session (F 9.04, P .01). There was signicantly less ankle dorsiexion at initial contact during the noFES walking trials at the end ( 9.5 1.6) versus the beginning ( 7 1.8) of the session.

Discussion
Our results showed that during dorsiexor FES, VFTs produced greater increases in ankle dorsiexion during the swing phase compared with

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Effects of Dorsiexor Muscle Functional Electrical Stimulation on Poststroke Gait with the enhanced rates of rise of force produced by the VFTs.31 The observed muscle fatigue may be an important factor limiting gait performance during prolonged walking with FES.29,30 These results pave the way for future studies investigating the use of VFTs during prolonged bouts of walking to test whether VFTs can help generate repeated foot drop correction for a greater number of steps compared with CFTs. We also found a trend (P .07) toward greater dorsiexion at initial contact (at the end of the swing phase) during FES using VFTs, despite the fact that the high-frequency burst that differentiated the VFTs from the CFTs occurred at the beginning of the swing phase. Evidently, the force enhancement produced by the high-frequency burst at the onset of the VFTs lasted long enough to generate some enhancement in ankle dorsiexion throughout the paretic swing phase, further supporting the advantages of VFTs for FES applications. Typically, CFTs are delivered during dorsiexor FES, but there is a dearth of data in the literature quantifying the immediate effects of FES using CFTs on poststroke gait. In our study, as expected, we observed that delivering FES to the paretic ankle dorsiexor muscles during the swing phase produced greater ankle dorsiexion angles during the swing phase and at initial contact compared with walking without FES. Increased dorsiexion during the swing phase and at initial contact with FES using traditional stimulation patterns (CFTs) are not surprising and have been shown previously.52,53 However, in this study, we also presented an analysis of the effects of FES using CFTs on knee kinematics and circumduction. An interesting and novel nding of this study was the reduction in swing phase knee exion during dorsiJanuary 2010

Figure 6.
Graph showing average and standard error bars for (A) peak knee exion during swing and (B) ankle angle at toe-off for the paretic leg for 12 participants. Three walking conditions shown are: walking without functional electrical stimulation (noFES), walking with dorsiexor muscle functional electrical stimulation using constant-frequency trains (FES-CFT), and walking with dorsiexor muscle functional electrical stimulation using variable-frequency trains (FES-VFT). *Signicant difference from noFES (P .05). Signicant difference from FES-CFT (P .05).

exor FES. In their randomized controlled trial assessing the Odstock Drop Foot Stimulator, Burridge and colleagues anecdotally noted that the immediate effect of FES on the tibialis anterior and peroneal muscles was to bring the ankle into greater dorsiexion as the foot left the ground and facilitate a exor withdrawal response in which exion occurred at both hip and knee joints.3(pp208 209) In the present study, we did not have a directional hypothesis about the change in knee exion with FES. As stated by Burridge and colleagues, it can be argued that swing phase knee exion might increase during FES because of the exion withdrawal reex and the prevalence of exion synergy in peo-

ple poststroke. We were surprised to nd a decrease in swing phase knee exion during walking with dorsiexor FES versus walking without FES. The decrease in knee exion with dorsiexor FES is particularly important in individuals poststroke because they show a decreased swing phase knee exion in the paretic leg compared with the nonparetic leg and compared with control subjects without neurological impairment walking at matched speeds.5,50 Thus, dorsiexor FES seems to enhance a typical poststroke gait impairment that can negatively inuence foot clearance during swing. To our knowledge, decreased knee exion as an immediate effect of dorPhysical Therapy f 63

