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Changes of calf muscle-tendon biomechanical properties induced by passive-

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Changes of calf muscle-tendon biomechanical properties induced
by passive-stretching and active-movement training in children with
cerebral palsy
Heng Zhao,1,2 Yi-Ning Wu,1,2 Miriam Hwang,1,3 Yupeng Ren,1,2 Fan Gao,4 Deborah Gaebler-Spira,1,2
and Li-Qun Zhang1,2
1
Rehabilitation Institute of Chicago, Chicago, Illinois; 2Northwestern University, Chicago, Illinois; 3Department of
Rehabilitation Medicine, Korea University College of Medicine, Seoul, Korea; and 4University of Texas Southwestern
Medical Center, Dallas, Texas
Submitted 22 November 2010; accepted in final form 17 May 2011
Zhao H, Wu Y, Hwang M, Ren Y, Gao F, Gaebler-Spira D,
Zhang LQ. Changes of calf muscle-tendon biomechanical properties
induced by passive-stretching and active-movement training in chil-
dren with cerebral palsy. J Appl Physiol 111: 435– 442, 2011. First
published May 19, 2011; doi:10.1152/japplphysiol.01361.2010.—
Biomechanical properties of calf muscles and Achilles tendon may be
altered considerably in children with cerebral palsy (CP), contributing
to childhood disability. It is unclear how muscle fascicles and tendon
respond to rehabilitation and contribute to improvement of ankle-joint
properties. Biomechanical properties of the calf muscle fascicles of
both gastrocnemius medialis (GM) and soleus (SOL), including the
fascicle length and pennation angle in seven children with CP, were
evaluated using ultrasonography combined with biomechanical mea-
surements before and after a 6-wk treatment of passive-stretching and
active-movement training. The passive force contributions from the
GM and SOL muscles were separated using flexed and extended knee
positions, and fascicular stiffness was calculated based on the fascic-
ular force-length relation. Biomechanical properties of the Achilles
tendon, including resting length, cross-sectional area, and stiffness,
were also evaluated. The 6-wk training induced elongation of muscle
fascicles (SOL: 8%, P ⫽ 0.018; GM: 3%, P ⫽ 0.018), reduced
pennation angle (SOL: 10%, P ⫽ 0.028; GM: 5%, P ⫽ 0.028),
reduced fascicular stiffness (SOL: 17%, P ⫽ 0.128; GM: 21%, P ⫽
0.018), decreased tendon length (6%, P ⫽ 0.018), increased Achilles
tendon stiffness (32%, P ⫽ 0.018), and increased Young’s modulus
(20%, P ⫽ 0.018). In vivo characterizations of calf muscles and
Achilles tendon mechanical properties help us better understand
treatment-induced changes of calf muscle-tendon and facilitate devel-
opment of more effective treatments.
muscle fascicles; Achilles tendon; stiffness; pennation; ultrasonogra-
phy
CEREBRAL PALSY (CP) IS A COMMON disorder of movement and
posture caused by a nonprogressive injury to the developing
brain (10, 33). The neurological disorder can cause secondary
changes in the musculoskeletal system, such as muscle weak-
ness, spasticity, and/or contractures around joints, which
makes CP a leading cause of childhood disability (5, 34).
Unlike adults with disabilities, children with CP face the risk of
further losing functional mobility during adolescence because
of ongoing secondary impairments, such as soft-tissue short-
ening, weakness, and bony deformity (7). As a result, children
who are ambulatory may change the need for assistance over
Address for reprint requests and other correspondence: L-Q. Zhang, North-
western Univ., 345 East Superior St., Ste. 1406, Chicago, IL 60611 (e-mail:
l-zhang@northwestern.edu).
http://www.jap.org 8750-7587/11 Copyright © 2011 the American Physiological Society
J Appl Physiol 111: 435–442, 2011.
First published May 19, 2011; doi:10.1152/japplphysiol.01361.2010.
time and become reliant on walkers or wheelchairs. These
changes are complex but are attributable to loss of strength,
poor alignment, and motivation (11). Efficient walking has
been one of the treatment goals for children with CP. The
ability to translate the tibia over the foot decreases the work of
walking and improves the gait-normalcy index. Of all of the
modalities to decrease muscle tone and improve range of
motion (ROM), a temporary decrease of motoneuron function
through botulinum toxin injections, selective section of sensory
roots involved in the hyperactive reflex pathway, orthopedic
surgery, and serial casting can have a significant effect but are
costly and invasive. Passive-stretching and active-movement
training is readily available as a part of a physical therapy
treatment session and home-exercise program, although its
effect size may be moderate (e.g., ⬍10° improvement through
stretching) (31, 45). Clinically, a physical therapist (PT) ma-
nipulates the joint and moves it throughout the ROM to reduce
spasticity/contracture. Despite therapy and home programs that
include stretching, the effects of passive stretching may not
persist. In addition, manual stretching by PTs is laborious, and
the outcome depends on subjective assessments, such as the
PT’s “end feel”. Splints, casts, tilt-table, and some other
external devices are also applied to assist treating the patients,
among which, continuous passive motion (CPM) devices are
widely used to prevent postoperative adhesion and reduce joint
stiffness (24). However, CPM machines can only move the
limb at a constant speed between two prescribed joint posi-
tions. The passive movement does not usually stretch into the
extreme positions, where contracture/spasticity is significant.
Controlled, passive ankle stretching has been used to treat
ankle contracture and spasticity in neurologically impaired
patients (46). The stretching device is driven by a servomotor,
controlled by a digital signal processor. The stretching velocity
is controlled to be inversely proportional to the joint-resistance
torque, so that near the ROM limits, the muscles/tendons
involved are stretched slowly and safely. Once the specific
peak-resistance torque is reached, the motor holds the joint at
the extreme positions for a prescribed period of time, which
can be conveniently adjusted. In addition to the passive-
stretching mode, the intelligent ankle-stretching device can be
operated in active-movement mode and provide assistance or
resistance to the subject’s voluntary ankle movement. Moti-
vated by interactive games, the subject can actively move the
ankle through the ROM, and the exercise intensity can be
adjusted progressively by changing the training difficulty level
and the assistance/resistance level. In addition, the intelligent
435
436 MUSCLE-TENDON CHANGES AFTER PASSIVE-ACTIVE TRAINING IN CP

