PLOS ONE

RESEARCH ARTICLE

Tendon release reduced joint stiffness with

unaltered leg stiffness during gait in spastic
diplegic cerebral palsy
Chien-Chung Kuo1,2, Hsing-Po Huang3, Ting-Ming Wang ID4,5, Shih-Wun Hong6, Li-
Wei Hung3, Ken N. Kuo5, Tung-Wu Lu ID3,4*
1 Department of Orthopedics, China Medical University Hospital, Taiwan, R.O.C, 2 Department of
Orthopedics, School of Medicine, China Medical University, Taiwan, R.O.C, 3 Department of Biomedical
Engineering, National Taiwan University, Taiwan, R.O.C, 4 Department of Orthopaedic Surgery, School of
Medicine, National Taiwan University, Taiwan, R.O.C, 5 Department of Orthopaedic Surgery, National
Taiwan University Hospital, Taiwan, R.O.C, 6 Department of Physical Therapy, Tzu Chi University, Taiwan,
R.O.C
a1111111111
* [email protected]
a1111111111
a1111111111
a1111111111
a1111111111 Abstract
Biomechanical deviations at individual joints are often identified by gait analysis of patients
with cerebral palsy (CP). Analysis of the control of joint and leg stiffness of the locomotor
system during gait in children with spastic diplegic CP has been used to reveal their control
OPEN ACCESS
strategy, but the differences between before and after surgery remain unknown. The current
Citation: Kuo C-C, Huang H-P, Wang T-M, Hong S- study aimed to bridge the gap by comparing the leg stiffness—both skeletal and muscular
W, Hung L-W, Kuo KN, et al. (2021) Tendon
components—and associated joint stiffness during gait in 12 healthy controls and 12 chil-
release reduced joint stiffness with unaltered leg
stiffness during gait in spastic diplegic cerebral dren with spastic diplegic CP before and after tendon release surgery (TRS). Each subject
palsy. PLoS ONE 16(1): e0245616. https://doi.org/ walked at a self-selected pace on a 10-meter walkway while their kinematic and forceplate
10.1371/journal.pone.0245616
data were measured to calculate the stiffness-related variables during loading response,
Editor: Yih-Kuen Jan, University of Illinois at mid-stance, terminal stance, and pre-swing. The CP group altered the stiffness of the lower
Urbana-Champaign, UNITED STATES
limb joints and decreased the demand on the muscular components while maintaining an
Received: September 26, 2020 unaltered leg stiffness during stance phase after the TRS. The TRS surgery improved the
Accepted: January 4, 2021 joint and leg stiffness control during gait, although residual deficits and associated devia-
tions still remained. It is suggested that the stiffness-related variables be included in future
Published: January 15, 2021
clinical gait analysis for a more complete assessment of gait in children with CP.
Copyright: © 2021 Kuo et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original Introduction
author and source are credited.
Spastic diplegic cerebral palsy (CP) accounts for 22% of all types of cerebral palsy [1], with
Data Availability Statement: All relevant data are impaired motor control that may cause muscle tightness in the lower extremities, and postural
within the manuscript and its Supporting and movement deviations [2]. Decisions regarding surgical treatment of spasticity are made
information files.
based on the effects of neurological conditions on the bones and tissues of the growing child
Funding: The author(s) received no specific [3], aimed at maximizing function, reducing disability and facilitating mobility. Among the
funding for this work. surgical procedures in treating spastic CP, such as osteotomy, muscle release and tendon trans-
Competing interests: The authors have declared fer, tenotomy (tendon release) is often used to release the tendon to reduce the spasticity of
that no competing interests exist. the affected muscles for a greater passive range of motion while maintaining residual muscle

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PLOS ONE Leg and joint stiffness in children with diplegic cerebral palsy during gait after tendon release surgery

