Content uploaded by Emine Caliskan
Author content
All content in this area was uploaded by Emine Caliskan on Mar 11, 2019
Content may be subject to copyright.
Med Ultrason 2019:0, 1-8 Online rst
DOI:
Ahead of print
E
ffects of static stretching duration on muscle stiffness and blood
ow in the rectus femoris in adolescents
Emine Caliskan1, Orkun Akkoc2, Zuhal Bayramoglu3, Omer Batin Gozubuyuk4, Doga Kural2,
Sena Azamat3, Ibrahim Adaletli3
1Department of Pediatric Radiology, Seyhan State Hospital, Adana, 2Department of Moving and Training Science,
Faculty of Sports Science, Istanbul University, Istanbul, 3Department of Pediatric Radiology, Istanbul University
Faculty of Medicine, Istanbul, 4Department of Sports Medicine, Istanbul University Faculty of Medicine, Istanbul,
Turkey
Received 31.12.2018 Accepted 24.02.2019
Med Ultrason
2019:0 Online rst, 1-8
Corresponding author: Emine Caliskan
Haci Omer Sabanci Street, Seyhan,
Adana, Turkey, 11050
ORCID: 0000-0001-9869-1396
E-mail:eminecaliskanrad@gmail.com
Introduction
Cramps, spasms and traumatic damage cause micro-
structural disruptions in the muscle tissue [1]. They al-
ter the healthy condition and trigger muscle stiffening.
Muscle stretching increases the speed of recovery from
cramps [2] and it is popular among health therapists and
athletic trainers because it reduces muscle stiffness and
the incidence of muscle injury and increases exibility
[3-6].
Muscle stretching is widely performed as a warm-up
or cool-down exercises for subjects undergoing physical
activity. Stretching may be applied with different tech-
niques including mainly static (active tensioning, pas-
sive, isometric), ballistic, dynamic, and proprioceptive
neuromuscular facilitation (PNF). Static stretching (SS)
is a technique that increases exibility by the greatest
amount. Passive SS aims to preserve joint and muscle
stretching through the effect of an external force, such
as a partner’s push, wall, oor or machine, which is ap-
plied to attain and hold the end position [7]. It may be
applied for short (2–3 min or less) and longer (5–10 min
or longer) durations [8].
Skeletal muscle stretching is accepted as an adapta-
tion of low intensity exercise and it has signicant effects
on general health care and vascularity [9]. The microcir-
culation in normal skeletal muscle consists of a highly-
organized network of arterioles, capillaries and venules
Abstract
Aims: To compare the effects of 2 and 5 min of passive static stretching (SS) on stiffness and blood ow in the rectus
femoris in adolescent athletes using shear wave elastography (SWE) and superb microvascular imaging (SMI). Material and
methods: This prospective study included 20 male athletes with median age of 14.5 (12.5–16.5) years. The subjects were
divided into two groups based on the SS duration as follows: 2 min (n=10) and 5 min (n=10). At rest and after 2 and 5 min
of SS, stiffness and blood ow values were compared in the rectus femoris for each group. Inter-operator reliability was also
analysed. Results: There was no signicant difference between resting and 2 min of SS in terms of stiffness. The stiffness
values decreased signicantly from resting to 5 min of SS. The blood ow increased signicantly from resting to 2 and 5 min
of SS. Inter-operator reliability was moderate to perfect for SWE and SMI measurements (ICC: 0.52–0.83). Conclusions:
SWE and SMI can be used to acquire reliable quantitative data about muscle stiffness and blood ow in adolescents. While
stiffness parameters signicantly decreased from resting after only 5 min, blood ow signicantly increased both after 2 and
5 min. For physical rehabilitation protocols, 5 min of SS may be chosen to reduce stiffness. For competitions, 2 min of SS
may be sufcient for warm-up exercise because it increases the blood ow optimally. Five min of SS may be preferred for the
cool-down exercise to enhance recovery.
Keywords: blood ow; muscle stiffness; shear wave elastography; static stretching; superb microvascular imaging
DOI: 10.11152/mu-1859
2Emine Caliskan et al Effects of static stretching duration on muscle stiffness and blood ow
that are structurally arranged to optimize oxygen trans-
port. Voluntary or involuntary changes in local blood
ow physically and clinically affect the muscle structure.
