Gait & Posture 87 (2021) 177–183

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Gait & Posture

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Full length article

Effects of bi-axial ankle strengthening on muscle co-contraction during gait

in chronic stroke patients: A randomized controlled pilot study
Ji-Eun Cho a, Wan-Hee Lee b, Joon-Ho Shin c, Hogene Kim a, *
a
National Rehabilitation Research Institute, National Rehabilitation Center, Seoul, South Korea
b
Department of Physical Therapy, Sahmyook University College of Health Science, Seoul, South Korea
c
National Rehabilitation Hospital, National Rehabilitation Center, Seoul, South Korea

A R T I C L E I N F O A B S T R A C T

Keywords: Introduction: Ankle dysfunction in patients with stroke is a common but serious cause of balance and gait im­
Ankle pairments. However, comprehensive paretic ankle training seldom exists. Thus, we investigated the effects of a
Strengthening bi-axial ankle muscle training program using visual feedback as a means to improve ankle strength and per­
Coactivation
formance of functional activities in patients with stroke.
Feedback
Methods: This study was a randomized controlled pilot trial with concealed allocation and assessor blinding and
Gait
Stroke intention-to-treat analysis. Twenty-five patients with stroke and difficulty in walking (e.g., foot drop) or ankle
muscle weakness receiving inpatient rehabilitation were included. The experimental group underwent ankle
muscle training consisting of passive stretching, control of ankle muscles, and active-resistive strengthening
using visual feedback for 40 min per day, 5 times per week for 4 weeks. The control group underwent ankle-
related physical therapy, including ankle range-of-motion exercises. The amount of time for training was
equal between the two groups. The outcome measurements were isometric ankle contraction force to assess the
strength of ankle muscles, ankle proprioception, Fugl–Meyer lower extremity score, Berg balance scale score,
walking speed, and ankle co-contraction index to assess muscle efficiency during gait.
Results: The analysis revealed significant between-group differences in the ankle muscle strength in each di­
rection (P < 0.05), Fugl–Meyer score (P < 0.01), and stance-phase co-contraction index (P < 0.05). After
training, the experimental group displayed significant within-group differences in the strength of the ankle
muscles in each direction (P < 0.01), ankle proprioception (P < 0.05), and walking speed (P < 0.05).
Conclusions: Our findings demonstrate the significant short-term effects of ankle muscle training on strength,
walking speed, and muscle efficiency in patients with chronic stroke.

1. Introduction prominent than impairments of other proximal lower muscles; thus,

One of the most notable lower limb impairments after the develop­
ment of central nervous system disorders, such as stroke, is the inability
of the ankle joint to yield normal levels of muscle force. In a functional
task, such as locomotion, muscle weakness of the ankle muscles is
associated with reduced plantar flexion at the end of the stance phase
and reduced dorsiflexion at the swing phase [1]. In particular, reduced
forward propulsion owing to weakness of the plantar flexors can reduce
the walking speed, and decreased dorsiflexion can lead to injurious falls
[2]. Weakness of the ankle muscles in patients with stroke is more
affected patients often continuously need ankle–foot orthoses after
discharge, which may inhibit their performance of daily activities in the
long term [3].
There are a few targeted ankle muscle-stretching and -strengthening
training programs or devices for patients with stroke [4]. Ankle
muscle-stretching devices help increase ankle mobility (i.e., range of
motion [ROM]), and ankle muscle-strengthening programs help
improve muscle strength affected by reductions in muscle mass or
inadequate voluntary activation that requires muscle contractions [5].
Previously, robot-assisted gait training has helped yield a simple

Abbreviations: AMT, ankle muscle training; FM-L, Fugl–Meyer lower extremity; BBS, Berg balance scale; CI, co-contraction index; ROM, range of motion.
* Corresponding author at: Department of Clinical Rehabilitation Research, National Rehabilitation Research Institute, National Rehabilitation Center, 58
Samgaksan-ro, Gangbuk-gu, Seoul, 01022, South Korea.
E-mail address: hogenekim@korea.kr (H. Kim).

