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2743
Introduction
Mechanical load induced as cyclic strain, imposed externally
to fibrous connective tissues such as tendons, may induce
several signals at the extracellular matrix. This happens through
mechanotransduction pathways affecting the anabolic as well as
the catabolic responses (Brown et al., 1998; Hsieh et al., 2000;
Zeichen et al., 2000). It has been reported that the cells sense
the applied strain (Chiquet, 1999; Chiquet et al., 2003) and
regulate the synthesis of matrix proteins (Arnoczky et al., 2002;
Skutek et al., 2003; Miller et al., 2005), the gene expression of
proteoglycans and collagen (Robbins and Vogel, 1994; Kim et
al., 2002; Hsieh et al., 2000), the alignment and density of the
collagenous matrix (Pins et al., 1997; Wang et al., 2001; Wang
et al., 2003a) as well as the expression of several growth factors
(Skutek et al., 2001; Yang et al., 2004; Olesen et al., 2006).
Studies examining the influence of mechanical loading on the
regulation of the biosynthesis of connective soft tissues
demonstrated that the strain magnitude, strain frequency, strain
rate and strain duration of cells influence the cellular
biochemical responses (Skutek et al., 2003; Arnoczky et al.,
2002; Yang et al., 2004) and the mechanical properties of
collagen fascicles (Yamamoto et al., 2002; Yamamoto et al.,
2003; Yamamoto et al., 2005). Furthermore, the above studies
illustrate the highly plastic nature of fibrous connective tissues
and provide evidence that strain of tendon cells is an important
regulator for the homeostasis of connective tissues.
More than two decades ago, Woo et al. (Woo et al., 1982)
formulated the hypothesis that the homeostatic responses of soft
tissues subjected to mechanical loads may be represented by a
non-linear curve. Immobilisation causes a rapid decline in the
mechanical properties whereas long-term exercise initiates a
slight increase in mechanical properties compared with normal
daily activities (Woo et al., 1982). More recently, it has been
suggested that the applied strain on the connective tissues may
have a threshold or set-point to create a homeostatic
perturbation in the collagenous matrix that regulates the
catabolic and anabolic responses of the cells (Brown et al.,
1998; Lavagnino and Arnoczky, 2005). An external mechanical
loading of the tissue above the upper limit at which the
endogenous contraction of the fibroblasts may maintain their
tensional homeostasis should stimulate cells for remodelling,
whereas a reduction of the mechanical loading below the lower
limit will lead to tissue destruction (Lavagnino and Arnoczky,
2005; Lavagnino et al., 2006).
In agreement with both the hypothesis formulated by Woo et
al. (Woo et al., 1982) and the concept of the ‘homeostatic
calibration point’ (Lavagnino and Arnoczky, 2005; Lavagnino et
al., 2006), which supports the existence of an upper and a lower
Tendons are able to remodel their mechanical and
morphological properties in response to mechanical
loading. However, there is little information about the
effects of controlled modulation in cyclic strain magnitude
applied to the tendon on the adaptation of tendon’s
properties in vivo. The present study investigated whether
the magnitude of the mechanical load induced as cyclic
strain applied to the Achilles tendon may have a threshold
in order to trigger adaptation effects on tendon mechanical
and morphological properties. Twenty-one adults
(experimental group, N=11; control group, N=10)
participated in the study. The participants of the
experimental group exercised one leg at low-magnitude
tendon strain (2.85±0.99%) and the other leg at high-
magnitude tendon strain (4.55±1.38%) of similar frequency
and volume. After 14·weeks of exercise intervention we
found a decrease in strain at a given tendon force, an
increase in tendon-aponeurosis stiffness and tendon elastic
modulus and a region-specific hypertrophy of the Achilles
tendon only in the leg exercised at high strain magnitude.
These findings provide evidence of the existence of a
threshold or set-point at the applied strain magnitude at
which the transduction of the mechanical stimulus may
influence the tensional homeostasis of the tendons. The
results further show that the mechanical load exerted on the
Achilles tendon during the low-strain-magnitude exercise is
not a sufficient stimulus for triggering further adaptation
effects on the Achilles tendon than the stimulus provided by
the mechanical load applied during daily activities.
Key words: MRI, ultrasonography, tendon plasticity, in vivo, exercise,
strain.
Summary
The Journal of Experimental Biology 210, 2743-2753
Published by The Company of Biologists 2007
doi:10.1242/jeb.003814
Adaptational responses of the human Achilles tendon by modulation of the
applied cyclic strain magnitude
Adamantios Arampatzis*, Kiros Karamanidis and Kirsten Albracht
German Sport University of Cologne, Institute of Biomechanics and Orthopaedics, Carl-Diem-Weg 6, 50933 Cologne,
Germany
*Author for correspondence (e-mail: Arampatzis@dshs-koeln.de)
Accepted 14 May 2007
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2744
limit determining a homeostatic perturbation, we did not find a
graded response between exercise intensity and mechanical
properties of the human triceps surae tendon and aponeurosis by
comparing sprinters, endurance runners and subjects not being
active in sports (Arampatzis et al., 2007a). Only the sprinters
group showed a higher stiffness at the triceps surae tendon and
aponeurosis compared with the other two groups examined
(Arampatzis et al., 2007a). Further, we suggested (Arampatzis et
al., 2007a) that the mechanical properties of the human triceps
surae tendon and aponeurosis remain at control level in a wide
range of applied strains and that the strain magnitude, strain
frequency and strain rate should exceed a given threshold in
order to trigger additional adaptation effects. Although numerous
important studies have previously demonstrated the plasticity of
human tendons in response to resistance exercise (Kubo et al.,
2001a; Kubo et al., 2001b; Kubo et al., 2002; Reeves et al.,
2003a; Reeves et al., 2003b; Reeves et al., 2005), and even
though it is well accepted that tendons are able to remodel their
mechanical and morphological properties in response to
mechanical loading, there is little information about the effects
of controlled modulation in cyclic strain magnitude, frequency
or rate applied to the tendon on the adaptation of the mechanical
and morphological properties of tendons in vivo. Thus, it may be
concluded that the tendon responses to different cyclic strain
magnitudes in vivo remain a fundamental unanswered question.