Increasing blood ow provides a greater amount of oxy-
gen to the muscles and the opportunity to produce high-
er levels of physical performance [10]. As muscles are
stretched, blood ow and oxygen delivery are compro-
mised and consequently muscle function is impaired. It is
established that a robust angiogenesis and endothelium-
dependent vasodilatation response can occur following
an ischemic injury to the skeletal muscle in the acute or
chronic recovery period [11,12]. This neovascularization
response, together with the opening of collateral vessels,
can restore blood ow to the otherwise compromised
muscle. Hotta et al reported that 4 weeks of daily muscle
stretching enhanced endothelium-dependent vasodilata-
tion of skeletal muscle resistance arterioles in aged rats
[12]. However, no published data provide sufciently
quantitative information regarding acute changes in mus-
cular blood ow after stretching in humans.
Shear wave elastography (SWE) is a new imaging
technique that provides information regarding tissue
stiffness by a higher intensity pulse that is transmitted
into the body to produce shear waves, which extend lat-
erally from the target tissue and are then tracked with
low-intensity pulses to nd the shear velocity related to
Young’s modulus. Tissue stiffness measurements may be
benecial for the identication of muscles as well as a
variety of organ disorders [13-15]. Elastography stud-
ies investigating the acute effects of stretching (ranging
from 2–10 min duration) on the adult’s triceps surae,
hamstring and shoulder muscles have previously been
performed [16-21].
Superb microvascular imaging (SMI) is an advanced
Doppler method. It provides a great deal of data regard-
ing the intra-lesion vascular network. Compared to con-
ventional Doppler techniques such as power Doppler and
color Doppler, it uses a higher frame rate. Tiny vessels
can be clearly detected using SMI by suppressing scat-
tering and demonstrating signals of low-velocity ows
based on the ability to distinguish motion artifacts from
slow-velocity signals [22].
The pediatric population should be considered sep-
arately from adults because the pediatric population is
exposed to many hormonal and biological changes espe-
cially in the transition from childhood (under 10 years)
to adolescence (above 10 years), unlike adults. Accord-
ing to elastography studies on adults, stretching reduces
muscle stiffness [16-21]. However, no work evaluating
the effect of SS duration in adolescents exists in the liter-
ature. Studies related to muscle blood ow used conven-
tional Doppler, micro-CT analysis, gamma scintillation
counter or experimental model methods [12,23]. These
studies have concluded that there is a reduction in local
blood ow during stretching, with an acute post-stretch
hyperemic response after stretching and a vascularity in-
crease in the chronic period. Similarly, the acute effect
of stretching on blood ow using SMI has not been pre-
viously evaluated. Hypothetically, determination of the
acute effects of SS duration on stiffness and blood ow
will be benecial for physical rehabilitation, to prevent
muscle injury and to prepare for athletic performance in
adolescents. We also hypothesized that we can quantita-
tively show the acute increase in muscle blood ow using
SMI after stretching.
Therefore, we used SWE and SMI to determine the
effects of passive SS durations (2 and 5 minutes SS) on
muscle stiffness and blood ow. Our target population
and muscle were adolescent male athletes and the rectus
femoris (RF), respectively. We also investigated inter-
operator reliability for SWE and SMI.
Material and methods
Subjects
Twenty male athletes with the median age of 14.5
(12.5-16.5) years volunteered to participate in this pro-
spective study. All of them had played in young basket-
ball leagues for at least 5 years of duration. They had no
history of traumatic or non-traumatic lower extremity in-
juries in the last 6 months. Subjects with medical history,
chronic drug use, rheumatic, systemic and/or connective
tissue disorders were not included in the study. The study
was conducted with ethics approval from the local Ethics
Committee, and signed informed consent was obtained
from the parents in all cases.
Study design
Muscle stiffness and blood ow were measured in the
supine position with the knee extended for RF measure-
ments. The participants were informed about the pro-
cedure and asked to stay as relaxed as possible during
each measurement. Subjects were randomly divided into
two groups, each including ten participants. In group A,
outcome measures were assessed before (pre-) and after
(post-) 2 min of SS. In group B, measures were assessed
before (pre-) and after (post-) 5 min of SS. All subjects
were examined in the same day by two pediatric radi-
ologists with over 5 years of SWE and 2 years of SMI
experience. Each radiologist performed the acquisition of
SWE and SMI in the same position and was blinded to
the data gathered by the other operator. Statistical com-
parisons of stiffness and blood ow values were made
between the groups. Inter-operator reliability was also
analysed.