ankle-stretching device is portable, which provides convenient

and low-cost treatment for children with CP.
The functional outcome of treating ankle joints with con-
tracture/spasticity in stroke survivors using controlled stretch-
ing has been investigated (35, 46). However, the studies were
mainly focused on the biomechanical evaluations of the ankle
joint, including stiffness, viscosity, and ROM. A detailed
understanding of in vivo calf muscle fascicles and tendon
adaptations may help us to assess the efficacy of such treat-
ment. In vivo gastrocnemius (GS) muscle architecture in chil-
dren with CP has been investigated using ultrasonography, and
shortened muscle fascicles were reported (8, 23, 25, 26).
Several studies have also been carried out to investigate the
calf muscles or tendon mechanical changes induced by re-
peated stretching and resistant exercise in able-bodied subjects
(17, 27).
The objective of the present study was to investigate changes
in mechanical properties of calf muscle fascicles and Achilles
tendon in children with CP before and after a 6-wk combined
passive-stretching and active-movement training program. We
hypothesized that the 6-wk combined passive-stretching and
active-movement treatment would elongate the calf muscle
fascicles and reduce fascicular stiffness and pennation angle on
the one hand and reduce Achilles tendon length and increase its
stiffness and Young’s modulus on the other hand.
METHODS

Participants
Seven children with spastic CP participated in the study (four
hemiplegic and three diplegic; one female and six male). Mean age
was 9.3 ⫾ 3.2 (range 5⬃15) yr. All of the children could follow
instructions, and they were able to walk independently, with two of
them at Gross Motor Function Classification System (GMFCS) Level
II and five of them at GMFCS Level I.
Experimental Setup
The participants were treated over a 6-wk period of time using the
intelligent ankle-stretching device shown in Fig. 1A. The device was
attached to a chair, where the child was seated comfortably with the
leg supported by a brace and fixed at a prescribed position. The foot
of the patient was secured to a footplate with the center of rotation of
the ankle aligned with the motor-rotation axis. The ankle-joint torque
and position were sampled by a digital signal processor, which
controlled the joint movement and communicated with the display
computer to show the interactive games.
Before and after the 6-wk treatment, ultrasound evaluations were
performed. The setup was comprised of a custom-made knee–ankle-
joint driving device, a GE LOGIQ 9 ultrasound imaging system with
a 12-MHz high-resolution matrix probe M12L (GE Healthcare,
Waukesha, WI) and a data acquisition computer (Fig. 1B). Ultrasound
and biomechanical properties of the soleus (SOL) and GS muscle
fascicles and Achilles tendon were evaluated. The subject lay prone
with the ankle and knee aligned with the custom knee–ankle-joint
driving device and the joint torque and position measured synchro-
nously with the ultrasound images of calf fascicles and Achilles
tendon. Further information about the evaluation setup can be found
in ref. (47), except that the chair in the knee-ankle device was replaced
by a bed with the subject lying down in a prone position.
Experimental Design
Passive-stretching and active-movement training. The patients
went through a three-sessions/wk, 6-wk program of combined passive
Fig. 1. A: ankle intelligent stretching device used for the combined passive-
stretching and active-movement training over 6 wk. B: ultrasound and biome-
chanical evaluations of the soleus (SOL) and gastrocnemius (GS) muscle
fascicles and Achilles tendon. The subject lay prone with the ankle and knee
aligned with the custom knee–ankle-joint driving device with the joint torque
and position measured synchronously with the ultrasound images.
ankle-stretching and active-movement training (45). Each training
session consisted of 20-min passive-stretching, 30-min active-move-
ment training, followed by 10-min passive stretching on the subject’s
impaired (for hemiplegic CP) or more impaired (in diplegic CP) side
(45). The participants sat upright comfortably and were asked to relax
during the passive stretching; the predetermined torque was applied to
strenuously stretch the calf muscle toward extreme dorsiflexion.
During the active-movement training, the participants used the ankle
rehabilitation robot and actively engaged themselves in computer
games to exercise the ankle joint in both dorsiflexion and plantar
flexion. The robot provided assistance if the subject had difficulty
finishing the movement task, and it provided resistance if the subject
could perform the task easily (45).
Outcome Evaluations Using Ultrasonic and
Biomechanical Measurements
Before and after the 18 training sessions, biomechanical properties
of the calf muscles and Achilles tendon on the impaired (for hemi-
plegic CP) or more impaired (in diplegic CP) side were evaluated
using ultrasonography combined with biomechanical measurements.
The participant lay down in a prone position with the thigh and trunk
secured to the bed using Velcro straps. The leg and foot were securely
attached to the leg linkage and footplate, respectively, and the knee
and ankle joints aligned with the motor-rotation axes. To evaluate
muscle fascicle properties, the ankle was fixed at various positions (at

