Mechanical and morphological properties of different muscletendon units in the lower extremity and running mechanics: effect of aging and physical activity
Institute for Biomechanics and Orthopaedics, German Sport University of Cologne, Carl-Diem-Weg 6, 50933, Cologne, Germany
* Author for correspondence (e-mail: Arampatzis{at}dshs-koeln.de)
Accepted 10 August 2005
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Summary |
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The investigation was conducted on 30 old and 19 young adult males divided into two subgroups according to their running activity: endurance-runners vs non-active. To analyse the properties of the MTUs, all subjects performed isometric maximal voluntary (MVC) ankle plantarflexion and knee extension contractions at 11 different MTU lengths on a dynamometer. The activation of the TS and QF during MVC was estimated by surface electromyography. The gastrocnemius medialis and the vastus lateralis and their distal aponeuroses were visualized by ultrasonography at rest and during MVC, respectively. Ground reaction forces and kinematic data were recorded during running trials at 2.7 m s1.
The TS and QF MTU capacities were reduced with aging (lower muscle strength and lower tendon stiffness). Runners and non-active subjects had similar MTU properties, suggesting that chronic endurance-running exercise does not counteract the age-related degeneration of the MTUs. Runners showed a higher mechanical advantage for the QF MTU while running (lower gear ratio) compared to non-active subjects, indicating a task-specific adaptation even at old age. Older adults reacted to the reduced capacities of their MTUs by increasing running safety (higher duty factor, lower flight time) and benefitting from a mechanical advantage for the TS MTU, lower rate of force generation and force generation per meter distance. We suggest that the improvement in running mechanics in the older adults happens due to a perceptual motor recalibration and a feed-forward adaptation of the motor task aimed at decreasing the disparity between the reduced capacity of the MTUs and the running effort.
Key words: age effect, endurance running, skeletal muscle, tendon properties, gear ratio, rate of force generation, human
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Introduction |
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Past studies provided evidence that the aging process is associated with a
loss in muscle strength (Criswell et al.,
1997; Frontera et al.,
2000
; D'Antona et al.,
2003
; Trappe et al.,
2003
), changes in the mechanical properties of collagenous tissues
(Noyes and Grood, 1976
;
Vogel, 1980
;
Blevins et al., 1994
;
Komatsu et al., 2004
;
Reeves et al., 2004
) and
alterations in muscle architecture (Narici
et al., 2003
; Kubo et al.,
2003a
,b
).
Further, it has been shown that the performance capability of the neural
system also degenerates with aging (for a review, see
Prince et al., 1997
). It is
reasonable to assume that the age-related degeneration of the capacities of
the biological system will reduce the functional motor performance capacity
during daily activities. A clear example is the increased occurrence of falls
during daily activities in the older subjects (for a review, see
Schultz, 1992
). However,
humans are able to adapt and to modify their motor task organisation using
sensory feedback information (Kagerer et
al., 1997
; McNay and
Willingham, 1998
; Pai et al.,
2003
). This is especially true for repetitive motor tasks, where
the central nervous system may use sensory feedback information to update
internal models, adjusting the dynamic behaviour of the motor system to
achieve a new equilibrium between sensory inputs and motor outputs
(Wolpert et al., 1995
;
Shadmehr, 2004
). As the new
condition is adapted the human system knows how to behave and so the central
nervous system can select and execute an appropriate action in a feed-forward
control. Adaptive refinement of motor tasks (motor task reorganization) by
humans may be the mediator between changes in the musculoskeletal system
(internal changes) and those in the environment (external changes;
Mulder et al., 2002
). This
suggests that changes in the capacities of the musculoskeletal system would
lead to motor task adaptations in repetitive tasks like walking and running by
continuously updating the internal model, using feedback control. Thus, it is
reasonable to hypothesize that older subjects will change their running
strategy reflecting the reduction in the capacities of their MTUs (internal
changes). This hypothesis is supported by the fact that older subjects do not
show deficits in the adaptation level of non-strategic tasks
(McNay and Willingham, 1998
;
Fernández-Ruiz et al.,
2000
; Buch et al.,
2003
).