3
Med Ultrason 2019; 0: 1-8
Shear Wave Elastography and Superb
Microvascular Imaging Techniques
Measurements were examined using an Aplio 500
Platinum ultrasound device (Canon Medical Systems, Ja-
pan) with a high-frequency linear transducer (frequency
range, 7.2–14 MHz). The entire probe surface was cov-
ered with ultrasonic gel that was 3-4 mm thick to ensure
optimal image quality and to minimize the transducer
pressure on the skin.
The measurement location was determined based on
previous studies [24]. The same location was used for
both SWE and SMI examinations. RF was examined at
the midpoint between the lateral epicondyle of the fe-
mur, and the femoral greater trochanter. The orientation
of the transducer for the SWE technique was referenced
from previous studies to achieve accurate and reliable
measurements [25]. The muscle was located with the
transducer oriented axially. Then, the longitudinally ori-
ented transducer was turned perpendicular to the plane to
measure the stiffness. Same transducer orientation was
used for the SMI technique to measure blood ow.
While obtaining the images, pressure was not ap-
plied to the probe and care was taken that the operator’s
hand was motionless. In split-screen mode, 2D-SWE
map (left side) and quality mode (right side) were ex-
amined. The quality mode, which is identied as the
propagation mode (arrival time contour), is a mode in
which reliable data is obtained when the lines are par-
allel and smooth, and the increase in distance between
lines is parallel to the increase in stiffness. The speed
of ultrasound waves was either measured in kilopascal
(kPa) for elasticity and meters/second (m/s) for veloc-
ity; within seconds, the result was displayed on the ultra-
sound screen. During stabilization of SWE images for 5
seconds, SWE images were frozen and saved. The elas-
ticity range was set to 0–80 kPa and the velocity range
was set to 0–8 m/s on a standardized “musculoskeletal
preset mode”. Subsequently, a 5 mm diameter “region of
interest (ROI)” was used to take measurements at three
different points with three repeated acquisitions in the
longitudinal view (g 1). Mean elasticity and velocity
values were automatically calculated by averaging nine
values.
SMI investigation used a frame rate set at >50 Hz and
the pulse repetition frequency was set at 220–234 Hz. The
color gain was set to 30–40 decibels to suppress back-
ground artifacts and SMI imaging used the color mode.
The vascularity index (VI [%]) measurement method
was used to quantify blood ow. In the color mode, a
rectangular ROI was manually drawn on a xed window
with 15×10 mm dimensions. Within the ROI, the propor-
tion of color pixels in the whole area was automatically
calculated by the device in percentages to obtain VI (%)
values including the total arterial and venous vascularity
supply (g 2).
Passive static stretching protocols
The right leg was used as the dominant side in all
participants. The dominant leg was determined by deter-
mination of the leg that was used most frequently and
which felt comfortable in the tourniquets and in the ver-
tical jump that the subject enters while running during
offensive rebounds during a basketball game. Two differ-
ent RF SS exercises were performed. The rst movement
was knee exion of the right extremity behind the body
while facing forward and standing on the left support leg
(g 3a). The second movement involved the left sup-
port leg in 90-degree position while facing forward and
touching the kneecap of the right extremity to the ground.
The extremity with the knee on the ground had exion
performed by the subject to bring it close to the hip. The
stretching durations were determined based on previous
studies [26,27]. When the participants were able to per-
form the stretch without discomfort or pain, 30 seconds
of stretching was performed (g 3b). In group A, two
sets of two movements were performed for 30 seconds
Fig 1. SWE measurements of RF were made using circular
ROIs that were placed in the longitudinal view on homogenous
muscle parenchyma. 2D-SWE map (left side) and quality mode
(right side) are seen.
Fig 2. A typical example demonstrating how VI (%) was ob-
tained on SMI. Variation is observed in VI (%) in a subject be-
fore (a) and after (b) stretching.
4Emine Caliskan et al Effects of static stretching duration on muscle stiffness and blood ow
(2 min), and in group B, the same two movements were
performed for ve sets of 30 seconds (5 min). In both
groups, 30 seconds of rest were given between the sets.
Statistical Analysis
Statistical analysis was performed with the SPSS
(Statistical Package for the Social Sciences) program.
Descriptive statistics of elasticity (kPa), velocity (m/s),
and VI (%) obtained by two operators at rest, 2 and 5 min
of SS were presented as minimum, maximum and medi-
an. Normality was tested using the Kolmogorov-Smirnov
tests. The visual methods such as histograms and prob-
ability plots were also used to determine the normality.