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 MUSCLE-TENDON CHANGES AFTER PASSIVE-ACTIVE TRAINING IN CP
10° intervals) across the participant’s ankle ROM. All measurements
were obtained with the knee in 90° flexion and full extension to
separate ankle-joint torque contributions from the SOL and GS
muscles. The ankle-joint torque and the ultrasound image of the SOL
and GS medialis (GM) muscle, at every knee-ankle configuration,
were recorded, and the subject was asked to relax during the mea-
surement.
GM and SOL Fascicle Images
To improve the accuracy of the GM fascicle measurement, the
probe was moved, scanning the transverse plane of the distal mus-
cle belly of GM to locate the fascicle plane. Once the middle of the
ultrasound image at the deep aponeurosis of GM was parallel to the
bottom of the image, the probe was rotated 90°, and the image plane
was regarded as being aligned with the fascicle plane (2). The probe
was then moved proximally within the fascicle plane to cover the full
longitudinal image of the GM muscle using an extended field-of-view
technique called LOGIQView (41). To obtain the SOL fascicle image,
the probe was moved along the posterior lower leg, scanning the
sagittal plane using LOGIQView. The representative fascicle images
of GM and SOL muscles are shown in Fig. 2, A and B.
Measurement of Muscle Fascicle Length and Pennation Angle
In this study, the average fascicle length was defined as the length
of the fascicle halfway between the middle-muscle belly and the distal
muscle-tendon junction (MTJ). Usually, the clearest fascicle in the
region was selected for length measurement. For GM, the pennation
angle was defined as the angle between the fascicle selected for length
measurement and deep aponeurosis of GM. For SOL, the pennation
angle was defined as the angle between the fascicle selected for length
measurement and superficial aponeurosis of SOL. ImageJ (National
Institutes of Health, Bethesda, MD) software was used to measure the
fascicle length and pennation angles displayed in Fig. 2, A and B.
Achilles Tendon Mechanical Properties
The Achilles tendon was scanned in the sagittal plane at rest using
a special function of LOGIQ 9, called LOGIQView, and the tendon
Fig. 2. Representative LOGIQView images of (A) SOL and (B) GS medialis
(GM) muscles, demonstrating fascicle length and pennation angle measure-
ment. Some landmarks, including muscle-tendon junction and muscle belly,
are also marked on the images. MG, medial GS.
J Appl Physiol • VOL 111 • AUGUST 2011 •
437
resting length was measured using ImageJ. The transverse plane of the
Achilles tendon was scanned to measure the cross-sectional area
(CSA). The tendon moment arm was measured using a physical
measurement and ultrasonography combined method. Then, the sub-
ject performed a controlled isometric plantar flexion effort, following
the target and actual torques displayed in real-time on the monitor,
with the ultrasound video and ankle-joint torque recorded synchro-
nously. The tendon-length change was calculated by tracking the
displacement of MTJ between frames in the ultrasound video. The
tendon force was computed from the joint torque and tendon moment
arm. The tendon stiffness was further calculated based on the tendon
elongation and force. The detailed methods were described in
ref. (47).
SOL and GM Muscle Fascicular Stiffness
The Achilles tendon moment arm at 0° dorsiflexion was measured
for each subject. The values of the moment arm at other ankle-joint
angles were computed based on the moment arm at 0° dorsiflexion
and the moment arm–ankle-joint angle relation curve obtained from
Software for Interactive Muskuloskeletal Modeling (SIMM; Motion
Analysis, Santa Rosa, CA). It was assumed that the passive tension of
the GS muscle was negligible at 90° knee flexion (9, 27a). Therefore,
most of the ankle-resistance torque at 90° knee flexion came from the
SOL muscle. The SOL passive force was then calculated in the range
of 20° plantar flexion to 10° dorsiflexion. The corresponding SOL
fascicular force was scaled by 1/cos(␪SOL), with ␪SOL as the pennation
of SOL fascicles. The GS contribution to the ankle passive-resistance
torque was estimated as the difference of the passive ankle-resistance
torque between full knee extension and 90° knee flexion, as GS
muscles are major ankle plantar flexors crossing the knee joint. The
GS passive force was also calculated in the range of 20° plantar
flexion to 10° dorsiflexion. The passive force from GM was deter-
mined as 61% of the total passive GS force based on the method
described in refs. (6, 9). The corresponding GM fascicular force was
scaled by 1/cos(␪GM), with ␪GM as the pennation of GM fascicles. The
fascicular stiffness of GM and SOL was determined as the slope of
their force–fascicle length relation curves.
Statistical Analysis
Nonparametric analysis (Friedman test and Wilcoxon’s signed
ranks test) was used to analyze the response variables (fascicle length
and stiffness, pennation angle, and Achilles tendon length) with
respect to the factors (pre- and post-treatment, ankle position, knee
position). Spearman’s rank correlation was used to test the monotonic
trend (e.g., if one variable is increased, then the other one also
follows). The significance level was set at 0.05. The results were
presented as means ⫾ SD unless specified otherwise.
RESULTS
SOL and GM Fascicle Length and Pennation Angle
As a uniarticular muscle, the SOL muscle fascicle length
varied with ankle angle (P ⬍ 0.001). The fascicle length
increased monotonically as the ankle dorsiflexed (P ⫽ 0.003).
After the 6-wk treatment, SOL fascicle length increased
significantly at both full knee extension (Fig. 3A) and 90° knee
flexion (Fig. 3B; P ⬍ 0.001). For example, at full knee
extension and 0° ankle dorsiflexion, SOL fascicle length in-
creased significantly (P ⫽ 0.018) from 24.8 ⫾ 8.2 mm to
26.8 ⫾ 8.6 mm (Fig. 3A). At 90° knee flexion and 0° ankle
dorsiflexion, SOL fascicle length increased significantly (P ⫽
0.018) from 24.4 ⫾ 8.0 mm to 26.5 ⫾ 8.5 mm (Fig. 3).
Together with elongation of SOL fascicles after the 6-wk
treatment, the SOL pennation angle decreased significantly at
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438 MUSCLE-TENDON CHANGES AFTER PASSIVE-ACTIVE TRAINING IN CP