tension [3–6]. Tenotomy is a simple, reliable and effective procedure with minor risks [5]. Pre-
vious studies have shown that tenotomy could significantly improve the range of motion in
patients one year after surgery [4], reduce flexion deformity [7], and improve functional status
and walking capabilities of these patients [8].
The efficacy of tendon release on CP during level walking has been predominantly evalu-
ated using functional scores and/or clinical evaluation [9,10], such as using the Gross Motor
Function Classification System (GMFCS) [11] and the Functional Mobility Scale (FMS) [12].
Computerized gait analysis has been used for identifying more detailed changes in walking
performance in CP patients before and after tenotomy [13–17]. Depending on the location of
the surgery, tenotomy was found to help one or more of the following: decreased hip flexion
contracture, increased knee extension during stance, decreased knee flexion during swing and
decreased ankle plantarflexion throughout the gait cycle [13–16]. Since the different joints and
muscles of the lower extremities work together to meet the varying mechanical and balance
demands during different phases of gait, changing the tightness of one muscle may affect the
actions of the other muscles, and thus the motions of the joints. Identifying changes in individ-
ual muscles or joints without considering the coordination and interactions between muscles
and joints may complicate the evaluation and interpretation of the gait data, and thus also of
the CP gait performance [18]. A single index that combines the joint kinematics and kinetics
of the lower extremities may be helpful for simplifying the evaluation of the overall perfor-
mance of gait as an index for the efficacy of the surgical intervention.
Leg and joint stiffness during gait has been used for the assessment of pathology and of the
efficacy of treatment because of its critical role in modulating the kinematics and kinetics of
the locomotor system [19–21]. Changes in the leg and joint stiffness have been quantified in
various motor tasks in different populations [19,21–25]. In these studies, the human body dur-
ing walking was described as a simplified mass-spring model, with the leg modeled as a non-
linear spring bearing the point mass of the whole body against collapse. With this model, the
changes in the stiffness of the leg spring during gait represent the modulation of the kinematics
and kinetics of the locomotor system via leg stiffness control. Following a similar approach,
lower limb joints were modeled as a non-linear spiral spring, the stiffness changes of which
represent the modulation of the joint angles and moments during gait [21,26]. The leg stiffness
could be further decomposed into muscular (MC) and skeletal (SC) components according to
DeVita and Hortobagyi [27]. The SC is related to the forces transmitted through the joints and
bones, so a completely extended lower limb would have the leg stiffness provided solely by the
SC. On the other hand, the muscular component is related to the muscular torques at the joints
and the joint stiffness [26,27], so a flexing lower limb would be accompanied by an increasing
MC but a decreasing SC. Their relative contributions to the leg stiffness can be described by
the ratio of the MC and SC (MC/SC), which varies with the changes of the alignment of bones,
and the muscle moments required to maintain the posture and movement during gait [21,27].
A previous study quantified the non-linear leg and joint stiffness changes during gait in chil-
dren with spastic diplegic CP [21], and showed that leg stiffness played a critical role in modu-
lating the kinematics and kinetics of the locomotor system. The children decreased their leg
stiffness but increased the joint stiffness during most of the stance phase, indicating that they
relied more on muscular contributions to achieve the required leg stiffness for maintaining
body posture against collapse [21]. However, it remains unclear whether the leg stiffness
(including skeletal and muscular components) and joint stiffness would be altered in response
to a tenotomy in the lower leg in children with spastic diplegic CP.
The purpose of this study was to compare the leg and joint stiffness, the contributions of
skeletal and muscular components, and the associated joint kinematics and kinetics in chil-
dren with spastic diplegic CP during level walking before and after TRS versus healthy

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PLOS ONE Leg and joint stiffness in children with diplegic cerebral palsy during gait after tendon release surgery

controls. It was hypothesized that, when compared to healthy controls, the CP group would
have decreased leg stiffness but with increased muscular contributions and joints stiffness dur-
ing gait, and that after TRS the CP group would increase the leg stiffness with reduced muscu-
lar contributions and joint stiffness when compared to those before TRS.

Materials and methods

Ethics statement
The work was approved by the Institutional Review Board of National Taiwan University Hos-
pital, Taiwan, R.O.C (Permit Number: 201605138RIND). All participants were informed of the
procedure and they provided written informed consent prior to the study. This observational,
cohort study was conducted in the National Taiwan University Hospital Gait Laboratory.

Subjects
A convenience sample of twelve children with spastic diplegic cerebral palsy (CP) (12 males;
age: 10.9 ± 2.6 years; height: 140.7 ± 16.7 cm; mass: 32.6 ± 10.5 kg) was recruited from the out-
patient orthopedic clinics at National Taiwan University Hospital during August 2016 to July
2019, and 12 healthy controls (12 males; age: 11.2 ± 2.3 years; height: 141.1 ± 12.6 cm; mass:
34.4 ± 9.3 kg) were recruited from the local community to match the patient group for sex, age,
height and weight during the same time period (Table 1). Informed written consent signed
by both the subjects and their legal guardians was obtained as approved by the Institutional

