How To Walk On A Treadmill

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1 Perry Issue: Gait Rehab Gait Parameters Associated With Responsiveness to Treadmill Training With Body-Weight Support After Stroke: An Exploratory Study Sara J. Mulroy, Tara Klassen, JoAnne K. Gronley, Valerie J. Eberly, David A. Brown, Katherine J. Sullivan Background. Task-specific training programs after stroke improve walking function, but it is not clear which biomechanical parameters of gait are most associated with improved walking speed. Objective. The purpose of this study was to identify gait parameters associated with improved walking speed after a locomotor training program that included body-weight supported treadmill training (BWSTT). Design. A prospective, between-subjects design was used. Methods. Fifteen people, ranging from approximately 9 months to 5 years after stroke, completed 1 of 3 different 6-week training regimens. These regimens consisted of 12 sessions of BWSTT alternated with 12 sessions of: lower-extremity resistive cycling; lower-extremity progressive, resistive strengthening; or a sham condition of arm ergometry. Gait analysis was conducted before and after the 6-week intervention program. Kinematics, kinetics, and electromyographic (EMG) activity were recorded from the hemiparetic lower extremity while participants walked at a self-selected pace. Changes in gait parameters were compared in participants who showed an increase in self-selected walking speed of greater than 0.08 m/s (highresponse group) and in those with less improvement (low-response group). Results. Compared with participants in the low-response group, those in the high-response group displayed greater increases in terminal stance hip extension angle and hip flexion power (product of net joint moment and angular velocity) after the intervention. The intensity of soleus muscle EMG activity during walking also was significantly higher in participants in the high-response group after the intervention. Limitations. Only sagittal-plane parameters were assessed, and the sample size was small. Conclusions. Task-specific locomotor training alternated with strength training resulted in kinematic, kinetic, and muscle activation adaptations that were strongly associated with improved walking speed. Changes in both hip and ankle biomechanics during late stance were associated with greater increases in gait speed. S.J. Mulroy, PT, PhD, is Director, Pathokinesiology Laboratory, Rancho Los Amigos National Rehabilitation Center, 7601 E Imperial Hwy, Bldg 800, Room 33, Downey, CA (USA). Address all correspondence to Dr Mulroy at: smulroy@dhs.lacounty. gov. T. Klassen, MS, PT, NCS, is Clinical Instructor, Department of Physical Therapy, University of British Columbia, Vancouver, British Columbia, Canada. J.K. Gronley, PT, DPT, is Associate Director of Clinical Research, Pathokinesiology Laboratory, Rancho Los Amigos National Rehabilitation Center. V.J. Eberly, PT, NCS, is Research Physical Therapist, Pathokinesiology Laboratory, Rancho Los Amigos National Rehabilitation Center. D.A. Brown, PT, PhD, is Associate Professor and Associate Chair for Post-Professional Education, Department of Physical Therapy and Human Movement Sciences; Associate Professor, Department of Physical Medicine and Rehabilitation; and Adjunct Faculty, Department of Biomedical Engineering, Northwestern University, Chicago, Illinois. K.J. Sullivan, PT, PhD, is Associate Chair and Associate Professor of Clinical Physical Therapy, Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, California. [Mulroy SJ, Klassen T, Gronley JK, et al. Gait parameters associated with responsiveness to treadmill training with body-weight support after stroke: an exploratory study. Phys Ther. 2010;90: ] 2010 American Physical Therapy Association Post a Rapid Response or find The Bottom Line: February 2010 Volume 90 Number 2 Physical Therapy f 209

2 Stroke affects almost 1 person every 40 seconds and is the leading cause of serious, longterm disability in the United States. 1 Although physical therapists intervene with many facets of physical function, particular attention is focused on improving walking ability because this is one of the most common goals stated by people recovering from a stroke. 2 For people with mild to moderate motor impairment, eventual independent walking ability is likely; nevertheless, 60% of those who achieve physical independence in walking will be limited in community ambulation. 3 Evidence is building that for walking rehabilitation after stroke, innovations such as body-weight supported treadmill training (BWSTT) (ie, task-specific locomotor training) are more effective than approaches based on neurofacilitation or inhibition of muscle activity, which were used by physical therapists in the 1980s and 1990s. 4 6 Task-specific locomotor training has been associated with increases in strength (force-generating capacity), endurance, and walking speed. 7 9 These global outcomes indicate functional changes but do not provide insights about the underlying neuromuscular Available With This Article at ptjournal.apta.org Video: In honor of Dr Jacquelin Perry, view art by patients from Rancho Los Amigos National Rehabilitation Center. Podcast: Stepping Forward With Gait Rehabilitation symposium recorded at APTA Combined Sections Meeting, San Diego. Audio Abstracts Podcast This article was published ahead of print on December 18, 2009, at ptjournal.apta.org. or biomechanical contributors to the therapeutic improvements. With further insights into underlying contributors, interventions can be targeted to specific impairments with the expectation of improved outcomes at greater efficiency. Although many studies have demonstrated improved walking function after BWSTT for people with stroke, 7 9 the biomechanical parameters of gait underlying the long-term improvements seen in overground walking as a result of BWSTT have not been identified. Both hip flexion power (product of net joint moment and angular velocity) and ankle plantar-flexion power during late stance are critical determinants of improvements seen in gait speed as a result of other interventions after stroke However, it is not known whether BWSTT targets biomechanical functions that are uniquely affected by treadmill training and body-weight support. There is limited evidence that walking on a treadmill with body-weight support (compared with overground ambulation) results in immediate, short-term changes, including increased stance-swing symmetry, 13,14 increased hip extension during single-limb stance, and decreased gastrocnemius muscle activity. 