Knowledge of tendon plasticity in response to the magnitude of
the mechanical load induced as cyclic strain applied to the tendon
may help improve the intervention process of tendon adaptation
and tendon healing.
The purpose of this study was to examine the effect of two
different exercise interventions of cyclic strain applied to the
Achilles tendon on the adaptation of its mechanical and
morphological properties. Both interventions were performed at
the same frequency and volume but at different magnitudes of
tendon strain (2.85±0.99% vs 4.55±1.38% strain). Based on
reports about human tendon plasticity (Kubo et al., 2001a; Kubo
et al., 2001b; Kubo et al., 2002; Reeves et al., 2003a; Reeves et
al., 2003b; Reeves et al., 2005), the concept of the homeostatic
calibration point (Lavagnino and Arnoczky, 2005; Lavagnino et
al., 2006) and the non-graded response of the mechanical
properties of the human triceps surae tendon and aponeurosis in
an intensity-dependent manner of sport activity (Arampatzis et
al., 2007a), we expected an adaptation effect on the Achilles
tendon only after the high-strain-magnitude exercise
intervention, demonstrating a threshold in strain magnitude for
further adaptational effects in vivo.
Materials and methods
Participants
Twenty-one healthy, not strength-trained, adults (23–42·years
old) from the university population participated in the study
after giving informed consent to the experimental procedure,
complying with the rules of the local scientific board. Eleven of
them (eight females and three males; 64.1±5.0·kg body mass,
172±5·cm body height, 29.5±5.0 years old; means ± s.d.) were
recruited for the experimental group (exercise intervention). The
remaining 10 participants (six females and four males;
70.4±4.5·kg body mass, 172±4·cm body height, 28.6±4.5 years
old) formed the control group (no exercise intervention).
Exercise protocol
The intervention lasted 14·weeks. Four times per week the
experimental group performed five sets of repetitive (3·s
loading, 3·s relaxation), isometric plantar flexion contractions
(ankle angle at 85° dorsal flexion, knee angle fully extended at
180° and the hip flexed at 140°). Repetitive isometric plantar
flexion contractions were used to induce cyclic strains on the
triceps surae tendon and aponeurosis. The participants exercised
one leg at low-magnitude tendon–aponeurosis strain (low-
strain-magnitude exercise) and the other leg at high-magnitude
tendon–aponeurosis strain (high-strain-magnitude exercise).
The assignment of low and high strain exercise to each leg was
random. Based on earlier experience (Arampatzis et al., 2005a;
Mademli et al., 2006), we predicted that a plantar flexion
moment at 55% of the achieved maximum moment during a
maximum voluntary contraction (MVC) should induce a
tendon–aponeurosis strain between 2.5 and 3.0% whereas a
plantar flexion moment at 90% of the MVC should induce
between 4.5 and 5.0% strain. At each set, the leg exercised at
high strain magnitude performed four repetitions (3·s loading,
3·s relaxation) at 90% of the MVC whereas the other leg (low
strain magnitude) performed seven repetitions at 55% of the
MVC (Fig.·1). This way (four vs seven repetitions per set for
the high- and the low-strain-magnitude exercise, respectively),
both legs were trained at the same exercise volume (integral of
the plantar flexion moment over time). The above experimental
design provided an intervention of similar frequency and
volume but different magnitude of applied cyclic strain to the
triceps surae tendon and aponeurosis of each trained leg.
The exercise intervention was performed on a dynamometer
(Biodex-System 3; Biodex Medical Systems, Inc., Shirley, NY,
USA). During the 14·weeks of intervention and at each exercise
set, the participants had to match the target moment (55 or 90%
of MVC; 3·s loading, 3·s relaxation) displayed on a screen
(Fig.·1). Before and after the intervention we examined the
maximum plantar flexion moment during a MVC, the voluntary
activation (VA) during the MVC and the elongation–force
relationship of the triceps surae tendon and aponeurosis from all
21 participants. For the exercise group, we additionally
measured the cross-sectional area (CSA) of the Achilles tendon
of both legs. None of the examined subjects (exercise and
control group) participated in any other organised exercise
activity during the 14·weeks.
Measurement of plantar flexion moment and voluntary
activation
The subjects were seated on a dynamometer (Biodex-
System3) with the ankle angle in a dorsal flexed position at 85°
(tibia perpendicular to the sole, corresponding to 90° ankle
angle), the knee fully extended at 180° and the hip flexed at
140°. In this position, the subjects performed maximal isometric
plantar flexion contractions. After a warm-up period, consisting
of 2–3·min submaximal isometric contractions, and three MVCs
the participants were instructed to produce a maximal isometric
force ramp with the highest possible rate of force generation.