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Effects of Dorsiexor Muscle Functional Electrical Stimulation on Poststroke Gait siexor FES has not been reported previously in the literature. We believe that the decreased swing phase knee exion observed in our study was related to the decreased plantar exion that we observed at toe-off. The decreased plantar-exion angles could result in decreased push-off forces at the ankle during the stanceto-swing transition. Forwarddynamic simulations of healthy gait suggest that ankle plantar-exor force generation during terminal stance helps increase the knee exion velocity at toe-off, which is a critical contributor to swing phase knee exion.54 Interestingly, consistent with our ndings, preliminary results from our laboratory of forwarddynamic gait simulations of poststroke gait have predicted that enhanced excitation of ankle dorsiexor muscles would result in reduced swing knee exion.55 We posit that the timing of dorsiexor FES during gait could be a factor contributing to decreased plantar exion at toe-off and decreased knee exion during the swing phase. Because we triggered the FES using footswitches, dorsiexor stimulation began before actual toe-off (Fig. 1). Thus, the forces generated by the dorsiexor muscles at toe-off could have reduced the net plantar-exor moment at toe-off, potentially resulting in the observed decreased ankle plantar exion at toe-off, reduced push-off force generation during terminal stance, and reduced knee exion during swing. The timing of delivery of dorsiexor FES needs to be systematically manipulated and studied to test this hypothesis further. In addition, the effects of delivering FES to the ankle plantar-exor muscles to increase force generation during push-off needs to be investigated. An ideal FES intervention for management of foot drop poststroke would increase dorsiexion during the swing phase and at initial contact
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and increase plantar exion at toeoff. However, we found that although FES helped produce greater dorsiexion during swing and initial contact, it worsened the already reduced plantar exion at toe-off prevalent in the paretic leg. Similar to the onset of dorsiexor FES in our study, previous FES studies have shown that onset of dorsiexor FES was between heel-off and toe-off and that dorsiexion increased at toe-off during dorsiexor FES,52,53 suggesting that this issue is prevalent in other FES systems and needs to be addressed in future studies. We did not detect differences in circumduction among the 3 walking conditions tested in this study. The average values of circumduction demonstrated by the individuals tested in our study during walking without FES (X SD 4.0 2.9 cm) were similar to the amount of circumduction shown in individuals with poststroke hemiparesis by Chen and colleagues (4.6 3.2 cm).50 Because circumduction is a learned compensatory gait strategy, it is understandable that the amount of circumduction did not change as an immediate effect of FES, even though our participants were achieving greater ankle dorsiexion during the swing phase and, therefore, may not have required circumduction to clear the foot. Perhaps correction of gait compensations such as circumduction could occur if FES is used in conjunction with other interventions during gait retraining under the guidance of a physical therapist to help individuals with poststroke hemiparesis to unlearn the compensatory strategies they have developed over time. Nevertheless, a better understanding of the immediate and therapeutic effects (or the lack of effects) of FES on gait compensations, such as circumduction, may help to modify FES-based gait interventions to enable prevention and

correction of gait compensations poststroke. Our ndings suggest that novel FES systems capable of delivering VFTs during gait48,56 can produce enhanced correction of foot drop compared with traditional FES systems that deliver CFTs. The use of VFTs for dorsiexor FES during poststroke gait, as presented for the rst time in our study, is an example of the successful translation of research evidence from animal studies34,38 to isometric human studies27,31,33,51 and, nally, in the current study, to a clinical application. The present study also brings forward several interesting issues, such as the reduced swing-phase knee exion and reduced ankle plantar exion at toe-off with dorsiexor FES and the need for more precise timing of dorsiexor FES, that merit future investigation. One limitation of the present study is that we did not restrict handrail hold during testing. The use of handrails may affect kinematics and kinetics during gait57,58 and must be investigated adequately in future studies. There also is a need to investigate the effects of delivering FES to multiple muscles to address the many multijoint decits in poststroke gait. Finally, future studies are needed to investigate whether the use of VFTs during FES can enable the generation of targeted gait performance for a greater number of walking strides.
All authors provided concept/idea/research design. Dr Kesar, Dr Perumal, and Ms Angela Jancosko provided data collection. Dr Perumal provided hardware and software design for the functional electrical stimulation aspect of the data collection. Dr Reisman, Ms Jancosko, and Dr Rudolph assisted with data processing. Dr Kesar provided data analysis and manuscript writing. Dr Binder-Macleod, Dr Perumal, Ms Jancosko, Dr Reisman, and Dr Rudolph provided reviews of the manuscript before submission. The authors thank Ms Margie Roos, PT, NCS, for clinical testing and participant recruitment and Ms Leigh Shrewsbury for scheduling and recruitment. They also thank Dr Andrew Fuglevand for

