Clinical Biomechanics 107 (2023) 106011

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Clinical Biomechanics
journal homepage: www.elsevier.com/locate/clinbiomech

Eight weeks of proprioceptive neuromuscular facilitation stretching and

static stretching do not affect muscle-tendon properties, muscle strength,
and joint function in children with spastic cerebral palsy
Annika Kruse a, *, Andreas Habersack a, b, Guido Weide c, Richard T. Jaspers c, Martin Svehlik b,
Markus Tilp a
a
Department of Biomechanics, Training and Movement Science, Institute of Human Movement Science, Sport and Health, University of Graz, Graz, Austria
b
Department of Othopaedics and Trauma, Medical University of Graz, Graz, Austria
c
Department of Human Movement Science, Faculty of Behavioral and Movement Sciences, Vrije Universiteit Amsterdam, Amsterdam Movement Sciences, Amsterdam, the
Netherlands

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

Keywords: Background: While the effect of static stretching for individuals with cerebral palsy is questionable, recent results
Stretching suggest that the combination with activation seems promising to improve muscle-tendon properties and function.
Spasticity Therefore, this study analyzed the effects of 8-week proprioceptive neuromuscular facilitation stretching on the
Plantar flexors
gastrocnemius medialis muscle-tendon properties, muscle strength, and the ankle joint in children with spastic
Achilles tendon
Children
cerebral palsy in comparison to static stretching.
Autogenic inhibition Methods: Initially, 24 children with spastic cerebral palsy were randomly assigned to a static stretching (10.7 ±
1.8 years) or proprioceptive neuromuscular facilitation stretching group (10.9 ± 2.6 years). Plantar flexors were
manually stretched at home for 300 s and ~ 250–270 s per day four times a week for eight weeks, respectively.
Assessments of ankle joint function (e.g., range of motion), muscle-tendon properties, and isometric muscle
strength were conducted using 3D motion capture, 2D ultrasound, dynamometry, and electromyography. A
mixed analysis of variance was used for the statistical analysis.
Findings: Stretching adherence was high in the proprioceptive neuromuscular facilitation stretching (93.1%) and
static stretching group (94.4%). No significant changes (p > 0.05) were observed in ankle joint function, muscle-
tendon properties, and isometric muscle strength after both interventions. Moreover, no differences (p > 0.05)
were found between the stretching techniques.
Interpretation: The findings support the idea that manual stretching (neither proprioceptive neuromuscular
facilitation stretching nor static stretching) performed in isolation for eight weeks may not be appropriate to
evoke significant changes in muscle-tendon properties, voluntary muscle strength, or joint function in children
with spastic cerebral palsy.
Clinical trial registration number: NCT04570358

1. Introduction
Cerebral palsy (CP) is a well-recognized, neuro-developmental dis­
order resulting from a non-progressive brain lesion occurring early in
infancy or before (Graham et al., 2016). It is the most common cause of
motor disability in children (Koman et al., 2004). Most individuals
exhibit a spastic motor type with spasticity as main feature. Individuals
with spastic CP (SCP) present impairments in body function resulting
from positive features of the upper motor neuron syndrome (e.g.,
spasticity, co-contraction), but also from negative ones (e.g., muscle
weakness, poor selective motor control) (Graham et al., 2016). These
impairments cause gait abnormalities, joint dislocations, and highly
restrict the individuals’ performance of and participation in daily life
activities, as well as their quality of life.
Although the primary brain injury is not progressive, muscle pa­
thology, a leading sign of disability in individuals with SCP, is an on-
going process (Bell et al., 2002) with research emphasizing the impor­
tance of the pathomorphology of spastic muscles themselves. Several

* Corresponding author.
E-mail address: annika.kruse@uni-graz.at (A. Kruse).

https://doi.org/10.1016/j.clinbiomech.2023.106011
Received 12 December 2022; Accepted 22 May 2023
Available online 7 June 2023
0268-0033/© 2023 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
A. Kruse et al. Clinical Biomechanics 107 (2023) 106011