Fig. 3. Fascicle length before (gray lines) and

after (black lines) the 6-wk treatment of pas-
sive-stretching and active-movement training.
A: SOL fascicle length measured at full knee
extension; B: SOL fascicle length measured at
90° knee flexion. The error bars represent the
SEM. C: GM fascicle length measured at full
knee extension. D: GM fascicle length mea-
sured at 90° knee flexion. The error bars rep-
resent SEM. Shading indicates a significant
difference between before and after the 6-wk
treatment.

the extended (Fig. 4A) and flexed (Fig. 4B) knee positions (P ⬍ and 0° ankle dorsiflexion, SOL pennation angle decreased
0.001). For example, at 0° ankle dorsiflexion and full knee significantly (P ⫽ 0.028) from 24.9 ⫾ 4.9° to 22.3 ⫾ 4.6°.
extension, the pennation angle decreased significantly (P ⫽ As a biarticular muscle, the GM muscle fascicle length
0.028) from 24.5 ⫾ 4.8° to 22.1 ⫾ 4.5°, and at 90° knee flexion varied with both ankle (P ⬍ 0.001) and knee flexion (P ⬍

Fig. 4. Pennation angle before (gray lines) and

after (black lines) the 6-wk treatment. A: SOL
pennation angle measured at full knee exten-
sion; B: SOL pennation angle measured at 90°
knee flexion. The error bars represent the
SEM. C: GM pennation angle measured at full
knee extension; D: GM pennation angle mea-
sured at 90° knee flexion, with the error bars
also representing the SEM. Shading indicates
a significant difference between before and
after the 6-wk treatment.

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 MUSCLE-TENDON CHANGES AFTER PASSIVE-ACTIVE TRAINING IN CP 439

Fig. 6. Comparisons of the Achilles tendon resting length and SOL and GM
fascicle lengths measured at full knee extension and 0° ankle dorsiflexion
before and after the 6-wk treatment. ** Significant difference with P ⬍ 0.01.

the fascicles became longer and less stiff. For example, at 0°

ankle dorsiflexion and full knee extension, the passive SOL
fascicle stiffness decreased slightly (P ⫽ 0.128) from 33.3 ⫾
10.4 N/mm before training to 27.6 ⫾ 12.5 N/mm after training,
whereas the passive stiffness of GM fascicles reduced signif-
icantly (P ⫽ 0.018) from 12.2 ⫾ 3.8 N/mm to 9.6 ⫾ 3.6 N/mm.
Achilles Tendon Mechanical Properties
After training, Achilles tendon length decreased (P ⫽ 0.018)
from 55.7 ⫾ 9.9 mm to 52.6 ⫾ 9.4 mm, as opposed to a length
Fig. 5. A: SOL fascicular force-length relation curve before (gray line) and increase of SOL and GM fascicles measured at 0° dorsiflexion
after (black line) the 6-wk treatment of combined passive-stretching and and full knee extension (Fig. 6), whereas no significant change
active-movement training. B: GM fascicular force-length relation curve before of CSA was found (P ⫽ 0.063). Achilles tendon stiffness
(gray line) and after (black line) the treatment. The error bars represent the
SEM. Shading indicates a significant difference between before and after the
increased significantly from 86.8 ⫾ 16.9 N/mm to 114.4 ⫾
6-wk treatment. 16.0 N/mm (P ⫽ 0.018), and the Young’s modulus increased
significantly (P ⫽ 0.018) from 113.6 ⫾ 34.9 megapascals
(MPa) to 136.8 ⫾ 38.8 MPa, as opposed to stiffness decrease
0.001). The fascicle length increased monotonically as the
of SOL and GM fascicles, measured at 0° dorsiflexion and full
ankle dorsiflexed (P ⫽ 0.004) but decreased as the knee flexed
knee extension (Fig. 7).
(P ⬍ 0.0001).
Similar to the SOL muscle, the GM muscle showed signif-
icantly increased fascicle length (Fig. 3, C and D, P ⬍ 0.001)
and decreased pennation angle (Fig. 4, C and D, P ⬍ 0.001) at
both full knee extension and 90° knee flexion after the 6-wk
training. For example, at 0° ankle dorsiflexion and full knee
extension, GM fascicle length increased significantly (P ⫽
0.018) from 40.2 ⫾ 6.6 mm to 41.5 ⫾ 5.9 mm, and pennation
angle decreased significantly (P ⫽ 0.028) from 16.7 ⫾ 2.9° to
16.0 ⫾ 2.8°. At 90° knee flexion and 0° ankle dorsiflexion, GM
fascicle length increased significantly (P ⫽ 0.018) from 29.3 ⫾
6.2 mm to 30.9 ⫾ 5.5 mm, and pennation angle decreased
significantly (P ⫽ 0.043) from 21.9 ⫾ 4.0° to 20.8 ⫾ 3.3°.
SOL and GM Muscle Fascicular Stiffness
With the SOL and GM fascicular force at four ankle posi-
tions, calculated from the ankle-joint torque using the method
previously described (47), the mean results over the subjects
were plotted with respect to the fascicle length and curve fitted
Fig. 7. Comparisons of the Achilles tendon stiffness and SOL and GM
using second order polynomial as shown in Fig. 5, A and B. For fascicular stiffness lengths measured at full knee extension and 0° ankle
both SOL and GM, the force-length curves shifted to the right dorsiflexion before and after the 6-wk treatment. *Significant difference with
and became less steep after the 6-wk training, indicating that P ⬍ 0.05; **significant difference with P ⬍ 0.01.