Several studies have documented that exercise with high-magnitude
mechanical loads counteracts the age-related degeneration of the capacities of
the MTUs (Aagaard et al., 2001;
Reeves et al., 2003
,
2004
). For instance, strength
training increases tendon stiffness and muscle strength in older humans
(Reeves et al., 2003
,
2004
). However, several in
vitro (Viidik, 1969
;
Kiiskinen, 1977
;
Woo et al., 1981
;
Birch et al., 1999
) and in
vivo (Rosager et al.,
2002
; Hansen et al.,
2003
) studies have documented that exercise with high total
loading volume but relative low loads (e.g. endurance running) does not
provide a sufficient stimulus to provoke further adaptational effects on the
mechanical properties of high-load-bearing MTUs. Most studies analysing the
effect of running exercise on the properties of the MTUs were done with young
adult subjects. The influence of chronic running exercise on the age-related
degeneration of the mechanical and morphological properties of the MTUs has
not been clearly identified. For instance, endurance-running exercise in
rooster (Curwin et al., 1988
)
increases the Achilles tendon collagen deposition and decreases the amount of
collagen pyridinoline cross-links, suggesting a greater matrixcollagen
turnover, resulting in a reduced maturation of tendon collagen. Therefore, it
can be hypothesized that endurance-running exercise is a sufficient stimulus
to counteract the age-related changes in the capacities of the MTUs at the
lower extremity.
Further, empirical results show that experience or repeated practice causes
a task-specific adaptation (Erni and
Dietz, 2001; Pavol et al.,
2002
; Pai et al.,
2003
). Most of those studies indicated an improvement in
locomotion mechanics. Repeated practise during stepping over an obstacle
decreased leg joint trajectory and foot clearance
(Erni and Dietz, 2001
).
Moreover, this so-called `use-dependent' motor learning
(Erni and Dietz, 2001
) has
been described for locomotor movements in young and older subjects
(Pavol et al., 2002
;
Pai et al., 2003
). A clear
example is that age does not influence the outcome of a slipping perturbation
during repeated exposure (Pavol et al.,
2002
). Chronic exposure to repetitive loading while running
increases the risk of injury at the knee joint (e.g. patellofemoral pain
syndrome), which is speculated to be caused by the anatomical joint alignment
and the internal rotation of the tibia during the stance phase
(Messier et al., 1991
;
Nigg et al., 1993
). In
general, a certain magnitude of mechanical load and stress is tolerated and
even needed for the mechanical adaptation of the musculoskeletal system (for a
review, see: Kjaer, 2004
;
Wang, 2005
). However, when the
magnitude of the mechanical load or stress exceeds a certain threshold level
the biological system will change its control strategy
(DeVita et al., 1992
;
DeVita, 1994
;
DeVita and Hortobagyi, 2000
;
Hortobagyi et al., 2003
). In
other words, the neuromuscular system is flexible and enables humans to change
their locomotion strategy, obviously depending on the capacities of the
musculoskeletal system and on the functional demand of the task. From a
mechanical point of view we hypothesise that running experience will improve
running characteristics (kinematics and kinetics). Furthermore, we speculate
that running-task-specific adaptations will not be degraded with age.
Therefore, the main purposes of this work were (i) to investigate whether chronic endurance running is a sufficient stimulus to counteract the age-related changes in the mechanical and morphological properties of human triceps surae (TS) and quadriceps femoris (QF) muscle-tendon units (MTUs) by comparing runners and non-active subjects at different ages (young and old), (ii) to identify adaptational phenomena in running mechanics due to age-related changes in the mechanical and morphological properties of the TS and QF MTUs, and finally (iii) to examine whether chronic endurance-running exercise is associated with adaptational effects on running characteristics in old and young adults.
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Materials and methods |
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Measurement of maximal isometric ankle and knee joint moment
The subjects performed isometric maximal voluntary ankle plantarflexion and
knee extension contractions of their left leg on two separate test days. The
warm-up consisted of 23 min performing submaximal isometric
contractions and three maximal voluntary contractions (MVCs). Afterwards the
subjects performed isometric maximal voluntary ankle plantarflexion or knee
extension contractions at eleven different ankleknee and kneehip
joint angle configurations, respectively
(Table 2) on a Biodex
dynamometer (Biodex Medical Systems. Inc., Shirley, NY, USA). Different joint
angle configurations were chosen in order to examine TS and QF muscle force
potential over the whole range of achievable MTU lengths. The different joint
angle configurations were applied in random order. 3 min rest between
contractions were allowed. The subjects were instructed and encouraged to
produce a maximal isometric moment and to hold it for about 23 s.
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The resultant moments at the ankle and knee joints were calculated through
inverse dynamics (Arampatzis et al.,
2004,
2005a
). Kinematic data were
recorded using the Vicon 624 system (Vicon Motion Systems, Oxford, UK) with
eight cameras operating at 120 Hz. To calculate the lever arm of the ankle
joint during ankle plantarflexion the centre of pressure under the foot was
determined by means of a flexible pressure distribution insole from
Pedar-System (Novel GmbH, Munich, Germany) operating at 99 Hz
(Arampatzis et al., 2005a
). The
compensation of moments due to gravitational forces was done for all subjects
before each ankle plantarflexion or knee extension contraction. The exact
method for calculating the resultant joint moments has been previously
described (Arampatzis et al.,
2004
,
2005a
).