https://doi.org/10.1016/j.gaitpost.2021.04.011
Received 5 April 2020; Received in revised form 24 March 2021; Accepted 7 April 2021
Available online 15 April 2021
0966-6362/© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
J.-E. Cho et al.
repeated gait pattern movement, which was effective for improving the
gait speed and aerobic function, but has seldom improved gait symmetry
or ankle functions [6]. The anklebot is a rehabilitation robotics tool
aiming to enhance ankle motor control using a target-based video game
with visual feedback. The repetitive ankle dorsi-plantar flexions while
seated were effective in improving the movement velocity, smoothness,
and accuracy and the heel strikes during gait among moderately to
highly functional patients with stroke [4]. Children with cerebral palsy
have shown improvements in ankle biomechanics and lower limb motor
control after receiving an intelligent intervention of passive stretching
and active strengthening using a robotic training system [7]. However,
previous studies have not considered the effect of ankle joint function­
ality on mobility and strength. Therefore, ankle muscle training (AMT)
protocols should include comprehensive and effective ankle
muscle-stretching and -strengthening rehabilitation training to improve
ankle functions.
Appropriate control of muscle contraction in a target joint requires
proper sensory information on its interaction with the rest of the body
and with the environment. The proprioceptive feedback to motoneurons
presents information on changes in the threshold muscle lengths or joint
angles, thus setting the spatial activation range [8]. Therefore, the
proprioceptive feedback and muscle coordination should be considered
in ankle movement training in patients with stroke for improving ankle
motor control. Proprioception has been defined as the ability to inte­
grate sensory signals from various mechanoreceptors to determine body
position and movement in space [9]. Because the ankle–foot complex,
which provides essential proprioceptive feedback to enable adjustment
of the ankle position and movements of the upper body, is the only body
part that comes into contact with the ground, ankle proprioception plays
a crucial role in balance control [10]. Therefore, it is important to
improve AMT in consideration of the continuous interaction between
the external environment and the ankle proprioceptive feedback for the
proper control of ankle muscle contraction in patients with stroke.
Effectively enhancing ankle muscle strength and contraction control
can increase the performance of activities while standing. There are a
number of evidence stating that ankle muscle strength is correlated with
gait velocity and temporal symmetry [2]. However, in a study on highly
functional patients with stroke, impairments in ankle motor control, not
ankle muscle strength, have been reported to predict functional deficits
in walking [11]. In another study, both decreased ankle muscle strength
and motor control independently contributed to gait impairment in
patients with stroke [12]. As a factor that interferes with ankle motor
control, abnormal muscle co-contraction between the ankle dorsiflexors
and plantar flexors interferes with walking performance [13]. Further,
the decreased muscle coordination with respect to the timing of muscle
contraction is also caused by a decrease in ankle sensory function. Thus,
ankle motor control involves more complex factors, such as muscle
weakness, abnormal muscle activities, inadequate muscle co-activation,
sensory and visual deficits, and noncontractile soft-tissue tightness.
Therefore, protocols of AMT and assessments should consider these
factors rather than providing simple single-directional repetitive
movements.
Therefore, to provide comprehensive AMT for patients with stroke of
various functional levels, we developed an AMT program using a custom
ankle rehabilitation device that would apply three processes: passive
stretching, control of ankle muscle contraction, and active-resistive
strengthening. The aim of this study was to evaluate the effects of our
AMT program on ankle muscle strength, ankle proprioception, balance
ability, walking speed, and ankle muscle co-contraction during a gait
cycle in patients with chronic stroke; we hypothesized that the proposed
AMT program will affect their ankle muscle strength, ankle proprio­
ception, balance ability, walking speed, and ankle muscle co-
contraction.
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Gait & Posture 87 (2021) 177–183
2. Methods
2.1. Design
This study was a single-blinded, parallel-group, randomized
controlled trial with assessor blinding and concealed allocation. An in­
dividual not involved in the trial performed blocked random allocation
scheduled for 20 participants using Microsoft Excel. Blocking ensured
equal numbers of participants in the experimental and control groups.
The experimental group underwent AMT consisting of passive stretch­
ing, control of ankle muscle contraction, and active-resistive strength­
ening using visual feedback for 4 weeks. The control group underwent
general ankle-related physical therapy for 4 weeks. All participants were
re-assessed at the end of the 4-week intervention period (Fig. 1). All
applicable institutional and governmental regulations concerning the
