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Influence of Long-Lasting Static
Stretching on Maximal Strength,
Muscle Thickness and Flexibility
Konstantin Warneke
1
*, Anna Brinkmann
2
,
3
, Martin Hillebrecht
2
,
3
and Stephan Schiemann
1
1
Department for Exercise, Sport and Health, Leuphana University, Lüneburg, Germany,
2
Assistive Systems and Medical Device
Technology, Carl von Ossietzky University of Oldenburg, Oldenburg, Germany,
3
University Sports Center, Carl von Ossietzky
University of Oldenburg, Oldenburg, Germany
Background: In animal studies long-term stretching interventions up to several hours per
day have shown large increases in muscle mass as well as maximal strength. The aim of
this study was to investigate the effects of a long-term stretching on maximal strength,
muscle cross sectional area (MCSA) and range of motion (ROM) in humans.
Methods: 52 subjects were divided into an Intervention group (IG, n= 27) and a control
group (CG, n= 25). IG stretched the plantar flexors for one hour per day for six weeks using
an orthosis. Stretching was performed on one leg only to investigate the contralateral force
transfer. Maximal isometric strength (MIS) and 1RM were both measured in extended knee
joint. Furthermore, we investigated the MCSA of IG in the lateral head of the gastrocnemius
(LG) using sonography. Additionally, ROM in the upper ankle was investigated via the
functional “knee to wall stretch”test (KtW) and a goniometer device on the orthosis. A two-
way ANOVA was performed in data analysis, using the Scheffé Test as post-hoc test.
Results: There were high time-effects (p= 0.003, ƞ² = 0.090) and high interaction-effect
(p<0.001, ƞ²=0.387) for MIS and also high time-effects (p<0.001, ƞ²=0.193) and
interaction-effects (p<0.001, ƞ²=0,362) for 1RM testing. Furthermore, we measured a
significant increase of 15.2% in MCSA of LG with high time-effect (p<0.001, ƞ²=0.545)
and high interaction-effect (p=0.015, ƞ²=0.406). In ROM we found in both tests significant
increases up to 27.3% with moderate time-effect (p<0.001, ƞ²=0.129) and high
interaction-effect (p<0.001, ƞ²=0.199). Additionally, we measured significant
contralateral force transfers in maximal strength tests of 11.4% (p<0.001) in 1RM test
and 1.4% (p=0.462) in MIS test. Overall, there we no significant effects in control situations
for any parameter (CG and non-intervened leg of IG).
Discussion: We hypothesize stretching-induced muscle damage comparable to effects
of mechanical load of strength training, that led to hypertrophy and thus to an increase in
maximal strength. Increases in ROM could be attributed to longitudinal hypertrophy
effects, e.g., increase in serial sarcomeres. Measured cross-education effects could be
explained by central neural adaptations due to stimulation of the stretched muscles.
Keywords: static stretching, muscle cross sectional area, maximal strength, range of motion, hypertrophy
Edited by:
Gregory C. Bogdanis,
National and Kapodistrian University of
Athens, Greece
Reviewed by:
Masatoshi Nakamura,
Nishikyushu University, Japan
João Pedro Nunes,
Edith Cowan University, Australia
*Correspondence:
Konstantin Warneke
konstantin.warneke@
stud.leuphana.de
Specialty section:
This article was submitted to
Exercise Physiology,
a section of the journal
Frontiers in Physiology
Received: 18 February 2022
Accepted: 28 April 2022
Published: 25 May 2022
Citation:
Warneke K, Brinkmann A,
Hillebrecht M and Schiemann S (2022)
Influence of Long-Lasting Static
Stretching on Maximal Strength,
Muscle Thickness and Flexibility.
Front. Physiol. 13:878955.
doi: 10.3389/fphys.2022.878955
Frontiers in Physiology | www.frontiersin.org May 2022 | Volume 13 | Article 8789551
ORIGINAL RESEARCH
published: 25 May 2022
doi: 10.3389/fphys.2022.878955
INTRODUCTION
Regular stretch training over several weeks improves flexibility
and range of motion (ROM) (Young et al., 2013;Medeiros et al.,
2016). Reduced pain perception due to habituation effects in
humans (Freitas et al., 2018) and muscle fiber lengthening due to
serial accumulation of sarcomeres following intensive stretch
training could be determined in animals, which could be
responsible for enhanced flexibility (Williams et al., 1988;
Alway S. E., 1994). A transfer to human training studies can
be hypothesized, as Damas et al. (2018) demonstrated increased
serial sarcomere accumulation in humans in general. To
maximize ROM, stretch training should include a long
stretching duration with a high training frequency (Thomas
et al., 2018). In addition to stretching duration and frequency,
stretch intensity has a crucial influence on muscular adaptations.
At low stretching intensities, it can be assumed that the tension is
compensated primarily by the elastic components so that effects
on the contractile tissue are only achieved at a certain minimum
intensity (Apostolopoulos et al., 2015).
Long-term stretching of a muscle can also increases muscle
mass due to muscular hypertrophy in animals. A variety of
studies have been investigated in birds for this purpose, in
which a wing of the test animal was stretched from 30 min
daily to a 24-h continuous stretch over a period of 1 month
(Frankeny et al., 1983;Williams et al., 1988;Antonio et al., 1993;
Alway S. E., 1994;Czerwinski et al., 1994). In animal examination,
Antonio & Gonyea (1993) achieved an enhancement in muscle
mass of 318% with an intermittent stretching protocol by
increasing stretching intensity from 10% of the bodyweight to
25% over 33 days. Stretching one wing of quails and chickens for
different stretching durations demonstrated an increase in muscle
mass depending on stretching duration (Bates, 1993;Frankeny
et al., 1983; J.; Lee & Alway, 1996). Furthermore, gains in muscle
mass in listed studies can be related to longitudinal hypertrophy
and increases in muscle cross-sectional area of over 100%
(Frankeny et al., 1983;Matthews et al., 1990;Alway S. E.,
1994). Improvements in maximal strength are often related to
enhanced muscle cross sectional area (Seitz et al., 2016). In quail,
Alway S. E., 1994 found increments of maximal strength of 95%
by continuous stretching for 30 days compared to the
contralateral control muscle by in vitro studies.
