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PERSPECTIVE
published: 02 August 2018
doi: 10.3389/fphys.2018.01021
Frontiers in Physiology | www.frontiersin.org 1August 2018 | Volume 9 | Article 1021
Edited by:
Mikhail Lebedev,
Duke University, United States
Reviewed by:
Alexey Goltsov,
Abertay University, United Kingdom
Hu Zhou,
Shanghai Institute of Materia Medica
(CAS), China
*Correspondence:
Sheng Li
sheng.li@uth.tmc.edu
Specialty section:
This article was submitted to
Systems Biology,
a section of the journal
Frontiers in Physiology
Received: 25 April 2018
Accepted: 10 July 2018
Published: 02 August 2018
Citation:
Li S, Francisco GE and Zhou P (2018)
Post-stroke Hemiplegic Gait: New
Perspective and Insights.
Front. Physiol. 9:1021.
doi: 10.3389/fphys.2018.01021
Post-stroke Hemiplegic Gait: New
Perspective and Insights
Sheng Li 1,2
*, Gerard E. Francisco 1,2 and Ping Zhou 1,2, 3
1Department of Physical Medicine and Rehabilitation, University of Texas Health Science Center, Houston, TX, United States,
2TIRR Memorial Hermann Research Center, TIRR Memorial Hermann, Houston, TX, United States, 3Guangdong Work Injury
Rehabilitation Center, Guangzhou, China
Walking dysfunction occurs at a very high prevalence in stroke survivors. Human
walking is a phenomenon often taken for granted, but it is mediated by complicated
neural control mechanisms. The automatic process includes the brainstem descending
pathways (RST and VST) and the intraspinal locomotor network. It is known that leg
muscles are organized into modules to serve subtasks for body support, posture
and locomotion. Major kinematic mechanisms are recognized to minimize the center
of gravity (COG) displacement. Stroke leads to damage to motor cortices and their
descending corticospinal tracts and subsequent muscle weakness. On the other hand,
brainstem descending pathways and the intraspinal motor network are disinhibited
and become hyperexcitable. Recent advances suggest that they mediate post-stroke
spasticity and diffuse spastic synergistic activation. As a result of such changes, existing
modules are simplified and merged, thus leading to poor body support and walking
performance. The wide range and hierarchy of post-stroke hemiplegic gait impairments
is a reflection of mechanical consequences of muscle weakness, spasticity, abnormal
synergistic activation and their interactions. Given the role of brainstem descending
pathways in body support and locomotion and post-stroke spasticity, a new perspective
of understanding post-stroke hemiplegic gait is proposed. Its clinical implications for
management of hemiplegic gait are discussed. Two cases are presented as clinical
application examples.
Keywords: gait, stroke, hemiparesis, spasticity, botulinum toxin, motor recovery
INTRODUCTION
Stroke is a leading cause of serious long-term disability (Benjamin et al., 2017). Walking
dysfunction occurs in more than 80% of stroke survivors (Duncan et al., 2005). Despite of
rehabilitation efforts, 25% of all stroke survivors have residual gait impairments that require
full physical assistance before hospital discharge (Hendricks et al., 2002). Consequently, gait
impairments cause difficulties in performing activities of daily living and mobility. Gait abnormality
is characterized by a pronounced clinical presentation of gait asymmetry, as compared to healthy
people (Olney and Richards, 1996; Richards and Olney, 1996). Stroke survivors usually have
decreased stance phase and prolonged swing phase of the paretic side. Further, the walking speed
is decreased and the stride length is shorter (Perry and Burnfield, 2010). These gait abnormalities
along with muscle weakness place stroke survivors at a high risk of falls (Dobkin, 2005; Batchelor
et al., 2012). Falls usually occur during walking in community-dwelling stroke survivors (Hyndman
et al., 2002). Thus, improving walking safety and speed is the major goal for stroke survivors to
prevent falls and to improve quality of life (Olney and Richards, 1996; Dobkin, 2005).