15 Walking at higher speeds on the treadmill increases the activation of stance-phase muscles, including the gastrocnemius, vastus lateralis, biceps femoris, and gluteus medius muscles. 16 To our knowledge, no studies have included instrumented gait analysis before and after a program of BWSTT to determine the biomechanical parameters underlying the long-term improvements seen in overground walking. Understanding the gait mechanics and muscle activity patterns in people who respond well and in those who do not may suggest a different physiological basis for those with the best recovery versus those with persistent walking dysfunction. The primary purpose of this study was to identify the biomechanical gait parameters associated with responsiveness to a task-specific intervention that included BWSTT and that was designed to improve locomotor recovery after stroke. (In this issue, Kuo and Donelan 17 review the determinants of dynamic walking.) The secondary objective was to identify the baseline participant characteristics and changes in lowerextremity maximal isometric torque and maximal muscle activation that were associated with responsiveness to the intervention. We hypothesized that, compared with people who showed little or no improvement in walking speed after the BWSTT interventions, people who responded to the BWSTT interventions (ie, people with significant postintervention increases in selfselected overground walking speed) would show improvements in kinematic and kinetic parameters at the end of stance and at the stance-swing interface in the paretic hip and ankle joints; increased intensity of electromyographic (EMG) activity of the paretic ankle plantar-flexor, hip extensor, and hip flexor muscles during walking; and increased maximal isometric torque of the hip flexor and ankle plantar-flexor muscle groups in the paretic leg. Method Study Design The participants in the present study were a subset of those in a larger randomized clinical trial, the Strength Training Effectiveness Post-Stroke (STEPS) trial. 18 In the STEPS study, participants were randomly assigned to 1 of 4 intervention groups: task-specific BWSTT and upper-extremity ergometry (UE Ex), locomotor strength training (Cycle) and UE Ex, BWSTT and Cycle, and BWSTT and muscle- 210 f Physical Therapy Volume 90 Number 2 February 2010

3 Figure 1. Outline of Strength Training Effectiveness Post-Stroke (STEPS) study. BWSTT body-weight supported treadmill training, Cycle locomotor strength training, LE muscle-specific lower-extremity strength training, UE Ex upper-extremity ergometry. specific lower-extremity strength training (LE Ex). An exploratory instrumented gait analysis to examine the biomechanical mechanisms associated with the STEPS interventions was conducted at Rancho Los Amigos National Rehabilitation Center. The first 5 participants from each exercise group (n 20) enrolled at the University of Southern California or Rancho Los Amigos National Rehabilitation Center underwent the instrumented gait analysis at baseline (after group randomization but before intervention) and after the 6-week BWSTT period. All subjects read and signed an informed consent form that described the STEPS protocol approved by the institutional review board of each institution; subjects who participated in the gait analysis also signed an additional consent form specifically related to the gait analysis. The results of the primary STEPS study indicated that self-selected walking speed increased significantly and similarly after each of the 3 BWSTT interventions but not after the Cycle UE Ex intervention. Therefore, in the present study, we evaluated only data from the 15 participants assigned to the 3 BWSTTrelated groups (ie, BWSTT UE Ex, BWSTT Cycle, and BWSTT LE Ex). The STEPS study design and the additional allocation specifically related to the gait analysis are shown in Figure 1. Participants The 15 participants included in the present study met the inclusion and exclusion criteria for the STEPS trial. 18 In summary, the participants were 18 years of age or older; approximately 9 months to 5 years after the initial onset of an ischemic or hemorrhagic cerebrovascular ac- February 2010 Volume 90 Number 2 Physical Therapy f 211

4 cident; able to ambulate, at a selfselected walking speed of less than or equal to 1.0 m/s, at least 14 m with an assistive device, lowerextremity orthosis, or both and with the assistance of 1 person; and free from any serious medical, orthopedic, or premorbid condition that would physically or cognitively limit participation in the study. Intervention The 15 participants received BWSTT UE Ex, BWSTT Cycle, or BWSTT LE Ex. In brief, the UE Ex component consisted of lowresistance upper-extremity ergometry. The Cycle intervention was a program of progressive, resistive lower-extremity cycling on a Biodex semirecumbent cycle* that required resistance during the down stroke of the cycle (extension) to maintain the position of the seat in the target zone. Finally, the LE Ex component was a progressive, resistive exercise program for specific lower-extremity muscle groups of the hemiparetic leg (ie, hip extensor, knee extensor, plantar-flexor, hip flexor, knee flexor, and dorsiflexor muscles). Participants in all 3 intervention groups received the BWSTT interventions twice per week. This intervention included 20 minutes (in 4- to 5-minute bouts) of stepping on a treadmill with body-weight support at a treadmill speed of approximately 3.2 km/h (2.0 mph). A complete description of the exercise protocols is provided in the report of the primary STEPS study. 18 The BWSTT and strengthening exercises were alternated over 4 days per week (excluding weekends) for 6 weeks (for a total of 24 sessions). Each exercise session was 1 hour in duration and was conducted by a licensed physical therapist. * Biodex Medical Systems Inc, 20 Ramsay Rd, PO Box 702, Shirley, NY Outcome Measures Specific demographic and clinical data obtained from the baseline evaluation of the STEPS study also were used to characterize the participants in the present study. 