Since authors investigated significant muscular hypertrophy in
quail and chicken wings due to long lasting stretching
interventions of several hours, which are in correlation with
improvements in maximal strength (Alway S. E., 1994),
question arises whether effects in maximal strength as well as
in muscle cross-sectional area are transferable to humans. In a
meta-analysis, Medeiros & Lima (2017) determined a positive
effect of stretching on muscular performance measured via
functional tests and isotonic contractions in humans. In
addition, literature shows significant improvements in
maximal strength up to 32.4% in leg extension by stretching
the lower extremity. For this, a 40-min stretching workout was
performed three times per week which was divided into 15
different stretching exercises for lower extremities, each hold
for 3 × 15 s (Kokkonen et al., 2007). Highest stretching duration
was performed by (Yahata et al., 2021) by stretching the plantar
flexors with a specific stretching board for 30 min per session,
each session twice a week for 5 weeks. While Yahata et al. (2021)
reported improvements in maximal strength of 6.4%, Mizuno
(2019) showed increases in maximal strength of 20.2% in
maximal strength with a stretching intervention for 8 weeks.
However, other studies failed to point out any significant
changes in MCSA or maximal strength after several weeks of
stretching training (Sato et al., 2020;Longo et al., 2021;Nakamura
et al., 2021).
Furthermore, Panidi et al. (2021) and Kokkonen et al. (2007)
demonstrated improvements in jumping performance of up to
22% (Panidi et al., 2021). While Nunes et al. (2020) point out that
low intensity stretching intervention is not a sufficient stimulus to
induce muscular hypertrophy, Panidi et al. (2021) examined an
enhancement in muscle thickness of 23% due to a stretching
training for 12 weeks in volleyball players. Moreover, Simpson
et al. (2017) showed increments of 5.6% in muscle thickness due
to 3 minutes stretching stimulus on 5 days a week.
In addition to improved maximal strength of 29% in the
stretched leg, Nelson et al. (2012) showed significant increases
in maximal strength in the contralateral leg of 8%. Panidi et al.
(2021) also point out contralateral improvements in muscular
performance measured in unilateral CMJ. To this point, cross-
education effects are mostly known from strength training when
conducted unilaterally (Andrushko et al., 2018a;Andrushko et al.,
2018b; M.; Lee et al., 2009;Lee & Carroll, 2007). We were not able
to find other studies investigating long-term effects of stretching
durations lasting at least 1 hour per day on maximal strength as
well as muscle thickness.
Consequently, no statement about transferability of results
from animal studies can be given, so the aim of the present work is
to investigate the adaptive responses to a daily one-hour
stretching training in maximal strength, muscle cross-sectional
area as well as ROM. In addition, single-leg stretching is used to
investigate cross education effects by using the non-stretched leg
as an intra-inidividual control condition. We hypothesize, that
1 hour of stretching over 6 weeks lead to enhanced maximal
strength, muscle thickness and ROM in the stretched leg.
Furthermore, we suggest improvements in maximal strength
in the not intervened control leg.
METHODS
Subjects
G-Power analysis was performed to estimate the required sample
size showing a minimal total sample size of 36. 52 athletically
active subjects were recruited from sports study programs, sports
clubs, and fitness studios. Participants were classified as active
athletes if they performed two or more training sessions per week
in a gym or a team sport continuously for the previous 6 months.
Subjects performing daily stretching training or similar activities
like yoga as well as untrained subjects were excluded from the
study. Included subjects were randomly divided into an
intervention group (IG) and a control group (CG). One
participant was dropped out, because of a sports related injury
Frontiers in Physiology | www.frontiersin.org May 2022 | Volume 13 | Article 8789552
Warneke et al. Long-Lasting Stretching on Maximal Strength
of his knee joint. Characteristics of subjects are displayed in
Table 1.
All participants were informed about the experimental risks
and provided written informed consent to participate in the
present study. Furthermore, approval for this study was
obtained from the institutional review board (Carl von
Ossietzky Universität Oldenburg, No.121-2021). The study was
performed with human participants in accordance with the
Helsinki Declaration.
Intervention
The intervention consisted of daily stretching training of the calf
muscles lasting 1 hour each session for 6 weeks, which was
realized by wearing an orthosis designed for this purpose
(Figure 1). The intervention was performed with the
dominant leg only to give the opportunity to evaluate
potential cross-sectional effects. To define the dominant leg,
participants were asks about which leg they use when perform
single-leg jumps. Subjects were instructed to wear the orthosis
with extended knee joint and the stretch Intensity was controlled
by an goniometer which was also used to determine the angle
representing the starting value during the pre-test. To achieve
high intensity and muscle tension during the stretching training,
subjects were asked to reach maximal dorsiflexed position with an
individual stretching pain at eight on a scale 1 to 10. The angle of
the orthosis had to be set on corresponding angle to ensure
sufficient intensity. Consequently, set angle of the orthosis should
improve with enhanced ROM. The stretching was to be
performed 7 days a week in a standardized body posture: the
subjects were instructed to sit with their backs as straight as
possible and place their feet on a support plate at the same height
as their chair. All subjects in the intervention group borrowed one
orthosis for the duration of the intervention and had to complete
a stretching diary in which the daily stretching duration as well as
the set angle were written down to record stretching duration and
intensity. The control group did not perform any stretching
interventions.