We used the three MVCs to exclude the preconditioning effect
on the tendon strain–force relationship. The three MVCs at the
beginning of the intervention should not have any substantial
training effect. The twitch interpolation technique (Merton,
A. Arampatzis, K. Karamanidis and K. Albracht
4(%*/52.!,/&%80%2)-%.4!,")/,/'9
2745Cyclic strain and tendon adaptation
1954) was used to determine the VA of the plantar flexor
muscles during the contraction. We evoked a superimposed
twitch (three 500·!s square-wave pulses separated by 5·ms) at
the plateau of the MVC and three supramaximal twitches after
the MVC when the plantar flexor muscles were relaxed (Fig.·2)
using a stimulator (Model DS7A digitimer; Digitimer Ltd,
Welwyn Garden City, Hertfordshire, UK). The voluntary
activation was calculated by normalising the evoked
interpolated twitch torque (ITT) to the mean of the three resting
twitch torques (RTT): VA=[1–ITT/RTT)"100].
The resultant moments at the ankle joint were calculated
through inverse dynamics. The method for calculating the
resultant joint moments has been previously described
(Arampatzis et al., 2005b). Kinematic data were recorded using
the Vicon 624 system (Vicon Motion Systems, Oxford, United
Kingdom) with eight cameras operating at 120·Hz. To calculate
the lever arm of the ankle joint during ankle plantar flexion, the
centre of pressure under the foot was determined by means of
a flexible pressure distribution insole (Pedar-System, Novel
GmbH, Munich, Germany) operating at 99·Hz (Arampatzis et
al., 2005b). The compensation of moments due to gravitational
forces was determined for all subjects before each ankle plantar
flexion contraction. The antagonistic moment of the tibialis
anterior (TA) during MVC was estimated by establishing a
relationship between electromyographic (EMG) activity and
exerted moment for the TA, while working as agonist (Mademli
et al., 2004). This was established by measuring EMG and
moment during relaxation and during two submaximal ankle
dorsiflexion contractions (Mademli et al., 2004).
Measurement of tendinous tissue elongation
After the MVC with the superimposed twitches, the
participants were instructed to produce another maximal
isometric force ramp, gradually increasing the plantar flexion
effort over 3·s (loading), and to hold the achieved moment for
about 2–3·s. A 7.5·MHz linear array ultrasound probe (Aloka
SSD 4000; Tokyo, Japan; 43·Hz) was used to visualise the distal
tendon and aponeurosis of the gastrocnemius medialis (GM)
during the MVC. The ultrasound images were recorded on video
tapes for further analysis. On the video images, a clear visible
cross-point (intersecting point between the distal aponeurosis
and a fascicle of the GM muscle) was identified and its
displacement was measured in relation to a skin marker (Fig.·3).
The exact protocol for analysing the tendinous tissue elongation
during ankle plantar flexion is described in detail elsewhere
(Arampatzis et al., 2005a). Briefly, the ultrasound probe was
placed above the muscle belly at about 50% of its length. For
the analysis of the video tapes every single frame was digitised
using video analysis software (Simi Motion 5.0; SIMI Reality
Motion System GmbH, Unterschleißheim, Germany). The
effect of inevitable joint angular displacement on the observed
elongation of the tendon and aponeurosis during the MVC was
0 5 10 15 2520 30 35 40 45 0 5 10 15 2520 30 35 40 45
0
1
2
3
4
5
6
0
1
2
3
4
5
6
Low strain: 55% MVC
ADU
Time (s)
Signal
Moment
High strain: 90% MVC
Fig.·1. Each training day of the intervention protocol consisted of five sets of repetitive (3·s loading, 3·s relaxation) isometric plantar flexion
contractions to induce cyclic strain on the triceps surae tendon and aponeurosis. One leg exercised at low-magnitude tendon–aponeurosis strain
[55% of the maximum voluntary contraction (MVC)] whereas the other one exercised at high-magnitude tendon–aponeurosis (90% MVC). The
total exercise volume (integral of the plantar flexion moment over time) was identical for both legs. Signal: signal displayed on a computer monitor
(3·s loading, 3·s relaxation) for controlling the exercise loading. Moment: plantar flexion moment generated during an exercise set.
024681012141618
0
50
100
150
200
250
Moment (Nm)
Time (s)
Fig.·2. Plantar flexion moment–time history during a maximum
voluntary contraction (MVC) from one participant with superimposed
twitches. A superimposed twitch was evoked through a triplet
electrostimulation (three 500·!s square-wave pulses separated by
5·ms) at the plateau of the MVC. Three more twitches were evoked
after the MVC, when the triceps surae muscles were relaxed. The
vertical lines indicate the instant of the electrostimulation.
4(%*/52.!,/&%80%2)-%.4!,")/,/'9
2746
taken into account by capturing the motion of the tendons and
aponeuroses from the GM during a passive (inactive) motion of
the ankle joint (Muramatsu et al., 2001). The passive motion of
the ankle joint has been analysed during the plantar flexion
because the angular rotation at the ankle joint during the
‘isometric’ MVC was also a plantar flexion. The error of this
method on the strain value is ~0.3% and, thus, has a negligible
effect on the examined in vivo strain of the tendon and
aponeurosis (Arampatzis et al., 2007b). The analysed cross-
point at the aponeurosis was digitised during the inactive
condition at the same ankle angle changes as observed during
the MVC (Arampatzis et al., 2005a). The elongation of the GM
tendon and aponeurosis was calculated as the difference
between the measured and the passive (due to joint rotation)
displacement of the analysed point at the aponeurosis (Fig.·4).