ethical use of human volunteers were followed.
2.2. Participants
The participants were recruited from the National Rehabilitation
Center’s hospital between July and October 2018. The following eligi­
bility criteria were applied: (1) chronic post-stroke hemiparesis; (2)
weakness of the ankle muscles, defined using the Medical Research
Council scale (strength range grade 1–4); and (3) independent walking
with ankle impairment, such as foot drop (functional ambulatory cate­
gory score of >3). The following exclusion criteria were applied: (1)
complications of orthopedic disorders; (2) cognitive impairment (mini-
mental state examination score of ≤ 24); and (3) insufficient visual
acuity to see a screen (e.g., diplopia). This study was approved by the
Institutional Review Board of the National Rehabilitation Center, and all
participants provided informed consent before data collection began.
2.3. AMT system
The AMT device used in this study was developed for intensive and
selective training on the paretic ankle of patients with stroke. It con­
sisted of a force plate, a foot cradle, and supporting frames. Its main
feature was to reproduce actual bi-axial ankle movements applied by the
seesaw-type foot cradle that pivoted along the transverse ankle axis; the
force plate was rotated along a 42◦ -tilted subtalar axis relative to the foot
cradle. The AMT device had an interface of a control program that
included a passive/active ankle ROM evaluation mode and a personal­
ized passive training mode according to the joint range setting. During
training and evaluations, the force plate measured the four-quadrant
(anterior, posterior, medial, and lateral) ground-reaction forces
sampled at 1 kHz. The first motor (Model: EC-i40, Maxon Motor Inc.,
Sachseln, Switzerland) for the DF/PF was located around the lower
supporting column, and the motor torque was transmitted via a precise
timing belt and high-torque timing pulleys that rotated the foot cradle
along the transverse ankle axis. The second motor for the ankle INV/EV
was attached to the rear center of the foot cradle; it transmitted the
rotational torque for the ankle INV and EV via a beveled gear to a 90◦ -
flexed axis along a 42◦ -tilted subtalar axis in the sagittal plane. The
movement speed along the ankle (talocrural) and subtalar (talocalca­
neal) axes was 2.14◦ /s after the use of 14:1 high-powered planetary
gearheads (GP32HP, Maxon Motor Inc.).
2.4. Intervention
Before the training session, the participants were asked to comfort­
ably sit on a height-adjustable chair with their knees flexed at 90◦ , to
place their paretic foot on the footplate of the AMT device, and to place
their non-paretic foot on the height-matched footrest. The paretic foot
was fastened to the force plate in the foot cradle using three length-
adjustable straps. A monitor providing visual feedback was placed at
the eye level of the participants (Fig. 2-B). The AMT protocol consisted
J.-E. Cho et al.
Fig. 1. Flow chart of participant inclusion criteria.
of three processes (Fig. 2-A). In the first process (passive stretching
training), the maximum passive ankle ROM was measured, and passive
stretching training through repetitive ROM exercise according to the
movement direction was performed. In the second process (ankle muscle
contraction control training), the current and target positions of the
ankle were provided through a screen. When the ankle was passively
moved from the original position to the target position by the robotic
device, the participants actively contracted their ankle muscles to enable
movement toward the target position. A green light indicated the
coincidence between robotic passive movement and the participants’
active movement. In the third process (active-resistive strengthening
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Gait & Posture 87 (2021) 177–183
Fig. 2. The AMT (ankle muscle training) pro­
cess included three steps: (1) passive stretching
training, (2) directional perceiving training,
and (3) active-resistive strengthening training
(A). Participants in the AMT group were seated
on a height-adjustable custom chair with a
comfortable backrest that allowed their knees
to bend at 90◦ and enable natural ankle
movements. Velcro straps were used to restrain
knee, thigh and trunk movement, which guar­
anteed that only ankle movements occurred.
The paretic ankle was fixed firmly to the foot
cradle in AMT, and a monitor was placed at eye
level in front of the participant to provide vi­
sual ankle force feedback (B).
training), the participants actively moved their ankle from the original
position to the target position without an assistance force. Different
target sizes and progressive resistance thresholds were applied to
improve fine movements and muscle strengthening. The participants
were allocated a movement time of up to 30 s per target and were
allowed to fully rest for 5 s to alleviate muscle fatigue. All training was
performed within 80 % of the individual maximum ankle ROM. AMT
was performed for 40 min per day, 5 times per week for 4 weeks.
The participants in the control group underwent general ankle-
related physical therapy. Ankle ROM exercise with assistance and
functional electrical stimulation were provided to the affected
J.-E. Cho et al. Gait & Posture 87 (2021) 177–183