The moments arising from antagonistic coactivation during the ankle
plantarflexion and knee extension efforts were quantified by assuming a linear
relationship between surface electromyography (EMG) amplitude of the ankle
dorsiflexor or knee flexor muscles and moment
(Baratta et al., 1988). This
was established by measuring EMG and moment during one relaxed condition and
two submaximal ankle dorsiflexion or knee flexion contractions at each joint
angle configuration (Mademli et al.,
2004
). Therefore, in the text below, maximal knee and ankle joint
moments refer to the maximal joint moment values considering the effect of
gravitational forces, the effect of the joint axis alignment relative to the
dynamometer axis and the effect of the antagonistic moment on the moment
measured at the dynamometer.
Measurement of EMG activity during isometric contractions
Bipolar EMG lead-offs with pre-amplification (analogue RC-filter 10-500 Hz
bandwidth; Biovision, Wehrheim, Germany) and adhesive surface electrodes (blue
sensorMedicotest, Ballerup, Denmark) were used to analyse muscle
activity. Before placing the electrodes the skin was carefully prepared
(shaved and cleaned with ethanol) to reduce skin impedance. The electrodes
were positioned above the midpoint of the muscle belly as assessed by
palpation, parallel to the presumed direction of the muscle fibres. The
inter-electrode distance was 2 cm. The activation of the TS muscle was
assessed from the EMGs of the gastrocnemius medialis (GM), gastrocnemius
lateralis (GL) and soleus (SO). During knee extension the EMG-activities of
the vastus lateralis (VL), vastus medialis (VM) and rectus femoris (RF) were
analysed. The EMG signals were recorded at 1080 Hz using the Vicon system.
Before starting the experiment, tests including submaximal and maximal
isometric contractions for each muscle group were undertaken to determine
whether an adequate signal was obtained from each muscle and to adjust the
amplifier gains. Further, the EMG signal for each muscle was checked online
for artifacts due to mechanical causes by passively shaking the leg. The
preparation was renewed when such artifacts were observed. All isometric
contractions at the knee or the ankle joint were performed within one testing
session. No electrode replacement or re-adjusting of the EMG pre-amplification
gain were done during the measurements.
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Measurement of tendon properties
Tendon properties were determined on two additional test days. The subjects
performed MVC ankle plantarflexion (ankle joint angle 90°, knee joint
angle 180°) and knee extension (knee joint angle 115°, hip joint angle
140°) with their left leg on a dynamometer. 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 GM or VL, respectively
(Fig. 1). The exact protocol
for the analysis of the tendinous tissue elongation during ankle
plantarflexion and knee extension is described in detail elsewhere
(Arampatzis et al., 2005b;
Stafilidis et al., 2005
).
Briefly, the effect of inevitable joint angular rotation on the elongation
of the tendon and aponeurosis during the loading phase was taken into account
by capturing the motion of the tendons and aponeuroses from the GM and VL
during a passive motion of the ankle or the knee joint
(Muramatsu et al., 2001;
Magnusson et al., 2001
;
Bojsen-Møller et al.,
2003
). This allowed the correction of the elongation obtained for
the tendon and aponeurosis due to joint rotation for each maximal ankle
plantarflexion or knee extension trial. The ultrasound images taken during the
passive joint motion and during the MVCs were digitised frame by frame until
the maximal calculated tendon force was achieved. The tendon force was
calculated by dividing the ankle or knee joint moment by the corresponding
tendon moment arm. The tendon moment arms of the Achilles tendon and the
patellar tendon were calculated using the data provided by Maganaris et al.
(1998
) and Herzog and Read
(1993
), respectively. The
insertion of the fascicle into the deep aponeurosis
(Fig. 1) was tracked during
contraction and during a passive trial to determine the elongation of the
tendon and aponeurosis. The resting length of the GM (knee joint angle
180°, ankle joint angle 110°) and the resting length of the VL (knee
joint angle 130°, hip joint angle 140°) tendon and aponeurosis were
identified on the ultrasound images
(Arampatzis et al., 2005b
;
Stafilidis et al., 2005
). The
specific joint angle configurations were chosen in order to reduce passive
joint moments almost to zero (Riener and
Edrich, 1999
).
The normalised stiffness of the TS and QF tendon and aponeurosis were calculated by the relationship between the tendon force and the strain of the tendon and aponeurosis between 50% and 100% of the maximal tendon force, using a linear regression. The linearity between tendon force and strain was checked using the coefficient of determination (r2). This proved to be reasonably high (r2=0.980.99).