18 These data included participant demographics, stroke characteristics (including onset), and lower-extremity Fugl-Meyer motor scale score. The instrumented gait analysis was conducted within 1 week before and within 1 week after the 24-session exercise intervention. Participants walked in shoes without any lowerextremity orthoses but were permitted to use their customary assistive devices. Participants performed several practice walking trials to improve the likelihood of stepping with the tested foot landing entirely on the forceplate. Simultaneous recordings of foot-floor contacts, lower-extremity kinematics, and EMG activity were made as participants traversed a 10-m walkway at a self-selected speed; the middle 6 m of the walkway was delineated for data collection by photoelectric beams. Walking was repeated until 2 successful trials with the participant s foot landing completely on the forceplate were recorded. Any trial that resulted in only part of the foot landing on the forceplate was discarded. Assistive devices were not permitted to contact the forceplate. B & L Engineering, 3002 Dow Ave, Ste 416, Tustin, CA Vicon Motion Systems, 14 Minns Business Pk, West Way, Oxford OX2 0JB, United Kingdom. Foot-floor contact patterns were recorded by use of a Stride Analyzer System with compression-closing footswitches taped to the bottom of the participant s shoes. The 3- dimensional kinematics of the participant s hemiplegic lower extremity were documented by use of a Vicon Motion Analysis System. Six infrared, 50-Hz cameras recorded the locations of 14 retroreflective markers taped to the skin overlying the bony landmarks, including the midline sacrum at the level of the posterior iliac spines, anterior superior iliac spines (bilaterally), greater trochanter, anterior thigh, medial and lateral femoral condyles, anterior tibia, medial and lateral malleoli, dorsum of the foot, first and fifth metatarsal heads, and posterior heel. Motion data were acquired by use of a DEC PDP 11/23 computer. The ground reaction forces of the hemiparetic lower extremity were sampled at 2,500 Hz by use of a Kistler forceplate embedded in the walkway. Intramuscular EMG recording was accomplished with indwelling, finewire electrodes inserted into the belly of each of 8 lower-extremity muscles (gluteus maximus, gluteus medius, semimembranosus, adductor longus, rectus femoris, vastus intermedius, soleus, and anterior tibialis muscles) using the technique of Basmajian and Stecko. 19 Electrode placement was confirmed by palpating tension in the tendon or muscle belly during mild electrical stimulation through the inserted wires. Electromyographic signals were transmitted by FM-FM telemetry (model 2600 apparatus), # filtered through an analog band-pass filter (150 1,000 Hz), and sampled and digitized at 2,500 Hz. The overall signal gain was 1,000. Before the walking trials, EMG recording was performed to determine the baseline threshold of myoelectric activity for each muscle at rest and during a 5-second resisted isometric maximal voluntary contraction for normalization. Participants performed a practice maximal contraction for each muscle before data collection. Digital Equipment Corp, 1 Kendall Sq, Cambridge, MA Kistler Instrument Corp, 75 John Glenn Dr, Amherst, NY # Biosentry Telemetry Inc, G Earl St, Torrance, CA f Physical Therapy Volume 90 Number 2 February 2010

5 Maximal isometric torque was recorded with a Biodex dynamometer* for ankle dorsiflexion, ankle plantar flexion, and flexion and extension of both the hip and the knee. Participants performed a practice submaximal contraction and then 3 maximaleffort trials. Testing of the nonparetic extremity preceded that of the paretic extremity for each muscle group. The average peak torque from the 3 trials was recorded. Isometric torque at the ankle was measured with the participant in a long sitting position with the seat back reclined slightly (85 ) and the knee supported in 20 to 30 degrees of flexion. The ankle was positioned in 5 degrees of plantar flexion for recording isometric ankle plantarflexion torque and in 15 degrees of plantar flexion for the ankle dorsiflexion test. Knee torque testing was performed while the participant was sitting with the seat back reclined to 85 degrees. Torque for both isometric knee extension and knee flexion was measured in 45 degrees of knee flexion. Torque for hip flexion and hip extension was recorded with the participant in the supine position and the cuff attached just proximal to the popliteal fossa. Hip extension torque was measured with the hip flexed to 90 degrees, and hip flexion torque was measured with the hip flexed to 60 degrees. Data Management Footswitch data were used to calculate walking speed, cadence, and stride length and to identify gait cycle timing. Each stride was time normalized with initial contact defined as 0% of the gait cycle, the end of stance defined as 65%, and the end of swing defined as 100% to allow for comparison across participants. Ground reaction forces and segment kinematic data were filtered with a fourth-order, zero-lag, low-pass digital Butterworth filter (20- and 4-Hz cutoff frequencies, respectively). Kinematic data were processed with Adtech Motion Analysis Software** to produce 3-dimensional trajectories for each marker. The position and orientation of each lowerextremity segment were obtained, and lower-extremity joint angles for each percentage of the gait cycle were determined by use of computer algorithms with Euler embedded coordinates. An ensemble average for all complete strides (typically 4 6) was determined for the sagittal plane joint motions of each participant. The magnitude, orientation, and point of application of the resultant ground reaction forces were determined from the forceplate data. Measured body segment parameters were used in conjunction with empirical relationships, derived from cadaver studies, to estimate the mass, center of mass, and moments of inertia of body segments. 20 Joint and body segment kinematic data were combined with kinetic data to calculate the joint forces and moments by use of the inverse dynamics approach. 21 Joint moments were normalized to body weight and leg length. Joint power for the hip, knee, and ankle was calculated as the product of the joint moment and the angular velocity. Electromyographic signals were subjected to full-wave rectification and integrated over intervals of 0.01 second. A moving window was used to identify the highest EMG signal recorded in a 1-second interval during the 5-second maximal muscle contraction, and this value was used to calculate the average EMG signal in a 0.02-second interval. If the latter value was at least 122 mv, then it served as the normalization value for the EMG signals recorded during walking 22 ; ** Adtech Inc, 3465 Waialae Ave, Ste 200, Honolulu, HI however, if it was less than 122 mv, then the normalization value for the walking trials was set at 122. The use of this minimum normalization value, which was approximately 20% of a full interference pattern, prevented inflation of EMG signals during walking in muscles in which a participant lacked sufficient volitional control to produce a significant signal during manual muscle testing. 