studies have shown that muscles of individuals with SCP are structurally 2. Methods
and mechanically different compared to those of their typically devel­
oping (TD) peers (for review see Howard and Herzog, 2021). For 2.1. Participants
instance, there is evidence of reduced muscle size already present at
young age (Herskind et al., 2016; Weide et al., 2020a; Willerslev-Olsen The participants (Table 1) were recruited from the orthopaedic
et al., 2013) resulting from abnormalities in sarcomerogenesis, department of the local University hospital. All children were ambula­
increased connective tissue and fat content, and ribosomal dysfunction tory, able to accept and follow verbal instructions, and had no
(Booth et al., 2001; Lieber and Friden, 2018; Walden et al., 2018). In contracture of the plantar flexors (i.e., maxDF ≥0◦ with knees extended)
addition, increased tendon lengths (Kruse et al., 2018; Wren et al., 2010) as initially determined during a clinical examination beforehand by a
and reduced tendon cross-sectional area (Gao et al., 2011; Kruse et al., physician (MS). They had not undergone any surgical intervention and/
2018) have been reported. In sum, the reported changes restrict muscle or Botulinum toxin A application 12 or six months prior to the mea­
force and power generation capacity, therefore, contributing to both surements, respectively. The selective voluntary motor control was
weakness and possibly to muscle contracture (i.e., a unique muscle assessed by use of the “Selective Control Assessment of the Lower Ex­
adaptation in which the muscle increases passive stiffness resulting in tremity” (SCALE, (Fowler et al., 2009)). Randomized stratification of the
restricted joint RoM without active muscle force production (Smith participants to the PNF or SS group was performed based on both Gross
et al., 2011)) development (Lieber and Friden, 2018). Motor Function Classification System level (I + II vs. III) and age (6–10
Based on animal studies (for review see Kruse et al., 2021), specific years vs. 11–15 years).
treatment approaches such as stretching or orthoses/braces are usually Altogether 24 participants could be recruited for the study, whereby
applied to induce longitudinal muscle growth to prevent and/or coun­ data analyses were finally performed with 20 datasets (Fig. 1). The study
teract muscle contractures (Maas et al., 2014; Wiart et al., 2008; Zhao was approved by the local University’s Ethics Committee (registration
et al., 2011). However, the overall effectiveness especially of static number: 31–130 ex 18/19) and written consent was obtained in advance
stretching (SS) in individuals with contractures is still in question by the parents.
(Freitas et al., 2018; Harvey et al., 2017; Katalinic et al., 2011; Novak
et al., 2013) and inconsistent results regarding the effects on muscle-
2.2. Study design
tendon properties have been reported (Hösl et al., 2018; Kalkman
et al., 2018; Kalkman et al., 2019; Theis et al., 2015). However, a
Prior to the first measurement session, an initial session took place to
literature-based overview of the effects of different stretching tech­
familiarize the participants and their families with the whole study and
niques showed that stretching combined with activation might be
the procedures. This session was also used to determine the participants’
promising to cause positive effects on muscle-tendon level (Kruse et al.,
characteristics (Table 1) and to randomly allocate them to a stretching
2021). For instance, stretching combined with strength training/
group (SS/PNF). Both stretching groups were further examined before
strength exercises seems to be adequate to evoke muscle growth (e.g.,
and after the 8-week intervention. In each measurement session, as­
weighted post-set stretching, Silva et al., 2014). Moreover, increases in
sessments of ankle joint function (i.e., RoM, maxDF, and resting joint
resting fascicle lengths after resistance training combined with stretch­
angle), mechano-morphological properties of the GM MTU, and iso­
ing have also been reported for individuals with CP (Kalkman et al.,
metric muscle strength were conducted.
2019). This makes proprioceptive neuromuscular facilitation (PNF)
stretching a promising candidate to also cause beneficial changes on
muscle-tendon level in children with CP. 2.3. Data collection and processing
In contrast to SS, PNF additionally comprises an isometric contrac­
tion of the target muscle (“contract and relax”) and/or a concentric 2.3.1. Ankle joint parameters and passive torque
contraction of the opposing muscle (“contract relax and antagonistic The procedure followed to determine ankle joint function and pas­
contract”) in order to lengthen the target muscle (Sharman et al., 2006). sive torque is described in detail elsewhere (Habersack et al., 2022). In
In typically developed populations, studies showed that PNF stretching brief, the parameters were measured using a custom designed apparatus
can be equally (Konrad et al., 2017; Lempke et al., 2018) or more comprising an adjustable foot plate and a torque wrench equipped with
(Miyahara et al., 2013) effective than SS to increase joint range of mo­ an inclinometer (i.e., inclino-dynamometer) (Benard et al., 2010; Huij­
tion (RoM). In individuals with spasticity, studies on PNF stretching ing et al., 2013). The participants lay prone on an examination couch
were only performed in hemiplegic poststroke patients (Zhou et al., with the knee placed at ~20◦ of flexion and free sagittal plane
2014; Zhou et al., 2015; Zhou et al., 2016), indicating a positive impact
on biomechanical and functional measures (Zhou et al., 2016). For Table 1
instance, decreases in ankle joint stiffness and tendon length as well as Participant characteristics of the children with spastic cerebral palsy in the static
increases in maximum strength were found. Despite these promising stretching (SS) and proprioceptive neuromuscular facilitation (PNF) group.
findings, there are no studies to date that have investigated the effects of Means (SD).
PNF stretching on joint function (e.g., RoM), muscle-tendon properties, Anthropometrics SS PNF
and muscle strength of children with SCP. For patients with SCP, gaining Number 10 10
more insights into the effects of PNF stretching on muscle properties and Gender (female/male) 7/3 5/5
function is important to assess whether such a therapy is beneficial. Age (years) 10.7 (1.8) 10.9 (2.6)
The main aims of this study were 1) to determine the effects of an 8- Body mass (kg) 42.6 (12.7) 42.7 (16.6)
Body height (cm) 146.6 (9.1) 144.8 (18.5)
week PNF stretching intervention on the mechano-morphological
Lower leg length (cm) 35.6 (2.8) 34.2 (4.8)
properties of the gastrocnemius medialis (GM) muscle-tendon unit
(MTU) as well as muscle strength and joint function in children with
Patient characteristics
SCP, and 2) to evaluate its effects in comparison to an equal SS training. GMFCS level I/II/III 9/1/0 6/1/3
We hypothesized that PNF stretching would increase GM muscle belly Affected (unilateral/bilateral) 5/5 4/6
length and lengthening behavior, maximal dorsiflexion (maxDF), as well SCALE (points: 2/1/0) 1/7/2 0/9/1
as isometric muscle strength. Moreover, changes were assumed to be Grading of the “Selective Control Assessment of the Lower Extremity” (SCALE) is
larger after PNF than after SS, with the latter technique showing no presented for the more affected leg or the affected leg in children with bilateral
effect on muscle strength. and unilateral cerebral palsy, respectively. Grading was limited to the ankle
joint: Normal: 2 points; Impaired: 1 point; Unable: 0 points.