Measurement of muscle architecture
The muscle architecture of the GM and VL (fascicle length, pennation angle
and thickness) were determined by ultrasonography during the same test session
as for the analysis of the tendon properties and using the same joint angle
configurations (GM: ankle joint angle 90°, knee joint angle 180°; VL:
knee joint angle 115°, hip joint angle 140°). All measurements were
done on the relaxed muscles at the cited positions. The pennation angles of
the GM and VL were measured as the angle of insertion of the muscle fascicles
into the deep aponeurosis. Fascicle length was defined as the length of the
fascicular path between the insertions of the fascicle into the superficial
and deeper aponeuroses. The ratios between fascicle length of the GM and tibia
length, and between fascicle length of the VL and femur length, were also
analysed. Femur length was defined as the distance between the lateral femoral
condyle and the major trochanter, and tibia length as the distance between the
lateral malleolus and lateral femoral condyle. Muscle thickness was defined as
the distance between the deeper and superficial aponeurosis
(Fig. 1).
Measurement of running characteristics
On one additional test day, the ground reaction force (GRF) (1080 Hz) and
the kinematic data (Vicon 624 system, 12 cameras operating at 120 Hz) were
recorded as the subjects ran barefoot at 2.7 m s1 on a 16 m
track with two force platforms (60 cm x 90 cm, Kistler, Winterthur,
Switzerland) mounted beneath midway of the track. Barefoot running was chosen
to exclude any effects of running shoes on the running characteristics. The
distance covered by each subject in one trial was about 13 m. The running
velocity was chosen to be a normal training and/or marathon competition
velocity for the older runners. This running velocity if maintained would
result in a time of about 4:20 h to run the marathon, and is the mean marathon
time reported for the older runners examined. Running velocity was controlled
because running mechanics depend on running velocity
(Arampatzis et al., 1999).
All subjects were instructed to run along the track at the designed speed
(2.7 m s1). Subjects could perform as many practice trials
as they wanted (typically 23). The running velocity was indicated by a
customized electrical adjustable pacemaker stick hanging from the ceiling and
running along the whole track in front of the subjects. A trial was successful
when the subjects followed the stick at the same distance (50 cm) over
the whole track and both right and left touch-downs were centred on the
corresponding force platforms. Three valid trials were recorded and analysed
for each subject. The athletes had a 12 min rest between trials. Thirty
eight reflective markers (radius 14 mm) were used to track the whole body
kinematics. The markers defined the left and right foot, left and right lower
legs, left and right thigh, pelvis, thorax, left and right upper arm, left and
right forearm, left and right hand and the head. The three-dimensional
coordinates were smoothed using a Woltring filter routine
(Woltring, 1986
) with a
minimum mean squared error value of 15. The segmental masses and moments of
inertia were calculated basing on the data reported by Dempster et al.
(1959).
A whole stride cycle, from foot strike to ipsilateral foot strike, was
analysed. One step was defined to be from foot strike to contralateral foot
strike. Step length was defined as the anterior displacement of the foot
(midpoint of the distance between calcaneus and metatarsal markers) from foot
strike to contralateral foot strike. For both legs, the instants of touch-down
and take-off were determined from the vertical force data. The threshold for
determining touch-down and take-off was set at 20 N. Temporal characteristics,
sagittal angular joint angle kinematics and kinetics and GRFs were analysed
for both legs. A straight leg was defined as 180° knee joint angle. The
tibia being perpendicular to the ground while having the foot flat on it was
defined as 90° ankle joint. The limb angle was defined as the angle
between the line connecting the centre of mass (COM) and the midpoint of the
foot identified by the calcaneus and metatarsal markers and the vertical in
the sagittal plane. A posterior or anterior position of the COM relative to
the midpoint of the foot in the running direction was defined as a negative or
positive limb angle, respectively. The gear ratios of the TS and the QF MTUs
were calculated as the ratios (R/r) of the moment arm
(R) of the GRF acting about the joint to the agonist tendon moment
arm (r) according to Carrier et al.
(1994). The moment arms
(r) of the Achilles tendon and the patellar tendon were calculated
using the data provided by Maganaris et al.
(1998
) and Herzog and Read
(1993
), respectively. The gear
ratio and the moment arm (R) of the GRF acting about the joint were
determined for the left and right ankle and knee joints for five phases during
ground contact (Phase 1: 1026%; Phase 2: 2642%; Phase 3:
4258%; Phase 4: 5874%; Phase 5: 7490% of ground contact).
The gear ratio and the moment arm were not determined for the first and last
10% of ground contact because of the low GRF and the consequently unreliable
calculation of the moment arm (R) of the GRF.