quadriceps and tibialis anterior muscles on alternating occasions of the changes between the two groups were performed using inde­
including resting periods. Ankle-related physical therapy was performed pendent t-tests and within the groups using paired t-tests. For all tests,
for 40 min per day, 5 days per week for 4 weeks. statistical significance was set at 0.05.

2.5. Outcome measurements 3. Results

All outcome measurements were collected by trained therapists who 3.1. Participants
were blinded to group allocation. Baseline measurements were collected
prior to randomization (Week 0). After 4 weeks, the interventions were Thirty participants underwent pre-enrollment screening evaluation.
ceased, and the outcome measurements in both groups were collected A total of 25 participants, 13 in the experimental group and 12 in the
(Week 4). Further details on the outcome measurements are provided control group, who met the inclusion criteria were included in this
below. study. The participants’ baseline characteristics are presented in
The isometric contraction force of the paretic ankle was measured Table 1. At the baseline, no significant between-group differences in the
using a portable manual muscle strength tester (Lafayette, USA, 2018). demographics or measurements were found. Two individuals in the
The isometric strength of the ankle dorsiflexors, plantar flexors, inver­ control group dropped out owing to discharge during the training.
tors, and evertors was measured for 5 s, and the maximum value was Therefore, post-testing and analysis were completed for 13 individuals
recorded. in the experimental group and 10 individuals in the control group.
Using a position matching test, we evaluated ankle proprioception as
the difference between the actual movement angle and the remembered 3.2. Isometric contraction force of the paretic ankle
angle. Ankle proprioception was measured using the device moving at
constant velocities (2.14◦ /s) with passive movement. To avoid other After training, the experimental group showed significant within-
environmental stimuli, the participants wore eye masks and earplugs. group improvements in the isometric ankle contraction force in all di­
The motor domain of the Fugl–Meyer lower extremity (FM-L) rections (DF, PF, INV, and EV, P < 0.01). There were also significant
assessment was used to measure motor impairment. This domain between-group differences in the isometric ankle contraction force in all
included measurements of movement, coordination, and reflex action directions (P < 0.05).
for the hip, knee, and ankle. It is rated on a 3-point ordinal scale (0 =
cannot be performed, 1 = partially performed, and 2 = fully performed). 3.3. Ankle proprioception
The maximum possible score for the motor domain of the FM-L assess­
ment is 34, corresponding to full sensorimotor recovery. After training, both groups showed significant within-group im­
The Berg balance scale (BBS) was used as a clinical test to evaluate provements in ankle proprioception (P<0.05). Meanwhile, there was no
static and dynamic balance. It comprises a set of 14 simple balance- significant between-group difference found in ankle proprioception
related tasks, ranging from standing up from a sitting position to (Table 2).
