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Abstract
The aim of the present study was to examine whether or not the compliance of the gastrocnemius medialis (GM) tendon and
aponeurosis is influenced by submaximal fatiguing efforts. Fourteen elderly male subjects performed isometric maximal voluntary
plantarflexion contractions (MVC) on a dynamometer before and after two fatiguing protocols. The protocols consisted of: (1)
submaximal concentric isokinetic contractions (70% isokinetic MVC) at 601/s and (2) a sustained isometric contraction (40%
isometric MVC) until failure to hold the defined moment. Ultrasonography was used to determine the elongation and strain of the
GM tendon and aponeurosis. To account for the axis misalignment between ankle and dynamometer, the kinematics of the leg were
captured at 120 Hz. The maximum moment decreased from 85.9717.9 Nm prior fatigue to 79.2719 Nm after isokinetic fatigue and
to 69.9716.4 Nm after isometric fatigue. The maximal strain of the GM tendon and aponeurosis before fatigue, after isokinetic and
after isometric fatigue were 4.971.1%, 4.471.1% and 4.371.1% respectively. Neither the strain nor the elongation showed
significant differences before and after each fatiguing task at any 100 N step of the calculated tendon force. This implies that the
compliance was not altered after either the isokinetic or the isometric fatiguing task. Therefore it was concluded that the strains
during the performed submaximal fatiguing tasks, were too small to provoke any structural changes in tendon and aponeurosis.
r 2005 Elsevier Ltd. All rights reserved.
0021-9290/$ - see front matter r 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jbiomech.2004.12.016
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L. Mademli et al. / Journal of Biomechanics 39 (2006) 426–434 427
unit remains unchanged during a certain phase of the performed. The latter three trials were used for
step cycle whilst the tendon experiences a significant correcting the measured joint moment (see below in
elongation, the muscle fibres would benefit from the moment measurement). Afterwards 10 concentric iso-
force–velocity relationship since they could work at a kinetic plantarflexion contractions at 601/s were per-
lower shortening velocity. However De Zee et al. (2000) formed in a range of motion between 851 and 1201
reported that in vitro the possible alterations of the having the knee fully extended. The first 5 contractions
mechanical properties of the tendon at low level strains were submaximal and increased progressively to achieve
(3%) are too small to influence the functionality of the the maximum moment, the last 5 contractions were
muscle tendon unit, and that tendons are able to act as maximal. During the contractions real time visual
stable force transmitters during long term submaximal feedback of the exerted moment was given and the
cyclic-loading. Similarly Ettema (1997) basing on an in maximum achieved isokinetic moment was determined.
situ study, reported that the increase in tendon stiffness Seventy percent of this maximum moment was set as
during a submaximal cyclic fatiguing protocol was very target for the isokinetic fatiguing protocol. The subjects
low and had no effect on muscle performance. However had to perform concentric isokinetic contractions until
it has not been examined, if the above findings are also failure to match the target moment. Failure was defined
valid for in vivo conditions. as the instant at which the subject could not hold the
The present study aims to examine whether or not the defined moment for more than 5 s. Between 1.5 and
compliance of the gastrocnemius medialis (GM) tendon 2 min after task failure a second isometric MVC at 901
and aponeurosis is altered after two fatiguing protocols: ankle angle was performed. From now on in the text this
(a) submaximal concentric isokinetic contractions and MVC will be referred to as MVC_2. Again two
(b) a sustained submaximal isometric contraction until submaximal dorsiflexions and a passive ankle joint
task failure. The first fatiguing protocol was chosen rotation were performed to correct the measured joint
because it is close to daily activities; the second one moment.
because it is characterised by a long duration of After 15 min recovery the second protocol was
permanent strain. Former in vivo studies have investi- started. It consisted of a sustained submaximal isometric
gated the vastus lateralis tendon using repetitive contraction at the same position as during the MVCs 1
contractions with different modes and suggested that and 2. The level of 40% of the MVC_1 was displayed on
the duration of the contraction is the most important the feedback monitor as target. The subjects had to
factor influencing the changes in compliance (Kubo match the target by exerting the corresponding moment
et al., 2001b). and maintain this isometric contraction until failure.