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The anterior COM displacement during ground contact and flight phase was
calculated as the mean values of the anterior COM displacement during the
corresponding phases for the left and right leg. Vertical COM displacement was
defined as the difference between the maximum and minimum value of the
vertical COM trajectory during the stride cycle. The vertical COM displacement
during running was calculated using the kinematic data of the subjects. The
joint moments and the corresponding mechanical powers (left and right leg)
were calculated through inverse dynamics from the mean values of the left and
right leg. For all subjects and parameters the mean values from three trials
and both legs were utilised for further analysis. The symmetry and
reproducibility of temporal, kinematic and GRF parameters during submaximal
running velocity were analysed in previously studies and were reasonably high
(Karamanidis et al., 2003,
2004
).
Statistics
We used a two-factor (age-by-running activity) analysis of variance (ANOVA)
to detect group differences in (1) isometric maximal voluntary ankle
plantarflexion and knee extension moments at different MTU lengths, (2) EMG
activity (normalised RMS) of the TS and QF muscle at different MTU lengths,
(3) normalised stiffness of the TS and QF tendon and aponeurosis, (4) GM and
VL muscle architecture and (5) running mechanics. All significant
age-by-running activity interactions are reported. When a significant
age-by-running activity interaction was present a Bonferroni post hoc
test was conducted in order to determine where these differences occurred. The
F ratios were considered significant at P<0.05. The
Levene Test was used to test the homogeneity of variance across groups
(P<0.05). If variances were not equal across samples the
F ratios were considered significant at P<0.01. All
results in the tables and figures are presented as means ±
S.D. (standard deviation).
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Results |
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Joint moments during maximal isometric contractions
Older adults showed significantly (P<0.05, P<0.01
and P<0.001) lower maximal isometric ankle plantarflexion moments
compared to the young adults at all joint angle configurations
(Fig. 2). Conversely, the
comparison between runners and non-active subjects revealed significant
differences (P<0.05) on maximal isometric ankle plantarflexion
moment only for position 80/130° (ankle/knee joint angle), the maximal
moment being higher (P=0.020) for runners compared to non-active
subjects (Fig. 2).
Age-by-running activity interaction (P<0.05) was detected for
maximal ankle plantarflexion moment at position 100/110° (ankle/knee joint
angle). The post hoc analysis revealed a significantly
(P<0.05) higher ankle plantarflexion moment for the young runners
compared to all other groups (young and old non-active subjects and old
runners). As shown in Fig. 3,
significant differences (P=0.040 to P<0.001) between age
groups were present for the maximal isometric knee extension moment at
positions 140/115°, 140/140°, 110/100° and 110/150° (knee/hip
joint angle). The young adults were significantly stronger than the old
adults. By contrast, there were no significant differences
(P>0.05) between runners and non-active subjects on the maximal
isometric knee extension moment for any joint angle configuration
(Fig. 3).
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Tendon stiffness and muscle architecture
The normalised stiffness of the QF was significantly reduced
(P=0.001) in the old adults compared to the young adults
(Fig. 4). In contrast, no
significant differences (P>0.05) was found on the normalised
stiffness of the TS tendon and aponeurosis between age groups. No significant
differences (P>0.05) between runners and non-active subjects in
normalised stiffness of the TS or the QF was detected
(Fig. 4). As shown in
Table 3, there was almost no
group differences on GM or VL muscle architecture. Only the pennation angle of
the GM was significantly higher (P=0.016) for the runners compared to
the non-active subjects.
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Running characteristics
Fig. 5 displays the sagittal
plane angular motion at the ankle and knee joints as well as the limb angle
for the left leg during running (2.7 m s1) for the examined
groups. Fig. 6 shows the ankle
and knee joint moments and mechanical powers, and the vertical and
anteroposterior horizontal GRFs of the left leg during running. Again, all
statistical results regarding the running characteristics are related to the
mean values from three trials and both legs for each subject. When running at
the same speed as young adults, older adults displayed a significantly higher
stride frequency (P=0.002), lower step length (P=0.021),
lower flight time (P=0.001), lower anterior COM displacement during
flight phase (P=0.040), lower vertical COM displacement during the
stride cycle (P=0.007), lower angular displacement at the ankle joint
in plantarflexion direction during ground contact (P=0.008), higher
limb angle at take off (P<0.001) and a higher angular displacement
of the limb angle during ground contact (P=0.001) compared to the
young adults (Tables 4,
5 and
6). Furthermore, the duty
factor (P=0.003) and ratio displacement of the COM (P=0.007)
were significantly higher for the old adults compared to the young adults
(Tables 4 and
5). Runners exhibited a
significantly lower step length (P=0.032), lower anterior COM
displacement during ground contact (P=0.039), lower angular
displacement at the ankle joint in plantarflexion direction during ground
contact (P=0.006), lower limb angle at take-off (P=0.001)
and a lower angular displacement of the limb angle during ground contact
(P=0.040) compared to the non-active group (Tables
4,
5 and
6). There was a significant
(P=0.024) age-by-running activity interaction at the angular
displacement of the knee joint in knee extension during ground contact
(Table 6). The post
hoc analysis revealed significantly (P=0.049) higher values for
the young runners compared to the old runners.
