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 func-tion, 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 con-sisted 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 (high-response group) and in those with less improvement (low-(high-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 biomechan-ics during late stance were associated with greater increases in gait speed.S.J. Mulroy, PT, PhD, is Director, Pathokinesiology Laboratory, Ran-cho Los Amigos National Rehabil-itation Center, 7601 E Imperial Hwy, Bldg 800, Room 33, Downey, CA 90242 (USA). Ad-dress all correspondence to Dr Mulroy at: [email protected]. gov.
T. Klassen, MS, PT, NCS, is Clinical Instructor, Department of Physical Therapy, University of British Co-lumbia, Vancouver, British Colum-bia, Canada.
J.K. Gronley, PT, DPT, is Associate Director of Clinical Research, Pathokinesiology Laboratory, Ran-cho Los Amigos National Rehabil-itation Center.
V.J. Eberly, PT, NCS, is Research Physical Therapist, Pathokinesiol-ogy Laboratory, Rancho Los Ami-gos National Rehabilitation Center.
D.A. Brown, PT, PhD, is Associate Professor and Associate Chair for Post-Professional Education, De-partment of Physical Therapy and Human Movement Sciences; Asso-ciate Professor, Department of Physical Medicine and Rehabilita-tion; and Adjunct Faculty, Depart-ment of Biomedical Engineering, Northwestern University, Chi-cago, 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 sup-port after stroke: an exploratory study. Phys Ther. 2010;90:209 – 223.]
© 2010 American Physical Therapy Association
Perry Issue:
Gait Rehab
Post a Rapid Response or find The Bottom Line:
S
troke affects almost 1 person every 40 seconds and is the leading cause of serious, long-term disability in the United States.1Although physical therapists inter-vene with many facets of physical function, particular attention is fo-cused on improving walking ability because this is one of the most com-mon goals stated by people recover-ing from a stroke.2For 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 commu-nity ambulation.3
Evidence is building that for walking rehabilitation after stroke, innova-tions such as body-weight–sup-ported treadmill training (BWSTT) (ie, task-specific locomotor training) are more effective than approaches based on neurofacilitation or inhibi-tion of muscle activity, which were used by physical therapists in the 1980s and 1990s.4 – 6Task-specific
lo-comotor training has been associ-ated with increases in strength (force-generating capacity), endur-ance, and walking speed.7–9 These
global outcomes indicate functional changes but do not provide insights about the underlying neuromuscular
or biomechanical contributors to the therapeutic improvements. With fur-ther insights into underlying contrib-utors, interventions can be targeted to specific impairments with the ex-pectation of improved outcomes at greater efficiency.
Although many studies have demon-strated improved walking function
after BWSTT for people with
stroke,7–9 the biomechanical
param-eters 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.10 –12However, it is not known
whether BWSTT targets biomechani-cal functions that are uniquely af-fected by treadmill training and body-weight support.
There is limited evidence that walk-ing on a treadmill with body-weight support (compared with overground ambulation) results in immediate, short-term changes, including in-creased 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, bi-ceps femoris, and gluteus medius muscles.16 To our knowledge, no
studies have included instrumented gait analysis before and after a pro-gram of BWSTT to determine the bio-mechanical parameters underlying the long-term improvements seen in overground walking. Understanding the gait mechanics and muscle activ-ity patterns in people who respond well and in those who do not may suggest a different physiological ba-sis 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 re-sponsiveness to a task-specific inter-vention that included BWSTT and that was designed to improve loco-motor recovery after stroke. (In this issue, Kuo and Donelan17 review
the determinants of dynamic walk-ing.) The secondary objective was to identify the baseline participant characteristics and changes in lower-extremity maximal isometric torque and maximal muscle activation that were associated with responsiveness to the intervention. We hypothe-sized that, compared with people who showed little or no improve-ment in walking speed after the BWSTT interventions, people who responded to the BWSTT interven-tions (ie, people with significant postintervention increases in self-selected overground walking speed) would show improvements in kine-matic and kinetic parameters at the end of stance and at the stance-swing interface in the paretic hip and ankle joints; increased intensity of electro-myographic (EMG) activity of the pa-retic ankle plantar-flexor, hip exten-sor, and hip flexor muscles during walking; and increased maximal iso-metric 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 ran-domly assigned to 1 of 4 interven-tion groups: task-specific BWSTT
and upper-extremity ergometry
(UE Ex), locomotor strength train-ing (Cycle) and UE Ex, BWSTT and Cycle, and BWSTT and
muscle-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.
specific lower-extremity strength training (LE Ex).