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Effects of Dorsiexor Muscle Functional Electrical Stimulation on Poststroke Gait

providing helpful reviews of previous drafts of the manuscript. This study was approved by the Human Subjects Review Board of the University of Delaware. An oral presentation of some of the results was given at the 12th Annual International Functional Electrical Stimulation Society Conference; November 10 14, 2007; Philadelphia, Pennsylvania. These results also were presented at the annual meeting of the American Society of Biomechanics; August 26 29, 2009; University Park, Pennsylvania. This study was supported by National Institute of Nursing Research grant R01 NR010786 awarded to Dr Binder-Macleod. Funding for the laboratory instrumentation was provided by NIH Shared Instrumentation grant S10 RR022396 01 and DOD grant W911NF-051-0097. Part of the funding came from the University of Delaware Dissertation Fellowship awarded to Dr Kesar. This article was received April 29, 2009, and was accepted August 11, 2009. DOI: 10.2522/ptj.20090140 9 Shefer LR, Hennessey MT, Naples GG, Chae J. Peroneal nerve stimulation versus an ankle foot orthosis for correction of footdrop in stroke: impact on functional ambulation. Neurorehabil Neural Repair. 2006;20:355360. 10 Teasell RW, Foley NC, Bhogal SK, Speechley MR. An evidence-based review of stroke rehabilitation. Top Stroke Rehabil. 2003;10:29 58. 11 Liberson WT, Holmquest HJ, Scot D, Dow M. Functional electrotherapy: stimulation of the peroneal nerve synchronized with the swing phase of the gait of hemiplegic patients. Arch Phys Med Rehabil. 1961;42:101105. 12 Binder-Macleod SA, Lee SCK. Assessment of efcacy of functional electrical stimulation in patients with hemiplegia. Top Stroke Rehabil. 1997;3:88 98. 13 Robbins SM, Houghton PE, Woodbury MG, Brown JL. The therapeutic effect of functional and transcutaneous electric stimulation on improving gait speed in stroke patients: a meta-analysis. Arch Phys Med Rehabil. 2006;87:853 859. 14 Lyons GM, Sinkjaer T, Burridge JH, Wilcox DJ. A review of portable FES-based neural orthoses for the correction of drop foot. IEEE Trans Neural Syst Rehabil Eng. 2002;10:260 279. 15 Carnstam B, Larsson LE, Prevec TS. Improvement of gait following functional electrical stimulation, I: investigations on changes in voluntary strength and proprioceptive reexes. Scand J Rehabil Med. 1977;9:713. 16 Glanz M, Klawansky S, Stason W, et al. Functional electrostimulation in poststroke rehabilitation: a meta-analysis of the randomized controlled trials. Arch Phys Med Rehabil. 1996;77:549 553. 17 Taylor PN, Burridge JH, Dunkerley AL, et al. Clinical use of the Odstock dropped foot stimulator: its effect on the speed and effort of walking. Arch Phys Med Rehabil. 1999;80:15771583. 18 Hesse S, Werner C, Matthias K, et al. Nonvelocity-related effects of a rigid doublestopped ankle-foot orthosis on gait and lower limb muscle activity of hemiparetic subjects with an equinovarus deformity. Stroke. 1999;30:18551861. 19 Merletti R, Andina A, Galante M, Furlan I. Clinical experience of electronic peroneal stimulators in 50 hemiparetic patients. Scand J Rehabil Med. 1979;11:111121. 