In order to estimate the resting length of the GM tendon and
aponeurosis, the subjects were seated on the dynamometer with
the knee at 180° and the ankle at 110°. We used this specific
position because De Monte et al. (De Monte et al., 2006)
reported the existence of slackness in the inactive GM
muscle–tendon unit between 121° and 107° ankle angle and
180° knee angle and that the 110° ankle angle is a suitable
position to examine the resting length of the GM tendon and
aponeurosis. The length of the curved path from the tuberositas
calcanei (defined as the origin of the Achilles tendon) to the skin
marker (Fig.·3) was measured along the skin using flexible
measuring tape. Thus, the resting length of the GM tendon and
aponeurosis was defined as the length of the path between the
tuberositas calcanei and the analysed cross-points identified on
the ultrasound images. The tendon force was calculated by
dividing the plantar flexion moment by the tendon moment arm.
The moment arm of the Achilles tendon was calculated using
the data provided by Maganaris et al. (Maganaris et al., 1998).
The elongation and strain of the tendon and aponeurosis during
the MVC was identified and analysed
at the maximum calculated tendon
force and at every 100·N. The
stiffness of the triceps surae tendon
and aponeurosis has been calculated
as the slope of the calculated tendon
force vs tendon–aponeurosis
elongation between 50% and 100%
of the maximum tendon force by
means of linear regressions.
A. Arampatzis, K. Karamanidis and K. Albracht
Fig.·3. Ultrasound images of the gastrocnemius medialis (GM) at rest, at 50% of the maximum voluntary contraction (MVC) and at the plateau
of the MVC. The elongation of the tendon and aponeurosis was examined at the GM muscle belly at about 50% of its length. The displacement
of the analysed cross-point in relation to the skin marker was defined as measured elongation of the tendon and aponeurosis.
85
90
95
100
105
0
5
10
15
20
25
30
0 20 40 60 80 1000 20 40 60 80 100
Ankle angle (deg.)
Measured
Corrected
Passive
Displacement (mm)
Post-exercise
Measured
Corrected
Passive
tmax (%)
Pre-exercise
Fig.·4. Mean curves (N=11) of the
ankle angles and tendon–aponeurosis
displacement during the maximum
voluntary contraction (MVC) at the high-
strain-magnitude exercised leg before
(pre-exercise) and after (post-exercise)
the intervention. The elongation of the
tendon and aponeurosis (corrected) was
calculated as the difference of measured
displacement (measured) and the passive
displacement due to ankle joint rotation
(passive) of the analysed cross-point at
the aponeurosis of the gastrocnemius
medialis. tmax: time to achieve maximum
tendon force.
4(%*/52.!,/&%80%2)-%.4!,")/,/'9
2747Cyclic strain and tendon adaptation
Measurement of the CSA of the Achilles tendon
In order to determine the CSA of the Achilles tendon along
its length, transversal and sagittal T1 weighted magnet
resonance (MR) images (Fig.·5) were recorded using a scanner
(Magnetom Symphony; Siemens, Erlangen, Germany) with a
magnetic strength field of 1.5·T and an image frequency of
64·MHz. For the transversal images, the scanning parameters
were TR/TE 590/11, FOV 29.9"29.9·cm, pixel size
0.58594"0.58594·mm, slice thickness 4·mm, spacing between
slices 0.8·mm. For the sagittal images, the parameters were
TR/TE 665/11, FOV 29.9"29.9·cm, pixel size
0.58594"0.58594·mm, slice thickness 3·mm, spacing between
slices 0.6·mm. Throughout the scan process the subjects laid
unloaded in a supine position. No muscle contraction was
apparent during the measurements.
To standardise the levels of the transversal images, two
landmarks, the most proximal aspect of the tuberositas
calcanei and the most distal aspect of the soleus muscle, were
utilised. The sagittal images served to obtain the locations of
both points. On each transversal image, the boundaries of the
Achilles tendon were outlined manually using the software
3D Doctor (Able Software Corp., Lexington, MA, USA). The
tendon boundaries and the coordinates of the two landmarks
were exported and processed using Matlab (The Mathworks,
Natick, MA, USA). For each of the subsequent cross-sections,
the area and the location of the centroid were calculated. The
length of the Achilles tendon was calculated as the curved
path through the centroids of the cross-sections between the
two landmarks. The CSA of the Achilles tendon was
identified and analysed at every 10% of tendon length. To
examine the elastic modulus of the Achilles tendon we
calculated the relationship between tendon stress and
tendon–aponeurosis strain from 50% to 100% of the
maximum tendon stress by means of linear regressions. To
calculate the tendon stress (tendon force/tendon CSA) we
used the average value of the CSA of the Achilles tendon
from 10% to 100% of the tendon length.
Statistics
A T-test for two dependent samples was used to check the
intervention-related differences in the examined parameters
(maximum plantar flexion moment, voluntary activation,
tendon–aponeurosis strain at every 100·N and CSA of the
Achilles tendon at every 10% of the tendon length) in each
group. Further, to check the ratios (post- to pre-exercise values)
of the examined parameters we used a one-way analysis of
variance (ANOVA) and Bonferroni post-hoc comparisons
between the three groups (control group, no exercise
intervention; experimental group 1, low-strain-magnitude
exercise intervention; experimental group 2, high-strain-
magnitude exercise intervention). The level of significance for
all comparisons was set to #=0.05. In all figures, the data are
presented as means ± standard error of mean (s.e.m.), whereas
in the text and tables they are expressed as means ± standard
deviation (s.d.).