An exploratory instrumented gait analysis to examine the biomechani-cal mechanisms associated with the STEPS interventions was conducted at Rancho Los Amigos National Re-habilitation Center. The first 5 partic-ipants from each exercise group (n⫽20) enrolled at the University of Southern California or Rancho Los Amigos National Rehabilitation Cen-ter underwent the instrumented gait analysis at baseline (after group ran-domization but before intervention) and after the 6-week BWSTT period.
All subjects read and signed an in-formed consent form that described the STEPS protocol approved by the institutional review board of each in-stitution; 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 signifi-cantly and similarly after each of the 3 BWSTT interventions but not after the Cycle–UE Ex intervention. There-fore, in the present study, we evalu-ated only data from the 15
partici-pants assigned to the 3 BWSTT-related groups (ie, BWSTT–UE Ex, BWSTT–Cycle, and BWSTT–LE Ex). The STEPS study design and the ad-ditional allocation specifically re-lated 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
partici-pants were 18 years of age or older; approximately 9 months to 5 years after the initial onset of an ischemic or hemorrhagic cerebrovascular ac-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.
cident; able to ambulate, at a self-selected walking speed of less than or equal to 1.0 m/s, at least 14 m with an assistive device, lower-extremity orthosis, or both and with the assistance of 1 person; and free from any serious medical, orthopedic, or premorbid condi-tion that would physically or cog-nitively 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
low-resistance upper-extremity ergom-etry. 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 exten-sor, plantar-flexor, hip flexor, knee flexor, and dorsiflexor muscles). Participants in all 3 intervention groups received the BWSTT ventions twice per week. This inter-vention 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 pri-mary STEPS study.18The BWSTT and
strengthening exercises were alter-nated over 4 days per week (exclud-ing weekends) for 6 weeks (for a total of 24 sessions). Each exercise session was 1 hour in duration and was conducted by a licensed physi-cal therapist.
Outcome Measures
Specific demographic and clinical data obtained from the baseline eval-uation of the STEPS study also were used to characterize the participants in the present study.18 These data
included participant demographics, stroke characteristics (including on-set), 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 lower-extremity orthoses but were permit-ted to use their customary assistive devices. Participants performed sev-eral practice walking trials to im-prove the likelihood of stepping with the tested foot landing entirely on the forceplate. Simultaneous re-cordings of foot-floor contacts, lower-extremity kinematics, and EMG activity were made as partici-pants 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 partici-pant’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. Foot-floor contact patterns were re-corded 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 partic-ipant’s hemiplegic lower extremity were documented by use of a Vicon Motion Analysis System.‡ Six infra-red, 50-Hz cameras recorded the
lo-cations of 14 retroreflective markers taped to the skin overlying the bony landmarks, including the midline sa-crum at the level of the posterior iliac spines, anterior superior iliac spines (bilaterally), greater trochan-ter, anterior thigh, medial and lateral femoral condyles, anterior tibia, me-dial 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 force-plate储embedded in the walkway. Intramuscular EMG recording was accomplished with indwelling, fine-wire electrodes inserted into the belly of each of 8 lower-extremity muscles (gluteus maximus, gluteus medius, semimembranosus, adduc-tor longus, rectus femoris, vastus in-termedius, soleus, and anterior tibia-lis muscles) using the technique of Basmajian and Stecko.19 Electrode
placement was confirmed by palpat-ing tension in the tendon or muscle belly during mild electrical stimula-tion through the inserted wires. Elec-tromyographic signals were trans-mitted 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 deter-mine the baseline threshold of myo-electric activity for each muscle at rest and during a 5-second resisted isometric maximal voluntary con-traction for normalization. Partici-pants performed a practice maximal contraction for each muscle before data collection.