standing on one foot.
The repeated 10-meter walking test was used to evaluate the walking 3.4. Balance and gait
speed; it was performed at least four times on a 1.5 × 15-m walkway
covered with industrial carpeting at a comfortable speed. After training, both groups showed significant within-group im­
The ankle muscle co-contraction index (CI) was measured to eval­ provements in the FM-L score (P < 0.05); there was also a significant
uate ankle muscle efficiency during a gait sequence using a wireless between-group difference found (P < 0.05). Additionally, both groups
electromyogram (Delsys Trigno Wireless EMG, Delsys, USA, 1993). The achieved significant within-group improvements in the BBS score (P <
sensor was attached to both sides of the tibialis anterior and medial
gastrocnemius muscles. The sampling frequency was set to 2000 Hz, and
Table 1
a Butterworth bandpass filter of 10–350 Hz and full-wave rectification Participant characteristics at baseline.
were applied. We then calculated the root mean square of the signal with
AMT group (n = Control group (n P
a 100-ms window for analysis. To normalize the collected muscle ac­
13) = 10) value
tivity data according to the walking cycle, we calculated the percentage
Age (y) 58.0 (6.5) 57.2 (9.7) 0.837
reference voluntary contraction for maximum electromyography in the
Sex (M/F) 10/3 8/2 0.912
walking cycle. The CI was calculated on the basis of the method used in a Weight (kg) 68.9 (7.8) 68.1 (9.39) 0.836
previous study wherein the activity of the antagonist and agonist mus­ Height (m) 171.4 (6.9) 168.6 (8.7) 0.443
cles divided into the stance phase and swing phase was compared: Time post-stroke (months) 10.9 (6.5) 10.6 (3.3) 0.905
∫ t2 Stroke side (R/L) 5/8 4/6 0.821
EMGTA (t)dt Modified Ashworth Scale (0/1/ 1/3/6 1/3/9 0.723
t1
CI = ∫ t2 × 100 1+)
[EMGTA + EMGMG ](t)dt
t1 Functional Ambulation 4.6 (1.0) 4.5 (0.5) 0.885
Category (0− 5)
2.6. Data analysis K-MMES (score) 28.0 (4.7) 28.4 (1.2) 0.796
Fugl-Meyer lower extremity 18.3 (3.2) 19.1 (2.6) 0.575
(0− 34)
The sample size was calculated as previously described in a study Berg balance scale (0− 54) 48.0 (6.2) 47.6 (3.4) 0.862
that reported the effect of ankle training in patients with stroke over 6 ROM of ankle dorsiflexion 15.9 (9.5) 15.7 (6.8) 0.953
months [14]. The calculation was based on the pretest-posttest gait Ankle isometric contraction
velocity for the experimental group, using an alpha of 0.05 at 95 % force
Dorsiflexion (N) 14.7 (6.2) 14.0 (4.0) 0.784
power. The total sample size was determined to be 10 for the separate Plantarflexion (N) 14.3 (3.0) 14.8 (3.4) 0.752
groups (effect size: 1.062, actual power: 0.964). The program used was Inversion (N) 8.0 (1.6) 9.4 (2.2) 0.146
G* Power 3.1.9.2. Eversion (N) 7.5 (2.1) 7.8 (1.3) 0.748
All statistical analyses were performed using SPSS ver. 21.0 (SPSS for Walking speed (m/s) 0.5 (0.3) 0.3 (0.2) 0.126
Windows; SPSS Inc., USA). The results were presented as means ± AMT, ankle muscle control training; BMI, body mass index; K-MMES, Korean
standard deviations. Prior to all analyses, the normality of data was version of the mini-mental state examination.
assessed using the one-sample Kolmogorov–Smirnov test. Comparisons Values represent mean (SD).