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440 MUSCLE-TENDON CHANGES AFTER PASSIVE-ACTIVE TRAINING IN CP
DISCUSSION
In the present study, changes of GM and SOL muscle
fascicles and Achilles tendon mechanical properties induced by
passive-stretching and active-movement training were evalu-
ated in vivo and noninvasively using ultrasound in children
with CP. Results showed significant changes of physical di-
mension and biomechanical properties in calf muscle fascicles
and Achilles tendon after training, including increased calf
muscle fascicle length, decreased pennation angle, decreased
fascicular stiffness, shortened Achilles tendon, and increased
tendon stiffness, indicating the adaptability and responsiveness
of the children’s growing muscles and tendons to the treatment.
The results on GM muscle architecture, such as fascicle
length (ranged from 25.87 ⫾ 5.61 to 41.78 ⫾ 6.89 mm across
the tested ankle and knee positions) and pennation angle
(ranged from 15.76 ⫾ 2.82° to 24.90 ⫾ 5.05°; 20.17 ⫾ 4.36°
at ankle resting position and full knee extension), in children
with CP agree with previous studies (1, 23, 25, 26, 37, 38, 42a).
The Achilles tendon length quantified at neutral ankle and 90°
knee flexion changed from 55.7 ⫾ 9.9 mm to 52.6 ⫾ 9.4 mm
postintervention, which was in agreement with a previous
study (8), in which Achilles tendon length was measured
across larger ankle and knee range (45.7 ⫾ 3.8 mm to 64.1 ⫾
10.3 mm). There is a lack of published results on SOL muscle
fascicle length in children with CP for relevant comparisons,
but in young adults, SOL muscle fascicle length ranged from
29 ⫾ 5 mm to 43 ⫾ 5 mm across various ankle and knee
positions (12), which were considerably longer than those in
the children with CP in the current study (ranged from 21.3 ⫾
7.4 mm to 26.6 ⫾ 7.9 mm and from 24.2 ⫾ 7.9 mm to 28.2 ⫾
8.5 mm pre- and postintervention, respectively).
Achilles tendon stiffness (86.8 ⫾ 16.9 N/mm and 114.4 ⫾
16.0 N/mm pre- and postinterventions, respectively) in the
current study falls into the wide range of tendon stiffness
reported in the literature. For example, in adult human subjects,
the tendon stiffness was reported as 30 N/mm (17), 150 N/mm
(18a), 180 N/mm (18), and 330 N/mm (28). Young’s modulus
of the Achilles tendon was measured in vivo as 788 MPa in
adult male subjects (22) and in vitro on adult cadaver speci-
mens as 820 MPa (43), whereas the modulus in rats was
reported as 33–53 MPa (4). In the current study, Young’s
modulus of the Achilles tendon included 113.6 ⫾ 34.9 MPa
and 136.8 ⫾ 38.8 MPa pre- and postinterventions, respectively.
The tendon stiffness and Young’s modulus from kids in the
current study were lower than those reported on adults. The
difference might be attributed to factors including aging (30),
test protocol (e.g., loading rate) (43), and specimen condition
(i.e., in vivo or in vitro) (39), as well as experimental errors in
the different studies. It was reported that with growing and
aging, tendons become much stronger and stiffer than at birth
(36). Differences in Achilles tendon stiffness and Young’s
modulus between data in literature and our results might also
be attributed to overall nonlinear tendon stress-strain proper-
ties. In the present study, Young’s modulus and stiffness were
calculated under submaximal contractions within the manage-
able force range of children with CP, whereas some other
studies used much higher forces with muscles under maximal
voluntary contraction (19 –21).
As shown in RESULTS, the Achilles tendon was much stiffer
than GM and SOL fascicles under passive condition, which
J Appl Physiol • VOL
reflects the difference in stiffness between muscles and tendons
in general (Fig. 7). Furthermore, GM fascicles were less stiff
than SOL fascicles at both sides, which could be related to the
different functional roles played by the biarticular GM (mostly
fast-twitch fibers with strong contractions and rapid develop-
ment of large tension) and uniarticular SOL (mostly slow-
twitch fibers and long, sustaining contractions) muscles (40).
Significant fascicle elongation, reduction in pennation, and
decrease in fascicular stiffness were observed in both SOL and
GS muscles after the 6-wk intensive treatment of combined
passive-stretching and active-movement training, which indi-
cates that the passive-stretching and active-movement treat-
ment loosened up the stiff muscles and reduced the tension in