* Biodex Medical Systems Inc, 20 Ramsay Rd, PO Box 702, Shirley, NY 11967.
†B & L Engineering, 3002 Dow Ave, Ste 416, Tustin, CA 92780.
‡Vicon Motion Systems, 14 Minns Business Pk, West Way, Oxford OX2 0JB, United King-dom.
§Digital Equipment Corp, 1 Kendall Sq, Cam-bridge, MA 02139
储Kistler Instrument Corp, 75 John Glenn Dr, Amherst, NY 14228-2171.
#Biosentry Telemetry Inc, 207–20G Earl St, Torrance, CA 90503.
Maximal isometric torque was re-corded with a Biodex dynamometer* for ankle dorsiflexion, ankle plantar flexion, and flexion and extension of both the hip and the knee. Partici-pants performed a practice submaxi-mal contraction and then 3 maxisubmaxi-mal- maximal-effort 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 plantar-flexion torque and in 15 degrees of plantar flexion for the ankle dorsi-flexion test. Knee torque testing was performed while the participant was sitting with the seat back reclined to 85 degrees. Torque for both isomet-ric 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 calcu-late walking speed, cadence, and stride length and to identify gait cy-cle timing. Each stride was time nor-malized 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 digi-tal Butterworth filter (20- and 4-Hz
cutoff frequencies, respectively). Ki-nematic data were processed with Adtech Motion Analysis Software** to produce 3-dimensional trajecto-ries for each marker. The position and orientation of each lower-extremity 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 co-ordinates. 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 deter-mined from the forceplate data.
Mea-sured body segment parameters
were used in conjunction with em-pirical 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 mo-ments by use of the inverse dynam-ics approach.21Joint 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 maxi-mal muscle contraction, and this value was used to calculate the av-erage 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 walking22;
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 nor-malization value, which was ap-proximately 20% of a full interfer-ence pattern, prevented inflation of EMG signals during walking in mus-cles in which a participant lacked sufficient volitional control to pro-duce a significant signal during manual muscle testing.22The
inten-sity of EMG activity was expressed as a percentage of the maximal vol-untary contraction.
Phasing of EMG activity during walking was determined with EMG Analyzer Software.†,23The EMG
An-alyzer identified the onset and ces-sation times (as a percentage of the gait cycle) for each packet of mus-cle activity that had an intensity of at least 5% of the maximal volun-tary 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 0.02-second interval. Any signal lower than this value was not considered functionally significant. Packets of EMG activity separated by quies-cent intervals of less than 5% of the gait cycle were combined. The av-erage intensity of activation be-tween onset and cessation was cal-culated for each muscle.23
Data Analysis
Participants were stratified into ei-ther a high-response group or a low-response group on the basis of the magnitude of the change in self-selected walking speed between the baseline and postintervention ses-sions. Participants in the high-response 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 ** Adtech Inc, 3465 Waialae Ave, Ste 200,
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.24 –27
We tested the specific hypotheses
that participants who showed
greater improvements in
self-selected walking speed
(high-response group) after completing a 24-session program of task-specific locomotor training and strength training designed to improve walk-ing recovery would show the fol-lowing biomechanical changes in the hemiparetic lower extremity (compared with participants who showed minimal or no
improve-ments in walking speed
[low-response group]): increased hip extension angle, hip flexion mo-ment, and hip flexion power at ter-minal stance–pre-swing; increased
flexion angle and plantar-flexion power at terminal stance– pre-swing; increased intensity of EMG activity of the ankle plantar-flexor, 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 plantar-flexor muscles.
Two-way repeated-measures analysis-of-variance models were used to de-termine the interaction effects of group (high-response group and low-response group) and time (be-fore intervention and after interven-tion) for spatiotemporal characteris-tics; peak values for paretic lower-extremity joint motion, moment, and power; and average intensities of EMG activity of paretic lower-extremity muscles during walking. The main effect of time was evalu-ated 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 test-ing of each of the 8 muscles at the baseline and postintervention tests. The baseline clinical characteristics of the 2 response groups were com-pared by use of an independentttest or a chi-square test for categorical data. APvalue 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 walk-ing speed of greater than 0.08 m/s (high-response group) after the 24 exercise sessions, and 8
partici-pants 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 01906.