2
A. Kruse et al.
Fig. 1. Flow diagram of the participants included in the present study.
movement at the ankle (Bar-On et al., 2018). A varus or valgus deformity
of the foot was manually corrected using the footplate (Huijing et al.,
2013). The arm of the inclino-dynamometer was utilized to move the
foot plate (i.e., foot sole) into dorsal flexion within the sagittal plane,
while the externally applied torque was simultaneously measured
(Weide et al., 2020b). Two dorsiflexion rotations were performed at
slow velocity. Throughout the rotations, foot sole angles, muscle-tendon
properties, and muscle activity were measured synchronously using a
trigger signal, which started data capturing of the respective devices.
Furthermore, the angular movement velocity was also determined.
To assess the foot sole angles, a 3D motion capture system (10
cameras, Miqus M3, Qualisys AB, Gothenburg, Sweden) was used with
reflective markers attached to specific anatomical landmarks of the
lower extremity as described elsewhere (Habersack et al., 2022). Based
on these markers, a model of the lower extremities was built using
Visual3D software (C-Motion Inc., Germantown MD, USA). Foot sole
angle was defined in 3D as the sagittal angle between the plane of the
footplate and the shank. Foot sole angles are defined as 0◦ corresponding
to the foot sole orientated perpendicular to the shank (Weide et al.,
2020b)) with positive values indicating angles and external moments in
the dorsal direction.
Foot sole angles were computed for each trial to determine ankle
joint parameters (e.g., full RoM, maxDF). The mean values of two dor­
siflexion rotations were used for the statistical analyses. Foot sole angle
changes were also computed over a common standardized torque in­
terval (0 Nm to 6 Nm) which was reached by all the participants. The
ankle position at 0 Nm was defined as resting ankle joint angle.
2.3.2. Muscle-tendon properties
Throughout the rotations, passive lengthening behavior of the GM
MTU, GM muscle belly, and AT was also measured. A 5-cm linear array
ultrasound (US) transducer (LA523, MyLab60; Esaote S.p.A., Genova,
Italy) was used to detect the anatomical landmarks needed for the as­
sessments: the most superficial point of the medial epicondyle detected
3
Clinical Biomechanics 107 (2023) 106011
at the popliteal fossa (i.e., GM muscle origin), the GM muscle-tendon-
junction (MTJ), and the proximal tendinous insertion at the calcaneus
(Habersack et al., 2022).
Afterwards, a 59 mm linear array transducer (LogicScan 128; Tel­
emed, Vilnius, Lithuania) fitted with a rigid cluster of 4 reflective
markers (i.e., US markers) was fixated on the calf over the GM MTJ to
simultaneously record the MTJ displacement during the rotations
(Habersack et al., 2022). The US images were collected with a sampling
frequency of 60 Hz.
The MTJ displacement was manually tracked using Tracker software
(Tracker, version 4.91) (Kruse et al., 2017) and the tissues’ lengthening
behavior was analyzed using custom software programmed in MATLAB.
To determine absolute GM MTU, muscle belly, and AT length, as well as
the tissues’ behavior a previously validated approach was used (Hab­
ersack et al., 2022). Absolute MTU length was calculated as the linear
distance between the origin and proximal tendinous insertion at the
calcaneus. GM muscle belly length was computed as the linear distance
between the origin and the MTJ, and AT length as the distance between
the MTJ and the insertion site at the heel.
Individual GM muscle belly length changes were calculated over the
range from 0 Nm (i.e., resting length) to the maximally applied torque.
Furthermore, the tissues’ lengthening behavior was computed over the
common torque interval (0 to 6 Nm). Passive strain values were also
obtained by dividing muscle and tendon elongation by the tissues’
resting lengths. To account for possible growth changes during the 8-
week stretching intervention period, muscle-tendon properties were
normalized to lower leg length.
Absolute GM muscle fascicle lengths were determined at 0 Nm and 4
Nm externally applied torque using 3D freehand US as described by
Weide et al. (2017). While the foot was fixed at the corresponding
footplate angles, transverse ultrasound scans were made from muscle
origin via the MTJ to the insertion. The scanning was undertaken using
the linear array probe (LA523) and the motion capture system was used
to track a four-marker cluster, rigidly mounted to the probe. Sampling
A. Kruse et al.
frequency of the motion data was 100 Hz. The captured data was syn­
chronized and stored for further analysis (Weide et al., 2017). Post-
experimentally, the ultrasound probe position, video data, and motion
capture output data was utilized to create a 3D reconstruction of the
mid-longitudinal GM muscle fascicle plane (Weide et al., 2017; Weide
et al., 2020a). Fascicle length was determined three times in the re­
constructions at 2/3 from the GM origin in the mid-longitudinal fascicle
plane. The mean of the two fascicle lengths that showed the least dif­
ference was calculated and used for further analyses. The mean coeffi­
cient of variation, standard error of measurement, and minimal
detectable change for measuring fascicle lengths was 3.0%, 0.10 mm,
and 0.27 mm, respectively. Mean fascicle lengths were also normalized
to lower leg length.
2.3.3. Electromyography
Electromyographic (EMG, myon 320, myon AG, Zurich, Switzerland)
signals of the tibialis anterior and gastrocnemius lateralis were recorded
at 2000 Hz to evaluate whether voluntary muscle activation occurred
throughout the passive foot sole movement that could not directly be
detected by the examiner. Skin preparation and surface electrode
placement (Blue Sensor N, Ambu A/S, Ballerup, Denmark) was carried
out according to the SENIAM guidelines (Hermens et al., 2000) and
verified by US.
Raw EMG data was processed according to previous approaches in
individuals with CP (Bar-On et al., 2014; Bar-On et al., 2018; Schless
et al., 2015). The signals were filtered with a 6th-order zero-phase
Butterworth bandpass filter from 20 to 500 Hz and the root mean
square (RMS) envelope of the EMG signal was extracted by applying a
low-pass 30 Hz 6th-order zero-phase Butterworth filter on the squared
signal. The average RMS-EMG between 10 and 90% of the foot sole
rotation was computed (excluding the extremes of the RoM due to in­
fluences of examiner performance and/or participant discomfort (Bar-
On et al., 2014)). It was then expressed as percentage of the peak RMS-
EMG value resulting from the participants isometric maximum volun­
tary contraction (IMVC) measurement trial (see below), during which
the highest torque could be produced. Trials were discarded from the
analyses if average RMS-EMG ≥ 10% of peak RMS-EMG, which would
indicate voluntary activation.
2.3.4. Isometric muscle strength
To assess the maximum isometric muscle strength for indirect evi­
dence of possible changes in optimum muscle length, improved selective
motor control, and/or alterations in tendon properties (i.e., increased
tendon stiffness) due to PNF stretching, IMVCs of the plantar flexors
were performed in both groups by use of an isokinetic dynamometer
(CON-TREX MJ, CMV AG, Duebendorf, Switzerland). After familiariza­
tion with the procedure before start of each measurement session, the
participants conducted single IMVCs for 5 s with 2 min rest in between at
ankle angles corresponding to 25, 50, 75, and 100% of their joint RoM
(Barber et al., 2012), specified beforehand using the dynamometer. The
order of the trials was randomized beforehand. In case the participant
did not follow the instructions or did not push as hard as possible against
the footplate, the respective trial was discarded and repeated.
From each trial, peak and mean torques were determined. The latter
was calculated as mean value in the time range of 0.5 s before and after
the peak torque value was reached, therefore, reflecting the participants
ability to apply a specific amount of torque over a defined period. The
torque values were normalized to body mass.
2.4. Stretching interventions
Both stretching interventions were performed four times a week at
home for an 8-week period in addition to the participants’ usual physical
activity routine (e.g., physiotherapy). Each child and the parents were
informed about the manual stretching procedure in the familiarization
session. They were instructed on how to perform the stretching and how
4
Clinical Biomechanics 107 (2023) 106011
to properly fix the talocrural joint before the foot is moved into dorsi­
flexion to induce an increase in length of the MTU (Huijing et al., 2013)
in the first measurement session. Previous studies showed that parents
can be easily trained to perform such a technique correctly (Maas et al.,
2014). Stretching was performed with the participant lying prone in
both stretching groups.
During the SS training, the ankle joint was moved into maxDF with
the knee in full extension until the point of discomfort (but no pain) was
reached or joint resistance prevented any further movement. The ankle
joint was then held in this maximal position for 30 s (Ryan et al., 2008;
Wiart et al., 2008) followed by a rest period of 30 s. Afterwards, the
procedure was repeated with the knee in flexed position (~90◦ ) to
mainly stretch the soleus muscle.
The PNF stretching was performed similarly: With an extended knee
joint to stretch the gastrocnemii, the ankle joint was moved into maxDF
forcefully and safely (Zhou et al., 2016). While the foot was kept in this
position, the child performed a submaximal isometric contraction for at
least 3–5 s (Feland and Marin, 2004) against the resistance of their
parents. Afterwards, the ankle joint was moved passively further into
greater dorsiflexion and held there for the remaining 27–25 s followed
by 30 s of rest. Subsequently, the stretch was applied with the knee
flexed to predominantly stretch the soleus.
The respective stretching was repeated 10 times (upper limit of
repetitions as summarized by Wiart et al. (2008)) for each leg (five
stretches with knee extended/flexed) leading to an overall intervention
of 300 s (without rest) in both training groups.
In addition to the familiarization, an instructional video on how to
perform PNF stretching or SS was also provided to the families.
Furthermore, the project leader contacted the families personally within
the first two weeks, to assure that the training was performed correctly
and to check whether any problem had occurred. The participants were
also asked to fill in a stretching diary.
2.5. Statistical analyses
All statistical analyses were performed with SPSS (version 26, SPSS
Inc., Chicago, Illinois). Level of significance was set to p = 0.05. Data
was tested for normal distribution by use of the Shapiro-wilk test, his­
tograms, and Q-Q-plots.
Baseline differences between groups were assessed by use of an in­
dependent t-test or the Mann-Whitney U test as non-parametric alter­
native. A mixed ANOVA (independent variables: within = time; 2 levels:
pre-stretching, post-stretching; between = stretching groups; 2 levels:
SS, PNF) was further used to evaluate the stretching effects. Non-
normally distributed data was transformed by use of the Johnson
Transformation (Johnson, 1949).
3. Results
Stretching training adherence was high (93.1% and 94.4%) with a
mean adherence of 29.8 (4.0) and 30.2 (2.6) conducted sessions of the
required 32 sessions in the PNF and SS group, respectively. Mean
duration of each session was 20.3 (4.2) min and 18.9 (3.4) min for the
groups, respectively.
Anthropometric characteristics at baseline did not differ between
groups. Furthermore, no significant differences (p > 0.05) were found in
any outcome parameter between groups before start of the stretching
interventions. Individual data of the study participants can be found in
the supplementary material (supplementary Table 1 and 2).
3.1. Ankle joint range of motion and muscle activation
Externally applied peak torque did not differ pre- and post-stretching
(Table 2). Furthermore, no significant changes were observed in ankle
joint variables or muscle activation after both stretching interventions.
A. Kruse et al. Clinical Biomechanics 107 (2023) 106011