Table 1. Means (standard deviations) of the ranges of motion, muscle strength and muscle tone of the hip, knee and ankle joints for the diplegic CP group before
(Pre-OP) and after (Post-OP) TRS. Relevant demographic details including: age, height, mass and GMFCS level for CP group and Controls.
Range of Motion (degrees) Muscle Strength (MMT) Muscle Tone (Modified Ashworth Scale)
Hip
Pre-OP
Extension/Extensors 26.64 (6.57) 3.61(0.73) 0.15 (0.37)
Flexion/Flexors 116.8 (7.31) 3.95 (0.61) 0.15 (0.37)
Post-OP
Extension/Extensors 23.21 (10.12) 3.95 (0.81) 0.08 (0.29)
Flexion/Flexors 116.9 (7.28) 4.42 (063) 0.04 (0.14)
Knee
Pre-OP
Extension/Extensors -2.00 (6.63) 4.07 (0.53) 0.45 (0.70)
Flexion/Flexors 135.5 (2.13) 3.75 (0.48) 0.05 (0.16)
Post-OP
Extension/Extensors -1.42 (3.48) 4.42 (0.69) 0.31 (0.58)
Flexion/Flexors 134.5 (3.11) 4.10 (0.81) 0.00 (0.00)
Ankle
Pre-OP
Plantar-Flexion/Flexors 49.82 (5.00) 3.59 (0.84) 0.83 (0.64)
Dorsi-Flexion/Flexors 6.41 (10.88) 3.60 (0.57) 0.20 (0.42)
Post-OP
Plantar-Flexion/Flexors 48.58 (6.64) 4.23 (0.61) 0.69 (0.83)
Dorsi-Flexion/Flexors 9.54 (9.44) 3.98 (0.65) 0.08 (0.29)
Age (years) Height (cm) Mass (kg) GMFCS
CP 10.9 (2.6) 140.7 (16.7) 32.6 (10.5) II (0)
Controls 11.2 (2.3) 141.1 (12.6) 34.4 (9.3) N/A
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PLOS ONE Leg and joint stiffness in children with diplegic cerebral palsy during gait after tendon release surgery

Research Board. The subjects in the CP group met the following inclusion criteria: (1) graded
I-III in the Gross Motor Function Classification System (GMFCS), (2) moderate to normal
muscle strength, (3) mild to normal muscle tone, and (4) independent walking without assistive
device. Participants with CP were excluded if they had pain, noticeable leg length discrepancies,
serious muscle contractures, joint deformities, or any other pathology which might affect gait
and/or cognitive function. The children with CP who participated in the current study were
considered a good representation of typical children with GMFCS level II diplegic spastic CP
in Taiwan. Each patient with CP received gastrocnemius and hamstring TRS performed by a
senior paediatric orthopaedic surgeon (TMW) who made the decision based on clinical infor-
mation and data from a standard clinical gait analysis on the patient. Distal gastrocnemius
recession was performed by dividing the aponeurosis of the gastrocnemius. For the lengthening
of the distal hamstrings, an open approach was used for the intramuscular aponeurotic length-
ening of the semimembranosus, Z-lengthening of the semitendinosus, and either tenotomy or
Z-lengthening of the gracilis at a level proximal to the knee. When the lateral hamstrings were
included in the procedure, intramuscular aponeurotic lengthening of the biceps femoris was
performed [28]. Before TRS, and six months to one year afterwards, each subject was evaluated
for their lower limb stiffness control using computerized gait analysis. The healthy controls
(Control) were free from any musculoskeletal, neurological or cardiovascular disorders. An a
priori power analysis for a two-group independent sample t-test for the comparison of leg stiff-
ness between diplegic CP and healthy children based on pilot results using GPOWER [29]
determined that a projected sample size of seven subjects for each group would be needed
with a power of 0.8 and a large effect size (Cohen’s d = 0.88) at a significance level of 0.05.

Experimental protocol
In a hospital gait laboratory, each subject walked at a self-selected pace on a 10-meter walkway
while the motions of the body segments were measured at 200 Hz via 39 retro-reflective mark-
ers placed on specific anatomical landmarks [30] using an 8-camera motion capture system
(Vicon T-40s, OMG, U.K.), while the ground reaction forces (GRF) were measured at 2000 Hz
using three forceplates (OR6-7-2000/Gen-5, AMTI, U.S.A.) [31,32]. Before data collection, the
subjects were allowed to walk on the walkway several times to familiarize themselves with the
experimental environment. Data from three gait cycles for each limb were obtained for subse-
quent analysis, both for the Control and for the CP group before and after TRS.

Data analysis
The measured GRF and marker data were low-pass filtered using a fourth-order Butterworth
filter with cut-off frequencies of 25 Hz and 10 Hz, respectively [33]. With the processed kine-
matic and GRF data, angular motions, and muscle moments at the lower limb joints were
calculated using inverse dynamics analysis. Each body segment was modeled as a rigid body
embedded with an orthogonal coordinate system with the positive x-axis directed anteriorly,
the positive y-axis superiorly and the positive z-axis to the right in accordance with ISB recom-
mendations [34]. A Cardanic rotation sequence of z-x-y was used to describe the rotational
movements of each of the lower limb joints modeled as ball-and-socket joints [35]. Subject-
specific body segmental inertial properties were obtained using an optimization-based method
[36]. A global optimization method was used to reduce the effects of soft tissue artefacts associ-
ated with the skin markers on the pelvis-leg apparatus [37]. The calculated joint moments
were normalized to body weight (BW) and leg length (LL), the latter defined as the length
between the anterior superior iliac spine and the medial malleolus. Temporal-spatial parame-
ters, namely walking speed, step length, stride time, cadence and step width were obtained.