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.
nificant differences between the high-response group and the low-response group with respect to age, sex, time since stroke, intervention group, baseline self-selected walk-ing speed, or assistive device use
(Tab. 1). The baseline
lower-extremity 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 high-response group after the interven-tion was 0.153 m/s (SD⫽0.056); the increase in participants in the
low-response group was 0.017 m/s
(SD⫽0.034) (Tab. 2). Both cadence Table 1. Participant Characteristics Characteristic Participants P Effect Size All (Nⴝ15) High-Response Group (nⴝ7) Low-Response Group (nⴝ8) Age (y) .90 0.03 X (SD) 58.47 (14.86) 58.25 (13.00) 58.71 (17.83) Range 35–80 35–76 37–80
Sex 7 women, 8 men 3 women, 4 men 4 women, 4 men .78 0.04
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) .20 0.65
X (SD) 0.50 (0.24) 0.58 (0.18) 0.43 (0.27)
Range 0.11–0.93 0.40–0.90 0.11–0.93
Mo since stroke .72 0.15
X (SD) 25.43 (15.46) 25.57 (14.92) 23.23 (16.79)
Range 9.26–57.20 12.85–57.20 9.26–55.39
Baseline lower-extremity Fugl-Meyer motor scale score .02a 1.35
X (SD) 25.87 (4.69) 28.71 (3.60) 23.50 (4.11)
Range 17–34 25–34 16–30
Assistive device (no. of participants using the indicated device)
None (6) None (4) None (2) .21 0.91
Single cane (3) Single cane (1) Single cane (2)
Quad cane (5) Quad cane (2) Quad cane (3)
Single crutch (1) Single crutch (1)
aStatistically significant.
Table 2.
Baseline Values and Changes in Spatiotemporal Characteristics of Walking
Characteristic Participants P Effect Size High-Response Group (nⴝ7)a Low-Response Group (nⴝ8)a Speed (m/s) .001 2.94 Baseline 0.580 (0.177) 0.426 (0.275) Change ⫹0.153 (0.056) ⫹0.017 (0.034) Cadence (steps/min) .02 1.35 Baseline 76.70 (13.72) 63.69 (18.44) Change ⫹7.77 (4.88) ⫹1.51 (4.37) Stride length (m) .01 1.72 Baseline 0.891 (0.126) 0.744 (0.311) Change ⫹0.129 (0.048) ⫹0.022 (0.074)
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 ex-tension angle (⫹6.8° [SD⫽5.7] ver-sus⫺0.6° [SD⫽6.4]) (Tab. 3, Fig. 3A) and in hip flexor muscle power during stance (⫹0.195 W/kg䡠m [SD⫽0.18) versus ⫹0.004 W/kg䡠m [SD⫽0.09]) (Fig. 3B); these differ-ences were statistically significant (P⫽.02). In contrast, the increases in the peak thigh extension angle
(rel-ative to laboratory vertical) in both groups were nearly identical (⫹2.1° versus⫹2.5°), indicating that the dif-ferences in the hip extension angle between the groups reflected de-creased anterior pelvic tilt in the high-response group and increased anterior pelvic tilt in the low-response group.
Table 3.