The elasticity, velocity and VI values obtained before
and after stretching in the groups A and B were compared
with the Wilcoxon test for the values without normal dis-
tribution. Spearman’s correlation coefcient was used to
obtain the relationship between stiffness and blood ow
parameters and to evaluate the relationship between elas-
ticity and velocity values. P values of less than 0.05 were
considered statistically signicant. To evaluate the inter-
operator reliability, we used the Inter-class Correlation
Coefcient (ICC) and 95% condence interval.
Results
Descriptive statistics for elasticity, velocity, and VI
values obtained by two operators at rest and after 2 and 5
min of SS are presented in Table I. When we analysed all
SWE and SMI values from both operators, Spearman’s
correlation coefcient revealed a statistically signicant
negative correlation between elasticity and VI param-
eters (p=0.011, r=−0.282) and between velocity and VI
parameters (p=0.017, r=−0.266). A signicant positive
correlation was found between all the elasticity and ve-
locity parameters (p<0.001, r=0.9; g 4).
Shear wave elastography
In group A, there was no signicant difference in
elasticity and velocity between resting and 2 min of SS
for both operators (all p>0.05 for both operators).
In group B, there was a signicant decrease in elastic-
ity and velocity between resting and 5 min of SS for both
operators (rst operator p=0.009 and p=0.007, respec-
tively; second operator p=0.04 and p=0.03, respectively).
Fig 3. RF muscle stretch methods. a. Standing on one leg and
pulling the other foot up behind your bottom. b. Fully length-
ened position for RF with a exed knee and extended hip by
kneeling down.
Fig 4. The scatter plot shows a signicant positive correlation
between the elasticity (kPa) and velocity (m/s) parameters.
Fig 5. Boxplot showing variation in the median elasticity (kPa), velocity (m/s), and VI (%) parameters at rest, and after 2 and 5 min
of SS. There is a minimal decrease in stiffness after 2 min of SS but stiffness was signicantly different between rest and at 5 min
(a and b). Differences between rest and SS were signicant for VI (%) after both 2 and 5 min of SS (c).
5
Med Ultrason 2019; 0: 1-8
The elasticity and velocity parameters were signi-
cantly lower than resting only after 5 min of SS (g 4).
Superb microvascular imaging
In group A, there was a signicant increase in VI be-
tween resting and 2 min of SS for both operators (rst
operator p=0.007; second operator p=0.007).
In group B, there was a signicant increase in VI be-
tween resting and 5 min of SS for both operators (rst
operator p=0.007; second operator p=0.005).
The blood ow signicantly increased both after 2
and 5 min of SS (g 5).
Reliability
Inter-operator reliability was moderate to perfect for
measurement of elasticity, velocity and VI at rest and af-
ter 2 and 5 min of SS (range: 0.52–0.83; Table II).
Discussions
To our knowledge, this study was the rst to investi-
gate the effects of SS on RF stiffness in adolescents using
SWE. Additionally, the originality of the present study
comes from the SMI techniques, which have not been
evaluated before and which are used to determine the dif-
ferences before and after muscle stretching. Additionally,
this study investigated the inter-operator reliability for
SWE and SMI.
In the present study, no signicant reduction in RF
stiffness after 2 min of SS was observed in adolescents.
Maeda et al [4] and Nakamura et al [18] found a signi-
cant reduction in gastrocnemius medialis (GM) stiffness
after 2 min of SS in adults, which is different from our re-
sults. The differences may be a result of investigating dif-
ferent muscles. Different muscles in the body show pro-
portional changes resulting from previous training and
frequency of use or function. Another reason may be that
our study includes adolescents. Muscles are made from a
collection of contractile (e.g., actin and myosin) and non-
contractile (e.g., glycogen, water, enzymes) components.
Depending on age and hormonal changes, there may be
differences in these components. As a result, reactions
to SS may be different. Because the similar fundamental
stretching techniques and SS durations were used in oth-
er similar studies, differences in the protocols between
the studies are unlikely to affect the results. Similar to
our study, Umehara et al [21] found that the shear elas-
tic modulus of the superior and inferior portions of the
infraspinatus decreased signicantly after a cross-body
stretch (in total 2.5 min) with scapular stabilization.
Table I. Descriptive statistics of elasticity (kPa), Shear Wave velocity (m/s) and vascularity index (%) obtained by two operators at
rest and after SS and comparison results
At rest (n=10)
Median (Min.-Max.)