22 The intensity of EMG activity was expressed as a percentage of the maximal voluntary contraction. Phasing of EMG activity during walking was determined with EMG Analyzer Software.,23 The EMG Analyzer identified the onset and cessation times (as a percentage of the gait cycle) for each packet of muscle activity that had an intensity of at least 5% of the maximal voluntary contraction and a duration of at least 5% of the gait cycle. With the minimum normalization value of 122 mv, the threshold for 5% of the maximal voluntary contraction for significant EMG activity would correspond to 6 mv over a second interval. Any signal lower than this value was not considered functionally significant. Packets of EMG activity separated by quiescent intervals of less than 5% of the gait cycle were combined. The average intensity of activation between onset and cessation was calculated for each muscle. 23 Data Analysis Participants were stratified into either a high-response group or a lowresponse group on the basis of the magnitude of the change in selfselected walking speed between the baseline and postintervention sessions. Participants in the highresponse group showed increases in self-selected walking speed of greater than or equal to 0.08 m/s, whereas the low-response group comprised participants with walking February 2010 Volume 90 Number 2 Physical Therapy f 213

6 Figure 2. Change in walking speed (y-axis) versus baseline walking speed (A) and lower-extremity (LE) Fugl-Meyer motor scale score (B) for high-response and low-response groups. The bold horizontal line represents the minimum detectable change (MDC) threshold for walking speed (0.08 m/s). Participants above the walking speed MDC threshold were categorized as showing a high response; participants below this threshold were categorized as showing a low response. Two participants with high baseline walking speeds but relatively low baseline LE Fugl-Meyer motor scale scores are indicated with circles. speed changes of less than 0.08 m/s. The minimum detectable change in customary walking speed for older adults with stroke has been reported in most studies to range from 0.05 to 0.08 m/s; thus, we selected the higher range value of 0.08 m/s as the threshold for improvement in our analysis We tested the specific hypotheses that participants who showed greater improvements in selfselected walking speed (highresponse group) after completing a 24-session program of task-specific locomotor training and strength training designed to improve walking recovery would show the following biomechanical changes in the hemiparetic lower extremity (compared with participants who showed minimal or no improvements in walking speed [lowresponse group]): increased hip extension angle, hip flexion moment, and hip flexion power at terminal stance pre-swing; increased plantar-flexion angle and plantarflexion power at terminal stance pre-swing; increased intensity of EMG activity of the ankle plantarflexor, hip extensor, and hip flexor muscles (soleus, gluteus maximus, semimembranosus, and adductor longus muscles) during walking; and increased isometric torque of the hip flexor and ankle plantarflexor muscles. Two-way repeated-measures analysisof-variance models were used to determine the interaction effects of group (high-response group and low-response group) and time (before intervention and after intervention) for spatiotemporal characteristics; peak values for paretic lowerextremity joint motion, moment, and power; and average intensities of EMG activity of paretic lowerextremity muscles during walking. The main effect of time was evaluated only when the interaction was not statistically significant. Similar analyses were conducted for the maximal isometric lower-extremity torque and the maximal EMG signal elicited during manual muscle testing of each of the 8 muscles at the baseline and postintervention tests. The baseline clinical characteristics of the 2 response groups were compared by use of an independent t test or a chi-square test for categorical data. A P value of.05 was set as the criterion for statistical significance. The analyses were conducted by use of BMDP statistical software. Results Participant Characteristics Seven of the 15 participants showed improvements in self-selected walking speed of greater than 0.08 m/s (high-response group) after the 24 exercise sessions, and 8 participants showed improvements of less than 0.08 m/s (low-response group) (Fig. 2A). There were no sig- Statistical Solutions, Stonehill Corporate Center, 999 Broadway, Ste 104, Saugus, MA f Physical Therapy Volume 90 Number 2 February 2010

7 Table 1. Participant Characteristics Participants High-Response Low-Response Effect Characteristic All (N 15) Group (n 7) Group (n 8) P Size Age (y) X (SD) (14.86) (13.00) (17.83) Range Sex 7 women, 8 men 3 women, 4 men 4 women, 4 men Treatment group (no. of participants) BWSTT UE Ex (5) BWSTT UE Ex (2) BWSTT UE Ex (3).77 BWSTT Cycle (5) BWSTT Cycle (3) BWSTT Cycle (2) BWSTT LE Ex (5) BWSTT LE Ex (2) BWSTT LE Ex (3) Baseline evaluation self-selected speed (m/s) X (SD) 0.50 (0.24) 0.58 (0.18) 0.43 (0.27) Range Mo since stroke X (SD) (15.46) (14.92) (16.79) Range Baseline lower-extremity Fugl-Meyer motor scale score.02 a 1.35 X (SD) (4.69) (3.60) (4.11) Range Assistive device (no. of participants using the None (6) None (4) None (2) indicated device) Single cane (3) Single cane (1) Single cane (2) Quad cane (5) Quad cane (2) Quad cane (3) Single crutch (1) Single crutch (1) a Statistically significant. nificant differences between the high-response group and the lowresponse group with respect to age, sex, time since stroke, intervention group, baseline self-selected walking speed, or assistive device use (Tab. 1). The baseline lowerextremity Fugl-Meyer motor scale score was significantly higher in the high-response group (mean 28.7, SD 3.6) than in the low-response group (mean 23.5, SD 4.1) (P.02) (Fig. 2B). Spatiotemporal Characteristics The increase in average walking speed in participants in the highresponse group after the intervention was m/s (SD 0.056); the increase in participants in the lowresponse group was m/s (SD 0.034) (Tab. 2). Both cadence Table 2. Baseline Values and Changes in Spatiotemporal Characteristics of Walking Characteristic High-Response Group (n 7) a Participants Low-Response Group (n 8) a P Effect Size Speed (m/s) Baseline (0.177) (0.275) Change (0.056) (0.034) Cadence (steps/min) Baseline (13.72) (18.44) Change 7.77 (4.88) 1.51 (4.37) Stride length (m) Baseline (0.126) (0.311) Change (0.048) (0.074) a Values are reported as mean (SD). February 2010 Volume 90 Number 2 Physical Therapy f 215