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PLOS ONE Leg and joint stiffness in children with diplegic cerebral palsy during gait after tendon release surgery

The stride length was calculated as the distance between the COP positions of two consecutive
initial contacts of the same foot along the direction of progression, while the step width was
calculated as the distance between two successive bilateral COP positions at initial contacts
along the direction perpendicular to that of progression.
Each of the lower limbs was modeled as a non-linear spring which connected the center of
pressure (COP) of the GRF and the hip joint center (Fig 1). The varying leg stiffness could thus
be calculated as the slope (gradient) of the force vs. deformation curve during gait [21]. Simi-
larly, the joint stiffness of the ankle, knee and hip were calculated as the slope of the moment
vs. angle curve of the joint. The leg stiffness was further decomposed into muscular (MC) and
skeletal (SC) components (Fig 1). The decomposition of the MC and SC was related to the
angle (φ) between the longitudinal axis of the shank and the line joining the COP of the GRF
to the center of the hip joint. While completely extended (φ = 0) joints of the lower limb would
have the leg stiffness provided solely by the SC, the contribution of MC would increase with
increasing φ [21,27] (Fig 1). The ratio of the MC and SC (MC/SC) was calculated to assess
their relative contribution to the leg stiffness [21].
The leg stiffness, the skeletal and muscular components and their ratios, as well as the
angles, moments and stiffness at the hip, knee and ankle in the sagittal plane, were calculated
for each of the lower limbs. Time-averaged values of the variables were then calculated over
the sub-phases of the stance phase of each limb, i.e., loading response (LR, initial double-limb
support), mid-stance (MS), terminal stance (TS) and pre-swing (PS, terminal double-limb sup-
port). For each subject of both groups, the calculated variables from both limbs were averaged
for subsequent statistical analysis.

Statistical analysis
For each of the calculated variables, the time-averaged values of each sub-phase of the CP
group were compared with those of the Control group for both Pre-OP and Post-OP using an
independent t-test, while within-group comparisons of the CP group were performed using a
paired t-test. All significance levels were set at α = 0.05. All the statistical analyses were per-
formed using SPSS version 20.0 (SPSS Inc., Armonk, N.Y.: IBM, U.S.A.).

Results
Compared to Control, both Pre-OP and Post-OP of the CP group showed significantly
decreased gait speed and stride length but increased step width, while only the Pre-OP showed
decreased cadence and increased stride time (p<0.05) (Table 2). No significant within-group
differences in the temporal-spatial parameters were found in the diplegic CP group (p>0.05).
Compared to Control, the CP group showed significantly increased hip and knee flexion in
both Pre-OP and Post-OP throughout the stance phase, and increased plantar flexion during
MS and TS, but increased ankle plantarflexion only in the Pre-OP during LR and PS (p<0.05)
(Fig 2) (Table 3). The CP group showed increased hip extensor moments during MS to TS,
increased ankle plantarflexor moments during LR to MS, but decreased ankle plantarflexor
moments during TS to PS in both Pre-OP and Post-OP (Fig 2). The Pre-OP also showed
increased hip extensor moments during LR, increased knee extensor moments during TS to
PS, while the Post-OP showed a decreased hip flexor moment during PS, and a decreased knee
extensor moment during MS when compared to the Control (p<0.05) (Fig 2) (Table 3). Com-
pared to Pre-OP, the Post-OP of the CP group showed significantly decreased knee flexion
angles during LR, TS and PS, decreased ankle plantarflexion angles during TS to PS, and sig-
nificantly decreased hip extensor moments during LR, decreased hip flexor moments during
PS, and decreased knee extensor moments during TS to PS (p<0.05) (Fig 2) (Table 3).

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PLOS ONE Leg and joint stiffness in children with diplegic cerebral palsy during gait after tendon release surgery

Fig 1. Model of leg stiffness, and skeletal and muscular components of the leg stiffness. Stick figure of a lower limb
during stance phase of gait showing the definitions of the effective GRF (thin vector, Fe(t)) and effective leg length (Le
(t)). φ(t) is the angle between the longitudinal axis of the shank and the line joining the COP of the GRF to the center
of the hip joint; Ks,l (t) is the skeletal component in Kl (t); Km,l (t) is the muscular component in Kl (t); Ks(t) is the
skeletal stiffness; and Km(t) is the muscular stiffness. (Adapted from [21]).
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When compared to Control, both Pre-OP and Post-OP of the diplegic CP group showed
significantly decreased leg stiffness during LR and PS with increased MC/SC ratio during LR
and decreased SC during PS, while the Pre-OP also showed decreased leg stiffness during MS
and an increased MC/SC ratio during MS to TS (p<0.05) (Table 4). Compared to the Pre-OP,

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PLOS ONE Leg and joint stiffness in children with diplegic cerebral palsy during gait after tendon release surgery