Again 1.5–2 min after task failure a third MVC was
performed, followed by two submaximal dorsiflexions
2. Methods and a passive ankle joint rotation for the corrections of
the measured joint moment. From now on in the text
2.1. Experimental design this MVC will be referred to as MVC_3. Intensive verbal
encouragement was given to all subjects throughout
Fourteen elderly male subjects, all active in sport, both fatiguing tasks. The whole experimental protocol is
(means7standard deviation: 65.273.6 yr; 175.775.4 cm; described in Fig. 1.
76.278.8 Kg) participated in the study after giving
informed consent to the experimental procedure accom- 2.2. Measurement of the ankle joint moment
plishing with the rules of the local scientific board. The
subjects were seated on a dynamometer (Biodex System The moments were measured using an isokinetic
3 Biodex Medical Systems Inc., USA) with the ankle in dynamometer (Biodex-System3, Biodex Medical Sys-
neutral position (tibia perpendicular to the sole, ankle tems Inc., USA). Before each MVC the axis of rotation
angle 901), the knee fully extended at 1801, and the hip of the dynamometer was carefully aligned with the axis
flexed at 1401. Velcro straps around the foot and the of rotation of the ankle joint. This was defined to be
dynamometer foot plate were used to restrict the ankle parallel to the axis of the dynamometer and passing
movement. through the midpoint of the line connecting both
The warm up period consisted of several isometric malleoli. During the contraction there was a clear shift
submaximal and two or three maximal contractions. of the two axes despite of the fixation (Arampatzis et al.,
Then a maximum voluntary isometric plantarflexion 2004a). To account for this, the resultant moments
contraction (MVC) lasting 4–5 s was performed at 901 around the ankle joint were calculated through inverse
ankle angle. From now on in the text this will be referred dynamics (Arampatzis et al., 2004a; Herzog, 1988).
to as MVC_1. Then two submaximal dorsiflexion Kinematic data were recorded using a Vicon 624 system
contractions and a passive rotation of the ankle joint with 8 cameras operating at 120 Hz. To determine the
at 51/s in a range of motion between 801 and 1351 were point of force application under the foot a flexible
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428 L. Mademli et al. / Journal of Biomechanics 39 (2006) 426–434
Fig. 1. The experimental set up consisted of a warm up period, 3 MVCs and two fatiguing tasks: (a) repetitive submaximal isokinetic concentric
plantarflexion contractions and (b) a sustained submaximal isometric plantaflexion contraction until failure to hold the predefined moments. The
isokinetic maximum was defined by the greatest moment value achieved during 5 maximal isokinetic contractions.
pressure distribution insole (pedar-system, Novel moment arm of the Achilles tendon was calculated using
GmbH, Germany) operating at 50 Hz was used. The the data provided by Maganaris et al. (1998) as function
output TTL-signal from the pedar-system was also of the ankle angle and level of contraction.
registered by the vicon unit to synchronise both systems.
The compensation of moments due to gravitational 2.3. Measurement of the EMG-activity
forces was done for all subjects. They were instructed to
completely relax the muscles of their left leg at the Autoadhesive preamplified Ag/AgCl bipolar EMG
studied position. Then the foot was passively rotated at electrodes (bandwidth 10–500 Hz, pickup surface
51/s. After three cycles the kinematics and the moments 0.8 cm2, inter-electrode distance 2 cm) were used to
were captured during the passive plantarflexion. This record the electric activity of the GM, gastrocnemius
allowed to calculate the moment due to the gravitational lateralis (GL), soleus (SOL) and TA muscles. After
forces for each angular position. preparation, the EMG signals from each muscle were
The antagonistic moment of the tibialis anterior (TA) checked online for artefacts due to mechanical causes by
during MVC was estimated by establishing a relationship passively shaking the leg. Additionally several func-
between EMG amplitude and exerted moment for the tional tests were undertaken to determine whether a
TA, whilst working as agonist (Baratta et al., 1988; good signal was obtained from each muscle. The
Mademli et al., 2004). In order to do that the EMG preparation was renewed when artefacts or a poor
activity of the TA and the corresponding moment were signal were observed. The EMG signals and the
measured at three additional trials (Mademli et al., 2004): measured moments were synchronously registered by
(a) in relaxed situation, (b) producing a dorsiflexion the Vicon system at a sampling rate of 1080 Hz. During
moment displaying an EMG-amplitude of the TA below the MVCs the root mean square (RMS) of the EMG
the maximum amplitude achieved during plantarflexion signal were calculated from the raw signal over a 2 s
and (c) a second dorsiflexion where the EMG-amplitude period at the plateau of the calculated tendon force.