Li et al. Post-Stroke Hemiplegic Gait
Walking is a phenomenon that is taken for granted by
healthy individuals but requires an extremely complex process
of neuromusculoskeletal control. Activation of muscles in lower
limbs, trunk, and upper limbs in a certain spatiotemporal pattern
is required to ensure appropriate joint positions to support and
advance the body weight in different phases of gait cycles. In
most situations, human walking at a comfortable speed on the
level surface is primarily mediated by brainstem and spinal
mechanisms (Dietz, 1996; Nielsen, 2003). However, supraspinal
control adds complexity and flexibility of gait control and gait
versatility to meet dynamic environmental needs and challenges
(Dietz, 1996; Nielsen, 2003). Spasticity and paresis are main
motor impairments after stroke (Li, 2017). In the context of
spastic hemiparesis, muscles are weak and spastic and at different
levels of impairments involving different regions of the upper
limb, trunk and lower limb on one side. As a result, a wide
spectrum of gait abnormalities is seen clinically.
In this article, major kinematic determinants and neural
control of normal human gait are briefly reviewed from a
historical perspective. Current findings of post-stroke hemiplegic
gait as a result of altered neural control are then summarized.
Based on recent advances on pathophysiology of muscle
weakness and spasticity after stroke, a new perspective of
understanding post-stroke hemiplegic gait is proposed. Its
clinical implications for management of hemiplegic gait are
discussed.
MAJOR KINEMATIC DETERMINANTS OF
NORMAL HUMAN GAIT
For a biomechanical and kinesiological point of view, human
walking can be described as progression of alternating weight-
bearing limbs. As such, the displacement of the center of gravity
(COG) of the whole-body is viewed as the end result of all
muscle forces acting upon the body during the progression.
During normal level walking, the body COG follows a smooth
regular curve in the three-dimensional space. The peak-to-peak
amplitudes are ∼5 cm in the vertical and mediolateral planes,
respectively Saunders et al. (1953). Using a hypothetical bipedal
compass gait model and elementary geometrical arguments,
Saunders et al. (1953) proposed six kinematic mechanisms
that contribute to the efficient progress of the whole-body
COG in the three dimensional space. These mechanisms
are termed as six major determinants of human gait. They
include pelvic rotation in the transverse plane, pelvic tilt in
the coronal plan, knee flexion in the stance phase, foot and
knee mechanisms and lateral displacement of the pelvis (hip
adduction). This concept of major determinants was originally
proposed to understand and manage pathological gait after
orthopedic disorders, such as a fused hip joint (Saunders et al.,
1953). From a historical perspective, major determinants of
human gait are the fundamental concepts in understanding
control of human gait and providing a foundation for clinical
application of gait analysis. Although individual muscle activities
(electromyography, EMG), joint kinematics, and ground reaction
force were not available in the original “compass gait” model
that permits only hip flexion and extension during walking, these
determinants were able to explain the minimization of COG
displacement well.
The conclusion of six determinants of human gait has been
challenged in a number of studies (Gard and Childress, 1997,
1999; Croce et al., 2001; Kuo, 2007; Hayot et al., 2013). In the
most recent study (Lin et al., 2014), Lin et al. quantitatively
assessed the contribution of each determinant to the COG
displacement over a gait cycle in young and healthy people. Using
an “influence coefficient” concept, they found that hip flexion,
stance knee flexion, and ankle-foot interaction significantly
minimized the COG displacement in the sagittal plane; hip
adduction and pelvic tilt are the main determinants of the
mediolateral COG displacement in the coronal plane; however,
pelvic rotation and pelvic tilt do not significantly affect the
vertical COG displacement. Overall, there is general agreement
between Saunders et al.’s classic article and this study with
comprehensive quantitative kinematic data of individual joints.
It is confirmatory that pelvic girdle movements (pelvic tilt,
hip flexion, and adduction) contribute significantly to the
displacement of COG in the three-dimensional space during
walking.