Table 2. Means (standard deviations) of the temporal-spatial parameters of gait for children with diplegic CP (Pre-OP: Before surgery; Post-OP: After surgery) and
the Control group. P-values for pair-wise comparisons between Pre-OP, post-OP and Control are also given for each variable.
Group Cadence (steps/min) Gait speed (m/s) Stride time (s) Stride length (m) Step width (m)
Control (CON) 119.37 (11.92) 1.08 (0.17) 1.02 (0.11) 1.08 (0.11) 0.10 (0.02)
CP Pre-OP (Pre) 107.60 (20.69) 0.60 (0.18) 1.14 (0.27) 0.68 (0.25) 0.17 (0.05)
CP Post-OP (Post) 100.18 (14.88) 0.57 (0.18) 1.24 (0.20) 0.70 (0.21) 0.18 (0.06)
p (CON vs. Pre) 0.106 <0.001� 0.161 <0.001� <0.001�
� � � �
p (CON vs. Post) 0.002 <0.001 0.002 <0.001 0.001�
p (Pre vs. Post) 0.085 0.622 0.094 0.790 0.542

p (CON vs. Pre-OP): p-value between Pre-OP of diplegic CP group and Control.
p (CON vs. Post-OP): p-value between Post-OP of diplegic CP group and Control.
p (Pre-OP vs. Post-OP): p-value between Pre-OP and Post-OP of diplegic CP group.
�
: significant difference (p<0.05).

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the Post-OP maintained unaltered leg stiffness throughout the stance phase but showed a sig-
nificantly decreased MC/SC ratio during most of the stance phase except during TS (Table 4).
For the stiffness of individual joints, both Pre-OP and Post-OP of the CP group showed sig-
nificantly increased joint stiffness at the hip during TS, at the knee during PS, at the ankle dur-
ing LR to MS, and decreased joint stiffness at the knee during MS, when compared to Control.
The Pre-OP also showed increased hip joint stiffness during LR to MS and increased knee
joint stiffness during LR, while the Post-OP showed increased hip and ankle joint stiffness dur-
ing PS (Table 4). Compared to Pre-OP, the Post-OP of the CP group showed decreased hip
joint stiffness during LR, and decreased knee joint stiffness during MS and PS (p<0.05)
(Table 4).

Fig 2. Ensemble-averaged joint angles and moments in the sagittal plane. The angles and moments at the hip, knee, and ankle for the control
group are shown as dashed lines and those for the pre- and post-OP CP group as solid black and grey lines, respectively. The standard deviations are
shown as one-sided error bars in each group. %BW� LL indicates the moments normalized to the body weight and leg length. The vertical lines from
left to right are the beginning of single-limb support phase (contralateral toe-off), end of single-limb support phase (contralateral heel-strike), and
the beginning of swing phase (toe-off), respectively.
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PLOS ONE Leg and joint stiffness in children with diplegic cerebral palsy during gait after tendon release surgery

Table 3. Means (standard deviations) of the time-averaged angles and moments at the hip, knee and ankle in the sagittal plane over the stance phase of gait for chil-
dren with diplegic CP and the Control group. P-values for pair-wise comparisons between Pre-OP, post-OP and Control are also given for each variable.
Load Response (LR) Mid-Stance (MS) Terminal Stance (TS) Pre-Swing (PS)
Hip Angle (degrees) (+/-: flexion/extension)
Control (CON) 23.37 (6.05) 11.55 (4.30) -3.73 (3.17) -8.39 (4.88)
CP Pre-OP (Pre) 44.31 (8.03) 35.41 (9.16) 21.29 (9.00) 21.08 (9.16)
CP Post-OP (Post) 45.86 (6.93) 36.95 (8.60) 24.47 (11.66) 20.12 (12.00)
p (CON vs. Pre) <0.001� <0.001� <0.001� <0.001�
� � �
p (CON vs. Post) <0.001 <0.001 <0.001 <0.001�
p (Pre vs. Post) 0.484 0.519 0.631 0.956
Knee Angle (degrees) (+/-: flexion/extension)
Control (CON) 13.76 (7.63) 16.16 (8.58) 12.70 (7.88) 25.21 (8.09)
CP Pre-OP (Pre) 42.31 (20.33) 38.01 (23.10) 37.04 (20.72) 48.65 (19.12)
CP Post-OP (Post) 35.23 (19.29) 32.26 (21.32) 28.52 (20.55) 37.90 (19.63)
p (CON vs. Pre) <0.001� 0.006� 0.001� 0.001�
� � �
p (CON vs. Post) 0.002 0.024 0.021 0.050�
� �
p (Pre vs. Post) 0.031 0.109 0.037 0.027�
Ankle Angle (degrees) (+/-:dorsiflexion / plantarflexion)
Control (CON) -3.99 (3.06) 1.04 (4.73) 7.34 (3.17) -0.11 (3.16)
CP Pre-OP (Pre) -8.32 (4.94) -4.97 (4.68) -4.40 (5.60) -7.69 (9.08)
CP Post-OP (Post) -6.02 (5.62) -4.19 (2.88) -0.73 (5.55) -1.38 (7.86)
p (CON vs. Pre) 0.030� 0.007� <0.001� 0.017�
� �
p (CON vs. Post) 0.325 0.006 0.001 0.625
p (Pre vs. Post) 0.367 0.290 0.049� 0.029�
Hip moment (%BW� LL) (+/-:extensor / flexor)
Control (CON) 5.27 (1.50) 1.89 (0.87) -2.42 (1.21) -5.27 (1.16)
CP Pre-OP (Pre) 8.67 (5.42) 7.96 (5.31) -0.57 (2.50) -5.47 (2.58)
CP Post-OP (Post) 5.82 (2.56) 5.61 (3.25) 0.85 (2.35) -3.12 (1.92)
p (CON vs. Pre) 0.048� 0.001� 0.032� 0.807
p (CON vs. Post) 0.525 0.001� <0.001� 0.004�
p (Pre vs. Post) 0.035� 0.153 0.102 0.024�
�
Knee moment (%BW LL) (+/-:extensor / flexor)
Control (CON) 1.95 (1.99) 5.37 (2.07) 0.35 (0.38) 1.68 (0.57)
CP Pre-OP (Pre) 2.71 (2.88) 4.38 (3.80) 4.30 (3.39) 5.68 (3.29)
CP Post-OP (Post) 0.94 (3.76) 1.35 (5.49) 0.05 (2.32) 2.08 (2.62)
�
p (CON vs. Pre) 0.468 0.442 0.001 0.001�
�
p (CON vs. Post) 0.416 0.028 0.676 0.621
p (Pre vs. Post) 0.327 0.330 0.030� 0.025�
Ankle moment (%BW� LL) (+/-:plantarflexor / dorsiflexor)
Control (CON) - 0.95 (0.30) 2.41 (1.41) 12.23 (1.30) 8.97 (1.65)
CP Pre-OP (Pre) 4.25 (3.41) 7.63 (3.59) 9.34 (1.69) 6.23 (2.49)
CP Post-OP (Post) 2.45 (1.85) 6.99 (3.24) 9.47 (1.90) 6.71 (1.99)
p (CON vs. Pre) <0.001� <0.001� <0.001� 0.005�
� � �
p (CON vs. Post) <0.001 <0.001 <0.001 0.007�
p (Pre vs. Post) 0.118 0.411 0.804 0.470