20 Bajd T, Kralj A, Turk R, et al. Use of functional electrical stimulation in the rehabilitation of patients with incomplete spinal cord injuries. J Biomed Eng. 1989;11: 96 102. 21 Granat MH, Ferguson AC, Andrews BJ, Delargy M. The role of functional electrical stimulation in the rehabilitation of patients with incomplete spinal cord injury: observed benets during gait studies. Paraplegia. 1993;31:207215. 22 Gerrits HL, Hopman MT, Sargeant AJ, et al. Effects of training on contractile properties of paralyzed quadriceps muscle. Muscle Nerve. 2002;25:559 567. 23 de Kroon JR, van der Lee JH, IJzerman MJ, Lankhorst GJ. Therapeutic electrical stimulation to improve motor control and functional abilities of the upper extremity after stroke: a systematic review. Clin Rehabil. 2002;16:350 360. 24 Winchester P, Carollo JJ, Habasevich R. Physiologic costs of reciprocal gait in FES assisted walking. Paraplegia. 1994;32: 680 686. 25 Isakov E, Mizrahi J, Najenson T. Biomechanical and physiological evaluation of FES-activated paraplegic patients. J Rehabil Res Dev. 1986;23:9 19. 26 Riener R. Model-based development of neuroprosthesis for paraplegic patients. Philos Trans R Soc Lond B Biol Sci. 1999;354:877 894. 27 Binder-Macleod SA, Lee SC, Russ DW, Kucharski LJ. Effects of activation pattern on human skeletal muscle fatigue. Muscle Nerve. 1998;21:11451152. 28 Scott WB, Binder-Macleod SA. Changing stimulation patterns improves performance during electrically elicited contractions. Muscle Nerve. 2003;28:174 180. 29 Chou LW, Kesar TM, Binder-Macleod SA. Using customized rate-coding and recruitment strategies to maintain forces during repetitive activation of human muscles. Phys Ther. 2008;88:363375. 30 Kesar TM, Chou LW, Binder-Macleod SA. Effects of stimulation frequency versus pulse duration modulation on muscle fatigue. J Electromyogr Kinesiol. 2008;18: 662 671. 31 Binder-Macleod SA, Kesar TM. Catchlike property of skeletal muscle: recent ndings and clinical implications. Muscle Nerve. 2005;31:681 693. 32 Peckham PH, Knutson JS. Functional electrical stimulation for neuromuscular applications. Annu Rev Biomed Eng. 2005;7: 327360. 33 Binder-Macleod SA, Barker CB III. Use of a catchlike property of human skeletal muscle to reduce fatigue. Muscle Nerve. 1991;14:850 857. 34 Binder-Macleod SA, Barrish WJ. Force response of rat soleus muscle to variablefrequency train stimulation. J Neurophysiol. 1992;68:1068 1078. 35 Doucet BM, Grifn L. Variable stimulation patterns for poststroke hemiplegia. Muscle Nerve. 2009;39:54 62. 36 Grifn L, Godfrey S, Thomas CK. Stimulation pattern that maximizes force in paralyzed and control whole thenar muscles. J Neurophysiol. 2002;87:22712278. 37 Karu ZZ, Durfee WK, Barzilai AM. Reducing muscle fatigue in FES applications by stimulating with N-let pulse trains. IEEE Trans Biomed Eng. 1995;42:809 817. 38 Burke RE, Rudomin P, Zajac FE III. Catch property in single mammalian motor units. Science. 1970;168:122124. 39 Lee SC, Becker CN, Binder-Macleod SA. Catchlike-inducing train activation of human muscle during isotonic contractions: burst modulation. J Appl Physiol. 1999;87:1758 1767.