NEURAL CONTROL OF NORMAL HUMAN
GAIT
The above kinematic mechanisms are not able to account
for a near perfect kinematic trajectory during human walking
on a level surface, however. The distal part of the foot in
the swing phase is lifted only 1–2 cm with <4 mm step-to-
step variations (Winter, 1992). This displacement is enough to
prevent stumbling, but not more than necessary. This remarkable
precision of the foot position in the swing phase is determined
by and the end result of coordinated activation of muscles from
the lower extremities directly and of trunk and arm muscles
indirectly. The number of different combinations of muscle
activations that lead to the same foot position is almost infinite,
i.e., the problem of motor redundancy (Bernstein, 1967). As
suggested by Bernstein (1967), the brain may only control the
endpoint, i.e., the foot position in this case, while allowing
considerable flexibility for specific muscle activities. Using this
fundamental approach, the muscle activities are not controlled
individually. They are allowed to have a large range of flexibility
as long as they are all scaled to each other to ensure the endpoint:
the foot position within a desired range. These muscles are
coordinated and organized into functional groups. They are often
referred as muscle synergies or modules (Ting and McKay, 2007;
Drew et al., 2008).
Different modules are described according to their
biomechanical functions to the whole limb or the whole
body during different types of locomotor functions, such as
balance control or walking (Beyaert et al., 2015). There are five
modules that are sufficient to perform sub-tasks of walking
(Neptune et al., 2009). Module 1 includes gluteus medius, vasti,
and rectus femoris muscles, primarily contributing to body
support in early stance. Module 2 (soleus and gastrocnemius) is
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Li et al. Post-Stroke Hemiplegic Gait
activated during both body support and propulsion in late stance.
Module 3 (rectus femoris and tibialis anterior) acts to decelerate
the leg in early and late swing, as well as to generate energy to the
trunk throughout the swing phase. Module 4 mainly consists of
the hamstring muscles. Activation of these muscles decelerates
the ipsilateral leg prior to heel strike. Module 3 and Module 5
(iliopsoas) act together to accelerate the ipsilateral leg forward
in early swing. These modules represent a general repertoire of
motor actions that can be recruited in a variety of combinations
and at different times for different locomotion and balance
control needs, as well as for voluntary, rhythmic and reactive
locomotor behaviors (McGowan et al., 2010; Allen and Neptune,
2012; Beyaert et al., 2015).
Extensive neural structures and pathways are involved in the
process of gait control, including the spinal cord, brainstem,
cerebellum, basal ganglia, limbic system, and cerebral cortex,
as well as their interactions with the environment (see review
Nielsen, 2003; Beyaert et al., 2015). Briefly, the above motor
modules are largely controlled by the spinal cord and brainstem
under regulating control of the cerebellum. More specifically, the
pontine medullary reticular formation (PMRF) and vestibular
nuclei provide body support and balance control, thus providing
an upright posture against gravity by activating trunk and
lower extremity extensor muscles. The additional neurons in the
PMRF activate the spinal locomotor network under influence
of the mesencephalic locomotor region and subthalamic
locomotor region or cerebellum. Activation of this network
allows rhythmic locomotor activity. These structures constitute
automatic processes by simultaneously controlling body support,
balance and rhythmic locomotor activity. However, locomotion
occurs only when this automatic process is initiated “volitionally”
or “emotionally.” The volitional process involves the cerebral
cortex while an emotional process involves the limbic system.
The basal ganglia influence volitional, emotional and automatic
processes through its interactions with the cerebral cortex, limbic
system, and brainstem, respectively. Furthermore, real-time
sensory feedback via visual signals, vestibular, and proprioceptive
signals is crucial for locomotor adaptation. In summary,
walking is mainly a result of automatic process, involving the
spinal cord and brainstem mechanisms. It is usually achieved
and maintained without conscious awareness and cognitive
processing.
ALTERED NEURAL CONTROL AND
PATHOMECHANICS OF POST-STROKE
HEMIPLEGIC GAIT
Neural control mechanisms are altered in stroke survivors with
walking dysfunction. As compared to normal healthy controls,
stroke survivors have fewer modules during walking (Clark et al.,
2010). In their study (Clark et al., 2010), Clark and colleagues
analyzed modules based on EMG signals from eight leg muscles
in 55 subjects with chronic stroke and in 20 controls. Most of
affected legs had only just two or three modules. These modules
were merged from the modules observed in control subjects, thus
less independent neural control for affected leg. Furthermore,
the authors reported that the number of simplified modules was
correlated to preferred walking speed, speed modulation, step
length asymmetry, and propulsive asymmetry. In other words,
stroke survivors with fewer modules on the paretic limb walk
more slowly and demonstrate more gait asymmetry (Routson
et al., 2014).This modification of modular organization likely
reflects the central nervous system’s response to muscle weakness
and lack of voluntary muscle control on the affected side to
improve body support and locomotion. In addition to simplified
modular organization, abnormal muscle synergies and spastic
synergistic activation patterns are often resulted as well (Kline
et al., 2007; Finley et al., 2008). For example, Finley et al.
demonstrated a reflex-mediated coupling between hip flexion
and knee extension in stroke survivors (Finley et al., 2008). As
a result of abnormal patterns of muscle activation, joint positions
are altered at rest and joint movements are coupled during
walking.