muscle fascicles. It was reported that stretching of muscles
may delay atrophy and can even cause growth (3, 13, 14). The
passive-stretching and active-movement training may be espe-
cially effective in reducing muscle stiffness and preventing
contracture for growing children with highly adaptive muscles
and tendons. The treatment-induced tension reduction could be
due to tension reduction in muscle fascicles themselves and/or
in connective tissues around the muscle fascicles and the whole
muscle. Furthermore, the results showed relatively greater
changes in fascicles/tendon stiffness than the fascicles/tendon
length changes, which may be due to the combined effect of
the fascicle/tendon length and force changes on the stiffness
changes.
Biomechanical properties of the Achilles tendon were
changed significantly after the 6-wk combined passive-stretch-
ing and active-movement training, indicating that the growing
tendons of the children were responsive to the treatment. It was
reported that the combined stiffness of tendon and aponeurosis
increased significantly after 8-wk, 4 sessions/wk, resistance
training (18.8%) or resistance and static-stretching training
(15.3%) (17), whereas 3-wk static stretching at 35° dorsiflex-
ion with the ankle at the standing position induced reduction in
tendon-aponeurosis viscosity but no effect on its elasticity (16).
Achilles tendon mechanical properties were shown degraded in
the elderly, characterized as reduced stiffness, and a three
times/wk over 14-wk resistance exercise training reversed the
process and increased tendon stiffness significantly by ⬃65%
(32). In an animal study, 21-day passive stretching on the ankle
significantly increased the tendon maximum stress (⬃21%)
and modulus of elasticity (⬃55%) (4). The increase in tendon
stiffness could be attributed to adaptation and remodeling of
tendon structure subject to mechanical stimuli at the cellular level,
and evidences have been shown in both animal and human
experimental (4, 15) and theoretical studies (42). Further studies
need to be carried out to differentiate the changes induced by the
passive-stretching and active-movement training.
There were limitations with the study. The fascicular force-
length relation might be affected by the simplified model of
calculating the fascicular force from the ankle-joint dorsiflex-
ion-resistance torque. The model assumed that the torque
contribution from SOL did not change with knee flexion angle,
and most ankle torque at 90° knee flexion came from SOL.
Moreover, the model did not take into account the torque
contribution from other muscles and soft tissues, the intramus-
cular force, and the complicated relation between muscle force
and fascicular force. Nevertheless, according to Fig. 3, A and
B, the fascicle length of SOL did not change much from 90°
knee flexion to full knee extension, indicating the resistance
111 • AUGUST 2011 • www.jap.org
 MUSCLE-TENDON CHANGES AFTER PASSIVE-ACTIVE TRAINING IN CP
torque from SOL did not change with knee flexion angle. In
addition, the sample size of the present study was relatively
small. More subjects should be included in future studies.
In the present study, architectural and mechanical properties
of GM and SOL muscle fascicles and Achilles tendon in
children with CP were evaluated before and after a 6-wk
program of passive-stretching and active-movement training.
Increased calf muscle fascicle length and decreased fascicular
stiffness, decreased tendon resting length, and increased tendon
stiffness were induced by the 6-wk training. The combined
ultrasonic and biomechanical evaluations help us understand
calf muscle and Achilles tendon functions and gain insight into
the closely related biomechanical changes of calf muscles and
Achilles tendon in neurological disorders, provide quantitative
assessment for rehabilitation treatment, and conduct CP reha-
bilitation more effectively.
GRANTS
The authors acknowledge the support of the National Institutes of Health
and National Institute on Disability and Rehabilitation Research.
DISCLOSURES
The rehabilitation robotic device used in the 6-wk treatment part in this
study is developed by Rehabtek LLC (Wilmette, IL) under federal Small
Business Technology Transfer grant support. L-Q. Zhang and Y. Ren have
equity positions in Rehabtek.
REFERENCES
1. Barrett RS, Lichtwark GA. Gross muscle morphology and structure in