8 Table 3. Baseline Values and Changes in Peak Hip Joint Angles, Moments, and Power During Walking Measurement High-Response Group (n 7) a Participants Low- Response Group (n 8) a P Effect Size Hip flexion angle during loading ( ) Baseline 29.6 (8.21) (8.49) Change 2.16 (5.84) 2.73 (5.66) Hip extension angle during stance ( ) Baseline 1.99 (3.95) 3.68 (10.70) Change 6.79 (5.66) 0.63 (6.41) Thigh extension angle during stance ( ) Baseline (6.16) 9.43 (6.17) Change 2.10 (3.98) 2.53 (4.26) Hip flexion angle during swing ( ) Baseline (6.08) (8.01) Change 1.59 (6.57) 4.47 (5.54) Thigh flexion angle during swing ( ) Baseline (5.89) (7.90) Change 2.98 (4.94) 2.52 (3.41) Medial (internal) hip extension moment during loading (N m/kg m) Baseline (0.211) (0.292) Change (0.236) (0.218) Medial (internal) hip flexion moment during stance (N m/kg m) Baseline (0.120) (0.252) Change (0.230) (0.128) Hip extension power generation during loading (W/kg m) Baseline (0.302) (0.309) Change (0.392) (0.144) Hip flexion power absorption during stance (W/kg m) Baseline (0.167) (0.268) Change (0.325) (0.139) Hip flexion power generation during pre-swing (W/kg m) Baseline (0.231) (0.160) Change (0.18) (0.09) a Values are reported as mean (SD). and stride length also improved to a greater extent in the high-response group than in the low-response group (P.02 and P.01, respectively). Kinematics and Kinetics Compared with participants in the low-response group, participants in the high-response group displayed greater increases in the peak hip extension angle ( 6.8 [SD 5.7] versus 0.6 [SD 6.4]) (Tab. 3, Fig. 3A) and in hip flexor muscle power during stance ( W/kg m [SD 0.18) versus W/kg m [SD 0.09]) (Fig. 3B); these differences were statistically significant (P.02). In contrast, the increases in the peak thigh extension angle (relative to laboratory vertical) in both groups were nearly identical ( 2.1 versus 2.5 ), indicating that the differences in the hip extension angle between the groups reflected decreased anterior pelvic tilt in the high-response group and increased anterior pelvic tilt in the lowresponse group. 216 f Physical Therapy Volume 90 Number 2 February 2010

9 Figure 3. Mean curves for high-response (HIGH) and low-response (LOW) groups at preintervention (PRE) and postintervention (POST) assessments for hip motion (A) and power (B) and ankle motion (C) and power (D). Curves for participants in the high-response group are depicted with black lines, and curves for participants in the low-response group are depicted with blue lines. Preintervention data are represented by dashed lines, and postintervention data are represented by solid lines. The vertical lines indicate the end of stance and the beginning of swing. Changes in hip extension motion and hip flexor muscle power generation during terminal stance pre-swing were significantly greater in the high-response group than in the low-response group. Changes in ankle plantarflexion motion and power generation also tended to be greater in the high-response group. Asterisk indicates significant at P.05. The peak ankle plantar-flexion angle during initial double-limb support (loading) increased more in participants in the high-response group ( 2.8 [SD 2.7]) than in participants in the low-response group ( 1.6 [SD 3.9]) (P.03) (Tab. 4, Fig. 3C). In terminal double-limb support (pre-swing), the increases in the peak ankle plantar flexion angle ( 4.2 [SD 3.8] versus 0.04 [SD 4.9]) and peak ankle plantarflexion power ( W/kg m [SD 0.236] versus W/kg m [SD 0.146]) (Fig. 3D) also were greater in the high-response group than in the low-response group; however, these differences did not reach statistical significance (P.09 and P.08, respectively). The effect sizes for both of these comparisons exceeded 0.9. EMG Activity During Walking and Manual Muscle Testing A difference in the intensity of EMG activity between participants in the high-response group and participants in the low-response group was observed only for the soleus muscle. The increase in the average intensity of soleus muscle EMG activity during walking was significantly greater in the high-response group after the intervention (12.7% maximal [SD 10.8] versus 1.2% maximal [SD 8.5]) (P.05, effect size 1.18) (Fig. 4A). Changes in maximal muscle activation during manual muscle testing from the preintervention gait analysis to the postintervention gait analysis were not significantly different (no significant interaction between time and group) between the high-response group and the lowresponse group for any muscle tested. However, the main effects of time on maximal activation of the semimembranosus muscle during manual muscle testing and on the intensity of EMG activity during walking (Fig. 4B and 4D) were statistically significant. For both groups, the intensity of semimembranosus February 2010 Volume 90 Number 2 Physical Therapy f 217

10 Table 4. Baseline Values and Changes in Peak Ankle Joint Angles, Moments, and Power During Walking Participants High-Response Low-Response Effect Measurement Group (n 7) Group (n 8) P Size Plantar-flexion angle during loading ( ) Baseline (3.91) (5.59) Change 2.83 (2.72) 1.60 (3.90) Dorsiflexion angle during stance ( ) Baseline 9.67 (3.56) 7.66 (6.70) Change 2.10 (2.05) 0.31 (3.56) Plantar-flexion angle during pre-swing ( ) Baseline 4.14 (3.78) 1.56 (3.93) Change 4.23 (3.75) 0.04 (4.85) Dorsiflexion angle during swing ( ) Baseline 0.84 (3.76) 0.08 (4.28) Change 2.58 (2.06) 1.64 (5.12) Medial (internal) dorsiflexion moment during loading (N m/kg m) Baseline (0.057) (0.039) Change (0.047) (0.040) Medial (internal) plantar flexion moment during stance (N m/kg m) Baseline (0.150) (0.194) Change (0.111) (0.103) Dorsiflexion power absorption during loading (W/kg m) Baseline (0.055) (0.047) Change (0.167) (0.070) Plantar-flexion power absorption during stance (W/kg m) Baseline (0.183) (0.242) Change (0.191) (0.158) Plantar-flexion power generation during pre-swing (W/kg m) Baseline (0.432) (0.219) Change (0.236) (0.146) a Values are reported as mean (SD). muscle EMG activity after the intervention was significantly higher than that before the intervention. Maximal activation during manual muscle testing before the intervention was 68.8 mv (SD 15.6), and that after the intervention was mv (SD 51.5) (P.01, effect size 1.63). Average EMG intensity of semimembranosus muscle activity during gait before the intervention was 13.3% maximal (SD 7.5), and that after the intervention was 22.1% maximal (SD 8.2) (P.05, effect size 1.12). Maximal Isometric Torque For most muscle groups, maximal isometric torque was not improved in either participant group. Only the knee flexion torque of the paretic limb showed a significantly greater change in participants in the highresponse group than in participants in the low-response group ( 9.0 N m [SD 12.4] versus 7.1 [SD 9.1]) (P.02, effect size 1.43). Discussion Kinetic and Kinematic Changes After Intervention After a task-specific intervention that included BWSTT, participants who exhibited a clear increase in selfselected overground walking speed (ie, higher than 0.08 m/s) showed greater and more consistent changes in the kinematics and kinetics of the hip than of the ankle during late stance, providing partial support for our hypotheses. The increase in the maximal hip extension angle during 218 f Physical Therapy Volume 90 Number 2 February 2010