Table 2
Ankle joint range of motion variables, externally applied torque, and mean muscle activation measured during dorsiflexion rotations before (Pre) and after (Post) both
8-weeks of proprioceptive neuromuscular facilitation (PNF) stretching and static stretching (SS) in children with spastic cerebral palsy. Data are presented as mean
(SD).
Parameters Group n Pre Post %ΔPre-Post Effect F p partial η2

Range of motion (deg) PNF 10 50.0 (8.0) 48.9 (8.0) − 2.2 Time 0.549 0.468 0.030
SS 10 49.1 (3.1) 51.5 (3.9) 5.0 Time × Group 3.617 0.073 0.167
Maximum dorsiflexion (deg) PNF 10 − 12.3 (9.6) − 10.3 (10.0) − 16.2 Time 0.184 0.673 0.010
SS 10 − 14.3 (7.1) − 10.7 (8.8) − 24.9 Time × Group 0.000 0.984 0.000
Foot sole angle changecommonT (deg) PNF 7 32.2 (6.7) 29.6 (4.3) − 8.2 Time 1.979 0.181 0.124
SS 9 30.9 (2.7) 30.2 (3.1) − 2.2 Time × Group 0.690 0.420 0.047
Resting angle (deg) PNF 10 − 51.3 (9.3) − 47.6 (9.3) − 7.2 Time 1.547 0.230 0.079
SS 10 − 52.0 (6.5) − 50.4 (11.1) − 3.2 Time × Group 0228 0.639 0.013
Peak externally applied torque (Nm) PNF 10 8.1 (1.6) 8.3 (2.0) 2.9 Time 1.307 0.268 0.068
SS 10 8.6 (1.2) 9.2 (1.2) 7.5 Time × Group 0.275 0.607 0.015
Muscle activation (% of MVC)§ PNF 8 3.0 (3.3) 2.1 (2.2) − 29.9 Time 0.006 0.938 0.000
SS 10 0.8 (0.5) 0.8 (0.5) − 3.4 Time × Group 0.003 0.959 0.000
Muscle activationcommonT (% of MVC)§ PNF 8 2.5 (2.4) 2.0 (2.2) − 20.9 Time 0.389 0.542 0.024
SS 10 0.7 (0.6) 0.8 (0.5) 1.9 Time × Group 0.419 0.527 0.026

Negative angle values indicate plantarflexion; n.a., not applicable; MVC, maximum voluntary contraction; commonT, parameter calculated over a common moment
interval ranging from 0 Nm to 6 Nm externally applied torque.
§
Variables were logarithmically transformed for analysis but displayed with original means and standard deviations for comprehensibility.

3.2. Gastrocnemius medialis muscle-tendon properties each predefined ankle joint angle.

No significant changes could be found for the resting lengths of the
GM MTU, the GM muscle belly, or the AT as well as in the lengthening
behavior of the tissues after both stretching interventions (Table 3).
3.3. GM muscle fascicle lengths and lengthening
GM muscle fascicle length data could only be evaluated in five par­
ticipants of each stretching group due to technical problems. No sig­
nificant differences were observed for resting muscle fascicle lengths,
fascicle lengthening behavior, and fascicle strain (Table 4).
3.4. Isometric muscle strength
No significant effects could be found for normalized peak (Fig. 2) and
mean (supplementary Table 3) isometric muscle torques produced at
4. Discussion
In this study, we assessed the effects of 8 weeks of both PNF
stretching and SS on the GM mechano-morphological properties, muscle
strength, and joint range of motion in children with SCP. We did not find
any significant changes after the application of both stretching tech­
niques. Therefore, we had to reject the hypothesis that PNF stretching
would lead to increased GM muscle length and reduced resistance to
elongation and an increased maxDF, or an improved voluntary muscle
strength production. Moreover, no significant differences were observed
between the effects of the stretching techniques.
Stretching is a commonly used treatment in individuals with SCP
applied with the aim to maintain or increase joint RoM, increase muscle
belly extensibility and length, decrease muscle stiffness, and delay the
onset of contractures (Wiart et al., 2008). Static stretching is often the

Table 3
Gastrocnemius medialis muscle-tendon unit (MTU) length, muscle belly length, and Achilles tendon length changes as well as strain values measured during dorsi­
flexion rotations before (Pre) and after (Post) 8-weeks of both proprioceptive neuromuscular facilitation (PNF) stretching and static stretching (SS) in children with
spastic cerebral palsy. Original data (mm) are normalized to lower leg length (mm) and presented as mean (SD).
Parameters Group n Pre Post %ΔPre-Post Effect F p partial η2

Resting MTU length §

PNF 7 0.97 (0.02) 0.96 (0.04) − 0.8 Time 0.235 0.635 0.017
SS 9 0.94 (0.04) 0.95 (0.02) 0.3 Time × Group 0.455 0.511 0.031
MTU lengtheningcommonT PNF 5 0.05 (0.01) 0.05 (0.01) − 7.3 Time 1.025 0.338 0.102
SS 6 0.05 (0.00) 0.05 (0.01) − 2.7 Time × Group 0.218 0.652 0.024
MTU straincommonT§ (%) PNF 5 5.5 (0.7) 5.1 (0.8) − 7.3 Time 0.131 0.726 0.014
SS 6 5.6 (0.6) 5.4 (0.9) − 4.0 Time × Group 0.024 0.880 0.003
Resting muscle belly length PNF 7 0.47 (0.04) 0.47 (0.03) − 1.7 Time 0.044 0.836 0.003
SS 9 0.49 (0.06) 0.50 (0.07) 1.1 Time × Group 1.145 0.303 0.076
Max. muscle belly lengthening§ PNF 7 0.05 (0.01) 0.04 (0.02) − 11.1 Time 1.072 0.318 0.071
SS 9 0.05 (0.01) 0.05 (0.02) 4.1 Time × Group 2.322 0.150 0.142
Max. muscle belly strain§ (%) PNF 7 9.9 (1.5) 8.9 (3.3) − 9.6 Time 0.023 0.883 0.002
SS 9 9.3 (2.2) 9.7 (3.2) 4.1 Time × Group 1.566 0.231 0.101
Muscle belly lengtheningcommonT§ PNF 7 0.04 (0.01) 0.04 (0.02) − 4.7 Time 1.122 0.308 0.074
SS 9 0.04 (0.01) 0.04 (0.01) − 1.9 Time × Group 0.219 0.647 0.015
Muscle belly straincommonT (%) PNF 7 8.1 (2.0) 7.8 (3.2) − 3.0 Time 0.146 0.708 0.010
SS 9 8.1 (1.9) 7.9 (2.1) − 2.3 Time × Group 0.002 0.963 0.000
Resting tendon length PNF 7 0.50 (0.05) 0.50 (0.06) − 0.1 Time 0.056 0.817 0.004
SS 9 0.46 (0.08) 0.45 (0.08) − 0.6 Time × Group 0.038 0.848 0.003
Tendon lengtheningcommonT PNF 5 0.02 (0.01) 0.02 (0.01) − 5.6 Time 0.031 0.865 0.003
SS 6 0.02 (0.01) 0.02 (0.01) 1.2 Time × Group 0.059 0.813 0.007
Tendon straincommonT (%) PNF 5 4.1 (2.1) 3.8 (1.2) − 6.0 Time 0.030 0.865 0.003
SS 6 3.7 (2.0) 3.7 (2.1) 0.9 Time × Group 0.053 0.823 0.006
§
Variables were logarithmically transformed for analysis but displayed with original means and standard deviations for comprehensibility commonT, parameter
measured over a common moment interval ranging from 0 Nm to 6 Nm externally applied torque.