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J.-E. Cho et al. Gait & Posture 87 (2021) 177–183

Table 2
Change in outcomes between pre- and post-training.
P value
Measure Group Pre Post Within Between
group groups

14.7 22.3
AMT 0.009*
(6.2) (11.1)
DF 0.034*
14.0 14.0
control 0.994
(3.9) (6.6)
14.3 26.5
AMT 0.005*
(3.0) (10.6)
PF 0.003*
14.8 15.1
Ankle isometric control 0.832
(3.3) (6.0)
contraction
8.0 15.6 < 0.001
force (N) AMT
(1.6) (4.7) *
INV < 0.001*
9.3 9.8
control 0.601
(2.1) (2.9)
7.5 17.2
AMT 0.009*
(2.1) (8.7)
EV 0.004*
7.8 8.3
control 0.388
(1.2) (1.9)
21.6 11.3
AMT 0.046*
(9.2) (7.7)
Ankle proprioception (◦ ) 0.254
14.2 10.0
control 0.031*
(4.8) (2.8)
18.3 25.8 < 0.001
AMT
Fugl-Meyer lower (3.2) (4.5) * Fig. 3. Boxplots of the differences (delta) in the ankle co-activation index CI)
0.001*
extremity (score) 19.1 21.5 between pre- and post-AMT (ankle muscle training) for both groups during the
control 0.029*
(2.6) (2.9) stance phase of walking. CI was calculated using muscle activities and elec­
48.0 52.4
AMT 0.002* tromyography (EMG), agonist (tibialis anterior) and antagonist (medial
Berg balance scale (6.2) (3.9)
0.214 gastrocnemius) information during the stance phase. There was a statistically
(score) 47.6 50.2
control 0.029* significant difference in stance-phase CI between the AMT group and the con­
(3.3) (2.6)
0.99 1.22 trol group.
AMT 0.022*
(0.31) (0.33)
Walking speed (m/s) 0.090
0.77 0.84
control 0.137 In our AMT program, the first process was passive stretching, which
(0.24) (0.29)
allowed repetitive bi-axial passive ROM movements (i.e., DF, PF, INV,
AMT, ankle muscle training; DF, dorsifiexion; PF, plantarflexion; INV, inversion; and EV). A previous study has reported that repetitive bi-axial passive
EV, eversion. ROM exercises can change the biomechanical properties of the ankle,
Values represent mean (SD).
*
including ankle stiffness and ankle passive ROM, resulting in improved
p < 0.05.
walking performance over an uneven surface in patients with chronic
stroke [17]. Other studies have reported positive improvements in ankle
0.05); conversely, no significant between-group difference was joint properties with feedback-controlled passive stretching intervention
observed. The experimental group showed significant within-group [18]. Passive ankle muscle-stretching methods commonly influence the
improvements in the maximum walking speed (P < 0.05); meanwhile, excitability of lower motor neurons, reduce spasticity, and increase
no between-group difference was found. Conversely, there was a sig­ muscle and soft tissue extensibility, thereby providing sensory infor­
nificant between-group difference in the stance-phase CI during gait mation associated with movement of the ankle muscles [19]. In addi­
(Fig. 3; P < 0.05). tion, unlike conventional stretching or stretching by a physical therapist,
the robotic device used can quantitatively stretch the muscle until the
4. Discussion set point repeatedly, which can be maintained throughout the experi­
ment; consequently, tolerance to stretching and pain could also be
This study successfully determined the effect of a comprehensive evaluated [20].
feedback-controlled bi-axial ankle movement training program and The second process was targeted ankle muscle contraction to match a
observed increased ankle muscle strength and improved ankle muscle given visual target that provides information on the ankle movement
co-activation during gait after the intervention in comparison with those direction, range, and force. This process allowed the patients with stroke
after conventional therapy. to repeat movement control and movement modification through visual
Four weeks of AMT significantly improved the bi-directional ankle feedback, contracting the paretic ankle muscles to complete the targeted
muscle strength and increased the gait speed in the patients with stroke. movement. Using the robotic device coupled with biofeedback enables a
The majority of studies have documented positive effects of lower-limb patient to easily achieve intense repetitive practice of ankle movements,
strength training on poststroke weakness [15]. Although there is limited which can facilitate motor relearning and neuroplasticity following
knowledge on the underlying neural and muscular adaptation mecha­ stroke. This multisensory feedback is important for motor learning by re-
nisms of strength gains in response to strength training in adults with establishing the sensorimotor loop that is disrupted by stroke because
stroke, more than 50 studies describe the relationships between synchronization between sensory and motor information facilitates
lower-limb muscle strength and performance of functional activities, neural plasticity [21].
such as sit-to-stand, stand-pivot-sit transfer, ambulation, and stair The final process was active-resistive strengthening, which rein­
climbing [16]. The muscle strength of the lower limbs, including the forced efficient ankle movements through appropriate use of proprio­
ankle dorsiflexors and plantar flexors, has been reported to be correlated ception and muscle contractions. This proposed process includes the
most with gait speed [16]. Therefore, ankle interventions should include three general principles of muscle-strengthening training: (1) to perform
ankle muscle-strengthening training to improve the performance of repetitions until fatigue; (2) to allow sufficient rest for recovery; and (3)
functional activities among patients with stroke. to progressively increase the resistance [5]. Our AMT program appeared