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For the GRF parameters the average (P=0.002) and the maximal values (P=0.016) of the vertical force as well as the vertical (P=0.002) and horizontal (deceleration phase: P=0.009; acceleration phase: P=0.028) impulses during ground contact were significantly lower for the old adults compared to the young adults (Table 7). The comparison between runners and non-active subjects revealed significant differences in the horizontal impulse (deceleration phase: P=0.043; acceleration phase: P=0.010), leading to lower values for the endurance runners compared to the non-active group (Table 7). Significant differences (P<0.05) between age groups on joint kinetics were identified at the ankle joint, with virtually no differences (P>0.05) at the knee joint (Table 8). The old adults showed a significantly lower maximal ankle plantarflexion moment (P=0.017) and mechanical power (P=0.005) during ground contact compared to young adults (Table 8). No significant differences (P>0.05) in ankle and knee joint kinetics between endurance runners and non-active subjects were found. There was a significant age-by-running activity interaction (P=0.010) for the maximal mechanical power at the knee joint (Table 8). The post hoc analysis revealed a significantly (P<0.05) higher maximal mechanical power at the knee joint for the old non-active subjects compared to the old runners and young non-active subjects (Table 8).
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Regarding the gear ratio (R/r), older adults showed significantly lower (P<0.05) values at the ankle joint from 26% to 58% of the ground contact duration (for phase 2: P=0.040 and for phase 3: P=0.009) compared to the young adults. This was due to a lower moment arm of the GRF acting about the ankle joint (Fig. 7; for phase 2: P=0.048 and for phase 3: P=0.009). Conversely, no significant differences between individuals who run regularly and those who do not run in the gear ratio or the moment arm of the GRF at the ankle joint were noted (P>0.05). Concerning the knee joint no significant differences (P>0.05) between older and young adults in the gear ratio or moment arm of the GRF were detected (Fig. 8). Runners demonstrated a significantly lower gear ratio at the knee joint from 10 to 42% of the ground contact duration (for phase 1: P=0.030 and for phase 2: P=0.026) compared to the non-active group. This was due to a lower moment arm of the GRF acting about the knee joint (Fig. 8; for phase 1: P=0.032 and for phase 2: P=0.027).
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Discussion |
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The present study shows that age (>60 years) is accompanied by a reduced
maximal voluntary isometric ankle and knee joint moment. This is in agreement
with previous findings (Klitgaard et al.,
1990; Frontera et al.,
1991
; Kubo et al.,
2003c
; Savelberg and Meijer,
2004
). For the plantarflexion moment at the ankle joint, this
age-related reduction was present at all analysed joint angle configurations,
which indicates a similar relative contribution of the components of the TS to
the total moment developed by this muscle group between age groups.
Conversely, for the knee extensor muscles the age-related reduction in maximal
moment was present at only some of the studied joint angle configurations.
While aging revealed a clear reduction in maximal knee extension moment at
intermediate knee joint angles (140° and 110°), there was virtually no
age affect at more extended (160° and 170°) or flexed (80°) knee
joint positions.
Three potential explanations, all of which are probably contributing to
these observations, are suggested. (1) It has been reported that the
momentknee-joint angle relationship of the Vastii describe a parabolic
curve having its vertex (maximum value) between 100° and 120°. In
contrast, the RF has a rather flat joint momentlength curve
(Savelberg and Meijer, 2004).
This observation would result in a higher relative contribution of the RF to
the total knee extension moment at more extended or flexed knee joint
positions (Savelberg and Meijer,
2004
), where no age effects on QF muscle strength were noted.
Recently, it has been reported that the age-related degeneration of the muscle
strength at the Vastii is higher than that at the RF
(Savelberg and Meijer, 2004
).
Accordingly, our data might indicate that the age-related reduction in muscle
force capacity is distinct within the QF, with a greater decline in
monoarticular (Vastii) than biarticular (RF) muscles. (2) At rest (knee/hip
joint angle 115°/140°), the fascicle lengths of the VL were similar
for both age groups. This suggests that the working ranges (widths) of the
forcelength relationship of the Vastii are similar for old and young
adults. Consequently, the observed age-related differences in muscle strength
of the Vastii would be reduced at short fascicle lengths (extended knee joint)
because of the parabolic curve of the forcelength relationship of the
Vastii (Herzog et al., 1991
).
(3) Finally, the age-related patterns observed for the knee extension moment
at different joint angle configurations might be caused by a modulation of the
EMG-activity. Older adults showed an increased QF muscle EMG-activity at more
extended (160° and 170°) as well as at more flexed (80°) knee
joint angles in comparison to younger adults. This was not observed at
intermediate knee joint angles (110° and 140°).