Results
The body mass of neither the experimental nor the control
group changed after the 14·weeks of intervention (experimental:
64.1±5.0·kg pre-exercise, 64.8±4.8·kg post-exercise; control:
70.4±4.5·kg pre, 70.2±4.3·kg post). The mean values of the
applied tendon–aponeurosis strain during the exercise
intervention were 2.85±0.99% and 4.55±1.38% for the 55% and
90% MVC-exercised legs, respectively. After the 14·weeks of
intervention, the maximum plantar flexion moment and the
maximum calculated tendon force showed a statistically
significant increase (P<0.05) in both exercise protocols
(Table·1). However, statistically significant changes in the
maximum elongation and strain before and after the exercise
were found only in the low-strain-exercise intervention. Both
Lateral Medial
40
30
20
10
0
–10
–20
–30
Length (mm)
Length (mm)
Length
(mm
)
50 40 20 10
80
70
60
30
C
A
B
Fig.·5. Sagittal (A) and transversal (B)
magnetic resonance images as well as the
digitised Achilles tendon boundaries (C).
The sagittal images served to obtain the
location of the most proximal aspect of
the tuberositas calcanei and the most
distal aspect of the soleus muscle. On
each transversal image, the boundaries of
the Achilles tendon were outlined
manually. The length of the Achilles
tendon was calculated as the curved path
passing through the centroids of the cross
sections (C).
4(%*/52.!,/&%80%2)-%.4!,")/,/'9
2748
the maximum elongation and maximum strain were higher after
the intervention in the low-strain-exercised leg (Table·1).
Tendon–aponeurosis stiffness increased significantly (P<0.05)
only in the high-strain-exercised leg (Table·1). The control
group did not show any statistically significant (P>0.05)
differences in the above-reported parameters (maximum
moment and strain and tendon–aponeurosis stiffness) before and
after 14·weeks (Table 1). The voluntary activation during the
maximal voluntary plantar flexion efforts were, on average,
97–99% and were similar (no statistically significant changes,
P>0.05) before and after the intervention for both experimental
groups and the control group (Table 1).
The ratios (post- to pre-exercise values) of the maximum
plantar flexion moment of the two exercised legs were
significantly higher than those of the control group, and the
moment ratio of the high-strain-exercised leg was significantly
(P<0.05) higher than that of the low-strain-exercised leg
(Fig.·6). These results indicate a higher increase in the
maximum plantar flexion moment for the leg exercised at 90%
of the MVC. The maximum strain ratios (post- to pre-exercise)
of the control and the high-strain-exercised leg did not show any
statistically significant differences (P>0.05), whereas the strain
ratio for the low-strain-exercised leg was higher than those of
the other two groups (Fig.·6).
After the 14·weeks intervention applying cyclic loading to the
Achilles tendon, the tendon–aponeurosis strain for a given
tendon force (every 100·N) did not show any statistically
significant (P>0.05) changes in the low-strain-exercised leg
(Fig.·7), indicating no alteration in the strain–force relationship
of the tendon and aponeurosis due to the intervention. By
contrast, after the 14·weeks intervention at high strain
magnitude, the strain values for a given tendon force (every
100·N) up to 600·N were significantly (P<0.05) lower than
before (Fig.·7), demonstrating a higher gradient in the
force–strain curve as compared with the pre-exercise curve. As
expected, the control group did not show any differences in the
strain–force relationship before and after the 14-week period
(Fig.·7). Up to 1200·N tendon force, the ratios of the strain
values (post- to pre-exercise) were significantly (P<0.05) lower
for the leg loaded with the high strain magnitude than for the
low-strain-exercised leg and the control group (Fig.·7).
The rest length of the Achilles tendon (from tuberositas
calcanei to soleus muscle) did not alter (P>0.05) after the 14-
week intervention in either the low-strain- or the high-strain-
exercised legs (low strain: 60.4±15.4·mm pre-exercise,
61.3±15.9·mm post-exercise; high strain: 59.8±11.1·mm pre-
exercise, 60.9±11.2·mm post-exercise). The CSA of the
Achilles tendon is greater in its distal portion than it is in its
proximal part (Fig.·8). Following 14·weeks of exercise at low
strain magnitude, the CSA of the Achilles tendon at every 10%
of the tendon length did not show any statistically significant
(P>0.05) differences from the pre-exercise values (Fig.·8).
Although in most cases we did not find any statistically
significant (P>0.05) differences in the CSA before and after the
A. Arampatzis, K. Karamanidis and K. Albracht
Table 1. Comparison of the maximum values of the examined parameters during the maximal voluntary contraction before
(pre-exercise) and after (post-exercise) the intervention
Low strain (N=11) High strain (N=11) Control (N=10)
Parameter Pre-exercise Post-exercise Pre-exercise Post-exercise Pre Post
Moment (Nm) 114.4±12.7 137.7±15.8* 109.5±15.2 144.1±22.7* 135.0±38.3 141.2±39.2
Force (N) 2093±325 2688±350* 2084±447 2992±444* 2702±896 2869±735
Activation (%) 96.7±3.3 98.8±0.9 98.2±1.7 98.9±1.3 98.1±1.2 97.3±1.8
Elongation (mm) 12.4±3.7 14.4±3.4* 13.8±4.3 13.6±2.8 15.1±2.6 16.2±3.4
Strain (%) 4.6±1.5 5.4±1.3* 4.8±1.6 4.8±0.9 5.1±0.9 5.5±1.2
Rest length (mm) 275.0±36.2 272.4±38.9 288.6±20.6 282.8±14.8 294.3±20.8 293.9±24.5
Stiffness (N·mm–1)186.7±38.3 201.4±41.2 167.7±36.8 228.1±39.7* 180.2±42.5184.1±39.7
For the Control group, ‘pre’ corresponds to the values at the start of the experiment and ‘post’ corresponds to the values at the end of the
experiment. Moment is the maximum plantar flexion moment, force is the maximum calculated tendon force, activation is the voluntary
activation, elongation is the maximum elongation of the tendon and aponeurosis, strain is the maximum strain of the tendon and aponeurosis, rest
length is the length of the curved path from tuberositas calcanei to the examined cross-point on the ultrasound images, and stiffness is the
tendon–aponeurosis stiffness of the triceps surae. Low strain is the low-strain-magnitude exercise intervention, high strain is the high-strain-
magnitude exercise intervention, and control is the group without any specific exercise during the 14·weeks of the intervention.