5
A. Kruse et al. Clinical Biomechanics 107 (2023) 106011

Table 4
Gastrocnemius medialis resting fascicle lengths (determined at 0 Nm), fascicle lengthening, and fascicle strain values measured before (Pre) and after (Post) 8-weeks of
both proprioceptive neuromuscular facilitation (PNF) stretching and static stretching (SS) in children with spastic cerebral palsy. Fascicle properties (mm) are
normalized to lower leg length (mm), while fascicle strain is calculated with regard to resting fascicle lengths. Parameters are presented as mean (SD).
Parameters Group n Pre Post %ΔPre-Post Effect F p partial η2

Absolute resting fascicle lengths (mm) PNF 5 32.1 (7.8) 33.7 (7.7) 5.2 Time 0.000 0.992 0.000
SS 5 31.2 (9.1) 30.1 (8.0) − 3.5 Time × Group 2.919 0.126 0.267
Normalized resting fascicle lengths PNF 5 0.09 (0.02) 0.10 (0.01) 1.8 Time 0.112 0.746 0.014
SS 5 0.09 (0.02) 0.08 (0.02) − 4.3 Time × Group 0.784 0.402 0.089
Normalized fascicle lengthening$ PNF 3 0.02 (0.01) 0.01 (0.01) − 32.9 Time 0.021 0.890 0.004
SS 4 0.01 (0.01) 0.01 (0.01) − 26.1 Time × Group 1.140 0.334 0.186
Fascicle strain (%) PNF 3 23.1 (15.1) 14.3 (7.1) − 38.0 Time 2.614 0.167 0.343
SS 4 18.5 (11.8) 11.9 (5.0) − 35.7 Time × Group 0.052 0.828 0.010
$
Length changes and strain values were calculated between 0 Nm to 4 Nm externally applied torque.

Fig. 2. Normalized isometric peak torque values exerted before (Pre) and after (Post) 8 weeks of (A) static stretching (SS) and (B) proprioceptive neuromuscular
facilitation (PNF) stretching at ankle joint angles of 25, 50, 75, and 100% of the individual joint range of motion (RoM). The ankle joint angle at 100% reflects the
maximal dorsiflexion angle.

method of choice, however, PNF stretching has also been used in the
therapy of specific patient groups, e.g., stroke survivors. Although it is
still not clear, which stretching technique might lead to the most
favorable results, studies in healthy populations showed that both
methods can increase joint RoM/maxDF (Thomas et al., 2018).
In contrast to the reported effects for healthy populations, no sig­
nificant changes in ankle joint parameters could be found after both 8
weeks of PNF stretching and SS in children with SCP in the present
study, despite slight improvements in maxDF in both groups (PNF:
+2.0◦ ; SS: +4.0◦ ). However, a similar increase in maxDF was found
previously: Theis et al. (2015) observed an increase in maxDF by 3◦ after
6 weeks of passive stretching applied for 4 days a week in children with
SCP. Moreover, they reported decreases in ankle joint and GM muscle
stiffness of 32% and 12%, respectively, which were accompanied by
increases in muscle (+23%) and fascicle strain (+13%). The authors
concluded that the children’s muscle offered greater plasticity than the
related tendon, therefore, demonstrating a tissue-dependent response to
SS. In contrast, Hösl et al. (2018) showed no significant change in
maxDF and ankle joint stiffness after 9 weeks of SS and reported no
alterations in GM muscle and tendon stiffness, while GM fascicle lengths
at rest were decreased by ~3%. Since studies on casting in individuals
with CP found significant changes in maxDF of +4.1◦ (McNee et al.,
2006) and + 10.0◦ (post median, Peeters et al., 2020), it may be assumed
that a longer duration under stretch (e.g., several hours a day) and a
higher load as applied to the calf muscles during walking with the casts
may be needed to cause effects on joint level. However, we emphasize
that functional improvements observed after casting and bracing seem
to be a result of changes occurring mainly in tendon but not muscle belly
length (Hösl et al., 2015; McNee et al., 2006; Peeters et al., 2020). This
likely negatively impacts force transfer, and therefore, strength of the
individuals.
In the present study, no significant changes in resting muscle-tendon
properties were found, which is in line with previous studies investi­
gating 9 to 20 weeks of different stretching interventions in individuals
with CP (Hösl et al., 2015; Hösl et al., 2018; Kalkman et al., 2019). Thus,
although not significant, we observed that the GM MTU elongation (over
a torque range from 0 Nm to 6 Nm) was slightly reduced in the PNF as
well as SS group. These results for a spastic MTU indicate a different
response when compared to responses of healthy muscles. In healthy
populations, it seems that PNF stretching targets the tendon stiffness to a
greater extent than other methods (Freitas et al., 2018; Konrad et al.,
2015; Mahieu et al., 2009), leading to reductions in tendon stiffness after
PNF. In contrast, SS may rather decrease muscle belly stiffness (Blaz­
evich et al., 2014; Nakamura et al., 2017). In contrast, the present results
indicate an increase in MTU stiffness (for instance by an increase in
muscle tone by altered calcium handling or altered intrinsic properties
of the cytoskeleton and/or the extracellular matrix, or an increase in
muscle physiological cross-sectional area) together with a decrease
mainly in tendon elongation after PNF. In contrast, tendon elongation
over the common torque interval (up to 6 Nm) remained nearly unal­
tered after SS (however not significantly different to PNF). Since
strength exercises combined with stretching (Kalkman et al., 2019) and
isometric contractions performed at high strain amplitude (Arampatzis
et al., 2010) may evoke increases in tendon stiffness, PNF stretching may