spastic cerebral palsy: a systematic review. Dev Med Child Neurol 52:
794 –804, 2010.
2. Benard MR, Becher JG, Harlaar J, Huijing PA, Jaspers RT. Anatom-
ical information is needed in ultrasound imaging of muscle to avoid
potentially substantial errors in measurement of muscle geometry. Muscle
Nerve 39: 652–665, 2009.
3. Buschbacher RM, Porter CD. Deconditioning, conditioning, and
the benefits of exercise. In: Physical Medicine and Rehabilitation
(2nd ed.), edited by Braddom RL. Philadelphia, PA: W. B. Sauders,
2000, p. 702–726.
4. de Almeida F, Tomiosso T, Nakagaki W, Gomes L, Matiello-Rosa S,
Pimentel E. Effects of passive stretching on the biochemical and biome-
chanical properties of calcaneal tendon of rats. Connect Tissue Res 50:
279 –284, 2009.
5. Engsberg JR, Ross SA, Olree KS, Park TS. Ankle spasticity and
strength in children with spastic diplegic cerebral palsy. Dev Med Child
Neurol 42: 42–47, 2000.
6. Fukunaga T, Roy RR, Shellock FG, Hodgson JA, Day MK, Lee PL,
Wong-Fu H, Edgerton VR. Physiological cross-sectional area of human
leg muscles based on magnetic resonance imaging. J Orthop Res 10:
926 –934, 1992.
7. Gajdosik CG, Cicirello N. Secondary conditions of the musculoskeletal
system in adolescents and adults with cerebral palsy. Phys Occup Ther
Pediatr 21: 49 –68, 2001.
8. Gao F, Zhao H, Gaebler-Spira D, Zhang L-Q. In vivo evaluations of
morphological changes of gastrocnemius muscle fascicles and Achilles
tendon in children with cerebral palsy. Am J Phys Med Rehab 90:
364 –371, 2011.
9. Gao F, Grant TH, Roth EJ, Zhang LQ. Changes in passive mechanical
properties of the gastrocnemius muscle at the muscle fascicle and joint
levels in stroke survivors. Arch Phys Med Rehabil 90: 819 –826, 2009.
10. Hagberg B, Hagberg G, Olow I. The changing panorama of cerebral
palsy in Sweden. IV. Epidemiological trends 1959 –78. Acta Paediatr
Scand 73: 433–440, 1984.
11. Hanna SE, Rosenbaum PL, Bartlett DJ, Palisano RJ, Walter SD,
Avery L, Russell DJ. Stability and decline in gross motor function among
children and youth with cerebral palsy aged 2 to 21 years. Dev Med Child
Neurol 51: 295–302, 2009.
12. Kawakami Y, Ichinose Y, Fukunaga T. Architectural and functional
features of human triceps surae muscles during contraction. J Appl Physiol
85: 398 –404, 1998.
J Appl Physiol • VOL 111 • AUGUST 2011 •
441
13. Kemp TJ, Sadusky TJ, Saltisi F, Carey N, Moss J, Yang SY, Sassoon
DA, Goldspink G, Coulton GR. Identification of Ankrd2, a novel skeletal
muscle gene coding for a stretch-responsive ankyrin-repeat protein.
Genomics 66: 229 –241, 2000.
14. Kemp TJ, Sadusky TJ, Simon M, Brown R, Eastwood M, Sassoon DA,
Coulton GR. Identification of a novel stretch-responsive skeletal muscle
gene (Smpx). Genomics 72: 260 –271, 2001.
15. Kjaer M, Langberg H, Heinemeier K, Bayer ML, Hansen M, Holm L,
Doessing S, Kongsgaard M, Krogsgaard MR, Magnusson SP. From
mechanical loading to collagen synthesis, structural changes and function
in human tendon. Scand J Med Sci Sports 19: 500 –510, 2009.
16. Kubo K, Kanehisa H, Fukunaga T. Effect of stretching training on the
viscoelastic properties of human tendon structures in vivo. J Appl Physiol
92: 595–601, 2002.
17. Kubo K, Kanehisa H, Fukunaga T. Effects of resistance and stretching
training programmes on the viscoelastic properties of human tendon
structures in vivo. J Physiol 538: 219 –226, 2002.
18. Lichtwark GA, Wilson AM. In vivo mechanical properties of the human
Achilles tendon during one-legged hopping. J Exp Biol 208: 4715–4725,
2005.
18a.Maganaris CN. Tensile properties of in vivo human tendinous tissue. J
Biomech 35: 1019 –1027, 2002.
19. Maganaris CN, Paul JP. In vivo human tendon mechanical properties. J
Physiol 521: 307–313, 1999.
21. Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M. Load-displace-
ment properties of the human triceps surae aponeurosis in vivo. J Physiol
531: 277–288, 2001.
22. Magnusson SP, Hansen P, Aagaard P, Brond J, Dyhre-Poulsen P,
Bojsen-Moller J, Kjaer M. Differential strain patterns of the human
gastrocnemius aponeurosis and free tendon, in vivo. Acta Physiol Scand
177: 185–195, 2003.
23. Malaiya R, McNee AE, Fry NR, Eve LC, Gough M, Shortland AP. The
morphology of the medial gastrocnemius in typically developing children
and children with spastic hemiplegic cerebral palsy. J Electromyogr
Kinesiol 17: 657–663, 2007.
24. McNair PJ, Dombroski EW, Hewson DJ, Stanley SN. Stretching at the