After SS (n=10)
Median (Min.-Max.)
p
Opr. 1
(0-2 min)
Elasticity (kPa)
Velocity (m/s)
VI (%)
10.5 (8.3-12.9)
1.87 (1.67-2.07)
2.98 (0.8-5.8)
9.9 (8.7-12)
1.82 (1.71-1.99)
5 (1.5-11.2)
0.284
0.308
0.007
Opr. 1
(0-5 min)
Elasticity (kPa)
Velocity (m/s)
VI (%)
9.8 (8.6-11.3)
1.81 (1.71-1.95)
4.3 (2.5-9.4)
9 (8-10.8)
1.73 (1.64-1.9)
5.7 (3.8-9)
0.009
0.007
0.074
Opr. 2
(0-2 min)
Elasticity (kPa)
Velocity (m/s)
VI (%)
10.4 (8.7-12.8)
1.86 (1.71-2.08)
4.06 (0.7-10.8)
9.5 (8.5-11.5)
1.82 (1.69-1.97)
6 (1.6-14.7)
0.180
0.200
0.007
Opr. 2
(0-5 min)
Elasticity (kPa)
Velocity (m/s)
VI (%)
10.1 (9.1-11.8)
1.84 (1.75-1.98)
3.4 (1.7-7.4)
9.5 (7.7-11.8)
1.76 (1.61-1.99)
5.4 (2.5-8.6)
0.044
0.028
0.005
kPa: KiloPascal; m/s: meters/second; Max: Maximum; Min: Minimum; min.: minutes; n: number of subjects; Opr: Operator; SS: Static
Stretching; VI: Vascularity Index
Table II. Inter-operator reliability
Variables At rest (n=20) 2 min of SS (n=10) 5 min of SS (n=10)
ICC
coefcient SEM MDC95 CV
ICC
coefcient SEM MDC95 CV
ICC
coefcient SEM MDC95 CV
Elasticity (kPa) 0.81 0.087 0.241 7.1 0.62 0.129 0.357 9.2 0.52 0.159 0.440 7.8
Velocity (m/s) 0.79 0.008 0.022 36.3 0.57 0.012 0.033 4.5 0.54 0.014 0.039 3.8
VI (%) 0.82 0.165 0.457 22.9 0.77 0.395 1.094 40.8 0.83 0.146 0.404 13.4
CV: Coefcient of Variation; ICC: Inter-class Correlation; kPa: KiloPascal; m/s: meters/second; MDC: Minimum Detectable Change; min:
minutes; SEM: Standard Error of Measurement; SS: Static Stretching; VI: Vascularity Index
6Emine Caliskan et al Effects of static stretching duration on muscle stiffness and blood ow
Studies have been performed using elastography after
more than 2 min of SS. In the present study, there was a
signicant decrease in RF stiffness after 5 min SS in ado-
lescents. Similarly, Nakamura et al [19] and Taniguchi et
al [20] and found a decrease in the stiffness of GM and
gastrocnemius lateralis (GL) muscles after 5 min SS in
adults using SWE. Akagi et al [16] found a signicant
decrease in GM muscle stiffness after 6 min of SS. These
results suggest that RF and GM muscles respond with
similarly prolonged SS effects. Nordez et al [28], using
transient elastography in young adults argued that 10 min
of SS did not reduce GM muscle stiffness. The reason
for this difference may be related to the use of different
elastography methods and the difference in SS duration.
Responses to the mechanical stimuli of stretch and
shear stress play an important role in preserving normal
vascular functions. Any disruption in these variables
causes a variety of vascular disorders. Hotta et al [12]
suggested that acute stretching produces a mechani-
cal lengthening and local ischemia within muscle. Ad-
ditionally, 4 weeks of daily muscle stretching increases
blood ow to skeletal muscles during exercise, enhances
endothelium-dependent vasodilatation of resistance arte-
riole sand increases several morphological indices of O2
delivery capacity in stretched muscles in old rats. This
result investigated the chronic effects of stretching. Stud-
ies of animal models found that an increase in muscle
length during stretching caused pressure strains in capil-
laries. Thus, mean capillary diameter and muscle blood
ow decrease and vascular resistance increases during
stretching [29]. After stretching, mean leg blood ow in-
creases suggesting that there is a post-stretch hyperemic
response [26].