A full spectrum of gait abnormality is observed clinically,
depending on the level of muscle weakness, severity of spasticity,
compensatory mechanisms, and their interactions. Primarily due
to muscle strength on the paretic side, there is a hierarchy of gait
impairments. According to walking speeds which correspond to
muscle weakness, stroke survivors are classified into four groups
with different features of gait impairments (Mulroy et al., 2003).
They are: Fast walker, Moderate walker, Slow-Extended walker
(circumductory gait), and Slow-Flexed walker.
In the Fast walker group, a stroke survivor has ∼44% of
a normal walking speed. There is a lack of heel rise in the
terminal stance, due to inadequate plantarflexor (PF) muscle
strength. Otherwise, discriminating gait events are within normal
limits. Knee hyperextension in the stance phase is observed
to compensate for lack of heel rise so that the body can roll
forward onto the forefoot. As such, the step length is compromise
secondary to lack of transition of momentum from the unaffected
limb.
A typical Moderate walker has ∼21% of a normal walking
speed. The stroke survivor is able to walk without any
assistance. The plantar flexor muscles on the paretic side are
further weakened. There are some weakness in hip extensors
(gluteus maximum) and knee extensors (quadriceps muscle).
Along with weakness, Gluteus maximum muscles, quadriceps,
and plantarflexors start to show spastic responses to quick
stretch. As a result, excessive knee flexion and hip flexion
occur at the mid stance phase. Due to the lack of pre-
swing forward progression over the toe rocker, ankle plantar
flexion, knee flexion, and heel-off are inadequate in the
terminal stance. However, the survivor is still able to achieve
a neutral foot position for clearance in the mid swing
phase.
In the Slow-Extended walker group, quadriceps muscles are
further weakened, and are not able to support the knee during the
stance phase. Though weak, the gluteus maximus muscle is still
strong enough to retract the femur into knee hyperextension to
support the body. There are also some plantarflexors contracture
and spasticity to provide necessary ankle stability. During the
swing phase, there is persistent gluteus maximum and ankle
plantarflexor spasticity. Hip hiking and leg circumduction occur
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Li et al. Post-Stroke Hemiplegic Gait
for foot clearance. Stroke survivors in this group usually require
assistive devices to walk. The walking speed is further decreased
at ∼11% of a normal speed.
In the Slow-Flexed walker group, the gluteus maximus muscle
is weakened further to the extent that it is not able to retract
the femur to stabilize the knee. Strength limitation across hip,
knee and ankle joints leaves stroke survivors with the boardline
walking ability. In the mid stance, there is excessive hip and
knee flexion, ankle dorsiflexion, and trunk forward leaning. This
posture persists in the swing phase with assistance. The assisted
walking speed is at about 10% of a normal speed.
PATHOPHYSIOLOGY OF HEMIPARESIS
AND SPASTICITY AFTER STROKE
Spasticity and muscle weakness (i.e., spastic paresis) are the
primary motor impairments and impose significant challenges
for patient care. Spasticity is estimated to be present in about 20–
40% of stroke survivors (Zorowitz et al., 2013). Clinically, post-
stroke spasticity is easily recognized as a phenomenon of velocity-
dependent increase in tonic stretch reflexes (“muscle tone”) with
exaggerated tendon jerks, resulting from hyperexcitability of
the stretch reflex (Lance, 1980). Based on decades of animal
studies and recent human research (Brown, 1994; Gracies,
2005; Nielsen et al., 2007; Mukherjee and Chakravarty, 2010;
Burke et al., 2013; Stecco et al., 2014; Li and Francisco,
2015), there are advances in understanding the pathophysiology
of spasticity and its relation with paresis (Li and Francisco,
2015; Li, 2017). A brief summary is presented here. In a
stroke survivor with spastic hemiplegia, damages occur to the
motor cortices and their descending corticospinal tract (CST).