Testing Procedure
Before testing a five-minute warm up routine consisting of 5 min
with a 130-bpm heart rate ergometer cycling was performed.
Maximal Strength Measurement
All subjects participated in the pre- and post-test. Maximal
isometric and dynamic strength were assessed using single-leg
testing in extended as well as in flexed knee joint. A 45°leg press
was used to measure maximal strength in the extended knee joint.
A force plate was attached to the footpad to record the maximal
strength in the calf muscles with extended knee joint. We used an
50 × 60 cm force plate with a measuring range of ± 5000N and a
13-bit analog-to-digital converter. To measure maximal isometric
strength, the subject was instructed to place the feet on the
attached force plate such as that the metatarsophalangeal
joints of the feet were placed on the edge flush (Figure 2).
The starting position was chosen to give a 90°ankle joint
TABLE 1 | Characteristics of test subjects.
Group N Age (in years) Height (in cm) Weight (in kg)
Total 52 (f = 21, m = 31) 27.0 ± 3.1 175.9 ± 5.2 80.5 ± 7.3
IG 27 (f = 11, m = 16) 27.4 ± 3.1 176.2 ± 5.6 81.0 ± 6.2
CG 25 (f = 10, m = 15) 26.8 ± 2.9 175.6 ± 4.9 79.3 ± 5.3
FIGURE 1 | Orthosis used for calf muscle stretching. FIGURE 2 | Testing device for maximal isometric strength in extended
knee using leg press (LP).
Frontiers in Physiology | www.frontiersin.org May 2022 | Volume 13 | Article 8789553
Warneke et al. Long-Lasting Stretching on Maximal Strength
angle, which was controlled via the placement of an angle
template. The force plate was fixed to form an impassable
resistance from this position. The subject was instructed to
perform a maximal voluntary contraction with a plantarflexion
in response to an audible signal. Participants had to hold maximal
contraction for at least one second after reaching perceived
maximal strength. Force-time curve was recorded for 5 s. After
each trial, a one-minute rest was observed to avoid fatigue.
Measurements were conducted until no improvement in
maximal strength was recorded but for a minimum of three
trials. Reliability was determined between best trial and second-
best trial, for which a high reliability can be considered Table 2.In
the following, after taking a recovery break of 5 min, the maximal
dynamic strength of the calf muscles was tested with the knee
joint extended. The subject was instructed to assume the starting
position (90°ankle joint angle) and to press the applied weight
into a maximal plantarflexed position. For this purpose, the
covered distance was recorded with a motion sensor from the
company “MicroEpsilon”with an accuracy of 0.1 mm. Based on
isometric data of the previous testing, we added weight
corresponding to 60% of the maximal strength. After each
trial, we added weight (first 10 kg, then 5 or 2.5 kg) on the leg
press until the participant was no longer able to perform the 1RM
for full ROM. The criterion for the end of measurement was the
distance measurement via the motion sensor. Best trial with full
ROM measured was used for further analysis.
Measuring Muscle Thickness
Measures of skeletal muscle architecture were done using two-
dimensional B-mode ultrasound (Mindray Diagnostic
Ultrasound System). Here, muscle thickness represents the
most employed measure of muscle dimension (Sarto et al.,
2021) according to its correlation to muscle cross-sectional
area, which is proportional to the number of parallel
sarcomeres, thereby influencing maximal force production
(Lieber & Fridén, 2000;Narici et al., 2016;May et al., 2021).
In our examination, ultrasound images from the lateral
gastrocnemius were recorded using a linear transducer with a
standardized frequency of 12–13 MHz. Each participant was
placed prone on a table with the feet hanging down at the end
to ensure no contraction in the calf muscles. Then, the
sonographer identified the proximal and distal landmark of
the lateral gastrocnemius for each participant and
measurement (Perkisas et al., 1999). The transducer was
placed at 30% of the distance from the most lateral point of
the articular cleft of the knee to the most lateral top of the lateral
malleolus (see Figure 3)(Perkisas et al., 1999). For measuring
muscle thickness, the transducer was positioned at the midpoint
of the muscle belly perpendicular to the long axis of the leg (Sarto
et al., 2021). The muscle belly was determined as the center of
the muscle between its medial and lateral borders. This is the
point where the muscle’s anatomical cross-sectional area is
maximal (Fukunaga et al., 1992). In addition, the image plane
is best aligned with the muscle’s fascicles, including minimal
fascicle curvature (Bénard et al., 2009; May et al., 2021; Raj
et al., 2012). Before starting the measurement, transmission
gel was applied to improve acoustic coupling and to reduce the
transducer pressure on the skin. Then, the sonographer
ensured that the superficial and deep aponeuroses were as
parallel as possible by holding and thereby rotating the
transducer around the sagittal-transverse axis to the
determined point on the skin without compressing the
muscle. Hence, the visibility of the fascicles as continuous
striations from one aponeurosis to the other was optimized.
Muscle thickness is defined as the linear, perpendicular
distance between the two linear borders of the skeletal
muscle and was obtained by averaging three measurements
across the proximal, central, and distal portions of the
acquired ultrasound images (Franchi et al., 2017;Sarto
et al., 2021). Two persons independently evaluated muscle
thickness using the image processing software GIMP 2.10.28.