Baseline Values and Changes in Peak Hip Joint Angles, Moments, and Power During Walking
Measurement Participants P Effect Size High-Response Group (nⴝ7)a Low-Response Group (nⴝ8)a
Hip flexion angle during loading (°) .12 0.85
Baseline 29.6 (8.21) 26.09 (8.49)
Change ⫺2.16 (5.84) ⫹2.73 (5.66)
Hip extension angle during stance (°) .04 1.23
Baseline ⫺1.99 (3.95) ⫺3.68 (10.70)
Change ⫹6.79 (5.66) ⫹0.63 (6.41)
Thigh extension angle during stance (°) .85 0.10
Baseline ⫺15.06 (6.16) ⫺9.43 (6.17)
Change ⫹2.10 (3.98) ⫹2.53 (4.26)
Hip flexion angle during swing (°) .07 1.00
Baseline 31.05 (6.08) 25.99 (8.01)
Change ⫺1.59 (6.57) ⫹4.47 (5.54)
Thigh flexion angle during swing (°) .83 0.11
Baseline 17.86 (5.89) 20.58 (7.90)
Change ⫹2.98 (4.94) ⫹2.52 (3.41)
Medial (internal) hip extension moment during loading (N䡠m/kg䡠m) .20 0.70
Baseline 0.340 (0.211) 0.363 (0.292)
Change ⫹0.109 (0.236) ⫺0.050 (0.218)
Medial (internal) hip flexion moment during stance (N䡠m/kg䡠m) .09 0.92
Baseline ⫺0.364 (0.120) ⫺0.347 (0.252)
Change ⫺0.144 (0.230) ⫹0.028 (0.128)
Hip extension power generation during loading (W/kg䡠m) .64 0.25
Baseline 0.309 (0.302) 0.221 (0.309)
Change ⫹0.116 (0.392) ⫹0.043 (0.144)
Hip flexion power absorption during stance (W/kg䡠m) .24 0.62
Baseline ⫺0.167 (0.167) ⫺0.196 (0.268)
Change ⫺0.201 (0.325) ⫺0.045 (0.139)
Hip flexion power generation during pre-swing (W/kg䡠m) .02 1.34
Baseline 0.268 (0.231) 0.168 (0.160)
Change ⫹0.195 (0.18) ⫹0.004 (0.09)
The peak ankle plantar-flexion angle during initial double-limb support (loading) increased more in partici-pants in the high-response group (⫹2.8° [SD⫽2.7]) than in partici-pants in the low-response group (⫺1.6° [SD⫽3.9]) (P⫽.03) (Tab. 4, Fig. 3C). In terminal double-limb sup-port (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 plantar-flexion power (⫹0.219 W/kg䡠m [SD⫽0.236] versus ⫹0.026 W/kg䡠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 andP⫽.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 partici-pants 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 mus-cle activation during manual musmus-cle testing from the preintervention gait analysis to the postintervention gait analysis were not significantly differ-ent (no significant interaction be-tween time and group) bebe-tween the high-response group and the low-response 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 statis-tically significant. For both groups, the intensity of semimembranosus 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. Preinter-vention data are represented by dashed lines, and postinterPreinter-vention 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 plantar-flexion motion and power generation also tended to be greater in the high-response group.Asterisk indicates significant atP⬍.05.
muscle EMG activity after the inter-vention was significantly higher than that before the intervention. Maxi-mal activation during manual muscle testing before the intervention was 68.8 mV (SD⫽15.6), and that after the intervention was 131.0 mV (SD⫽51.5) (P⬍.01, effect size⫽1.63). Average EMG intensity of semimem-branosus 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 high-response group than in participants in the low-response group (⫹9.0 N䡠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 self-selected 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 Table 4.
Baseline Values and Changes in Peak Ankle Joint Angles, Moments, and Power During Walking
Measurement Participants P Effect Size High-Response Group (nⴝ7) Low-Response Group (nⴝ8)
Plantar-flexion angle during loading (°) .03 1.32
Baseline 11.21 (3.91) 11.00 (5.59)
Change ⫹2.83 (2.72) ⫺1.60 (3.90)
Dorsiflexion angle during stance (°) .26 0.62
Baseline 9.67 (3.56) 7.66 (6.70)
Change ⫺2.10 (2.05) ⫺0.31 (3.56)
Plantar-flexion angle during pre-swing (°) .09 0.97
Baseline 4.14 (3.78) 1.56 (3.93)
Change ⫹4.23 (3.75) ⫹0.04 (4.85)
Dorsiflexion angle during swing (°) .06 1.08
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䡠m/kg䡠m) .45 0.39
Baseline ⫺0.041 (0.057) ⫺0.027 (0.039)
Change ⫺0.021 (0.047) ⫺0.004 (0.040)
Medial (internal) plantar flexion moment during stance (N䡠m/kg䡠m) .16 0.77
Baseline 0.753 (0.150) 0.512 (0.194)
Change ⫹0.032 (0.111) ⫹0.114 (0.103)
Dorsiflexion power absorption during loading (W/kg䡠m) .99 0.01
Baseline ⫺0.181 (0.055) ⫺0.121 (0.047)
Change ⫺0.071 (0.167) ⫺0.070 (0.070)
Plantar-flexion power absorption during stance (W/kg䡠m) .62 0.26
Baseline ⫺0.458 (0.183) ⫺0.326 (0.242)
Change ⫺0.075 (0.191) ⫺0.029 (0.158)
Plantar-flexion power generation during pre-swing (W/kg䡠m) .08 0.98
Baseline 0.504 (0.432) 0.249 (0.219)
Change ⫹0.219 (0.236) ⫹0.026 (0.146)
late stance in participants in the high-response group was attribut-able to a combination of increased thigh extension and decreased ante-rior pelvic tilt. In contrast, partici-pants in the low-response group showed increased anterior pelvic tilt. Participants in the high-response group exhibited a tendency toward greater increases in ankle plantar-flexion 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 flex-ion power also were identified as the
mechanisms used to increase walk-ing speed in both people who were able-bodied28and people with stroke