These damages cause muscle weakness (usually hemiparesis)
immediately after stroke, including upper extremity, trunk, and
lower extremity muscles on the affected side. On the other
hand, neuroplasticity occurs after stroke as well. Due to lesions
of corticobulbar pathways accompanied with lesion of motor
cortices and/or descending CST, bulbospinal hyperexcitability
develops due to loss of supraspinal inhibition. This is mainly
a phenomenon of disinhibition, or unmasking effects. There
are several potential candidates, including reticulospinal (RST),
vestibulospinal (VST), and rubrospinal projections (Miller et al.,
2014; Li and Francisco, 2015; Owen et al., 2017). Medial RST
hyperexcitability appears to be the most likely mechanism
related to post-stroke spasticity (Li and Francisco, 2015).
RST hyperexcitability provides unopposed excitatory descending
inputs to spinal stretch reflex circuits, resulting in elevated
excitability of spinal motor neurons. This adaptive change can
account for most clinical findings on spasticity, for example,
exaggerated stretch reflex, velocity-dependent resistance to
stretch, muscle overactivity, or spontaneous firings of motor
units. Spasticity usually leads to a synergistic pattern of activation
during standing and walking, e.g., flexor synergy in the upper
extremity and extensor synergy in the lower limb (Francisco and
Li, 2016). The inter-limb activation coupling between upper and
lower extremities is also reported (Kline et al., 2007).
A NEW PERSPECTIVE FOR
UNDERSTANDING HEMIPLEGIC GAIT
These recent advances in understanding the pathophysiology
of spasticity and its relations to muscle weakness can help us
better understand hemiplegic gait in stroke survivors. Given
the disinhibited brainstem descending pathways (RST and VST)
are linked to post-stroke spasticity, reorganization of modular
control, and spastic synergistic activation, a new perspective
for understanding hemiplegic gait is schematically illustrated in
Figure 1. Muscle weakness is primarily a result of damage to
motor cortices and their descending CST after stroke. Muscle
strength, especially knee extensor strength determines gait
independence (Akazawa et al., 2017). Disinhibited brainstem
descending pathways (RST and VST) are hyperexcitable. These
descending projections are diffuse and the activated muscles are
organized into fewer modules or motor synergies that provide
body support and posture stability and locomotion (Nielsen,
2003; Beyaert et al., 2015). In addition, they also mediate
spasticity and spastic synergistic patterns. The most commonly
observed abnormal patterns include flexor synergies in the upper
extremity and extensor synergies in the lower extremity. These
spastic activations also lead to abnormal coupling within a limb
(Finley et al., 2008) and between limbs (Kline et al., 2007).
The interactions among muscle weakness, spasticity, and spastic
activations act on the trunk, pelvis and the legs. Mechanical
consequences of these interactions are the clinically observed
gait impairments. They are exemplified in the stereotypical
hemiplegic gait. It is usually described as hip extension,
adduction, and medial rotation, knee extension, ankle plantar
flexion, and inversion. The spastic muscles are synergistically
activated into hip and knee extension during the stance phase of
walking. The abnormal activation does not allow the hip and knee
to flex for foot clearance. To compensate for these impairments,
stroke survivors usually hike hip and circumduct the affected leg
during the swing phase for foot clearance. As such it is known as
a “circumductory gait.” Depending on the severity of weakness
and spasticity, and the degree of involvement (focal, regional,
or extensive), a wide spectrum of gait impairments are clinically
observed, as described above.