The objectivity of the evaluators was found to be between 0.85
(control leg) and 0.94 (intervention leg).
TABLE 2 | Reliability for the pre-test values. ICC = intraclass correlation coefficient,
CV = coefficient of variance, SD = Standard deviation.
Parameter ICC CV (%) SD
LPisoil 0.954 1.68 24.29
LPisocl 0.971 1.82 25.58
LPisoCGR 0.968 2.21 35.28
LPisoCGL 0.964 1.83 27.27
SONOil 0.947 2.99 4.6
SONOcl 0.971 1.93 7.07
KtWil 0.987 1.74 0.21
KtWcl 0.992 0.94 0.13
KtWCGR 0.979 1.81 0.24
KtWCGL 0.991 1.40 0.16
ORTil 0.997 0.64 0.38
ORTcl 0.997 0.62 0.38
ORTCGR 0.989 0.78 0.7
ORTCGL 0.990 1.16 0.8
LP, leg press; iso, isometric maximal strength; il, intervened leg; cl, control leg; Wt, weight
in dynamic maximal strength; CG, control group; R, right; L, left.
FIGURE 3 | Sonography to investigate muscle thickness in the calf
muscle.
Frontiers in Physiology | www.frontiersin.org May 2022 | Volume 13 | Article 8789554
Warneke et al. Long-Lasting Stretching on Maximal Strength
In the literature, high-reliability values of up to r = 0.9 for
determining muscle thickness via ultrasound for within-day
reliability (Nabavi et al., 2014;Cuellar et al., 2017) and with
ICC values of up to 0.88 for between-day reliability are considered
high (König et al., 2014;Rahmani et al., 2019a,2019b).
Reliability was determined between best and second-best value
and the “with-in day”reliability determined in this paper can be
classified as high with a value of r = 0.98. ICC, CV and SD are
listed in Table 2, too. Two persons evaluated the ultrasound
images independently from each other.
ROM Measurement
ROM in the upper ankle joint was recorded in IG and CG via the
functional “knee to wall stretch”test (KtW) and the angle-measuring
device on the orthosis. A sliding device was used for the KtW. The
subject was instructed to place the foot on the attached marker. The
contralateral leg was held in the air, and the subject was allowed to
hold onto the wall with his hands. To record the range of motion, the
subject pushed the board of the sliding device forward until the heel of
the standing leg lifted off. For this purpose, the investigator pulled on
a sheet of paper placed under the subject’s heel. The measurement
was finished as soon as this could be removed. The mobility was read
incmfromtheattachedmeasuringtape(Figure 4). Depending on
ankle ROM, this measurement can be seen as screening flexibility in
bended knee. Three valid trials were performed per leg, and the
maximal value was used for evaluation. Reliability was determined
between best trial and second-best trial and can be classified as high
Table 2.
Since we measured maximal strength in extended knee joint, we
used the angle measurement device of the orthosis which could be
used as goniometer (ORT) to measure maximal dorsiflexion in
extended knee joint (see Figure 5). For this purpose, the foot of
the participant should place his foot on a support plate at the same
height as the chair. While wearing orthosis the foot was pushed into
maximal dorsiflexed position with extended knee joint. Starting
position was neutral 0 position in the ankle. Each big mark of the
angle measurement device corresponds to a distance of 5°, and each
little mark corresponds to a distance of 2.5°. The achieved marker was
read off from the angle measurement device of the orthosis. Reliability
was determined between best trial and second-best trial and can be
classified as high, Table 2.
To improve comprehension of testing procedure, in Figure 6
the study design is presented graphically.
Data Analysis
The analysis was performed with SPSS 28. We used one-way
ANOVA with Scheffé post-hoc test to ensure that there were no
differences in pre-test values for any measurement. Thus, two-way
ANOVA with repeated measures was performed for the collected
parameters. Scheffé test was used as post-hoc for mean differences of
one-way ANOVA. p-Values for percentage changes were determined
with pared t-test between pre- and posttest. Effect sizes were
presented as Eta squares (ƞ
2
) and categorized as: small effect
ƞ
2
<0.06, medium effect ƞ
2
=0.06–0.14, large effect ƞ
2
>0.14 as
well as Cohen’sd.(Cohen, 1988) Effect sizes with Cohen’sdwere
categorized as: small effects d <0.5, medium effect d = 0.5–0.8, large
effect d >0.8. In addition, Pearson correlations were determined
between maximal strength and muscle thickness as well as between
changes in maximal strength and muscle thickness.
FIGURE 4 | Sliding device for the KtW to evaluate flexibility in the ankle.
FIGURE 5 | Measuring device for maximal dorsiflexion via goniometer
attached to the orthosis.
Frontiers in Physiology | www.frontiersin.org May 2022 | Volume 13 | Article 8789555
Warneke et al. Long-Lasting Stretching on Maximal Strength
RESULTS
All subjects who appeared for the pretest completed the examination.
No significant problems with the orthosis were reported and the daily
wearing durations were adhered to all subjects.
Results of descriptive statistics as well as the two-way ANOVA
are presented in Table 3. P- and F- Values of the two-way
ANOVA as well as effect sizes ƞ
2
for time dependent effect
and interaction effects are displayed.
Analysis of Maximal Strength With Extended
Knee Joint via Leg Press
One-way ANOVA showed no significant differences between
pretest values of all parameters (p>0.05).
Progression and comparison of mean values of maximal strength
in pre- and post-testing in the stretched and the control leg of the
intervention group is presented in Supplementary Figure S1.
Two-way ANOVA demonstrated high effects for the time
dependent effect (ƞ
2
= 0.09 and 0.193) and for the time × group
interaction (ƞ
2
= 0.387 and 0.362).