11 Figure 4. Electromyographic (EMG) activity during walking at baseline (pre-exercise) and postintervention (post-exercise) assessments for the soleus muscle (A and C) and the semimembranosus muscle (SMEMB) (B and D) in the high-response group (A and B) and the low-response group (C and D). At the postintervention assessment, participants in the high-response group walked with a significantly higher intensity of soleus muscle activation during mid stance and terminal stance (A) and a higher intensity of activation of the semimembranosus muscle during terminal swing and early loading, as expected with more typical gait activation (B). MMT manual muscle testing. late stance in participants in the high-response group was attributable to a combination of increased thigh extension and decreased anterior pelvic tilt. In contrast, participants in the low-response group showed increased anterior pelvic tilt. Participants in the high-response group exhibited a tendency toward greater increases in ankle plantarflexion angle and power generation during pre-swing than participants in the low-response group. The large effect sizes for these data (0.92 and 0.98) (Tabs. 3 and 4) indicated that these differences likely would have been statistically significant with a larger sample size. Increases in ankle plantar-flexion power and hip flexion power also were identified as the mechanisms used to increase walking speed in both people who were able-bodied 28 and people with stroke after traditional interventions. 29,30 Also in agreement with the results of the present study, Jonsdottir and colleagues 31 reported that after stroke, most people increased walking speeds from preferred to high speeds by preferentially increasing work production at the hip to a greater extent than at the ankle; these findings suggested that after stroke, the capacity to increase work production at the ankle may be limited. Increased joint power generation during walking implies an increase in the intensity of muscle activation, force generated for a given activation level (hypertrophy or improved length tension relationship), or an improved moment arm. 32 Only the soleus muscle showed a greater increase in activation during walking in participants in the high-response group than in participants in the lowresponse group. Although the soleus muscle is a uniarticular muscle crossing only the ankle joint, musculoskeletal models have determined that its activity, in addition to providing ankle plantar flexion and forward propulsion of the trunk, 33 also accelerates both the hip and the knee into extension during the second half of stance. 34 This description is consistent with the improved mechanics February 2010 Volume 90 Number 2 Physical Therapy f 219

12 seen at both the hip and the ankle in the high-response group. The lack of change in ankle angle or power in participants in the lowresponse group could be explained by neural factors, such as the size and location of the stroke lesion. Corroborating evidence for this explanation was documented in a previous case study of a 38-year-old woman from the low-response group who had severe stroke-related impairment (lower-extremity Fugl- Meyer motor scale score 24/34) and severe walking limitation (initial gait speed 0.33 m/s). 35 Her minimal improvements in walking speed after BWSTT were associated with increased motion at the hip but little change at the ankle. 35 Magnetic resonance imaging after the stroke revealed extensive white matter tract damage to the internal capsule, which could indicate limited distal recovery potential. Muscle Activation and Torque Changes All participants, regardless of the extent of improvements in walking speed, showed increases in activation of the semimembranosus muscle during both manual muscle testing and walking. A closer examination of the EMG profiles of participants in the high-response and lowresponse groups before and after the intervention indicated that participants in the high-response group showed increased intensity of semimembranosus muscle EMG activity during the period of normal phasing, from mid swing through loading, whereas those in the low-response group exhibited increased intensity more diffusely throughout the gait cycle (Fig. 4B). Increased semimembranosus muscle activation in early swing actually would inhibit swing limb advancement by resisting thigh flexion. 36 The hamstring muscles are biarticular hip extensor and knee flexor muscles during isolated voluntary contractions. During walking, the hamstring muscles function primarily as hip extensor muscles, acting to decelerate the flexing hip from mid swing to initial contact as well as to extend the hip during the first half of stance. 33,34,37 The proximal attachment of the hamstring muscles on the ischial tuberosity also results in posterior tilting of the pelvis, particularly during stance, when its distal attachment is relatively fixed. 38 Thus, the kinematic changes seen in participants in the high-response group (increased hip extension and decreased anterior pelvic tilt) are consistent with the function of the semimembranosus muscle during walking. Maximal isometric knee flexion torque was increased after the intervention only for participants in the high-response group. However, hip extension torque was not significantly improved in participants in either group. Hip extension torque likely was more reflective of torque generation of the uniarticular hip extensor muscles (gluteus maximus, gluteus medius, and adductor magnus muscles) because the resistance cuff was placed proximal to the knee and the knee was flexed with minimal support of the lower leg. In contrast, the hamstring muscles are the primary contributors to isolated knee flexion torque. 32 Thus, it is likely that although all of the participants showed increased activation of the semimembranosus muscle during walking, increased strength in this muscle group was seen only in participants with a greater increase in walking speed. We did not find evidence of increased EMG intensity of either of the hip flexor muscles studied (adductor longus and rectus femoris muscles). We did not expect that increased rectus femoris muscle activation would correspond to increased walking speed because of its role in knee extension, which would inhibit knee flexion during swing. In contrast to the findings of the present study, increased activation of the adductor longus and soleus muscles was strongly associated with improved walking speeds over the first 6 months after stroke in 2 other studies. 