This study is the rst concerned with acute changes in
blood ow in humans after stretching: 2 min of SS seems
to be sufcient to increase muscle vascularity. Although
there is no clear in vivo information, it would not be sur-
prising that the increased blood ow is useful for the
muscle structure. Increased blood ow provides better
perfusion, enhances the amount of oxygen and nutrition
reaching the muscles, thereby allowing a higher level of
physical performance [30]. Increased venous ow may
be benecial to clear the accumulated lactic acid after
exercise, whereas increased oxygenation will aid in mus-
cle healing. Thus, the results of the present study may
be useful for physical rehabilitation protocols and sports
science. For example, in adult chronic stroke or pediatric
cerebral palsy, patients who are undergoing rehabilita-
tion of spastic muscles, 5 min of SS stretching may be
chosen in rehabilitation protocols instead of 2 min of
SS to ensure optimal softening of the RF. Mathevon et
al [31] mentioned that ultrasound associated with SWE
shows promise for assessing structural changes in spastic
muscles. With some methodological adaptations, that ap-
proach could guide spasticity treatment. In addition to the
previous data, the present study can make recommenda-
tions regarding the optimal time.
In sports sciences, it is widely acknowledged that
warming up before vigorous activity is important. The
overall goal of any pre-activity routine is to prevent mus-
cle injury and to prepare athletes for practice or competi-
tion. The period following warm-up and vigorous physi-
cal activity is called the “cool down”, or the post-training
period. In routine practice, it is widely assumed that
cool-down strategies may be used to enhance recovery
and reduce muscle injury after training [32]. Warm-up
and cool-down stretching is accepted as an adaptation of
low intensity exercise. Research indicates that periods of
low intensity exercise such as stretching can contribute to
long-term positive changes in the elastic properties of the
connective tissue within the muscle-tendon architecture
[32]. Increasing blood ow provides a greater amount
of oxygen to the muscles and better perfusion of mus-
cles allows the possibility of better nutrition. Better in-
tramuscular blood ow provides the opportunity to pro-
duce higher levels of physical performance [10]. Despite
these well-known benets of stretching, there are stud-
ies proposing that, because SS reduces muscle stiffness,
it negatively affects athletic performance [33,34]. Our
results show that stiffness parameters did not decrease
from resting after 2 min of SS and that blood ow signi-
cantly increased both after 2 and 5 min of SS. As a result,
for successful sporting performance, 2 min of SS may
be sufcient for the RF in warming up because reduc-
ing stiffness negatively affects athletic performance and
it may be sufcient for an optimal increase in blood ow.
Five minutes of SS may be chosen in cooling down to
reduce muscle damage formed during racing, and to help
with the recovery process.
Currently, various ultrasound elastography techniques
are available. Each technique has advantages and limita-
tions [35,36]. Strain elastography (SE) and acoustic ra-
diation force impulse (ARFI) elastography were the rst
methods developed for this purpose. However, the over-
all use of SWE has increased in recent years because it
is easy to apply, more operator-independent and provides
quantitative results. SMI is a novel Doppler method, and
its greatest advantage is that it shows very ne vascular
structures compared to color Doppler and power Doppler
[22]. The present study supports this information and the
inter-operator reliability indicates signicant correlation
for SWE and SMI. They may reliably be used for im-
mobile and surface organs such as muscles, especially in
physical rehabilitation and training sciences. Similarly,
7
Med Ultrason 2019; 0: 1-8
Jeon et al found that the inter-observer reliability for
ARFI was excellent for ankle-plantar exion with sub-
maximal isometric contraction (ICC=0.968) and good
for the relaxed position (ICC=0.891) [13]. Alfuraih et al
studied the combination of medium ROI and longitudi-
nal orientation from the lateral location for SWE resulted
in a strong internal agreement of intra-class correlation
of 0.76 (0.57–0.89) for the new system and an almost
perfect agreement of 0.92 (0.82–0.97) for the established
system [15]. Inter-system reproducibility for the best
combination was 0.71 (0.48–1) with a mean velocity of
0.07±0.49 m/s.
There are several limitations to our study. Firstly, the
study cohort could be expanded to include a greater num-
ber of participants of both genders. Another limitation
is that subjects performed SS under their own control
and determined the limit of stretch based on their own
pain threshold. A dynamometer was not used to ensure
more objective stretching. Finally, acute effects were re-
searched with no investigation into the effects of stretch-
ing durations in the chronic period on muscle stiffness.