p (CON vs. Pre-OP): p-value between Pre-OP of diplegic CP group and Control.
p (CON vs. Post-OP): p-value between Post-OP of diplegic CP group and Control.
p (Pre-OP vs. Post-OP): p-value between Pre-OP and Post-OP of diplegic CP group.
�
: significant difference (p<0.05).
BW: body weight; LL: leg length.

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PLOS ONE Leg and joint stiffness in children with diplegic cerebral palsy during gait after tendon release surgery

Table 4. Means (standard deviations) of the leg and joint stiffness, and skeletal and muscular components of the leg stiffness in children with diplegic CP and the
Control group during gait. P-values for pair-wise comparisons between Pre-OP, post-OP and Control are also given for each variable.
Load Response (LR) Mid-Stance (MS) Terminal Stance (TS) Pre-Swing (PS)
Leg Stiffness (N/m)
Control (CON) 15.02 (6.42) 14.64 (5.98) 8.83 (2.02) 5.90 (2.25)
CP Pre-OP (Pre) 9.12 (5.63) 9.22 (4.09) 9.27 (3.60) 3.71 (1.60)
CP Post-OP (Post) 9.58 (4.70) 11.20 (5.87) 12.05 (5.98) 3.40 (1.89)
p (CON vs. Pre) 0.026� 0.017� 0.712 0.012�
�
p (CON vs. Post) 0.027 0.169 0.091 0.008�
p (Pre vs. Post) 0.774 0.259 0.141 0.651
Skeletal Component (N/m)
Control (CON) 14.69 (6.37) 13.87 (5.82) 8.01 (1.88) 4.60 (1.77)
CP Pre-OP (Pre) 7.82 (5.29) 8.11 (4.32) 7.69 (3.15) 2.65 (1.31)
CP Post-OP (Post) 8.74 (4.79) 10.36 (5.94) 10.89 (5.96) 2.67 (1.69)
p (CON vs. Pre) 0.009� 0.012� 0.764 0.006�
�
p (CON vs. Post) 0.017 0.158 0.125 0.012�
p (Pre vs. Post) 0.569 0.203 0.084 0.974
Muscular Component (N/m)
Control (CON) 0.33 (0.18) 0.76 (0.26) 0.81 (0.20) 1.30 (0.52)
CP Pre-OP (Pre) 1.35 (0.97) 1.14 (0.86) 1.50 (1.20) 1.04 (0.70)
CP Post-OP (Post) 0.85 (0.67) 0.85 (0.70) 1.25 (1.07) 0.71 (0.56)
p (CON vs. Pre) 0.002� 0.162 0.064 0.317
p (CON vs. Post) 0.016� 0.693 0.174 0.013�
p (Pre vs. Post) 0.058 0.047� 0.482 0.012�
Ratio of Muscular & Skeletal components (%)
Control (CON) 2.59 6.18 10.40 30.29
CP Pre-OP (Pre) 21.77 19.91 21.97 47.81
CP Post-OP (Post) 13.66 12.54 15.25 33.02
p (CON vs. Pre) 0.001� 0.012� 0.027� 0.052
p (CON vs. Post) 0.016� 0.203 0.379 0.722
p (Pre vs. Post) 0.020� 0.013� 0.072 0.042�
�
Hip joint stiffness (%BW LL /degree)
Control (CON) 3.06 (1.00) 0.29 (0.06) 0.55 (0.16) 0.59 (0.19)
CP Pre-OP (Pre) 7.95 (5.92) 0.57 (0.32) 1.13 (0.70) 0.77 (0.38)
CP Post-OP (Post) 4.22 (2.98) 0.61 (0.60) 0.99 (0.36) 1.12 (0.50)
� � �
p (CON vs. Pre) 0.010 0.007 0.010 0.157
p (CON vs. Post) 0.214 0.078 0.001� 0.003�
p (Pre vs. Post) 0.031� 0.833 0.544 0.097
�
Knee joint stiffness (%BW LL /degree)
Control (CON) 1.32 (0.36) 1.15 (0.23) 0.41 (0.13) 0.11 (0.03)
CP Pre-OP (Pre) 2.65 (1.79) 0.89 (0.21) 0.53 (0.29) 0.83 (0.59)
CP Post-OP (Post) 1.80 (0.75) 0.73 (0.26) 0.48 (0.16) 0.26 (0.21)
p (CON vs. Pre) 0.020� 0.009� 0.231 0.000�
�
p (CON vs. Post) 0.059 0.000 0.260 0.021�
�
p (Pre vs. Post) 0.203 0.006 0.696 0.011�
�
Ankle joint stiffness (%BW LL /degree)
Control (CON) 0.46 (0.13) 0.82 (0.30) 2.03 (1.17) 0.74 (0.18)
CP Pre-OP (Pre) 1.06 (0.53) 1.43 (0.84) 1.33 (0.80) 0.98 (0.65)
CP Post-OP (Post) 1.07 (0.69) 1.58 (0.79) 1.34 (0.50) 1.14 (0.61)
(Continued )