22,39 It is possible that other hip flexor muscles, including the iliopsoas, sartorius, and gracilis muscles, contributed to the increased hip flexor muscle power generation seen in participants in the highresponse group, but we did not record data from these muscles. The increased hip flexor muscle power generation also might have resulted from the increased angular velocity over the greater arc of flexion created by the increased hip extension angle during late stance. The hip adductor muscles, which function as hip flexor muscles during gait, would have a greater moment arm for hip flexion at angles of greater extension and could generate a larger moment with the same amount of force. 32 In addition, greater hip extension would increase the elastic energy storage and release of the passive joint structures of the hip, reducing the amount of work required of the hip flexor muscles to accelerate the leg into swing. 33 Contrary to our hypothesis, maximal isometric torque of the ankle plantar flexor and hip flexor muscle groups was not increased in participants in the high-response group. This finding is consistent with the overall results of the STEPS trial. 18 Among the 3 interventions that included BWSTT in the STEPS trial, increases in maximal torque were seen only for the combined flexor muscles of the paretic limb and the combined extensor muscles of the nonparetic limb and only in the BWSTT UE Ex 220 f Physical Therapy Volume 90 Number 2 February 2010

13 group. Lower-extremity torque was not increased in the other 2 BWSTTrelated groups, although walking speed was increased to similar degrees in all 3 BWSTT-related groups. Strength gains in the knee flexor muscle group for the other 2 BWSTTrelated groups in the STEPS trial might have been masked by combining all of the flexor torque values into 1 variable. Taken together, the results of these studies indicated that the observed improvements in walking speed were not dependent on the strength gains for most of the muscle groups. Instead, the observed improvements in walking speed and muscle activation in the present study are more consistent with neural adaptation. Several studies have provided evidence of neural plasticity in people with stroke after BWSTT, including increased corticomotor excitability and activation 40,41 and increased activation of cortical and subcortical networks. 42,43 Our study is the first to identify the specific long-term changes in muscle activation that accompany improved biomechanics of overground walking after BWSTT. Implications for Clinical Practice On the basis of the results of the present study, we recommend emphasizing hip extension in late stance during BWSTT and training at increased walking speeds to facilitate more rapid and appropriately phased muscle activation. Hornby and colleagues 9 showed that BWSTT with manual facilitation produced greater improvements in walking function than robot-supported treadmill training after stroke. The ability to facilitate specific components of walking mechanics, such as increased hip extension with decreased anterior pelvic tilt, likely is more feasible with manual guidance than with mechanical support. The lower-extremity Fugl-Meyer motor scale score was the baseline characteristic that best differentiated participants in the high-response group from those in the low-response group. Participants in the highresponse group had greater selective motor control at baseline. The extent of walking speed improvements after the intervention also tended to correspond to a higher baseline speed and no assistive device. These factors likely would have reached statistical significance with a larger sample size. Two participants in the low-response group had baseline walking speeds of greater than 0.7 m/s but showed no increases in walking speed after the intervention (Fig. 2A). These 2 participants had baseline Fugl-Meyer motor scale scores of 23 and 25, suggesting that they had achieved relatively high baseline walking speeds through compensatory strategies 44,45 but might have had limited capacity for further improvement. Norton and Gorassini 46 also found that the response to BWSTT in people with incomplete spinal cord injury was related to the amount of preserved corticospinal drive. However, lowerextremity Fugl-Meyer motor scale scores would not have been sufficiently discriminating to predict individual responses because the scores of both groups overlapped considerably (Fig. 2B). Limitations This exploratory study had several limitations. The small sample size increased the possibility of a type II statistical error limiting the ability to detect true changes. Analysis of effect sizes could identify comparisons that likely would have reached statistical significance with a larger sample. Moreover, conducting multiple comparisons increased the probability of a type I statistical error; consequently, the results must be viewed with caution. However, the inclusion of variables from multiple domains (kinematic, kinetic, and muscle activation) provided evidence about the gait parameters that were associated with improved walking speeds as well as an indication about how the changes occurred. Because of the low statistical power, correcting for the number of comparisons would have been overly conservative and likely would have eliminated many valid results along with any type I errors. A comparison of the changes in gait parameters between participants in the highresponse group and participants in the low-response group controlled for variability and learning associated with repeated testing. The differences in joint angle changes between the groups were modest (6.8 at the hip and 4.2 at the ankle) but exceeded the average error associated with repeated testing of sagittalplane motion during walking (2 3 at the ankle and 2 5 at the hip). 47 Measurement error would be expected to vary equally in either direction and irrespective of group membership. Only the paretic leg was evaluated, and only kinematic and kinetic variables in the sagittal plane were examined. However, gluteus medius muscle activation was studied, and this muscle, with primarily frontalplane function, did not show a change in the intensity of activation in either group. Moreover, all gait trials were conducted without the use of any lower-extremity orthosis. The BWSTT interventions also were conducted without bracing, but 6 participants (3 in the low-response group and 3 in the high-response group) customarily wore an anklefoot orthosis during community ambulation. We based our decision to record gait biomechanics without the orthosis to avoid the potential for masking any distal changes, particularly activation of the anterior tibialis muscle. However, the participants who customarily walked with the an- February 2010 Volume 90 Number 2 Physical Therapy f 221