6
A. Kruse et al.
also have the potential to induce such changes. However, this assump­
tion could not be verified in this study.
Although not statistically significant, SS resulted in shorter resting
fascicles (− 3%), similar as observed by Hösl et al. (2018), while a slight
increase was observed in the PNF group (+5%). However, fascicle
lengthening, and strain were reduced in both stretching groups. Possible
factors for the reduced lengthening could be the increased muscle tone
in the PNF group, which is yet speculative.
As proposed by Freitas et al. (2018), it can be assumed that a
stretching intervention period longer than 8–12 weeks might have been
needed to cause significant effects on muscle-tendon level also in in­
dividuals with SCP. However, more likely, we presume that the stretch
intensity (i.e., magnitude of strain of the muscle fascicles and muscle
belly) evoked by manual stretching as performed in this study might not
have been high enough to stimulate tissue adaptations as seen in pre­
vious studies (e.g., Kalkman et al., 2019). For instance, Kalkman et al.
(2019) may have caused a higher stretch intensity since some partici­
pants performed self-stretching (i.e., stretching the calf muscles while
standing at a wall). Since this procedure is not influenced by the force of
the parents limiting the application, a higher intensity might have been
reached. Moreover, the combination with calf raises, might have helped
causing warm-up effects and assumably acutely affecting the tendinous
tissue (i.e., stiffening of the tendon due to tendon length changes during
heel-raises). However, we note that calf raises cannot be performed by
individuals more severely affected such as children classified as GMFCS
III and higher. We further propose that also weighted post-set stretching
(Silva et al., 2014) might be an interesting approach, whereby prolonged
stretching with casts (McNee et al., 2006; Peeters et al., 2020) might not
be appropriate to cause positive muscle alterations in individuals with
spastic CP. Nevertheless, also other factors, such as the restricted
adaptation potential of the muscles and tendons themselves as well as
the age of the individuals with CP, might be influencing factors (for
further discussion see Walhain et al., 2021).
Based on previous studies in individuals with stroke, we assumed
that manual PNF stretching would lead to beneficial effects on muscle-
tendon level and increases in voluntary torque production in children
with SCP (Zhou et al., 2016). However, no significant changes were
observed in both groups. We assume that the intensity of contraction/
muscle activation during the PNF stretching might not have been high
enough to affect the tissues’ properties and isometric muscle strength.
Although nine out of ten children were able to perform isometric con­
tractions, verified by direct observation of the produced IMVC curves
and assessments of selective motor control, produced torques were low
(PNF group: mean peak torque: 0.44 Nm/kg) in comparison to those
produced by typically developing peers (1.5 Nm/kg, (Kruse et al.,
2017)). While even performing submaximal contractions in PNF
stretching may be just as beneficial as maximal contractions (Feland and
Marin, 2004), generated activation in individuals with SCP might be too
low and not continuously enough to evoke (strengthening) effects, but
also to induce autogenic inhibition upon stretching. Therefore, the PNF
stretching approach may have to be modified for this patient group, for
instance, using electrical stimulation or supporting devices.
This study has some limitations. The small sample size indicates that
our study might have been underpowered to achieve significant results.
A post-hoc power analysis based on the study results (Table 2–4) indeed
showed low power values mainly between 0.01 and 0.46. However, the
values are based on very low effects observed for most of the parameters
(partial eta squared 0.000–0.124). Greater, non-significant, effects
(partial eta squared >0.140) were only observed for RoM, and maximal
GM muscle belly lengthening (power values: 0.92, and 0.84 respec­
tively). Therefore, we conclude that the stretching interventions had
only marginal effects on most outcome parameters and most results are
not affected by the small sample size. Moreover, following suggestions
about intervention durations required to cause MTU adaptations (>
8–12 weeks) (Freitas et al., 2018), future studies with longer treatment
durations are needed. In addition, some factors have to be considered
7
Clinical Biomechanics 107 (2023) 106011
influencing the measurement of maxDF (Section 2.3.1): handling of the
inclino-dynamometer is assumed to be influenced by the stature and
hand size of the examiner (Habersack et al., 2022), whereby taller raters
with larger hands might be able to move the joint into greater dorsi­
flexion by applying greater force. However, this issue could not be
solved during the study, therefore, we note that reported maxDF values
(Table 2) might underestimate the true maxDF. Nevertheless, since
externally applied torque was not significantly different throughout the
measurement sessions (Table 2), effects on muscle-tendon level should
have been detectable. We further note that only one IMVC was per­
formed at each ankle joint angle. However, great care was taken to
ensure high quality of the trials by 1) familiarizing (i.e., performing
submaximal contractions with simultaneously following the torque
signal) the participants with the procedure before start of each mea­
surement session, and 2) repeating trials if the instructions were not
followed or the participant did not push as hard as possible. Finally, we
emphasize that the measurements are mainly restricted to the plantar
flexors. Therefore, the presented results cannot be transferred to other
muscles/muscle groups.
5. Conclusions
This is the first study investigating the effects of 8-week PNF
stretching in comparison to SS on the mechano-morphological GM
muscle-tendon properties, isometric muscle strength, and joint function
in children with SCP. Based on our findings, we support the idea of other
authors that manual stretching performed in isolation for eight weeks
may not be appropriate to evoke significant changes on muscle-tendon
level and in muscle function in this population. According to previous
studies on healthy individuals, we assume that high-intensity or a high
stretching (over-) load applied over a longer period (> 8–12 weeks) may
be needed to cause adaptations.
Funding
Open access funding was provided by the University of Graz. The
whole project was supported by the Austrian Science Fund [Grant
Number T 1017]. AH is currently funded by the Austrian Academy of
Sciences (25940).
Declaration of Competing Interest
None.
Data availability
The data that support the findings of this study are available from the
corresponding author, [AK], upon reasonable request.
Acknowledgements
The authors acknowledge the financial support by the University of
Graz. Furthermore, we acknowledge the support of the Austrian Science
Fund for AK and the financial support of the Austrian Academy of Sci­
ences for AH, who is a recipient of a DOC Fellowship (25940) at the
Department of Orthopaedics and Trauma, Medical University of Graz,
and the Institute of Human Movement Science, Sport and Health, Uni­
versity of Graz. Moreover, we would like to thank Prof. Jaap Harlaar for
the support in initial project proposal writing.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.clinbiomech.2023.106011.
A. Kruse et al. Clinical Biomechanics 107 (2023) 106011