The Scheffé test determined significant differences for the
mean differences between pre- and posttest values in the
LPisoil and the LPisocl as well as LPisoil and CGR (p<
0.001) and LPisoil and CGL (p<0.001). No significant
difference could be determined between the control leg and
CGR (p= 0.415) as well as control leg and CGL (0.812).
Between the legs of the CGs, no significant difference could be
detected (p=0.927).
For maximal dynamic strength there were significant
differences for the mean differences between pre- and
posttest values in LPWtil and LPWtcl (p=0.026),LPWtil
and CGR (p<0.001), LPWtil and CGL (p<0.001) as well as
LPWtcl and CGR (p= 0.026) and LPWtcl and CGL (p=
0.014). No significant difference could be determined
between CGR and CGL (p=0.987).
FIGURE 6 | Graphical presentation of study design.
TABLE 3 | Descriptive statistics and two-way ANOVA of maximal strength tests.
Parameter Pretest (M±SD) Posttest (M±SD) Pre-post differences
in %
Time effect Time x group
LPIsoil 1478.4 ± 309.7N 1726.8 ± 315.8N 16.8 (p<0.001) p<0.003 p<0.001
LPIsocl 1542.3 ± 339.1N 1564.5 ± 300.5N 1.4 (p= 0.462) F = 9.108 F = 19.387
CGR 1585.4 ± 215.1N 1559.0 ± 217.8N −1.6 (p= 0.075) ƞ
2
= 0.090 ƞ
2
= 0.387
CGL 1540.1 ± 184.94N 1518.0 ± 202.55N −1.4 (p= 0.164) d = 0.629 d = 1.589
LPWtil 91.9 ± 35.0 kg 115.0 ± 32.3 kg 25.1 (p<0.001) p<0.001 p<0.001
LPWtcl 93.5 ± 32,3 kg 104.2 ± 34.4 kg 11.4 (p<0.001) F = 22.028 F = 17.434
CGR 96.9 ± 27.6 kg 95.0 ± 28.6 kg −1.2 (p= 0.467) ƞ
2
= 0.193 ƞ
2
= 0.362
CGL 98.6 ± 27.8 kg 95.0 ± 28.4 kg −3.6 (p= 0.214) d = 0.978 d = 1.506
LP = leg press; iso = isometric maximal strength; il = intervened leg; cl = control leg; Wt = weight in dynamic maximal strength; CG = control group; R = right; L = left.
Frontiers in Physiology | www.frontiersin.org May 2022 | Volume 13 | Article 8789556
Warneke et al. Long-Lasting Stretching on Maximal Strength
Analysis of Muscle Thickness via
Sonography
Table 4 shows descriptive statistics as well as time dependent
effect and interaction effects of tow-way ANOVA for determining
muscle thickness in the calf muscle.
Figure 7 shows examples of sonography measurements from
pre to posttest of the control leg and the intervened leg.
Progression and comparison of mean values of muscle thickness
in pre- and post-testing in the stretched and the control leg of the
intervention group is presented in Supplementary Figure S2.
Two-way ANOVA demonstrated high effects for the time
dependent effect (ƞ
2
= 0.545) and for the time × group interaction
(ƞ
2
= 0.406).
Analysis of ROM Values
Progression and comparison of mean values of ROM tested via
KtW and the angle measurement device of the orthosis (ORT) in
pre- and post-testing in the stretched and the control leg of the
intervention group is presented in Table 5 and in Supplementary
Figure S3.
TABLE 4 | Descriptive statistics and two-way ANOVA of muscle thickness via sonography.
Parameter Pretest (M±SD)
in mm
Posttest (M±SD)
in mm
Pre-post differences
in %
Time effect Time x group
SONOil 14.31 ± 2.42 16.5 ± 2.78 15.3 (p<0.001) p<0.001 p= 0.015
SONOcl 14.54 ± 2.32 14.85 ± 2.08 2.1 (p= 0.03) F = 33.588 F = 19.166
ƞ
2
= 0.545 ƞ
2
= 0.406
d = 2.189 d = 1.653
SONO, sonography; il, intervened leg cl, control leg.
TABLE 5 | Descriptive statistics and two-way ANOVA of ROM tests.
Parameter Pretest (M±SD) Posttest (M±SD) Pre-post differences
in %
Time effect Time x group
KtWil 12.1 ± 3.0 cm 13.7 ± 2.6 cm 13.2 (p<0.001) p= 0.011 p<0.001
KtWcl 12.7 ± 3.9 cm 12.6 ± 3.7 cm −0.8 (p= 0.701) F = 6.674 F = 16.925
CGR 12.6 ± 1.1 cm 12.3 ± 2.0 cm −2.4 (p= 0.007) ƞ
2
= 0.068 ƞ
2
= 0.356
CGL 12.2 ± 1.8 cm 12.1 ± 1.5 cm −0.8 (p= 0.506) d = 0.54 d = 1.487
ORTil 6.7 ± 1.9 8.4 ± 2.0 27.3 (p<0.001) p<0.001 p<0.001
ORTcl 6.8 ± 1.9 7.2 ± 2.1 7.5 (p= 0.211) F = 13.527 F = 7.613
CGR 7.6 ± 1.4 7.6 ± 1.3 0.7 (p= 0.724) ƞ
2
= 0.129 ƞ
2
= 0.199
CGL 7.6 ± 1.6 7.6 ± 1.6 0 (p=1.000) d=0.77 d=0.997
KtW, knee to wall stretch; il, intervened leg; cl, control leg; CG, control group; ORT, angle measuring device of the orthosis; R, right; L, left.