*Statistically significant differences between pre- and post-exercised values (P<0.05).
1.0
1.1
1.2
1.3
1.4
1.5
1.6
Strain
Moment
*
Ratio (post/pre)
Low strain (N=11)
High strain (N=11)
Control (N=10)
*†
*†
Fig.·6. Ratio (post- to pre-exercise values) of the maximum plantar
flexion moment and strain of the triceps surae tendon and aponeurosis
during the maximum voluntary contraction (MVC). *Statistically
significant differences to the control group (P<0.05). †Statistically
significant differences between low- and high-strain-magnitude
exercised legs (P<0.05).
4(%*/52.!,/&%80%2)-%.4!,")/,/'9
2749Cyclic strain and tendon adaptation
intervention along the tendon length of the leg exercised at high
strain magnitude either, the CSA at 60 and 70% of the tendon
length displayed greater values after the intervention than before
(Fig.·8), demonstrating a region-specific hypertrophy of the
Achilles tendon. In the same manner, the ratios of the CSA
(post- to pre-exercise) showed higher values at the 60 and 70%
of the Achilles tendon length for the high-strain- compared with
the low-strain-exercised leg (Fig.·9). The Achilles tendon elastic
modulus showed a statistically significant (P<0.05) increase
after the intervention in the high-strain-exercised leg. However,
the maximal stress values during the MVC increased
significantly (P<0.05) in both legs (Fig.·10).
Discussion
The present study investigated whether the magnitude of the
mechanical load induced as cyclic strain applied to the Achilles
0 500 1000 1500 2000 2500 3000 3500
0 500 1000 1500 2000 2500 3000 3500
0 500
200 400 600 800 1000 1200 1400 1600 1800
1000 1500 2000 2500 3000 3500
0
1
2
3
4
5
6
7Low strain (N=11)
Strain (%)
Pre-exercise
Post-exercise
0
1
2
3
4
5
6
7
*
*
**
*
*
*
*
*
*
*
*
High strain (N=11)
Strain (%)
Pre-exercise
Post-exercise
0
1
2
3
4
5
6
7Control (N=10)
Pre
Post
0.6
0.8
1.0
1.2
1.4
1.6
††††††
Strain ratio (post/pre)
Tendon force (N)
Low strain (N=11)
High strain (N=11)
Control (N=10)
Fig.·7. Strain values and strain ratio (post- to pre-exercise) at every 100·N calculated tendon force of the triceps surae tendon and aponeurosis
during the maximum voluntary contraction (MVC). *Statistically significant differences between pre- and post-exercise values (P<0.05).
†Statistically significant differences between high-strain-magnitude intervention and the other two groups (P<0.05).
Fig.·8. Cross-sectional area (CSA) values of the Achilles tendon before (pre-exercise) and after (post-exercise) the exercise intervention at every
10% of the tendon length. *Statistically significant differences between pre- and post-exercise values (P<0.05).
10 20 30 40 50 60 70 80 90 100 10 20 30 40 50 60 70 80 90 100
30
40
50
60
70
80
ProximalDistal
Low strain (N=11)
Pre-exercise
Post-exercise
CSA (mm²)
Tendon length (%)
30
40
50
60
70
80
ProximalDistal
High strain (N=11)
*
*
Pre-exercise
Post-exercise
4(%*/52.!,/&%80%2)-%.4!,")/,/'9
2750
tendon may have a threshold in order to trigger adaptation
effects on tendon mechanical and morphological properties.
Therefore, we examined the effects of two different exercise
interventions of cyclic mechanical load of similar frequency and
volume but different magnitudes of strain (2.85±0.99% vs
4.55±1.38% strain) on the strain–force relationship and
hypertrophy of the Achilles tendon. After 14·weeks of exercise
intervention, we found a decrease in strain at a given tendon
force, an increase in tendon–aponeurosis stiffness and tendon
elastic modulus and a region-specific hypertrophy of the
Achilles tendon only in the leg exercised at high strain
magnitude. These findings provide evidence for the existence
of a threshold or set-point at the applied strain magnitude at
which the transduction of the mechanical stimulus may
influence the tensional homeostasis of the tendon’s extracellular
matrix and, consequently, the regulation of the anabolic
responses of the tendon cells (Wang, 2006; Wang and
Thampatty, 2006; Lavagnino et al., 2006).