14 kle orthosis might have exhibited greater increases in walking speed after the intervention with the distal stabilization of the brace. Finally, we recorded maximal torque only with isometric contractions in isolated positions. Changes in muscle strength at higher speeds or in synergy patterns might not have been reflected in the isometric tests. Conclusion Participants who responded to a 6-week (24-session) intervention including BWSTT not only showed increases in walking speed but also showed improvements in gait biomechanics and muscle activation consistent with improved forward propulsion during walking. Participants who exhibited clear increases in walking speed after the intervention did so with increased activation of both the soleus muscle and the semimembranosus muscle during walking that was sufficient to reduce the anterior tilt of the pelvis and extend the thigh during terminal stance and that tended to increase plantar flexion during pre-swing. These kinematic changes resulted in increased hip flexion power generation and a tendency toward increased plantarflexion power generation. Thus, stabilization of the limb during stance was increased both distally and proximally. [Readers may want to compare the results of this intervention, which Reisman et al 48 in this issue discuss as motor learning, to the results from intervention using the split-belt treadmill ( motor adaptation ).] Of all of the baseline participant characteristics, only the lowerextremity Fugl-Meyer motor scale score was significantly higher in participants with a positive response to the intervention, suggesting that significant improvements after the intervention were dependent on a threshold capacity for selective motor control. The present study provided preliminary evidence that a task-specific lower-extremity training program that includes BWSTT can promote improved gait biomechanics and neural adaptation in people who have stroke but who have sufficient hemiparetic lowerextremity motor control. Dr Mulroy, Dr Gronley, Dr Brown, and Dr Sullivan provided concept/idea/research design. Dr Mulroy, Ms Klassen, Dr Brown, and Dr Sullivan provided writing and project management. Ms Klassen and Ms Eberly provided data collection. All authors provided data analysis. Dr Brown and Dr Sullivan provided fund procurement. Ms Klassen provided participants. Dr Mulroy provided facilities/equipment. Dr Sullivan provided institutional liaisons. Ms Klassen, Dr Gronley, Ms Eberly, Dr Brown, and Dr Sullivan provided consultation (including review of manuscript before submission). The authors acknowledge the STEPS Research Team: University of Southern California Robbin Howard, PT, DPT, NCS, Didi Matthews, PT, DPT, NCS, Bernadette Currier, PT, DPT, NCS, Arlene Yang, PT, MSPT, NCS, Barbara Lopetinsky, PT, BS, and Maria Caro, PT, DPT; Northwestern University Nicole Furno, PT, BS, Nicole Korda, PT, BS, Carolina Carmona, PT, BS, Allie Hyngstrom, PT, MSPT, Sheila Schindler-Ivens, PT, PhD, and Lynn Rogers, MS; and Rancho Los Amigos National Rehabilitation Center Craig Newsam, PT, DPT, Valerie J. Eberly, PT, NCS, JoAnne K. Gronley, PT, DPT, Jennifer Whitney, PT, MPT, Betsy King, PT, DPT, and Louis Ibarra, PTA. The authors acknowledge the Foundation for Physical Therapy for funding the Physical Therapy Clinical Research Network (PTClinResNet). The PTClinResNet Network Principal Investigator is Carolee J. Winstein, PT, PhD, FAPTA, and the Co-Principal Investigator is James Gordon, PT, EdD, FAPTA (both at University of Southern California, Los Angeles, California). Project Principal and Co-Principal Investigators include David A. Brown, PT, PhD (Northwestern University, Chicago, Illinois); Sara J. Mulroy, PT, PhD, and Bryan Kemp, PhD (Rancho Los Amigos National Rehabilitation Center, Downey, California); Loretta M. Knutson, PT, PhD, PCS (Missouri State University, Springfield, Missouri); Eileen G. Fowler, PT, PhD (University of California, Los Angeles, Los Angeles, California); and Sharon K. DeMuth, PT, DPT, Kornelia Kulig, PT, PhD, and Katherine J. Sullivan, PT, PhD (University of Southern California, Los Angeles, California). The Data Management Center is located at the University of Southern California and is directed by Stanley P. Azen, PhD. The members of the Data Safety and Monitoring Committee are Nancy Byl, PT, PhD, FAPTA, Chair (University of California, San Francisco, San Francisco, California); Hugh G. Watts, MD (Shriners Hospital for Children LA Unit, Los Angeles, California); June Isaacson Kailes, MSW (Western University of Health Sciences, Pomona, California); and Anny Xiang, PhD (University of Southern California, Los Angeles, California). The authors acknowledge Biodex Medical Systems Inc, which donated 3 Cyclocentric semirecumbent ergometers used in the Strength Training Effectiveness Post-Stroke (STEPS) study. This research study was approved by the Institutional Review Board of Los Amigos Research and Education Institute. Parts of the data were presented as a poster at the Combined Sections Meeting of the American Physical Therapy Association; January 31 February 4, 2006; San Diego, California; and as part of an accepted symposium at the Combined Sections Meeting of the American Physical Therapy Association; February 14 18, 2007; Boston, Massachusetts. A case study of 1 of the participants was given as a platform presentation at the III STEP Conference: Linking Movement Science and Intervention; July 15 21, 2005; Salt Lake City, Utah. Data in these presentations were from all 4 of the STEPS intervention groups; data in this article were from those participants in 1 of the 3 interventions that included body-weight supported treadmill training. This article was received May 1, 2009, and was accepted August 13, DOI: /ptj References 1 Heart Disease and Stroke Statistics 2009 Update. Dallas, TX: American Heart Association; 2009: Harris JE, Eng JJ. Goal priorities identified by individuals with chronic stroke: implications for rehabilitation professionals. Physiother Can. 2004;56: Jorgensen HS, Nakayama H, Raaschou HO, Olsen TS. Recovery of walking function in stroke patients: The Copenhagen Stroke Study. Arch Phys Med Rehabil. 1995;76: Laufer Y, Dickstein R, Chefez Y, Marcovitz E. 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