was slightly above the maximum amplitude registered During the fatiguing tasks the EMG-signals, the
during the plantarflexion. The dorsiflexion moments plantarflexors moment and kinematics were recorded
measured for each of the three steps were fitted by a during the first 10 s from every minute.
linear regression curve as function of the corresponding
rectified and smoothed EMG-values of the TA. All 2.4. Measurement of tendinous tissue elongation during
measured data (kinematics, moment, centre of pressure, MVC
and EMG-signal) were interpolated using quintic splines
(Engeln-Müllges and Reutter, 1991) to achieve a A 7.5 MHz linear array ultrasound probe (Aloka SSD
common frequency (1080 Hz). 4000, 43 Hz) was used to visualise the distal tendon and
The tendon force was calculated by dividing the aponeurosis of the GM (Fig. 2). The ultrasound probe
plantarflexors moment by the tendon moment arm. The was placed above the muscle belly at about 50% of its
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L. Mademli et al. / Journal of Biomechanics 39 (2006) 426–434 429
Elongation [mm]
video data (ultrasound sequences) with the data from
the Vicon system, a synchronisation box (Peak Perfor-
mance Technologies) was used. The experiment leader 15
manually triggered an analogue signal (0–5 v) which was
overlaid on the video images and simultaneously 10
captured by the Vicon system.
As mentioned above, during maximum ‘‘isometric’’ 5
plantarflexion efforts it is extremely difficult to com-
pletely prevent any joint rotation; this has a significant
0
influence on the measured elongation of the GM tendon
and aponeurosis (Magnusson et al., 2001; Muramatsu et 0 20 40 60 80 100
al., 2001). To determine the displacement of the tendon Tmax [%]
and aponeurosis due to joint rotation, the motion of the Fig. 3. Mean curves (n ¼ 14) of the measured elongation (DL
GM tendon and aponeurosis was recorded during a measured), the corrected elongation considering the joint rotation
passive motion (same as for the correction for gravita- (DL corrected), and the passive elongation due to joint rotation (DL
tional forces). This allowed the correction of the passive) of the GM tendon and aponeurosis during maximal voluntary
isometric contraction. Tmax: time to achieve maximal tendon force.
elongation measured during MVC due to joint rotation
(Fig. 3). For the analysis of the video tapes every single
frame was digitised using a video analysis software (Simi
Motion 5.0). to compare the elongation and the strain between the
The elongation and strain of the GM tendon and MVC before and after the fatiguing tasks at the same
aponeurosis during the MVC_1, MVC_2 and MVC_3 given tendon force.
were identified and analysed at the maximum calculated
tendon force and at every 100 N. This procedure allowed 2.5. Statistics
3. Results
Fig. 4. Raw EMG signal from the GM, GL, SOL, TA, and the corresponding moment during the concentric submaximal isokinetic fatiguing task
from one subject. The first column shows data captured during the first minute of the fatiguing task, the second column during the middle interval of
the total duration and the third column during the last minute.
Fig. 5. Raw EMG signal from GM, GL, SOL, TA, and the corresponding moment during the submaximal isometric fatiguing task from one subject.
The first column shows data captured during the first minute of the fatiguing task, the second column during the middle interval of the total duration
and the third column during the last minute.