IMPLICATIONS FOR MANAGEMENT OF
HEMIPLEGIC GAIT
Improving walking safety and speed is the major goal for
gait rehabilitation for stroke survivors to prevent falls and
subsequently to improve quality of life (Olney and Richards,
1996; Dobkin, 2005). A multi-modality interdisciplinary
approach is usually employed and encouraged to bring
the maximum clinical outcomes for stroke survivors. Gait
rehabilitation programs include muscle strength training, task-
specific gait training, treadmill training, electromechanical and
robot-assisted gait training, functional electrical stimulations,
ankle foot orthoses (AFOs), virtual reality, mental practice with
motor imagery, and botulinum toxin injection of spastic muscles
(Verma et al., 2012; Tenniglo et al., 2014; Beyaert et al., 2015;
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Li et al. Post-Stroke Hemiplegic Gait
FIGURE 1 | Altered neural control for post-stroke gait. CST, corticospinal tract; RST, reticulospinal tract; VST, vestibulospinal tract.
Hsu et al., 2017; Jacinto and Reis Silva, 2018). The proposed
new perspective also has clinical implications to improve
management of hemiplegic gait. A few areas are discussed here
as examples.
Spastic Kinetic Chain and Orthotic
Management
As outlined above and in Figure 1, gait abnormality is a
mechanical consequence of altered neural control after stroke.
Abnormal joint posture during the stance phase represents the
net result of interactions between ground reaction force and
activation of spastic paretic muscles. For example, inadequate
quadriceps support often results in a unique joint abnormality
during the stance phase, i.e., greater knee flexion in the Moderate
walker group. This knee position places the ground reaction force
further anterior to the ankle joint, posterior to the knee joint, and
anterior to the hip joint. In response to the increased moment
imposed to each joint of the kinetic chain, spastic activation of
gluteus muscles to assist hip extension, of quadriceps muscles to
assist knee extension, and of ankle plantarflexors and invertors
to assist ankle dorsiflexion and stabilization. For such a spastic
kinetic chain, bracing with ankle-foot-orthosis to decrease ankle
dorsiflexion angle is likely effective in changing the vector of
ground reaction force (Owen, 2010). The forces required for
maintaining joint position at each joint are reduced, and body
support and joint stability are improved.
Muscle Selection for Botulinum Toxin
Therapy
Botulinum toxin therapy is often used for spasticity management
of leg muscles to improve gait (Esquenazi et al., 2015; Baker
et al., 2016). Botulinum toxin (BoNT) acts to block presynaptic
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Li et al. Post-Stroke Hemiplegic Gait
release of acetylcholine at the neuromuscular junction, therefore,
intramuscular injection of BoNT can lead to spasticity reduction
(Jahn, 2006). Due to this, BoNT injection also results in
muscle weakness. As stated above, increased spasticity of
quadriceps is likely to be part of synergistic activation for
body support and posture stabilization. Quadriceps strength
and support determines walking independence (Akazawa et al.,
2017). Though quadriceps spasticity is often linked to knee joint
stiffness, judicious consideration of treatment for spasticity is
required because of the side effect of muscle weakness from
BoNT. Another common observation is that stroke survivors
have ankle plantarflexion and ankle inversion. Intramuscular
EMG exams may detect spontaneous motor unit activation
potentials (MUAPs) in most relevant muscles, such as tibialis
posterior, gastrocnemius, soleus, tibialis anterior, extensor hallux
longus muscles, i.e., spasticity (Mottram et al., 2009, 2010; Chang
et al., 2013). It is not surprising to detect spasticity in all of
these muscles, given diffused activation of brainstem descending
pathways. The clinical presentation of ankle plantarflexion and
ankle inversion suggests that this abnormality is primarily caused
by tibialis posterior, gastrocnemius, and soleus, or spasticity
of these muscles overrides spasticity of tibialis anterior and
extensor halluces longus muscles. Not all muscles with spasticity
need botulinum toxin injection in this case. Rather, selection
of muscles is based on mechanical consequences of spastic
muscles and their relation to ankle and foot positioning during
walking.
Muscles for Pelvis and Posture Control
Major kinematic determinants were originally proposed to
explain contributions of individual joints (pelvic movement, hip,
knee, and ankle joints) to minimize the COG displacement.
The purpose was to understand human gait in general and
to explain gait abnormality after orthopedic disorders in
particular, such as hip joint fusion. As mentioned above,
these kinematic determinants were in general validated by the
modern instrumented gait analysis. Even though three out of six
kinematic determinants involve pelvic movement, EMG studies
are almost limited to leg muscles. Only one muscle (gluteus
maximus) related to pelvic movement is commonly studied
(Perry and Burnfield, 2010). The neural control mechanisms
(brainstem-spinal network) involve trunk muscles and other
pelvic movement related muscles as well. Post-stroke spastic
hemiparesis could involve all muscles on the affected side.