In conclusion, SWE and SMI can be used to acquire
reliable quantitative data on muscle stiffness and blood
ow in adolescents. In medical physical rehabilitation
protocols, 5 min of SS may be chosen to reduce RF stiff-
ness and to prevent cramps, spasms, and muscle damage.
Additionally, because reducing stiffness negatively af-
fects athletic performance, 2 min of SS may be sufcient
for an optimal increase in blood ow during warm-up
procedures. Five min of SS may enhance recovery and
reduce injury during cool-down protocols after training.
Acknowledgements: We would like to acknowledge
Mrs. Manolya Kara for assisting with the review of the
publication and general academic editing.
Conict of interest: none
References
1. Page P. Current concepts in muscle stretching for exercise
and rehabilitation. Int J Sports Phys Ther 2012;7:109-119.
2. 2.Thompson AJ, Jarrett L, Lockley L, Marsden J, Steven-
son VL. Clinical management of spasticity. J Neurol Neu-
rosurg Psychiatry 2005;76:459-463.
3. Ayala F, De Ste Croix M, Sainz De Baranda P, Santonja
F. Acute effects of static and dynamic stretching on ham-
string eccentric isokinetic strength and unilateral hamstring
to quadriceps strength ratios. J Sports Sci 2013;31:831-839.
4. Maeda N, Urabe Y, Tsutsumi S, et al. The Acute Effects of
Static and Cyclic Stretching on Muscle Stiffness and Hard-
ness of Medial Gastrocnemius Muscle. J Sports Sci Med
2017;16:514-520.
5. Wilson GJ, Elliott BC, Wood GA. Stretch shorten cycle
performance enhancement through exibility training. Med
Sci Sports Exerc 1992;24:116-123.
6. Witvrouw E, Danneels L, Asselman P, D’Have T, Cambier
D. Muscle exibility as a risk factor for developing muscle
injuries in male professional soccer players. A prospective
study. Am J Sports Med 2003;31:41-46.
7. Ruan M, Zhang Q, Wu X. Acute Effects of Static Stretching
of Hamstring on Performance and Anterior Cruciate Liga-
ment Injury Risk During Stop-Jump and Cutting Tasks in
Female Athletes. J Strength Cond Res 2017;31:1241-1250.
8. Sá MA, Neto GR, Costa PB, et al. Acute Effects of Differ-
ent Stretching Techniques on the Number of Repetitions in
A Single Lower Body Resistance Training Session. J Hum
Kinet 2015;45:177-185.
9. Kuebler WM, Uhlig U, Goldmann T, et al. Stretch activates
nitric oxide production in pulmonary vascular endothelial
cells in situ. Am J Respir Crit Care Med 2003;168:1391-
1398.
10. Bassett DR Jr, Howley ET. Limiting factors for maximum
oxygen uptake and determinants of endurance performance.
Med Sci Sports Exerc 2000;32:70-84.
11. Arpino JM, Nong Z, Li F, et al. Four-Dimensional Micro-
vascular Analysis Reveals That Regenerative Angiogenesis
in Ischemic Muscle Produces a Flawed Microcirculation.
Circ Res 2017;120:1453-1465.
12. Hotta K, Behnke BJ, Arjmandi B, et al. Daily muscle
stretching enhances blood ow, endothelial function, cap-
illarity, vascular volume and connectivity in aged skeletal
muscle. J Physiol 2018;596:1903-1917.
13. Jeon M, Youn K, Yang S. Reliability and quantication of
gastrocnemius elasticity at relaxing and at submaximal con-
tracted condition. Med Ultrason 2018;20:342-347.
14. Akkoc O, Caliskan E, Bayramoglu Z. Effects of passive
muscle stiffness measured by Shear Wave Elastography,
muscle thickness, and body mass index on athletic perfor-
mance in adolescent female basketball players. Med Ultra-
son 2018;20:170-176.
15. Alfuraih AM, O’Connor P, Tan AL, Hensor E, Emery P,
Wakeeld RJ. An investigation into the variability between
different shear wave elastography systems in muscle. Med
Ultrason 2017;19:392-400.
16. Akagi R, Takahashi H. Acute effect of static stretching on
hardness of the gastrocnemius muscle. Med Sci Sports Ex-
erc 2013;45:1348-1354.
17. Hirata K, Miyamoto-Mikami E, Kanehisa H, Miyamoto
N. Muscle-specic acute changes in passive stiffness of
human triceps surae after stretching. Eur J Appl Physiol
2016;116:911-918.