FIGURE 7 | Comparison of muscle thickness from pre-to posttest in the non-stretched control leg (A) and the intervened leg (B).
Frontiers in Physiology | www.frontiersin.org May 2022 | Volume 13 | Article 8789557
Warneke et al. Long-Lasting Stretching on Maximal Strength
Two-way ANOVA demonstrated high effects for the time
dependent effect (ƞ
2
= 0.068 and 0.129) and for the time × group
interaction (ƞ
2
= 0.356 and 0.199). The Scheffé test determined
significant differences for the mean differences between pre-to
posttest KtWil and KtWcl (p<0.001) as well as between KtWil
and CGR (p<0.001) and CGL (p<0.001). No significant
difference was found between the control leg and CGR (p=
0.941) and CGL (p= 1.000). Furthermore, no significant
difference was found between CGR and CGL (p= 0.959).
Significant differences were found for the mean differences
between pre-to posttest for ORTil and the ORTcl (p= 0.019) and
ORT and CGR (p= 0.002) and CGL (0.002). No significant
differences were found between ORTcl and CGR (p= 0.838) and
CGL (p= 0.783), as well as CGR and CGL (p= 1.000) measured
via angle measuring device of the orthosis.
Pearson correlations determined for muscle thickness and
maximal strength show correlations of r = 0.594 in the pre-
test as well as 0.74 for post-test values. However, Pearson
correlation for increases from pre-to post-test show no
significant relationship with r = 0.02 (p= 0.935).
DISCUSSION
In previous research, we already compared effects of one hour vs.
two hours static stretching on maximal isometric strength in
bended knee joint. Significant differences in required muscle
groups in maximal strength testing between bended and
extended knee joint (Signorile et al., 2002;Arampatzis et al.,
2006) as well as type of contraction—isometric vs. dynamic
testing condition—(Murphy & Wilson, 1996;Feeler et al.,
2010) can be assumed.
In this work, a significant improvement in maximal strength in
the calf muscles was achieved by daily one-hour stretching
training. There was a significant improvement in maximal
isometric strength production determined in the extended
knee joint by approximately 16.8% from 1478.4 ± 309.7N in
pretest to 1726.8 ± 315.8N in the stretched leg. In comparison, an
average maximal strength increase of 1.4% from 1542.3 ± 339.1N
to 1564.5 ± 300.5N was determined in the non-stretched control
leg while no significant increase was determined between legs of
CG. Furthermore, we determined enhanced maximal dynamic
strength via 1RM testing by 25.1% and 11.4% from 91.9 ± 35 kg to
115 ± 32.3 kg and 93.5 ± 32.3 kg to 104.2 ± 34.4 kg in the stretched
and non-stretched control leg, respectively. In both legs in CG no
significant change in 1RM could be determined. For all maximum
strength measurements, large effect sizes were shown for
interaction effect in ANOVA (ƞ
2
>0.14 and d >0.8). In
addition, we measured significant hypertrophy effects in the
lateral head of the gastrocnemius of 15.2% from in the
intervention leg vs. 2.1% in the control leg. In the intervened
leg, we determined and increase 14.31 ± 2.42 mm to 16.5 ±
2.78 mm. In control leg muscle thickness, we found muscle
thickness of 14.54 ± 2.32 in pretest and 14.85 ± 2.08 mm in
posttest. Furthermore, moderate correlations between maximal
strength values in the extended knee joint and muscle thickness in
the pre-test (r = 0.594; p= 0.012) and between maximal strength
values and muscle thickness in the post-test (r = 0.74; p<0.001)
were determined but no correlation was found for increases in
maximal strength and muscle thickness from pre-to post-test.
From this, it can be assumed that maximal strength increases are
not related to increases in muscle thickness so that further
investigations are required to examine the origin of maximal
strength increases. The initial hypothesis can be accepted to a
large extent. We examined high interaction effects (ƞ
2
>0.14 and d
>0.8) in the extended knee joint in isometric and dynamic
conditions. In both maximum strength tests there were
significant increases in maximum strength values in the
intervened leg. However, Scheffé test showed no significant
differences between maximal strength increases in non-
stretched control leg and both legs of the control group.
Although the changes in maximal strength of the control leg
are not significantly different from the control group under
isometric conditions, while Scheffé test showed significant
differences between the non-stretched control leg of the
intervention group compared to both legs of CG.
In the present work, a stretching duration of 1 hour per day
and a weekly volume of 7 hours was realized, which led to
comparable results in maximal strength as can be expected
from strength training performed two to three times per week
(Aube et al., 2020;Pearson et al., 2021). The recorded maximal
strength gains can possibly be attributed to muscular adaptations
to the mechanical stimuli. A mechanical tension can be seen as an
initiating stimulus to induce various cellular processes or signal
transduction and induce changes in muscle morphology
(Tatsumi, 2010;Mohamad et al., 2011;Riley & van Dyke,
2012;Boppart and Mahmassani, 2019). This so-called
mechanotransduction can induce tension-induced muscle
hypertrophy (Aguilar-Agon et al., 2019). Smith et al. (1993)
and Jacobs & Sciascia (2011) previously showed that stretching
tension of sufficient intensity can lead to DOMS and associated
inflammation. After this microtraumatization of muscle tissue,
the repair processes are related to stimulation of protein synthesis
rate (Goldspink & Harridge, 2003;Brentano & Kruel, 2011).