after traditional interventions.29,30
Also in agreement with the results of the present study, Jonsdottir and col-leagues31reported 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 in-crease in activation during walking in participants in the high-response group than in participants in the low-response group. Although the soleus muscle is a uniarticular muscle cross-ing only the ankle joint, musculoskel-etal models have determined that its activity, in addition to providing an-kle plantar flexion and forward pro-pulsion of the trunk,33 also
acceler-ates both the hip and the knee into extension during the second half of stance.34 This description is
consis-tent with the improved mechanics 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.
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 low-response group could be explained by neural factors, such as the size and location of the stroke lesion. Corroborating evidence for this ex-planation was documented in a pre-vious 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).35Her minimal
improvements in walking speed af-ter BWSTT were associated with in-creased motion at the hip but little change at the ankle.35Magnetic
res-onance imaging after the stroke re-vealed 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 ex-tent of improvements in walking speed, showed increases in activa-tion of the semimembranosus mus-cle during both manual musmus-cle testing and walking. A closer exami-nation of the EMG profiles of partic-ipants in the high-response and low-response groups before and after the intervention indicated that partici-pants in the high-response group showed increased intensity of semi-membranosus 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 semimem-branosus muscle activation in early swing actually would inhibit swing limb advancement by resisting thigh flexion.36
The hamstring muscles are biarticu-lar hip extensor and knee flexor mus-cles during isolated voluntary con-tractions. During walking, the hamstring muscles function primar-ily 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
attach-ment of the hamstring muscles on the ischial tuberosity also results in posterior tilting of the pelvis, partic-ularly 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 inter-vention only for participants in the high-response group. However, hip extension torque was not signifi-cantly improved in participants in ei-ther group. Hip extension torque likely was more reflective of torque generation of the uniarticular hip ex-tensor muscles (gluteus maximus, gluteus medius, and adductor mag-nus muscles) because the resistance cuff was placed proximal to the knee and the knee was flexed with mini-mal support of the lower leg. In con-trast, the hamstring muscles are the primary contributors to isolated knee flexion torque.32 Thus, it is
likely that although all of the partic-ipants showed increased activation of the semimembranosus muscle during walking, increased strength in this muscle group was seen only in participants with a greater in-crease in walking speed.
We did not find evidence of in-creased EMG intensity of either of the hip flexor muscles studied (ad-ductor longus and rectus femoris muscles). We did not expect that
in-creased rectus femoris muscle activa-tion would correspond to increased walking speed because of its role in knee extension, which would inhibit knee flexion during swing. In con-trast to the findings of the present study, increased activation of the ad-ductor longus and soleus muscles was strongly associated with im-proved walking speeds over the first 6 months after stroke in 2 other stud-ies.22,39 It is possible that other hip
flexor muscles, including the ilio-psoas, sartorius, and gracilis muscles, contributed to the increased hip flexor muscle power generation seen in participants in the high-response 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 cre-ated by the increased hip extension angle during late stance. The hip ad-ductor 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 in-crease the elastic energy storage and release of the passive joint structures of the hip, reducing the amount of work required of the hip flexor mus-cles 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 find-ing is consistent with the overall re-sults of the STEPS trial.18Among the
3 interventions that included BWSTT in the STEPS trial, increases in max-imal torque were seen only for the combined flexor muscles of the pa-retic limb and the combined exten-sor muscles of the nonparetic limb and only in the BWSTT–UE Ex
group. Lower-extremity torque was not increased in the other 2 BWSTT-related groups, although walking speed was increased to similar de-grees in all 3 BWSTT-related groups. Strength gains in the knee flexor muscle group for the other 2 BWSTT-related groups in the STEPS trial might have been masked by combin-ing all of the flexor torque values into 1 variable. Taken together, the results of these studies indicated that the observed improvements in walk-ing speed were not dependent on the strength gains for most of the muscle groups.