18. Nakamura M, Ikezoe T, Kobayashi T, et al. Acute effects of
static stretching on muscle hardness of the medial gastroc-
nemius muscle belly in humans: an ultrasonic shear-wave
elastography study. Ultrasound Med Biol 2014;40:1991-
1997.
19. Nakamura M, Ikezoe T, Nishishita S, Umehara J, Kimura
M, Ichihashi N. Acute effects of static stretching on the
shear elastic moduli of the medial and lateral gastrocnemius
8Emine Caliskan et al Effects of static stretching duration on muscle stiffness and blood ow
muscles in young and elderly women. Musculoskelet Sci
Pract 2017;32:98-103.
20. Taniguchi K, Shinohara M, Nozaki S, Katayose M.
Acute decrease in the stiffness of resting muscle belly due
to static stretching. Scand J Med Sci Sports 2015;25:32-40.
21. Umehara J, Hasegawa S, Nakamura M, et al. Effect of scap-
ular stabilization during cross-body stretch on the hardness
of infraspinatus, teres minor, and deltoid muscles: An ul-
trasonic shear wave elastography study. Musculoskelet Sci
Pract 2017;27:91-96.
22. Machado P, Segal S, Lyshchik A, Forsberg F. A Novel Mi-
crovascular Flow Technique: Initial Results in Thyroids.
Ultrasound Q 2016;32:67-74.
23. Kruse NT, Silette CR, Scheuermann BW. Inuence of pas-
sive stretch on muscle blood ow, oxygenation and central
cardiovascular responses in healthy young males. Am J
Physiol Heart Circ Physiol 2016;310:1210-1221.
24. Chino K, Kawakami Y, Takahashi H. Tissue elasticity of in
vivo skeletal muscles measured in the transverse and longi-
tudinal planes using shear wave elastography. Clin Physiol
Funct Imaging 2017;37:394-399.
25. Gennisson JL, Defeux T, Mace E, Montaldo G, Fink M,
Tanter M. Viscoelastic and anisotropic mechanical proper-
ties of in vivo muscle tissue assessed by supersonic shear
imaging. Ultrasound Med Biol 2010;36:789-801.
26. Ryan ED, Beck TW, Herda TJ, et al. The time course of
musculotendinous stiffness responses following different
durations of passive stretching. J Orthop Sports Phys Ther
2008;38:632-639.
27. Bandy WD, Irion JM. The effect of time on static stretch
on the exibility of the hamstring muscles. Phys Ther
1994;74:845-850.
28. Nordez A, Gennisson JL, Casari P, Catheline S, Cornu C.
Characterization of muscle belly elastic properties during
passive stretching using transient elastography. J Biomech
2008;41:2305-2311.
29. Poole DC, Mathieu-Costello O. Capillary and ber geom-
etry in rat diaphragm perfusion xed in situ at different sar-
comere lengths. J Appl Physiol 1992;73:151-159.
30. Bassett DR Jr, Howley ET. Limiting factors for maximum
oxygen uptake and determinants of endurance performance.
Med Sci Sports Exerc 2000;32:70-84.
31. Mathevon L, Michel F, Aubry S, et al. Two-dimensional
and shear wave elastography ultrasound: A reliable method
to analyse spastic muscles? Muscle Nerve 2018;57:222-
228.
32. Popp JK, Bellar DM, Hoover DL, et al. Pre- and Post-Ac-
tivity Stretching Practices of Collegiate Athletic Trainers in
the United States. J Strength Cond Res 2017;31:2347-2354.
33. Bradley PS, Olsen PD, Portas MD. The effect of static,
ballistic, and proprioceptive neuromuscular facilitation
stretching on vertical jump performance. J Strength Cond
Res 2007;21:223-226.
34. Peck E, Chomko G, Gaz DV, Farrell AM. The effects
of stretching on performance. Curr Sports Med Rep
2014;13:179-185.
35. Bamber J, Cosgrove D, Dietrich CF, et al. EFSUMB guide-
lines and recommendations on the clinical use of ultrasound
elastography. Part 1: Basic principles and technology. Ul-
traschall Med 2013;34:169-184.
36. Cosgrove D, Piscaglia F, Bamber J, et al. EFSUMB guide-
lines and recommendations on the clinical use of ultrasound
elastography. Part 2: Clinical applications. Ultraschall Med
2013;34:238-253.