Participants
Fifteen individuals with chronic stroke (67.7±7.22 yrs; 5 females; time since stroke 12±12 yrs; 4 right paretic; CMSA score of the leg 4.9 ± 1.3 and foot 3.7 ± 1.8) and fifteen age-matched able-bodied controls (67.7±5.87 yrs; 4 females; 13 right dominant) participated in the study (Table 1). The inclusion criteria were: 1) Hemiparesis as a result of a stroke greater than 6 months prior to the study for participants with stroke; 2) Able to walk 10 meters with or without a walking aid; and 3) Able to stand unsupported for 5 minutes. Controls were included if they had no self-reported history of a neurological injury or condition. The exclusion criteria were: 1) unable to follow instructions; 2) medical conditions beyond the effects of the stroke precluding participation in regular exercise; and 3) pregnancy. The study was approved by the Institutional Review Board of the University of Maryland Baltimore and all participants provided written informed consent to participate.
Testing procedure
Clinical Assessment: All participants completed the clinical Step Test (ST) and Four-Square Step Test (FSST) to assess balance and mobility. A transfer belt was worn by all participants performing the clinical tests to ensure their safety. During the ST, participants stood 5 cm from the step, placed one foot onto a 7.5-cm-high step and then returned it to the floor. Participants repeated this movement as fast as possible for 15 seconds (30). The number of steps completed in the 15-second period was recorded. Participants performed two trials stepping on and off of the step using the paretic limb (non-dominant leg stepping for control), and the trial with the greatest number of steps was used for analysis. ST has been previously shown to have excellent test-retest reliability (30) and is responsive to change during rehabilitation in people post-stroke (31). In addition, among several clinical measures, the ST has been found to have moderately strong association with peak vertical ground reaction forces measured from force platforms beneath the paretic limb (r2 = 0.76) (11).
During the FSST, participants completed a rapid sequential stepping task clockwise and counterclockwise while avoiding four canes arranged in a cross pattern on the floor with the tips of the canes facing together. The test procedure was demonstrated, and one practice trial was performed prior to administering the test. Two trials were performed, and the best time was taken as the score. The FSST involves the time-dependent capacity to limb loading during stepping in multiple directions and has been shown to be an effective and valid tool for measuring dynamic balance (32).
The Chedoke McMaster Stroke Assessment Impairment Inventory (CMSA) leg and foot subscales assessed motor recovery. The CMSA score describes the motor recovery by assessing the range of motion, ability to move in and out of synergistic patterns, and capacity to generate rapid movements. The score ranges from 1-7, with 7 representing full recovery and the ability to perform rapid complex joint movements.
Figure 1. Unilateral platform perturbation system (A) induced lateral tilt of the body and forced vertical weight-bearing (B).
Imposed Weight Transfer Assessment: All participants wore a safety harness during the imposed weight transfer assessment. Two movable platforms (height~37 cm) were placed adjacent to each other (see Fig.1). Participants stood with one foot on each platform. Each of the standing platforms was held securely to the support structure using ten electromagnets (12 V DC, Magnetech Corp). Disengagement of the magnets, via computer control, released the support surface causing it to drop 4.3 cm vertically. A layer of carpet was glued on the bottom of the drop surface and a foam pad (thickness ~ 5mm) was placed between the platform and the force plate to reduce the impact sound to less than 70 dB, below the threshold know to elicit a startle response (33,34). Participants were instructed to stand naturally with their weight evenly distributed on each leg. An investigator monitored the vertical ground reaction forces that were depicted on the screen to ensure an approximate symmetrical weight-bearing at the start of each trial. Two familiarization trials (one trial for each side) were provided for each participant. Next, four unilateral support surface lowering perturbation trials were delivered to each leg. The order of the drop was randomized. Participants were told to respond naturally to the drop to maintain their upright posture. An investigator stood in close proximity to the participant to assist as needed. The outline of each participant’s feet was traced to ensure the same initial position. Shoes were worn during the testing protocol, and individuals with ankle-foot orthoses (AFO) were allowed to keep the AFO on during the clinical tests if they felt it was necessary.
Data recording
Kinematic recordings: Body segment position data were recorded using a 10 camera Vicon acquisition system (Vicon-USA, Denver, CO). Reflective markers were placed on the forehead and bilaterally on the acromion process, lateral epicondyle of the humerus, distal end of the radius, anterior superior iliac spine, posterior superior iliac spine, greater trochanter (hip), lateral epicondyle of the femur (knee), lateral malleolus (ankle), second metatarsal, and heel. Signals were sampled at 120 Hz for 5 seconds and then low-pass filtered offline at 6 Hz.
Kinetic Recordings: Ground reaction forces and center of pressure (COP) data were measured using two AMTI force platforms (Advanced Mechanical Technology Inc., Watertown, MA) located beneath the standing platforms. Signals were sampled at 600 Hz for 5 seconds and then low-pass filtered offline at 30 Hz.
Data Analyses
Sagittal plane ankle and knee joint angular displacements and peak velocities were calculated during the shock absorption phase, which was defined as the time from maximal ankle plantarflexion to maximal dorsiflexion (see Figure 2). Inter-joint timing for flexion onset was calculated as the difference between knee flexion onset time and ankle dorsiflexion onset time (35,36). Similarly, inter-joint timing for flexion end timing was defined as the difference between knee flexion end timing and ankle dorsiflexion end timing. Knee flexion onset timing was defined as the instant where the knee flexion angle reached the first minimum following perturbation. Knee flexion end timing was defined as the instant where knee flexion reached the first maximum. Similarly, ankle dorsiflexion timing onset was defined as the instant where ankle dorsiflexion angle reached the first minimum. Ankle dorsiflexion end timing was defined as the instant where ankle dorsiflexion reached the first maximum. Maximum trunk and body COM displacement in vertical, anterior-posterior (AP), and medial-lateral (ML) directions were measured following perturbation. Body COM was estimated by calculating the average position between right and left anterior and posterior superior iliac spine (37). The trunk segment was defined by using bilateral iliac crest and the acromion process markers (38). Center of the trunk was determined as the average position between the acromion and the anterior and posterior superior iliac spine markers.
Vertical ground reaction force (VGRF) was normalized to bodyweight and used to determine perturbation onset and the amplitude of weight-bearing. In addition, VGRF at the end of the shock absorption phase and at the maximal weight- bearing was measured.
Stabilization time of the COP velocity (COPv) was defined as the time elapsed from initial ground contact to the instant that COPv settled within 3 standard deviations of its final stabilized value (as previously done in ground reaction forces stabilization analyses (39)). COP stabilization times in the medial-lateral (COPv,M-L) and the anterior-posterior (COPv,A-P) directions were calculated. In addition, maximal stabilization time (COPv,Max) was determined by selecting the greater value between COPv,M-L and COPv,A-P stabilization time (i.e. the longer time).
Data averaged across trials from the paretic limb in the stroke group and the non-dominant limb in the control group were compared using 2-tailed t-tests. In addition, COPv,M-L, COPv,A-P, and COPv,Max stabilization times were used in a bi-directional stepwise linear regression model to predict clinical ST and FSST testing scores. The significance level was set at an α of 0.05. All statistics were determined using SPSS (version 25.0, SPSS, Inc).
Figure 2. Representative data for vertical force (A), knee (B), and ankle (C) angular displacement for a control participant in a single trial. The area highlighted in red represents the shock absorption phase. DF: ankle dorsiflexion.