In the literature, it is well accepted that mechanical load
induced as cyclic strain on connective soft tissues such as
tendons is an important regulator of the fibroblast’s metabolic
activity as well as a regulator of the maintenance of the tendon
matrix (Arnoczky et al., 2002; Barkhausen et al., 2003; Screen
et al., 2005; Webb et al., 2006). Furthermore, the modulation of
the mechanical stimuli affects several physiological parameters
of human fibroblasts and coordinates the amount of
proliferation, apoptosis and expression of proteins (Zeichen et
al., 2000; Skutek et al., 2001; Skutek et al., 2003; Barkhausen
et al., 2003). For example, loading of tendon cells causes a
downregulation of catabolic gene expression and an
upregulation of anabolic gene expression (Lavagnino and
Arnoczky, 2005; Lavagnino et al., 2006) whereas
immobilisation promotes catabolic responses (i.e. degeneration
of the extracellular matrix) imposed by an upregulation of
matrix metalloproteinases (Amiel et al., 1982; Hannafin et al.,
1995; Brown et al., 1998; Arnoczky et al., 2004). Although there
is little information in the literature about the effects of
controlled tendon strain magnitudes on the homeostatic
perturbation and the induced adaptational responses of tendons
in vivo, in vitro studies have demonstrated the existence of a
threshold in tendon strain magnitude for triggering fibroblast
proliferation (Yang et al., 2004), stimulation of the gene
expression of inflammatory mediators such as interstitial
collagenase (Lavagnino et al., 2003) or prostaglandin E2(Wang
et al., 2003b) and changes in the elastic modulus and tensile
strength of cultured collagen fascicles after loading (Yamamoto
et al., 2003). Recently, Kubo et al. (Kubo et al., 2006) reported
an increase in human vastus lateralis tendon–aponeurosis
stiffness after high-load isokinetic training of the knee extensor
muscles (80% of the isokinetic MVC) but no changes in
tendon–aponeurosis stiffness after low-load isokinetic knee
extension training (20% of the isokinetic MVC), which is in
agreement with our results.
The homeostatic perturbation in the connective tissues
induced by mechanical loading affects several biochemical
cellular responses (Robbins and Vogel, 1994; Hsieh et al., 2000;
Kim et al., 2002). The concept of homeostatic calibration point
(Lavagnino and Arnoczky, 2005; Lavagnino et al., 2006)
predicts that mechanical loading of the tendon above the
homeostatic calibration point (upper limit) will trigger anabolic
responses whereas a reduction of tendon loading below the
homeostatic level (lower limit) will lead to catabolic cell
responses. The findings of the present study showing
adaptational effects on the Achilles tendon only at the leg
A. Arampatzis, K. Karamanidis and K. Albracht
10 20 30 40 50 60 70 80 90 100
0.8
0.9
1.0
1.1
1.2
1.3
1.4
1.5
ProximalDistal
Low strain (N=11)
High strain (N=11)
CSA ratio (post/pre)
Tendon length (%)
**
Fig.·9. Ratio (post- to pre-exercise values) of the cross sectional area
(CSA) of the Achilles tendon at every 10% of the tendon length.
*Statistically significant differences between low- and high-strain-
magnitude exercised legs (P<0.05).
Fig.·10. Elastic modulus and maximal stress values of the Achilles tendon during the maximum voluntary contraction (MVC) before (pre-exercise)
and after (post-exercise) the exercise intervention. *Statistically significant differences between pre- and post-exercise values (P<0.05).
0.6
0.8
1.0
1.2
1.4
1.6
1.8
Pre-exercise
Post-exercise
High strain
Low strain
E modulus (GPa)
30
40
50
60
70
80
Pre-exercise
Post-exercise
High strain
Low strain
Stressmax (MPa)
*
*
*
4(%*/52.!,/&%80%2)-%.4!,")/,/'9
2751Cyclic strain and tendon adaptation
exercised at a high strain magnitude indicate that the mechanical
load applied to the leg exercised at a low tendon strain
magnitude did not influence the existing internal tensional
homeostasis of the tendon cells regulating the anabolic or
catabolic responses. The results further show that the
mechanical load exerted on the Achilles tendon during the low-
strain-magnitude exercise is no more a sufficient stimulus for
triggering further adaptation effects on the Achilles tendon than
the stimulus provided by the mechanical load applied during
daily activities. Furthermore, our findings indicate that the
4.55% strain applied during the high-strain-magnitude
intervention was above the homeostatic calibration point and
thus was sufficient to elicit a homeostatic perturbation at the
Achilles tendon that triggered anabolic cell responses, causing
the changes observed at the tendon–aponeurosis strain–force
relationship and the region-specific hypertrophy of the tendon.
In the present study, we controlled the strain magnitude, strain
frequency and the exercise volume but not the strain rate during
the interventions. The participants achieved the target moment
as fast as possible and, therefore, the strain rate should not be
very different between the two examined interventions.
However, based on our experimental design it is not possible to
investigate a potential effect of the strain rate on the tendon
adaptational responses that we discovered.