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PLOS ONE Leg and joint stiffness in children with diplegic cerebral palsy during gait after tendon release surgery

Table 4. (Continued)

Load Response (LR) Mid-Stance (MS) Terminal Stance (TS) Pre-Swing (PS)
� �
p (CON vs. Pre) 0.001 0.026 0.101 0.241
p (CON vs. Post) 0.006� 0.005� 0.073 0.043�
p (Pre vs. Post) 0.932 0.509 0.959 0.484

p (CON vs. Pre-OP): p-value between Pre-OP of diplegic CP group and Control.
p (CON vs. Post-OP): p-value between Post-OP of diplegic CP group and Control.
p (Pre-OP vs. Post-OP): p-value between Pre-OP and Post-OP of diplegic CP group.
�
: significant difference (p<0.05).
BW: body weight; LL: leg length.

https://doi.org/10.1371/journal.pone.0245616.t004

Discussion
The current study aimed to quantify and compare the leg stiffness and the associated skeletal
and muscular components, as well as lower limb joint stiffness during the stance phase of gait
between healthy controls and children with diplegic CP before and after tendon release sur-
gery. Before TRS, the patients with diplegic CP walked with decreased leg stiffness but with
increased muscular contributions and joint stiffness when compared to healthy controls. After
TRS, the CP group kept the leg stiffness unaltered with significantly decreased muscular con-
tributions (i.e., decreased MS/SC ratio) and decreased joint stiffness at the hip and knee. This
was accompanied with postural adjustments, including decreased knee flexion and decreased
ankle plantarflexion during stance, for a more extended posture with reduced extensor
moments at the knee and a more stable base of support (better foot contact).
The TRS appeared to improve the lower limb joint kinematics and kinetics of the diplegic
CP group to be closer to those of the healthy controls, except for hip flexion and ankle plantar-
flexor moments which remained unchanged. The improvement included reduced hip extensor
moments during LR, reduced knee flexion angles during most of the stance phase, and
reduced knee extensor moments and ankle plantarflexion angles during TS and PS when com-
pared to Pre-OP. These results suggest that release of the tight tendons of the gastrocnemius
and hamstrings helped improve the motions at the ankle and knee, and thus the dynamic
alignment of the lower limb segments, contributing to the reduction of the extensor moments
at the knee and hip. The underlying strategy of such kinematic and kinetic changes could be
revealed through further analysis of the stiffness-related variables.
During loading response, or during the initial double-limb support phase, the CP group
showed significantly reduced leg stiffness with increased muscular contribution, as well as
increased joint stiffness at the hip, knee and ankle before TRS when compared to the Controls.
It has been suggested that the reduced leg stiffness in the CP group was as a result of the more
flexed posture of the lower limbs during body weight-transfer, as was the increased effort of
the muscles [21]. The TRS significantly decreased the hip joint stiffness and the muscular con-
tributions to the leg stiffness to be closer to those of the Control while keeping the leg stiffness
unaltered. The decreased joint stiffness at the hip helped reduce the effort for the subsequent
extension with improved dynamic lower limb alignment for weight-transfer during this
period. These changes may also be helpful for impact absorption with reduced muscle effort at
heel-strike in the relatively jerky CP gait, reducing the energy expenditure and improving the
endurance during the movement [38,39].
During mid-stance, similar to loading response, the CP group also showed significantly
reduced leg stiffness with increased muscular contribution, as well as increased joint stiffness
when compared to the Controls. These parameters are also related to the more flexed posture
of the stance limb [21]. The TRS improved the lower limb alignment and maintained the leg