Table 1
Comparison of the maximum values of the examined parameters during the pre-fatigue MVC (MVC_1) with those during the MVCs after isokinetic
(MVC_2) and isometric fatigue (MVC_3) (means7 SD, n ¼ 14)
Moment: maximal exerted moment from the plantarflexor muscles during MVC; tendon Force: maximal calculated tendon force during MVC;
elongation: maximal elongation of the tendon and aponeurosis of the GM during MVC; strain: maximal strain of the tendon and aponeurosis of the
gastrocnemius medialis during MVC.
a
Significantly different to MVC_1 (Po0:05).
b
Significantly different to MVC_2 (Po0:05).
were compared with themselves before and after reduction of the force generating capacity of the muscle
each fatiguing task. Thus this error would be systematic due to fatigue. After the isokinetic fatiguing task these
and therefore should not influence the presented values were about 93% of the maximum value measured
findings. during the MVC_1 (Table 1). After the isometric
The decrease in maximum moment and calculated fatiguing task the maximum calculated tendon force
tendon force after the fatiguing tasks confirmed the and moment were significantly lower (Po0:05) and
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432 L. Mademli et al. / Journal of Biomechanics 39 (2006) 426–434
Table 2
Means7standard deviations of the elongation of the GM tendon and aponeurosis at every 100 N of the calculated tendon force during the MVCs
before fatigue (MVC_1), after isokinetic fatigue (MVC_2), and after isometric fatigue (MVC_3)
Tendon force [N] MVC_1 Elongation [mm] MVC_2 Elongation [mm] MVC_3 Elongation [mm]
The table ends at 900 N, which corresponds to the maximum common force achieved by all subjects during the MVCs (n ¼ 14).
EMGRMS [ADU]
every 100 N calculated tendon force without considering
the joint rotation we find significant differences in 200
elongation between MVC_1 and MVC_2 above 300 N.
The present study shows that tendon compliance was 150
not altered after the two presented fatiguing protocols.
100
It seems that tendons are capable to resist submaximal
contractions without any alteration in their mechanical 50
properties, which would have an impact on their
muscle’s function. This is in agreement with earlier MVC_1 MVC_2 MVC_3
reports from in vitro (De Zee et al., 2000) and in situ
studies (Ettema, 1997). However Ettema (1997) found Fig. 7. Means and SEM of the RMS of the EMG signal from the GM,
that the compliance of the rat GM tendon shows a small GL and SOL during the MVC before fatigue MVC_1, after isokinetic
fatigue (MVC_2), and after isometric fatigue (MVC_3) (n ¼ 14).
but statistically significant decrease after submaximal
repetitive contractions when using electro stimulation.
The differences in tendon elongation prior and after
fatigue in the study of Ettema (1997) were about 7-8% went any changes, we compared the RMS values of the
and were too small to influence muscle function EMG-activity from the different muscles during the
(Ettema, 1997). The discrepancy with the results of the three MVCs. We found similar relative EMG-activities
present study might be due to the different accuracies of in GM, GL and SOL (Fig. 7). This suggests that the
both applied methods. Such small changes in elongation relative contribution of each muscle was not substan-
can hardly be detected in vivo by means of ultrasound tially altered and therefore this issue should have no
imaging. At our study 8% change in elongation would influence on the presented results.
correspond to about 0.8 mm at 900 N calculated tendon In conclusion no differences in strain and elongation
force. This is within the accuracy of the ultrasonography of the GM tendon and aponeurosis were found at any
(0.7 0.4 mm resolution of the ultrasound images). given calculated tendon force. This implies that the
However some factors influencing the finding of the compliance was not altered after the isokinetic and
present study may be: (a) changes in the initial length of isometric fatiguing task. It can therefore be suggested
the tendon and aponeurosis and (b) different relative that the strains during the performed submaximal
contributions of the GM, GL and SOL to the tendon fatiguing tasks, are too small to provoke any structural
force during the three MVCs. Regarding the first changes in the GM tendon and aponeurosis, which are
possible factor, it is well known from the literature that presumably subjected to high loads during daily
changes in the initial length of the tendon influence its activities.
compliance (Rigby, 1964; Schwerdt et al., 1980). It can
be hypothesised that after the performed fatiguing tasks
creep could alter the initial length of the GM tendon and References
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