Depending on clinical presentations, these pelvic muscles could
be the primary contributors of the gait impairments (Figure 2).
Two cases are presented here to highlight the importance of
spastic latissimus dorsi muscle and gluteus medius and tensor
fasciae latae (TFL) muscles in post-stroke gait control. Written
informed consent was obtained for scientific publication from
both patients.
Case 1
A 62 year old right-handed female suffered right middle cerebral
artery ischemic stroke 6 years ago with a residual left spastic
hemiplegia. She was able to ambulate without any assistive
device at a moderate walking speed. She presented with a mild
FIGURE 2 | (A,B) A stroke survivor with spasticity that resulted in dramatic
trunk lateral flexion and hip hiking before and after botulinum toxin injections;
(C,D) A stroke survivor with spasticity that resulted in dynamic hip adduction
and pelvic anterior rotation before and after botulinum toxin injection. See text
for details.
circumductory gait. Lateral trunk flexion to the left side and her
left hip hiking were prominent and constant during walking.
According to its spread origin of latissimus dorsi muscle from
inferior 3–4 ribs, low thoracic spine, lumbar spine and iliac crest,
and its insertion to the intertubercular groove of the humerus,
a spastic latissimus dorsi muscle was viewed to be responsible
for this patient’s abnormal posture during walking, including
pelvic vertical elevation in the coronal plane, trunk lateral flexion,
shoulder adduction, and internal rotation (Figure 2A). A total of
150 units of onabotulinumtoxin A were injected into this muscle
under ultrasound imaging guidance. Trunk lateral flexion and
pelvic elevation were much improved at 6 weeks after injection.
As shown on Figure 2B, pelvic vertical elevation was decreased
from 19 to 9◦after injection.
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Li et al. Post-Stroke Hemiplegic Gait
Case 2
A 27 year old right handed female had a history of stroke
after a traumatic brain injury 20 years ago which resulted in
right spastic hemiplegia. She received botulinum toxin injections
several times in the first 3 years after the accident. At a seated or
supine position, she only had very mild muscle weakness in the
right upper and lower extremities with minimum to negligible
spasticity. The chief complaint was that her right toes were hitting
the left toes during the mid-swing phase, i.e., problematic right
hip internal rotation and adduction secondary to dynamic tone
(Figure 2C). According to possible pathomechanics, dynamic
spasticity in right anterior gluteus medius and TFL muscles could
cause excessive anterior rotation of the pelvis in the transverse
plane and hip internal rotation, while hip adductor spasticity
contributes further to hip adduction. A total of 200 units of
incobotulinumtoxin A were injected to these muscles under
ultrasound imaging guidance (75 units to gluteus medius, 50
units to TFL, and 75 units to hip adductors). Improved walking
posture in the follow up visit at 6 weeks after injection validated
the pathomechanics analysis (Figure 2D).
CONCLUDING REMARKS
Given the disinhibited brainstem descending pathways (RST
and VST) are linked to post-stroke spasticity, reorganization
of modular control, and spastic synergistic activation, a new
perspective for understanding hemiplegic gait is proposed.
This new perspective highlights post-stroke hemiplegic gait
impairments as mechanical consequences of altered neural
control mechanisms of human gait. Hemiplegic gait is not
a result of isolated skeletal muscular disorder, as often seen
after orthopedic disorders. In clinical observational analysis,
muscle weakness, spasticity, and spastic activation on the paretic
arm, trunk and leg need to be taken into consideration. This
new perspective also advances clinical management strategies
as outlined above. However, these are examples and cases.
They need to be validated in future laboratory and clinical
studies.
AUTHOR CONTRIBUTIONS
SL developed the initial version of the manuscript and created
the figures. GF and PZ critically revised the manuscript and
contributed substantially to the manuscript development. All
authors read and approved the final manuscript.
FUNDING
This study was supported in part by NIH NICHD/NCMRR
R21HD087128, R21HD090453.
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Conflict of Interest Statement: The authors declare that the research was
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