Because maximal strength production is closely related to the
muscle cross-sectional area of the force-generating muscle, we
assume that the muscle tension generated by the one-hour
stretching intervention was sufficient to produce muscle
hypertrophy and maximal strength gains. We determined
muscle thickness via ultrasound measurement to investigate
structural adaptations of the one-hour stretching training. A
similar procedure has already been used by Simpson et al.
(2017). The authors investigated the adaptive responses of a
three-minute stretching training performed five times per
week on maximal strength, muscle thickness, and muscle
architecture. Although there were no significant improvements
in maximal strength while authors showed muscular hypertrophy
(+5.6% in muscle thickness) in addition, Panidi et al. (2021) were
also able to determine an enhanced muscle cross-sectional area of
23 ± 14% in the intervention leg vs. 13 ± 14% in the control leg by
a 12-week stretching intervention. The cause of the structural
change on the control leg seems questionable here due to
stretching intervention and possibly are attributed to regular
training of the included participants. While central nervous
Frontiers in Physiology | www.frontiersin.org May 2022 | Volume 13 | Article 8789558
Warneke et al. Long-Lasting Stretching on Maximal Strength
adaptations may be responsible for the contralateral force
transfer, which was also recorded in this study, the source of
hypertrophic effects on the contralateral leg of 13% must be
considered critically, especially since no control group was
included in the study. Thus, habituation effects and associated
performance gains cannot be ruled out to improve maximal
strength production in the non-stretched control leg either.
Another possible explanation for enhanced maximum
strength production can be seen in possible changes in muscle
architecture, e.g., changes in pennation angle and fascicle length
(Cormie et al., 2011a;2011b). The enhanced maximal strength
due to a larger pennation angle is achieved by allowing more
sarcomeres to be arranged parallel. In contrast, a higher fascicle
length results in optimizing the muscle’s tension-length
relationship. While we did not examine muscle architecture
and fascicle length, Simpson et al. (2017) found a decrease in
pennation angle and an increase in fascicle length in addition to
muscle hypertrophy. Normally, a bigger muscle cross sectional
area is correlated to an increased pennation angle (Cormie et al.,
2011a,2011b;Suchomel et al., 2018). Consequently, further
studies should investigate the influence of long-lasting
stretching interventions on muscle architecture as a potential
factor for improved maximal strength values. In addition, the
changes in muscle architecture recorded by Simpson et al. (2017)
suggest an influence on the contraction velocity of the stretched
muscle. In addition, study by (Möck et al., 2019) established
moderate to high correlations between maximal strength in the
calf muscles and sprint performance. Because of achieved
significant increase in maximal strength due to one-hour
stretching intervention, the influence on sport-specific
parameters as jumping and sprinting performance should be
investigated in further investigations. Therefore, Panidi et al.
(2021) provide first results by recording jumping performance
after a twelve-week intervention and examined 27% enhanced
vertical jumping heights due to one legged counter
movement jump.
While there are studies showing positive effects of stretching
interventions on maximal strength (Kokkonen et al., 2007;
Nelson et al., 2012;Mizuno, 2019;Yahata et al., 2021) and
muscle thickness (Abdel-Aziem & Mohammad, 2012;
Moltubakk et al., 2021), there are also studies showing no
effects on strength capacity (Sato et al., 2020;Nakamura et al.,
2021), hypertrophy and muscle architecture (Nunes et al., 2020;
Yahata et al., 2021). Assuming significant influence of stretching
intensity on adaptations of the muscle-tendon unit
(Apostolopoulos et al., 2015;Nakamura et al., 2021) partially
differences in results may be explainable due to heterogeneity in
study design of these studies. Most studies did not quantify
stretching intensity (Kokkonen et al., 2007;Nelson et al., 2012;
Mizuno, 2019) and stretching duration varied to a high degree
from 4 × 30 s on 3 days per week (Nelson et al., 2012;Mizuno,
2019) to 6 × 5 min on 2 days per week (Yahata et al., 2021) with
very different exercises. Consequently, comparability of results
must be questioned and quantification in particular regarding is
requested.
Previous studies showing significant increases in maximal
strength and/or muscle thickness used shorter stretching
duration. Highest stretching volume found in literature was
6 × 5min per session with a weekly volume of 1 h, which was
used in our study within 1 day. Compared to Yahata et al. (2021)
determining a mean enhancement in maximal isometric strength
of 6.4% and 7.8% in maximal dynamic strength with no
improvement in muscle thickness, our results show higher
increases in maximal strength capacity as well as an
improvement in muscle thickness. Considering that we used
seven times of the stretch volume compared to Yahata et al.
(2021), we demonstrated that increasing the stretching duration
leads to increased adaptations as well. Further investigations
should examine the most economic stretching duration to
improve maximal strength.
Since a contralateral force transfer could be recorded,
especially in 1RM measurement, increments in MSt cannot be
exclusively attributed to tension-induced hypertrophy effects.
After performing intensive strength training, improved
distribution of anabolic hormones can be hypothesized, which
also have an anabolic effect on the non-stretched calf muscle.
However, it seems questionable whether a stretching of the calf
muscles of 1 h can result in such a deflection, since especially the
amount of hormonal change seems to depend on the size of the
involved muscles (Fleck & Kraemer, 2004) and the calf can be
considered a relatively small muscle group. In addition to
hypertrophy effects in the stretched leg, we hypothesize
neuromuscular adaptation through stretching as an additional
reason for the effect on maximal strength, since contralateral
force transfer due to strength training is also primarily explained
by neuromuscular adaptations (Green & Gabriel, 2018; M.; Lee
et al., 2009; M.; Lee & Carroll, 2007). Therefore, the inclusion of
EMG studies is necessary to clarify neuromuscular adaptations.