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J.-E. Cho et al.
to have effectively improved ankle muscle strength through repetitive
training and full resting for 5 s to alleviate muscle fatigue, which was
performed by imposing progressively increased resistance and ROM for
each individual. As another important feature, AMT reproduced the
actual complex movements according to the anatomical characteristics
of the subtalar joint by adding diagonal movements that are practically
applicable in daily activities, including walking and simple ankle
bi-axial movement tasks [22]. Therefore, the AMT protocol of this study
may have a positive effect on paretic ankle function and balance- and
gait-related movements in patients with stroke.
Increase in ankle proprioception after ankle training is associated
with improved control of ankle muscle contraction while standing.
Sensory information, such as touch, joint sensation, and proprioception,
is an important factor for the quality of movements. Approximately one-
third of patients with stroke have reported impairments in propriocep­
tion, which make it difficult to retrain normal movements, even when
repeatedly performing functional movements [23]. In our analysis,
ankle proprioception, which was measured using the position error
value, decreased by 10.3 in the experimental group (P < 0.05) and by
4.2 in the control group (P < 0.05). However, the influence of sensory
information, including ankle proprioception, on gait remains contro­
versial. It has been reported that the tactile and proprioception im­
pairments of the affected lower limb affect the walking velocity [24].
Meanwhile, insignificant correlations between the FM-L sensory score
and gait velocity have been noted in other studies [25]. Another study
carefully suggested that uncertain foot positions during walking could
alter the step length and affect the walking speed through relationships
between ankle proprioception and step length [26]. Therefore, consid­
ering that the improvement of ankle motor control requires proprio­
ceptive feedback on continuous muscle lengths and joint angles, it can
be inferred that the improvement of ankle proprioception has some ef­
fect on the improvement of ankle muscle strength and performance.
Ankle muscle co-contraction has important implications for ankle
muscle control during walking on the relative agonist and antagonist
muscle activities during walking. In this study, the experimental group
showed a significant improvement in the ankle CI after training
compared with the control group (P < 0.05). Paretic ankle muscle co-
contraction, which represents the activity ratio of the agonist and
antagonist muscles in the stance phase, contributes to the compensation
strategy, postural control, and regulation of joint stiffness [27]. Exces­
sive muscle co-contraction can even cause severe joint stiffness, which
reduces the degree of freedom [28]. The decrease in ankle muscle
co-contraction during the stance phase after AMT showed the possibility
of improvements in gait parameters, including a low peak plantar
flexion moment on the paretic side and increased energetic cost and
walking speed in patients with stroke [29]. Fundamentally, patients
with stroke with activities that require community walking and difficult
task-solving skills, including walking on rugged surfaces and ramps,
require continuous control of the ankle–foot for the external environ­
ment. Such control will require several factors, such as muscle strength,
proper muscle activities, adequate muscle co-contraction, and sensory
and visual abilities [24,25]. The improvements in the balance ability,
walking speed, and ankle CI during gait after the AMT program in this
study show the effect of AMT and imply the need for an intensive ankle
rehabilitation program to improve balance and gait in patients with
stroke. Motor control relies on sensory feedback to control movements
using a continuous process of accessing sensory information on perfor­
mance and specific sensory input from the environment to achieve a
more accurate motion performance [30]. Therefore, this study incor­
porated three training processes into the training method, reflecting the
integrated sensory and motor interventions in patients with stroke with
various functional levels to improve ankle motor control.
In conclusion, the ankle training method performed in this study,
which included ankle passive stretching, control of ankle muscle
contraction, and active-resistive strength training, is an effective ankle
rehabilitation technique that improves the ankle muscle strength and
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Gait & Posture 87 (2021) 177–183
gait quality, with a focus on ankle muscle co-contraction in patients with
chronic stroke. Nevertheless, this study has some limitations. The
number of participants was relatively small, and no follow-up for
confirmation of the sustained effect of training was performed. More­
over, the number of training repetitions in the three training processes
varied for each level of ankle function. Further studies that would
investigate the intensity, frequency, and duration of an appropriate
ankle training protocol according to the functional level of each indi­
vidual are needed.
Funding
This work was supported by Translational Research Project for
Rehabilitation Robots, National Rehabilitation Center, Ministry of
Health & Welfare, South Korea (#NRCTR-IN18003).
Declaration of Competing Interest
The authors report no declarations of interest.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.gaitpost.2021.04.011.
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