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PLOS ONE Leg and joint stiffness in children with diplegic cerebral palsy during gait after tendon release surgery

stiffness with reduced, closer-to-normal knee joint stiffness and demands on the muscles. Dur-
ing terminal-stance, the CP group showed similar leg and joint stiffness values as compared to
the Controls, except with increased muscular contribution and hip joint stiffness. Therefore,
while the TRS improved the lower limb alignment, no significant changes on the leg and joint
stiffness were found during this period. Overall, during single-limb support when the body was
moving over the stationary foot, the TRS helped improve the lower limb alignment and achieve
closer-to-normal muscular contributions to the leg stiffness, which will be helpful for reducing
the risk of collapse owing to insufficient muscle strength when facing a sudden external load.
During pre-swing, or the terminal double-limb support, when the body weight was transferred
to the contralateral limb, the CP group showed significantly reduced leg stiffness with reduced
skeletal contribution, as well as increased knee joint stiffness when compared to the Controls.
After the TRS, the leg stiffness was not altered but the knee joint stiffness and muscular contribu-
tion to the leg stiffness were significantly reduced, while the hip and ankle joints’ stiffness were
increased. These changes showed the redistribution of the stiffness between the lower limb joints
following TRS. The stiffer ankle and hip with a more flexible knee in the trailing limb were helpful
for pushing the body forward and for the transfer of the body weight to the leading stance limb,
as well as for the subsequent forward movement of the trailing limb. While the TRS helped
improve the weight transfer performance during the pre-swing phase, it did not bring the leg
and joint stiffness variables to normal values. Other surgical or rehabilitative intervention may
be needed for further improvement of the remaining deviations in children with diplegic CP.
The current study showed that the TRS altered the stiffness control of the lower limb joints
during walking while retaining an unaltered whole leg stiffness in children with diplegic CP.
Such a change of control strategy was helpful for reducing the demand on the muscles in main-
taining the same leg stiffness and body posture against collapse. However, residual deficits and
associated deviations in leg and joint stiffness still remained. Rehabilitative training such as
muscle strengthening after TRS may be needed for further improving the leg and joint stiffness
control. The current study was the first attempt to use leg and joint stiffness to evaluate the effi-
cacy of TRS in diplegic CP. The current patients were limited to GMFCS grade II; for children
with different GMFCS grades, further studies will be needed. Another limitation was that the
subjects in this study were all male patients. Further study would be needed to test whether the
current results would apply to female patients. The current results encourage future applica-
tion of such analysis in the assessment of the efficacy of orthopaedic and rehabilitative treat-
ment in patients with walking impairments.

Conclusions
The control strategy of body support during gait in children with diplegic CP after TRS was
revealed through the analysis of leg and joint stiffness, the contributions of skeletal and muscu-
lar components, and the associated joint kinematics and kinetics. The CP group altered the
stiffness of the lower limb joints and decreased the demand on the muscular components
while maintaining an unaltered leg stiffness during stance phase after the TRS. The TRS sur-
gery improved the joint and leg stiffness control during gait although residual deficits and
associated deviations still remained. The analysis of leg stiffness and related variables in clinical
gait analysis could provide more information on treatment effects in children with CP.

Supporting information
S1 File.
(XLSX)

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PLOS ONE Leg and joint stiffness in children with diplegic cerebral palsy during gait after tendon release surgery

Author Contributions
Conceptualization: Chien-Chung Kuo, Ken N. Kuo, Tung-Wu Lu.
Data curation: Chien-Chung Kuo, Hsing-Po Huang, Ting-Ming Wang.
Formal analysis: Hsing-Po Huang, Shih-Wun Hong, Li-Wei Hung.
Resources: Chien-Chung Kuo, Ting-Ming Wang.
Supervision: Tung-Wu Lu.
Writing – original draft: Chien-Chung Kuo, Hsing-Po Huang, Ting-Ming Wang, Tung-Wu
Lu.
Writing – review & editing: Shih-Wun Hong, Li-Wei Hung, Ken N. Kuo, Tung-Wu Lu.

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