Since neuromuscular deficits, as well as a loss of muscle mass and
cross-sectional area (sarcopenia), lead to reduced balance ability
and thus an increased risk of falls (Gschwind et al., 2013;Lacroix
et al., 2017), the influence of long-term stretching on balance
ability can be investigated in future studies. The calf muscles can
be considered relevant, especially in this context (Stolzenberg
et al., 2018;Reynoldsid et al., 2020).
Significant improvements in ROM, determined via the KtW,
were also found to average 13.2% from 12.1 ± 3.0 cm to 13.7 ±
2.6 cm in the intervention leg, while the values for the control leg
did not change significantly with −0.8% from 12.7 ± 3.9 cm to
12.6 ± 3.7 cm. ROM values in both control legs measured with
KtW did not change significantly. Measurement of ROM by the
orthosis revealed a significant improvement of 27.3% in
intervened leg from 6.7 ± 1.9 to 8.4 ± 2.0 which corresponds
to an angle of 33.5 ± 9.5°–42.5 ± 10°. The contralateral control leg
improved flexibility measured via the angle measurement device
of the orthosis by 7.5% from 6.8 ± 1.9 to 7.2 ± 2.1 with
corresponding angle improvement from 34 ± 9.5°to 36 ±
10.5°. No significant changes in ROM could be determined for
both legs of the control group.
The influence of stretch training on ROM has already been
extensively studied (Medeiros et al., 2016;Medeiros & Martini,
2018). Improvements in ROM in the present study of 13% in the
KtW and 27% measured via orthosis can possibly be attributed to
an increase in serial sarcomere number. In animal experiments,
Frontiers in Physiology | www.frontiersin.org May 2022 | Volume 13 | Article 8789559
Warneke et al. Long-Lasting Stretching on Maximal Strength
this so-called longitudinal hypertrophy has already been
demonstrated by a long-lasting stretch intervention (Antonio
et al., 1993;Alway S., 1994,Alway, S. E. 1994). Freitas et al. (2018)
and Magnusson (1998)point to an altered pain tolerance at high
stretch levels, rather than morphological muscle adaptation, as
the cause of expansions in ROM.
Highest effects of stretching the plantar flexors with the orthosis
on maximal strength and ROM were determined in testing
conditions in extended knee joint. This is explainable as stretching
was performed in extended knee joint as well. However, there were
significant improvements in maximal strength measured in previous
examination of our group and ROM in bended knee joint, too. For
listed testing conditions there were significant increases in maximum
strength and for 1RM testing significant improvements of the non-
stretched control leg. In ROM, no significant effect of the daily 1 h
stretching training could be determined in the non-stretched control
leg in regard to both control legs.
In conclusion, increases in maximum strength can be
commonly attributed to changes in innervation of the central
nervous system, changes in muscle architecture or, independently
from that, muscle hypertrophy (Loenneke et al., 2019)
Limitations
Several studies could be found in which ultrasound measurement was
used to determine muscle cross-sectional area (Nabavi et al., 2014;
Cuellar et al., 2017;Simpson et al., 2017;Messina et al., 2018;Albano
et al., 2020;Panidi et al., 2021). In particular, investigating muscle
cross-sectional area via sonography offers advantages over MRI
examinations in terms of cost and time (Sergietal.,2016).
However, stronger or weaker pressure of the ultrasound probe on
the muscle belly can influencemusclethickness,sothereisa
subjective influence on the result. To counteract this, in this study,
we took three image acquisitions in succession per leg for each
measurement and had the same examiner perform the pretest and
posttest of one subject. From a measurement methodology
perspective, sonography can be used to investigate structural
changes in the muscle, if investigators and evaluators are
experienced but the use of MRI images must be considered the
gold standard for determining muscle cross-section (Messina et al.,
2018;Albano et al., 2020), especially because all subjective factors can
be excluded. No randomization could be performed for the present
study because not all included subjects agreed to wear the orthosis for
1h per day.
PRACTICAL APPLICATIONS
The effects of the training method of long-term stretching on
maximal strength, muscle cross-sectional area, and flexibility
were investigated in this study can be used in diverse areas.
“The therapeutic applications of stretch should therefore be borne
in mind when designing regimes for rehabilitation or improved
athletic performance”(MacDougall, 2003). Its use in the
rehabilitation of orthopedic conditions or lower extremity
injuries that result in immobilization seems particularly
relevant. A stretching intervention would already be applicable
if, due to immobilization or corresponding injuries and diseases,
voluntary activation of the musculature in the context of strength
training is not (yet) feasible. This could minimize muscle atrophy
and loss of strength. Prostheses and cartilage transplants (in the
knee and hip) result in long periods of immobilization. This is
associated with muscular atrophy (Stevens et al., 2004;Perkin
et al., 2016).
DATA AVAILABILITY STATEMENT
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
ETHICS STATEMENT
The studies involving human participants were reviewed and
approved by the medical ethics committee of Carl von Ossietzky
University of Oldenburg. The patients/participants provided
their written informed consent to participate in this study.
AUTHOR CONTRIBUTIONS
KW carried out the experiment, performed the analytic
calculations and took the lead in writing the manuscript
with support from AB, SS, and MH. AB supervised and
directed the analysis of ultrasound images and helped and
assisted in writing the manuscript. MH conceived the main
conceptual ideas and planned the experiments in consultation
with KW and SS. SS supervised the project and provided
critical feedback to the design of the study and the statistical
analysis. All authors discussed the results and contributed to
the final version of the manuscript.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found online at:
https://www.frontiersin.org/articles/10.3389/fphys.2022.878955/
full#supplementary-material
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