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40 Lee SC, Binder-Macleod SA. Effects of activation frequency on dynamic performance of human fresh and fatigued muscles. J Appl Physiol. 2000;88:2166 2175. 41 Maladen RD, Perumal R, Wexler AS, Binder-Macleod SA. Effects of activation pattern on nonisometric human skeletal muscle performance. J Appl Physiol. 2007;102:19851991. 42 Garland SJ, Grifn L. Motor unit double discharges: statistical anomaly or functional entity? Can J Appl Physiol. 1999;24:113130. 43 Kottink AI, Hermens HJ, Nene AV, et al. A randomized controlled trial of an implantable 2-channel peroneal nerve stimulator on walking speed and activity in poststroke hemiplegia. Arch Phys Med Rehabil. 2007;88:971978. 44 Bogataj U, Gros N, Kljajic M, et al. The rehabilitation of gait in patients with hemiplegia: a comparison between conventional therapy and multichannel functional electrical stimulation therapy. Phys Ther. 1995;75:490 502. 45 Stein RB, Chong S, Everaert DG, et al. A multicenter trial of a footdrop stimulator controlled by a tilt sensor. Neurorehabil Neural Repair. 2006;20:371379. 46 Pomeroy VM, King L, Pollock A, et al. Electrostimulation for promoting recovery of movement or functional ability after stroke. Cochrane Database Syst Rev. 2006:CD003241. 47 Fugl-Meyer AR, Jaasko L, Leyman I, et al. The post-stroke hemiplegic patient, 1: a method for evaluation of physical performance. Scand J Rehabil Med. 1975;7: 1331. 48 Perumal R, Kesar TM, Wexler AS, BinderMacleod SA. Novel FES system to stimulate both dorsi- and plantar-exor muscles during stroke gait. Paper presented at: 12th Annual Conference of the International Functional Electrical Stimulation Society; November 10 14, 2007; Philadelphia, Pennsylvania. 49 Roth HR, Moore JL, Lewek MD, et al. Development and validation of circumduction assessment scale for individuals with hemiplegia. Paper presented at: Combined Sections Meeting of the American Physical Therapy Association; February 15, 2006; San Diego, California. 50 Chen G, Patten C, Kothari DH, Zajac FE. Gait differences between individuals with post-stroke hemiparesis and non-disabled controls at matched speeds. Gait Posture. 2005;22:5156. 51 Binder-Macleod SA, Lee SC, Fritz AD, Kucharski LJ. New look at force-frequency relationship of human skeletal muscle: effects of fatigue. J Neurophysiol. 1998;79: 1858 1868. 52 Voigt M, Sinkjaer T. Kinematic and kinetic analysis of the walking pattern in hemiplegic patients with foot-drop using a peroneal nerve stimulator. Clin Biomech (Bristol, Avon). 2000;15:340 351. 53 Preuss R, Stein RB, Fung J. Gait kinematics after forty weeks of use of the Walkaide 2: a case study. Paper presented at: 10th Annual Conference of the International Functional Electrical Stimulation Society; July 5 8, 2005; Montreal, Quebec, Canada. 54 Anderson FC, Goldberg SR, Pandy MG, Delp SL. Contributions of muscle forces and toe-off kinematics to peak knee exion during the swing phase of normal gait: an induced position analysis. J Biomech. 2004;37:731737. 55 Higginson JS, Kesar TM, Perumal R, Binder-Macleod SA. Simulation-guided stimulation for paretic ankle muscles during stroke gait. Paper presented at: ASME Summer Bioengineering Conference; June 20 24, 2007; Keystone, Colorado. 56 Hart DJ, Taylor PN, Chappell PH, Wood DE. A microcontroller system for investigating the catch effect: functional electrical stimulation of the common peroneal nerve. Med Eng Phys. 2006;28:438 448. 57 Chen G, Patten C, Kothari DH, Zajac FE. Gait deviations associated with post-stroke hemiparesis: improvement during treadmill walking using weight support, speed, support stiffness, and handrail hold. Gait Posture. 2005;22:57 62. 58 Siler WL, Jorgensen AL, Norris RA. Grasping the handrails during treadmill walking does not alter sagittal plane kinematics of walking. Arch Phys Med Rehabil. 1997;78: 393398.

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Novel Patterns of Functional Electrical Stimulation Have an Immediate Effect on Dorsiflexor Muscle Function During Gait for People Poststroke Trisha M. Kesar, Ramu Perumal, Angela Jancosko, Darcy S. Reisman, Katherine S. Rudolph, Jill S. Higginson and Stuart A. Binder-Macleod PHYS THER. 2010; 90:55-66. Originally published online November 19, 2009 doi: 10.2522/ptj.20090140

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