ankle joint: viscoelastic responses to holds and continuous passive motion.
Med Sci Sports Exerc 33: 354 –358, 2001.
25. Mohagheghi AA, Khan T, Meadows TH, Giannikas K, Baltzopoulos
V, Maganaris CN. Differences in gastrocnemius muscle architecture
between the paretic and non-paretic legs in children with hemiplegic
cerebral palsy. Clin Biomech (Bristol, Avon) 22: 718 –724, 2007.
26. Mohagheghi AA, Khan T, Meadows TH, Giannikas K, Baltzopoulos
V, Maganaris CN. In vivo gastrocnemius muscle fascicle length in
children with and without diplegic cerebral palsy. Dev Med Child Neurol
50: 44 –50, 2008.
27. Morse CI, Degens H, Seynnes OR, Maganaris CN, Jones DA. The
acute effect of stretching on the passive stiffness of the human gastroc-
nemius muscle tendon unit. J Physiol 586: 97–106, 2008.
27a.Muraoka T, Chino K, Muramatsu T, Fukunaga T, Kanehisa H. In
vivo passive mechanical properties of the human gastrocnemius muscle
belly. J Biomech 38: 1213–1219, 2005.
28. Muraoka T, Muramatsu T, Fukunaga T, Kanehisa H. Geometric and
elastic properties of in vivo human Achilles tendon in young adults. Cells
Tissues Organs 178: 197–203, 2004.
30. Nakagawa Y, Hayashi K, Yamamoto N, Nagashima K. Age-related
changes in biomechanical properties of the Achilles tendon in rabbits. Eur
J Appl Physiol Occup Physiol 73: 7–10, 1996.
31. Pin T, Dyke P, Chan M. The effectiveness of passive stretching in
children with cerebral palsy. Dev Med Child Neurol 48: 855–862, 2006.
32. Reeves ND. Adaptation of the tendon to mechanical usage. J Musculosk-
elet Neuronal Interact 6: 174 –180, 2006.
33. Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, Damiano D,
Dan B, Jacobsson B. A report: the definition and classification of cerebral
palsy April 2006. Dev Med Child Neurol 109: 8 –14, 2007.
34. Sanger TD, Delgado MR, Gaebler-Spira D, Hallett M, Mink JW.
Classification and definition of disorders causing hypertonia in childhood.
Pediatrics 111: e89 –e97, 2003.
35. Selles RW, Li X, Lin F, Chung SG, Roth EJ, Zhang LQ. Feedback-
controlled and programmed stretching of the ankle plantarflexors and
dorsiflexors in stroke: effects of a 4-week intervention program. Arch Phys
Med Rehabil 86: 2330 –2336, 2005.
36. Shadwick RE. Elastic energy storage in tendons: mechanical differences
related to function and age. J Appl Physiol 68: 1033–1040, 1990.
www.jap.org
442 MUSCLE-TENDON CHANGES AFTER PASSIVE-ACTIVE TRAINING IN CP
37. Shortland AP, Harris CA, Gough M, Robinson RO. Architecture of the
medial gastrocnemius in children with spastic diplegia. Dev Med Child
Neurol 43: 796 –801, 2001.
38. Shortland AP, Harris CA, Gough M, Robinson RO. Architecture of the
medial gastrocnemius in children with spastic diplegia. Dev Med Child
Neurol 44: 158 –163, 2002.
39. Smith C, Young I, Kearney J. Mechanical properties of tendons: changes
with sterilization and preservation. J Biomech Eng 118: 56 –61, 1996.
40. Staron RS, Kraemer WJ, Hikida RS, Fry AC, Murray JD, Campos
GER. Fiber type composition of four hindlimb muscles of adult Fisher
344 rats. Histochem Cell Biol 111: 117–123, 1999.
41. Weng L, Tirumalai AP, Lowery CM, Nock LF, Gustafson DE, Von
Behren PL, Kim JH. US extended-field-of-view imaging technology.
Radiology 203: 877–880, 1997.
42. Wren TA, Beaupre GS, Carter DR. Tendon and ligament adaptation to
exercise, immobilization, and remobilization. J Rehabil Res Dev 37:
217–224, 2000.
J Appl Physiol • VOL 111 • AUGUST 2011 •
View publication stats
42a.Wren TA, Cheatwood AP, Rethlefsen SA, Hara R, Perez FJ, Kay RM.
Achilles tendon length and medial gastrocnemius architecture in children
with cerebral palsy and equinus gait. J Pediatr Orthop 30: 479 –484, 2010.
43. Wren TA, Yerby SA, Beaupre GS, Carter DR. Mechanical properties of
the human Achilles tendon. Clin Biomech (Bristol, Avon) 16: 245–251,
2001.
45. Wu YN, Hwang M, Ren Y, Gaebler-Spira DJ, Zhang LQ. Combined
passive stretching and active movement rehabilitation of lower-limb im-
pairments in children with cerebral palsy using a portable robot. Neurore-
habil Neural Repair 25: 378 –385, 2011.
46. Zhang LQ, Chung SG, Bai Z, Xu D, van Rey EM, Rogers MW,
Johnson ME, Roth EJ. Intelligent stretching of ankle joints with con-
tracture/spasticity. IEEE Trans Neural Syst Rehabil Eng 10: 149 –157,
2002.
47. Zhao H, Ren Y, Wu YN, Liu SQ, Zhang LQ. Ultrasonic evaluations of
Achilles tendon mechanical properties post stroke. J Appl Physiol 106:
843–849, 2009.
www.jap.org