Instead, the observed improvements in walking speed and muscle activa-tion in the present study are more consistent with neural adaptation. Several studies have provided evi-dence of neural plasticity in people with stroke after BWSTT, including increased corticomotor excitability and activation40,41and increased
ac-tivation of cortical and subcortical networks.42,43 Our study is the first
to identify the specific long-term changes in muscle activation that ac-company improved biomechanics of overground walking after BWSTT. Implications for Clinical Practice On the basis of the results of the present study, we recommend em-phasizing hip extension in late stance during BWSTT and training at increased walking speeds to facili-tate more rapid and appropriately phased muscle activation. Hornby and colleagues9showed that BWSTT
with manual facilitation produced greater improvements in walking function than robot-supported tread-mill training after stroke. The ability to facilitate specific components of walking mechanics, such as in-creased hip extension with de-creased anterior pelvic tilt, likely is more feasible with manual guidance than with mechanical support.
The lower-extremity Fugl-Meyer mo-tor scale score was the baseline char-acteristic that best differentiated par-ticipants in the high-response group from those in the low-response group. Participants in the high-response group had greater selective motor control at baseline. The ex-tent 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 strategies44,45 but
might have had limited capacity for further improvement. Norton and Gorassini46 also found that the
re-sponse to BWSTT in people with in-complete spinal cord injury was re-lated to the amount of preserved corticospinal drive. However, lower-extremity Fugl-Meyer motor scale scores would not have been suffi-ciently discriminating to predict in-dividual responses because the scores of both groups overlapped considerably (Fig. 2B).
Limitations
This exploratory study had several limitations. The small sample size in-creased the possibility of a type II statistical error limiting the ability to detect true changes. Analysis of ef-fect sizes could identify comparisons that likely would have reached statis-tical significance with a larger sam-ple. Moreover, conducting multiple comparisons increased the probabil-ity of a type I statistical error; conse-quently, the results must be viewed with caution. However, the inclu-sion of variables from multiple
do-mains (kinematic, kinetic, and mus-cle 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, correct-ing for the number of comparisons would have been overly conserva-tive and likely would have elimi-nated many valid results along with any type I errors. A comparison of the changes in gait parameters be-tween participants in the high-response group and participants in the low-response group controlled for variability and learning associated with repeated testing. The differ-ences in joint angle changes be-tween the groups were modest (6.8° at the hip and 4.2° at the ankle) but exceeded the average error associ-ated with repeassoci-ated testing of sagittal-plane motion during walking (2°–3° at the ankle and 2°–5° at the hip).47
Measurement error would be ex-pected to vary equally in either di-rection and irrespective of group membership.
Only the paretic leg was evaluated, and only kinematic and kinetic vari-ables in the sagittal plane were ex-amined. However, gluteus medius muscle activation was studied, and this muscle, with primarily frontal-plane 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 ankle-foot orthosis during community am-bulation. We based our decision to record gait biomechanics without the orthosis to avoid the potential for masking any distal changes, particu-larly activation of the anterior tibialis muscle. However, the participants who customarily walked with the
an-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 po-sitions. Changes in muscle strength at higher speeds or in synergy pat-terns might not have been reflected in the isometric tests.