References Konrad, A., Stafilidis, S., Tilp, M., 2017. Effects of acute static, ballistic, and PNF
stretching exercise on the muscle and tendon tissue properties. Scand. J. Med. Sci.
Sports 27, 1070–1080.
Arampatzis, A., Peper, A., Bierbaum, S., Albracht, K., 2010. Plasticity of human Achilles
Kruse, A., Schranz, C., Svehlik, M., Tilp, M., 2017. Mechanical muscle and tendon
tendon mechanical and morphological properties in response to cyclic strain.
properties of the plantar flexors are altered even in highly functional children with
J. Biomech. 43, 3073–3079.
spastic cerebral palsy. Clin. Biomech. 50, 139–144.
Barber, L., Barrett, R., Lichtwark, G., 2012. Medial gastrocnemius muscle fascicle active
Kruse, A., Schranz, C., Tilp, M., Svehlik, M., 2018. Muscle and tendon morphology
torque-length and Achilles tendon properties in young adults with spastic cerebral
alterations in children and adolescents with mild forms of spastic cerebral palsy.
palsy. J. Biomech. 45, 2526–2530.
BMC Pediatr. 18, 156.
Bar-On, L., Aertbeliën, E., Molenaers, G., Desloovere, K., 2014. Muscle activation
Kruse, A., Rivares, C., Weide, G., Tilp, M., Jaspers, R.T., 2021. Stimuli for adaptations in
patterns when passively stretching spastic lower limb muscles of children with
muscle length and the length range of active force exertion-a narrative review. Front.
cerebral palsy. PLoS One 9, e91759.
Physiol. 12, 742034.
Bar-On, L., Kalkman, B.M., Cenni, F., Schless, S.-H., Molenaers, G., Maganaris, C.N.,
Lempke, L., Wilkinson, R., Murray, C., Stanek, J., 2018. The effectiveness of PNF versus
Bass, A., Holmes, G., Barton, G.J., O’Brien, T.D., Desloovere, K., 2018. The
static stretching on increasing hip-flexion range of motion. J. Sport Rehabil. 27,
relationship between medial gastrocnemius lengthening properties and stretch
289–294.
reflexes in cerebral palsy. Front. Pediatr. 6, 259.
Lieber, R.L., Friden, J., 2018. Muscle contracture and passive mechanics in cerebral
Bell, K.J., Ounpuu, S., DeLuca, P.A., Romness, M.J., 2002. Natural progression of gait in
palsy. J. Appl. Physiol. 126, 1492–1501.
children with cerebral palsy. J. Pediatr. Orthop. 22, 677–682.
Maas, J., Dallmeijer, A., Huijing, P., Brunstrom-Hernandez, J., van Kampen, P.,
Benard, M.R., Jaspers, R.T., Huijing, P.A., Becher, J.G., Harlaar, J., 2010. Reproducibility
Bolster, E., Dunn, C., Herndon, K., Jaspers, R., Becher, J., 2014. A randomized
of hand-held ankle dynamometry to measure altered ankle moment-angle
controlled trial studying efficacy and tolerance of a knee-ankle-foot orthosis used to
characteristics in children with spastic cerebral palsy. Clin. Biomech. 25, 802–808.
prevent equinus in children with spastic cerebral palsy. Clin. Rehabil. 28,
Blazevich, A.J., Cannavan, D., Waugh, C.M., Miller, S.C., Thorlund, J.B., Aagaard, P.,
1025–1038.
Kay, A.D., 2014. Range of motion, neuromechanical, and architectural adaptations
Mahieu, N.N., Cools, A., Wilde, B. de, Boon, M., Witvrouw, E., 2009. Effect of
to plantar flexor stretch training in humans. J. Appl. Physiol. 117, 452–462.
proprioceptive neuromuscular facilitation stretching on the plantar flexor muscle-
Booth, C.M., Cortina-Borja, M.J., Theologis, T.N., 2001. Collagen accumulation in
tendon tissue properties. Scand. J. Med. Sci. Sports 19, 553–560.
muscles of children with cerebral palsy and correlation with severity of spasticity.
McNee, A.E., Eve, L.D., Will, E., Lin, J.-P., Gough, M., Fry, N.R., Morrissey, M.C.,
Dev. Med. Child Neurol. 43, 314–320.
Shortland, A.P., 2006. Changes in muscle morphology following serial casting in
Feland, J.B., Marin, H.N., 2004. Effect of submaximal contraction intensity in contract-
chidlren with spastic cerebral palsy. Dev. Med. Child Neurol., AACPDM Abstracts,
relax proprioceptive neuromuscular facilitation stretching. Br. J. Sports Med. 38,
Free papers - Session A, 5-6.
E18.
Miyahara, Y., Naito, H., Ogura, Y., Katamoto, S., Aoki, J., 2013. Effects of proprioceptive
Fowler, E.G., Staudt, L.A., Greenberg, M.B., Oppenheim, W.L., 2009. Selective Control
neuromuscular facilitation stretching and static stretching on maximal voluntary
Assessment of the Lower Extremity (SCALE): development, validation, and interrater
contraction. J. Strength Cond. Res. 27, 195–201.
reliability of a clinical tool for patients with cerebral palsy. Dev. Med. Child Neurol.
Nakamura, M., Ikezoe, T., Umegaki, H., Kobayashi, T., Nishishita, S., Ichihashi, N., 2017.
51, 607–614.
Changes in passive properties of the gastrocnemius muscle-tendon unit during a 4-
Freitas, S.R., Mendes, B., Le Sant, G., Andrade, R.J., Nordez, A., Milanovic, Z., 2018. Can
week routine static-stretching program. J. Sport Rehabil. 26, 263–268.
chronic stretching change the muscle-tendon mechanical properties? A review.
Novak, I., McIntyre, S., Morgan, C., Campbell, L., Dark, L., Morton, N., Stumbles, E.,
Scand. J. Med. Sci. Sports 28, 794–806.
Wilson, S.-A., Goldsmith, S., 2013. A systematic review of interventions for children
Gao, F., Zhao, H., Gaebler-Spira, D., Zhang, L.Q., 2011. In vivo evaluations of
with cerebral palsy: state of the evidence. Dev. Med. Child Neurol. 55, 885–910.
morphologic changes of gastrocnemius muscle fascicles and achilles tendon in
Peeters, N., van Campenhout, A., Hanssen, B., Cenni, F., Schless, S.-H., van den
children with cerebral palsy. Am. J. Phys. Med. Rehabil. 90, 364–371.
Broeck, C., Desloovere, K., Bar-On, L., 2020. Joint and muscle assessments of the
Graham, H.K., Rosenbaum, P., Paneth, N., Dan, B., Lin, J.-P., Damiano, D.L., Becher, J.G.,
separate effects of botulinum NeuroToxin-A and lower-leg casting in children with
Gaebler-Spira, D., Colver, A., Reddihough, D.S., Crompton, K.E., Lieber, R.L., 2016.
cerebral palsy. Front. Neurol. 11, 210.
Cerebral palsy. Nat. Rev. Dis. Prim. 2, 15082.
Ryan, E.D., Beck, T.W., Herda, T.J., Hull, H.R., Hartman, M.J., Costa, P.B., Defreitas, J.
Habersack, A., Zussner, T., Thaller, S., Tilp, M., Svehlik, M., Kruse, A., 2022. Validity and
M., Stout, J.R., Cramer, J.T., 2008. The time course of musculotendinous stiffness
reliability of a novel 3D ultrasound approach to assess static lengths and the
responses following different durations of passive stretching. J. orthopaedic Sports
lengthening behavior of the gastrocnemius medialis muscle and the Achilles tendon
Phy. Ther. 38, 632–639.
in vivo. Knee Surg. Sports Traumatol. 30, 4203–4213.
Schless, S.-H., Desloovere, K., Aertbelien, E., Molenaers, G., Huenaerts, C., Bar-On, L.,
Harvey, L.A., Katalinic, O.M., Herbert, R.D., Moseley, A.M., Lannin, N.A., Schurr, K.,
2015. The intra- and inter-rater reliability of an instrumented spasticity assessment
2017. Stretch for the treatment and prevention of contractures. Cochrane Database
in children with cerebral palsy. PLoS One 10, e0131011.
Syst. Rev. 1, CD007455.
Sharman, M.J., Cresswell, A.G., Riek, S., 2006. Proprioceptive neuromuscular facilitation
Hermens, H.J., Freriks, B., Disselhorst-Klug, C., Rau, G., 2000. Development of
stretching: mechanisms and clinical implications. Sports Med. 36, 929–939.
recommendations for SEMG sensors and sensor placement procedures.
Silva, J., Lowery, R., Antonio, J., McCleary, S., Rauch, J., Ormes, J., et al., 2014.
J. Electromyogr. Kinesiol. 10, 361–374.
Weighted post-set stretching increases skeletal muscle hypertrophy. Nat. Strength
Herskind, A., Ritterband-Rosenbaum, A., Willerslev-Olsen, M., Lorentzen, J., Hanson, L.,
Cond. Assoc. 28, 65.
Lichtwark, G., Nielsen, J.B., 2016. Muscle growth is reduced in 15-month-old
Smith, L.R., Lee, K.S., Ward, S.R., Chambers, H.G., Lieber, R.L., 2011. Hamstring
children with cerebral palsy. Dev. Med. Child Neurol. 58, 485–491.
contractures in children with spastic cerebral palsy result from a stiffer extracellular
Hösl, M., Bohm, H., Arampatzis, A., Doderlein, L., 2015. Effects of ankle-foot braces on
matrix and increased in vivo sarcomere length. J. Physiol. 589, 2625–2639.
medial gastrocnemius morphometrics and gait in children with cerebral palsy.
Theis, N., Korff, T., Mohagheghi, A.A., 2015. Does long-term passive stretching alter
J. Child. Orthop. 9, 209–219.
muscle-tendon unit mechanics in children with spastic cerebral palsy? Clin.
Hösl, M., Bohm, H., Eck, J., Doderlein, L., Arampatzis, A., 2018. Effects of backward-
Biomech. 30, 1071–1076.
downhill treadmill training versus manual static plantarflexor stretching on muscle-
Thomas, E., Bianco, A., Paoli, A., Palma, A., 2018. The relation between stretching
joint pathology and function in children with spastic cerebral palsy. Gait Posture 65,
typology and stretching duration: the effects on range of motion. Int. J. Sports Med.
121–128.
39, 243–254.
Howard, J.J., Herzog, W., 2021. Skeletal muscle in cerebral palsy: from belly to
Walden, F. von, Gantelius, S., Liu, C., Borgström, H., Björk, L., Gremark, O., Stål, P.,
myofibril. Front. Neurol. 12, 620852.
Nader, G.A., Pontén, E., 2018. Muscle contractures in patients with cerebral palsy
Huijing, P.A., Benard, M.R., Harlaar, J., Jaspers, R.T., Becher, J.G., 2013. Movement
and acquired brain injury are associated with extracellular matrix expansion, pro-
within foot and ankle joint in children with spastic cerebral palsy: a 3-dimensional
inflammatory gene expression, and reduced rRNA synthesis. Muscle Nerve 58,
ultrasound analysis of medial gastrocnemius length with correction for effects of foot
277–285.
deformation. BMC Musculoskelet. Disord. 14, 365.
Walhain, F., Desloovere, K., Declerck, M., van Campenhout, A., Bar-On, L., 2021.
Johnson, N.L., 1949. Systems of frequency curves generated by methods of translation.
Interventions and lower-limb macroscopic muscle morphology in children with
Biometrika 36, 149–176.
spastic cerebral palsy: a scoping review. Dev. Med. Child Neurol. 63, 274–286.
Kalkman, B.M., Bar-On, L., Cenni, F., Maganaris, C.N., Bass, A., Holmes, G.,
Weide, G., van der Zwaard, S., Huijing, P.A., Jaspers, R.T., Harlaar, J., 2017. Ultrasound
Desloovere, K., Barton, G.J., O’Brien, T.D., 2018. Medial gastrocnemius muscle
imaging: fast and cost-effective morphometry of musculoskeletal tissue. J. Vis. Exp.
stiffness cannot explain the increased ankle joint range of motion following passive
e55943.
stretching in children with cerebral palsy. Exp. Physiol. 103, 350–357.
Weide, G., Huijing, P.A., Bar-On, L., Sloot, L., Buizer, A.I., Becher, J.G., Harlaar, J.,
Kalkman, B.M., Holmes, G., Bar-On, L., Barton, G.J., Maganaris, C.N., Bass, A., Wright, D.
Jaspers, R.T., 2020a. Gastrocnemius medialis muscle geometry and extensibility in
M., Walton, R., O’Brien, T.D., 2019. Resistance training combined with stretching
typically developing children and children with spastic paresis aged 6-13 years.
increases tendon stiffness and is more effective than stretching alone in children with
Front. Physiol. 11, 528522.
cerebral palsy: a randomised controlled trial. Front. Pediatr. 7, 333.
Weide, G., Huijing, P.A., Becher, J.G., Jaspers, R.T., Harlaar, J., 2020b. Foot flexibility
Katalinic, O.M., Harvey, L.A., Herbert, R.D., 2011. Effectiveness of stretch for the
confounds the assessment of triceps surae extensibility in children with spastic
treatment and prevention of contractures in people with neurological conditions: a
paresis during typical physical examinations. J. Biomech. 99, 109532.
systematic review. Phys. Ther. 91, 11–24.
Wiart, L., Darrah, J., Kembhavi, G., 2008. Stretching with children with cerebral palsy:
Koman, L.A., Smith, B.P., Shilt, J.S., 2004. Cerebral palsy. Lancet 363, 1619–1631.
what do we know and where are we going? Pediatr. Phys. Ther. 20, 173–178.
Konrad, A., Gad, M., Tilp, M., 2015. Effect of PNF stretching training on the properties of
Willerslev-Olsen, M., Lorentzen, J., Sinkjaer, T., Nielsen, J.B., 2013. Passive muscle
human muscle and tendon structures. Scand. J. Med. Sci. Sports 25, 346–355.
properties are altered in children with cerebral palsy before the age of 3 years and