In the present study, we found that 14·weeks exercise at high
strain magnitude had a clear influence on the strain–force
relationship of the tendon–aponeurosis unit and led to an
increase of the CSA of the Achilles tendon at 60 and 70% of its
length. The region-specific hypertrophy of the Achilles tendon
may partly explain the changes in the strain–force relationship
of the tendon–aponeurosis unit but not the increase in tendon
elastic modulus after the intervention. Besides tendon
hypertrophy, there are some other adaptation possibilities that
may affect the tendon stress–strain relationship. The
organisation of the extracellular matrix components includes
mechanisms transmitting tensile forces along the interfibrilar
matrix. Several studies have reported that cells have the ability
to produce a better organised collagen matrix modulated by
cyclic load (Steinmeyer and Knue, 1997; Wang and Grood,
2000; Wang et al., 2003a; Webb et al., 2006) and this way
achieve an increase in tissue stiffness (Brown et al., 1998; Lo
et al., 2000). The methods used in the present study do not
permit examination of such adaptation possibilities at the
Achilles tendon; nevertheless, the clear changes in the
tendon–aponeurosis strain–force relationship, the only region-
specific tendon hypertrophy, the increase of the tendon elastic
modulus, as well as reports of other studies demonstrating an
increase in human tendon stiffness and elastic modulus with no
changes in the tendon’s CSA (Kubo et al., 2002; Reeves et al.,
2003a) provide evidence for the plasticity of the organisation
of the tendon’s extracellular matrix in vivo (i.e. density of
matrix proteins, cell orientation, proteoglycan content and
composition).
The maximum plantar flexion moment increased after the
intervention in both exercised legs (on average 20 and 33% for
the low- and high-strain-magnitude exercised legs, respectively).
This is in agreement with other studies reporting an increase in
muscle strength after low- and high-intensity resistance training
(Kaneko et al., 1983; Takarada et al., 2000; Moore et al., 2004).
The voluntary activation of the plantar flexor muscles during the
MVC were quite high (97–99%) and did not show any
differences before and after both exercise interventions. This
indicates that the increase in muscle strength observed after the
14-week intervention was not due to neuronal factors. In the leg
exercised at high strain magnitude the maximum tendon–
aponeurosis strain during the MVC did not differ before and after
the intervention. These findings, namely an increase in muscle
strength with no changes in maximum tendon–aponeurosis
strain, suggest a coordinated muscle–tendon unit adaptation at
the high-strain-magnitude intervention. Recently, Miller et al.
(Miller et al., 2005) reported similar changes in the time course
of tendon collagen and myofibrillar protein synthesis rates
after non-damaging exercise, supporting a coordinated
musculotendinous adaptation. However, the results of the leg
exercised at low strain magnitude (i.e. increase in muscle
strength with no changes in the tendon–aponeurosis strain–force
relationship) do not show any coordinated muscle–tendon unit
adaptation. This indicates that the threshold of mechanical
loading necessary to trigger adaptational effects is higher for the
tendon than for the muscle.
We found an increase in tendon–aponeurosis stiffness, an
increase in tendon elastic modulus and a region-specific
hypertrophy of the Achilles tendon after the high-strain-
magnitude exercise (i.e. 90% MVC). The reported maximal
plantar flexion moment values calculated by inverse dynamic
during daily activities such as walking are about 120–130·Nm
(Winter, 1984). This means that the resultant maximal ankle
plantar flexion joint moment while walking is similar or even
higher than the applied plantar flexion moment at the high-
strain-magnitude intervention. Therefore, it can be argued that
the mechanical load on the Achilles tendon at the high-strain-
magnitude intervention was not higher compared with normal
walking and, thus, the applied mechanical stimulus does not
explain the adaptational effects. However, it is difficult to
compare the loading on the Achilles tendon induced by walking
with the loading induced during the examined strength training.
The maximal ankle plantar flexion joint moments while walking
do not last for long (instantaneous values). The mean ankle
plantar flexion joint moments while walking are about
50–55·Nm (Karamanidis and Arampatzis, 2007). The duration
of the loading is also different between walking (~600·ms) and
the exercise intervention used in the present study (3·s). Further,
the resultant joint moments during daily activities calculated by
inverse dynamics are not only compensated by muscles. Passive
structures as well as contact forces between bones also absorb
parts of these moments. For example, the maximal ankle plantar
flexion joint moment while walking occurs at a joint position of
15–20° dorsiflexion (Winter, 1984). At this ankle joint angle,
the passive joint moment can achieve values between 20 and
30·Nm (Riener and Edrich, 1999; Mullaney et al., 2006).
Moreover, due to the viscoelastic behaviour of the connective
tissues, in a dorsiflexed position the passive ankle joint moments
may be higher in a dynamic condition (Gajdosik et al., 2005)
such as walking. Studies examining the EMG activity of the
triceps surae muscles while walking reported values between 19
and 42% of the maximal isometric EMG value (Ericson et al.,
1986). Given that the muscle force depends at least on the force
potential due to the force–length–velocity relationship and the
4(%*/52.!,/&%80%2)-%.4!,")/,/'9
2752
activation level (Winters, 1990), submaximal EMG activity
suggests submaximal muscle forces.
In conclusion, our results demonstrate a decrease in
tendon–aponeurosis strain at a given tendon force and a region-
specific hypertrophy of the Achilles tendon after 14·weeks of
high-strain-magnitude exercise (~4.6% tendon–aponeurosis
strain) and no changes in tendon properties after the same period
of low-strain-magnitude exercise (~2.9% tendon–aponeurosis
strain) of similar frequency and volume. The contractile
capacity of the plantar flexor muscles increased in both levels
of exercised legs but the increase was higher at the high-strain-
magnitude than at the low-strain-magnitude exercise. The
results further show that the strain magnitude applied to the
human Achilles tendon should exceed a given threshold
to trigger adaptational effects on the mechanical and
morphological properties of the tendon and that applied strains
with low magnitude (2.5–3.0%) are not a sufficient stimulus to
trigger adaptation effects on the Achilles tendon beyond those
triggered by the mechanical load applied during daily activities.
This research was supported by The Federal Institute of
Sport Science (BISp) Germany.
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