Conclusion
Participants who responded to a 6-week (24-session) intervention cluding BWSTT not only showed in-creases in walking speed but also showed improvements in gait biome-chanics and muscle activation con-sistent with improved forward pro-pulsion 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 semi-membranosus muscle during walk-ing that was sufficient to reduce the anterior tilt of the pelvis and extend the thigh during terminal stance and that tended to increase plantar flex-ion during pre-swing. These kine-matic changes resulted in increased hip flexion power generation and a tendency toward increased plantar-flexion power generation. Thus, stabilization of the limb during stance was increased both distally and proximally. [Readers may want to compare the results of this inter-vention, which Reisman et al48 in
this issue discuss as “motor learn-ing,” to the results from intervention using the split-belt treadmill (“motor adaptation”).]
Of all of the baseline participant characteristics, only the lower-extremity Fugl-Meyer motor scale score was significantly higher in par-ticipants with a positive response to the intervention, suggesting that sig-nificant improvements after the in-tervention were dependent on a threshold capacity for selective mo-tor control. The present study
pro-vided preliminary evidence that a task-specific lower-extremity train-ing program that includes BWSTT can promote improved gait biome-chanics and neural adaptation in people who have stroke but who have sufficient hemiparetic lower-extremity motor control.
Dr Mulroy, Dr Gronley, Dr Brown, and Dr Sullivan provided concept/idea/research de-sign. Dr Mulroy, Ms Klassen, Dr Brown, and Dr Sullivan provided writing and project management. Ms Klassen and Ms Eberly pro-vided data collection. All authors propro-vided data analysis. Dr Brown and Dr Sullivan vided fund procurement. Ms Klassen pro-vided participants. Dr Mulroy propro-vided facil-ities/equipment. Dr Sullivan provided institutional liaisons. Ms Klassen, Dr Gronley, Ms Eberly, Dr Brown, and Dr Sullivan pro-vided consultation (including review of manuscript before submission).
The authors acknowledge the STEPS Re-search Team:University of Southern Califor-nia—Robbin Howard, PT, DPT, NCS, Didi Matthews, PT, DPT, NCS, Bernadette Cur-rier, 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; andRancho Los Ami-gos National Rehabilitation Center—Craig Newsam, PT, DPT, Valerie J. Eberly, PT, NCS, JoAnne K. Gronley, PT, DPT, Jennifer Whit-ney, PT, MPT, Betsy King, PT, DPT, and Louis Ibarra, PTA.
The authors acknowledge the Foundation for Physi-cal Therapy for funding the Physical Therapy Clin-ical Research Network (PTClinResNet). The PTClinResNet Network Principal Investigator is Carolee J. Winstein, PT, PhD, FAPTA, and the Co-Principal Investigator is James Gor-don, PT, EdD, FAPTA (both at University of Southern California, Los Angeles, California). Project Principal and Co-Principal Investiga-tors include David A. Brown, PT, PhD (North-western 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 Uni-versity, Springfield, Missouri); Eileen G. Fowler, PT, PhD (University of California, Los Angeles, Los Angeles, California); and Sha-ron K. DeMuth, PT, DPT, Kornelia Kulig, PT, PhD, and Katherine J. Sullivan, PT, PhD
(Uni-versity of Southern California, Los Angeles, California). The Data Management Center is located at the University of Southern Califor-nia and is directed by Stanley P. Azen, PhD. The members of the Data Safety and Moni-toring Committee are Nancy Byl, PT, PhD, FAPTA, Chair (University of California, San Francisco, San Francisco, California); Hugh G. Watts, MD (Shriners’ Hospital for Chil-dren–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 Re-search and Education Institute.
Parts of the data were presented as a poster at the Combined Sections Meeting of the American Physical Therapy Association; Jan-uary 31–FebrJan-uary 4, 2006; San Diego, Cali-fornia; and as part of an accepted sympo-sium at the Combined Sections Meeting of the American Physical Therapy Association; February 14 –18, 2007; Boston, Massachu-setts. A case study of 1 of the participants was given as a platform presentation at the III STEP Conference: Linking Movement Sci-ence and Intervention; July 15–21, 2005; Salt Lake City, Utah. Data in these presenta-tions were from all 4 of the STEPS interven-tion groups; data in this article were from those participants in 1 of the 3 interventions that included body-weight–supported tread-mill training.
This article was received May 1, 2009, and was accepted August 13, 2009.
DOI: 10.2522/ptj.20090141
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