8
A. Kruse et al.
are difficult to distinguish clinically from spasticity. Dev. Med. Child Neurol. 55,
617–623.
Wren, T.A.L., Cheatwood, A.P., Rethlefsen, S.A., Hara, R., Perez, F.J., Kay, R.M., 2010.
Achilles tendon length and medial gastrocnemius architecture in children with
cerebral palsy and equinus gait. J. Pediatr. Orthop. 30, 479–484.
Zhao, H., Wu, Y.-N., Hwang, M., Ren, Y., Gao, F., Gaebler-Spira, D., Zhang, L.-Q., 2011.
Changes of calf muscle-tendon biomechanical properties induced by passive-
stretching and active-movement training in children with cerebral palsy. J. Appl.
Physiol. 111, 435–442.
Clinical Biomechanics 107 (2023) 106011
Zhou, Z., Zhou, Y., Wang, N., Gao, F., Wang, L., Wei, K., Wang, Q., 2014. Changes of
Achilles tendon properties via 12-week PNF based robotic rehabilitation of ankle
joints with spasticity and/or contracture. In: IEEE Engineering in Medicine and
Biology Society. Annual Conference 2014, pp. 1214–1217.
Zhou, Z., Zhou, Y., Wang, N., Gao, F., Wei, K., Wang, Q., 2015. A proprioceptive
neuromuscular facilitation integrated robotic ankle–foot system for post stroke
rehabilitation. Robot. Auton. Syst. 73, 111–122.
Zhou, Z., Sun, Y., Wang, N., Gao, F., Wei, K., Wang, Q., 2016. Robot-assisted
rehabilitation of ankle plantar flexors spasticity: a 3-month study with
proprioceptive neuromuscular facilitation. Front. Neurorobot. 10, 16.