Besides the loss of TS and QF muscle strength we could confirm that aging
decreased the stiffness of the QF tendon and aponeurosis. Mechanical changes
in collagenous tissues in response to aging have been reported in
vivo (Reeves et al.,
2003; Kubo et al.,
2003c
) and in vitro
(Noyes and Grood, 1976
;
Vogel, 1980
;
Blevins et al., 1994
;
Komatsu et al., 2004
). The
fact that only the TS muscle strength and not the stiffness of the tendon and
aponeurosis is affected by aging might indicate that the time courses of
tendinous and muscular properties are different
(Karpakka et al., 1990
;
Kubo et al., 2004
). Analysing
subjects up to the sixth decade revealed no clear age-related changes in the
architecture of the GM and VL. However, although not significant, the older
adults of the present study showed a tendency towards a reduced pennation
angle (P=0.08) at the GM and reduced muscle thickness at VL and
GM.
Individuals who run regularly and those who do not run displayed no clearly
identifiable differences in the mechanical and morphological properties of the
TS or the QF MTUs, indicating that chronic endurance-running exercise does not
counteract the age-related degeneration of the MTUs. We suggest that the extra
stress and strain imposed on the MTUs during endurance running is not a
sufficient stimulus to provoke further clear adaptational effects on the
capacities of high-load-bearing MTUs. Analysing the effect of
endurance-running exercise on the mechanical properties of high-load-bearing
MTUs in young adult species led to similar findings
(Woo et al., 1981;
Birch et al., 1999
;
Rosager et al., 2002
;
Hansen et al., 2003
). Only the
pennation angle of the GM showed higher values in the endurance-runners group
compared to the non-active individuals. However, the absolute differences in
pennation angle between groups were less than 1.6°, which is probably too
low to have any relevant influence on muscle function.
In conclusion, our data indicate that the capacities of the TS and QF MTUs were reduced with aging. In contrast, runners and non-active subjects had no clearly identifiable differences in the mechanical or the morphological properties of the TS or QF MTUs. The relatively low oscillatory load imposed on the QF and TS MTUs during endurance-running exercise is apparently not sufficient to produce measurable changes in the parameters analysed. This is supported by the fact that endurance running does not appear to be able to counteract the influence of aging on the capacities of TS and QF MTUs.
Running mechanics
Older adults vs young adults
The second objective of this study was to test the hypothesis that older
adults would reveal a differing running strategy from those of young adults,
due to a reduction in the capacities of their TS and QF MTUs. The experimental
data supported these expectations. When running at the same speed as young
adults, older adults selected a different strategy, leading to lower average
and maximum vertical GRF, lower vertical and horizontal (during deceleration
and acceleration phase) impulses, a higher duty factor and ratio displacement,
a higher stride frequency and consequently lower step length, a lower anterior
COM displacement during the flight phase and a lower vertical COM displacement
during the stride cycle. However, the ground contact duration and the anterior
COM displacement during ground contact did not differ between the older and
young adults. The shift towards a higher duty factor and ratio displacement
with age probably increased the subjects' safety by increasing the amount of
COM transport and time with the foot on the ground while running.
From the mechanical point of view, the above findings indicate that older
adults had more advantageous running characteristics than young adults. In the
literature, it is generally accepted that there is an inverse relationship
between the rate of energy used for steady state running and the rate of force
generation applied to the ground to support the body weight during each stride
(Kram and Taylor, 1990;
Roberts et al., 1998
;
Wright and Weyand, 2001
;
Griffin et al., 2003
). To
calculate the rate of force generation (Frate, in N
s1 kg1) we divided the average vertical
force per kg body weight (
, in N
kg1) by the duration of the ground contact
(tcontact, in s) according to Kram and Taylor
(1990
):
![]() | (2) |
The comparison of the rates of force generation revealed a significant
(P=0.040) age effect, being lower in older adults than younger adults
(Fig. 9). These values show
that older adults generated about 9% less force per stride for a given running
speed compared to younger adults. Additionally, to calculate the force
generation per meter distance (Ftrans, N
m1 kg1), we divided the average vertical
GRF per kg body weight (, N
kg1) by the anterior COM displacement during ground contact
(
, in m) according
to Kram and Taylor (1990
)
(
was calculated as
the mean value from both legs). The results were the same as for the rate of
force generation: older adults demonstrated a reduced (P=0.004) force
generation per meter distance (Fig.
9). Furthermore, the integrals of the horizontal GRF during
deceleration and acceleration phase were lower for the older adults compared
to the younger adults. Chang and Kram
(1999
) provided evidence on
that an increased generation of horizontal forces (deceleration and
acceleration phase) during human running is accompanied by an increased
metabolic cost. The above findings (higher duty factor, higher ratio
displacement of the COM, lower rate of force generation, lower force
generation per meter distance and lower integrals of the horizontal GRF during
deceleration and acceleration phase) strongly suggest that older adults
demonstrated an improvement in running mechanics and increased the safety of
their musculoskeletal system while running at a given speed compared to the
young adults.
|
While the ankle joint kinetics altered in the older adults, no clear differences in knee joint kinetics were detected between age groups, even though the age-related decline in maximal joint moment during isometric MVC showed similar relative values at the ankle (25%) and knee joint (20%). A possible explanation could be the lower maximal knee joint moment compared to the maximal ankle joint moment (about 35%) during running and the higher knee extensor muscle strength compared to the plantar flexion muscles (about 60%) by the MVCs.
From a mechanical point of view the results confirm that the older adults
adopted a more advantageous running strategy than younger adults, despite the
general acceptance of the gradual decrease in the performance capacity of the
nervous system with ageing (for a review, see
Prince et al., 1997). It seems
reasonable to believe that the nervous system of the older subjects was able
to recalibrate its motor commands (the act of modifying their internal model
that predicts the dynamic behaviour of the motor system) to cope with the
running task. Running at submaximal velocities is a periodic (cyclic) motor
task, and thus it is possible that the older adults, having had feedback from
repeated practice, could update their running strategy and this way decrease
the disparity between the reduced capacities of the MTUs and running effort.
In the literature it is often reported that older adults show deficits in
performing a strategic task but not at the adaptation level of a non-strategic
task (McNay and Willingham,
1998
; Fernández-Ruiz et
al., 2000
; Buch et al.,
2003
). The lower gear ratios at the ankle joint and the
consequently increased mechanical advantage for the TS MTU in the older adults
at the mid-part of ground contact phase, where the GRF is near its maximal
value, support the idea that the observed improvement in the running mechanics
is a consequence of proprioceptive feedback from repeated practice to adjust
the running effort to the reduced capacity of the MTUs.
It would be interesting to identify the main changes in the motor task characteristics leading to the improvement in running mechanics. The changes in the rate of force generation and force generation per meter distance were related to the lower vertical COM displacement during stride cycle, due to aging. A lower vertical COM displacement may also affect the gear ratios during the initial and mid-part of the contact phase, due to a better control of the impact dynamics. The lower maximum of the mechanical power at the ankle joint, and the higher limb angle at take-off for the older adults, seem to be the main causes for the lower vertical COM displacement. Mechanical power at the ankle joint and the limb angle at take-off are parameters located in the second part of the contact phase. The above observations provide evidence that the older adults plan the initial conditions for collision with the ground in the second part of the support phase. In other words, the older adults prepared for the next collision with the ground during the preceding stride, which might indicate a shift from proprioceptive feed-back to a predictive feed-forward running control strategy for the older adults.
Based on the present results, however, it is difficult to explain why the
non-active older adults (not practiced in running) showed the same changes in
running characteristics as the older practiced runners. A possible explanation
could be a transfer of motor adaptation from daily activities (e.g. walking)
to running. In the literature, a transfer of motor adaptations to different
conditions has been reported (van Hedel et
al., 2002; Abeele and Bock,
2003
; Lam and Dietz,
2004
). Moreover the data from Bock
(2005
) confirmed that there is
no evidence of any age-dependence of such transfer and that transfer is not
degraded during aging. So, for example, our older adults displaying lower gear
ratios at the ankle during running also showed lower gear ratios at the ankle
joint during the initial and mid-part of the ground contact during walking
(data not presented in this article).
Runners vs non-active subjects
The final purpose of this study was to examine the hypothesis that
experienced runners would employ a task-specific adaptation in terms of higher
advantages in running mechanics compared to non-active subjects, even at old
age. The data supported this hypothesis. Although runners and non-active
subjects had similar properties of the TS and QF MTUs, running experience
decreased the gear ratios at the knee joint during the first 42% of the period
of ground contact (phases 1 and 2) to the same extent in the young as in the
older adults. This was due to a lower moment arm of the GRF acting about the
knee joint. The lower gear ratios due to running activity did not affect the
maximal knee joint moment because of its later occurrence during ground
contact (at about 50%). However, the higher mechanical advantage for the QF
MTU during the initial part of the ground contact indicates that endurance
runners have an advantageous running strategy at the beginning of ground
contact. A higher mechanical advantage during the initial running phase when
an eccentric QF contraction is necessary to control knee flexion and provide
shock absorption, could increase the ability of the knee to attenuate shock
and reduce the mechanical load on the knee joint. However, it is not likely
that such changes in gear ratio would happen due to reactive corrections,
because the available time is too short. Instead, it can be argued that
runners use a predictive feed-forward running control strategy. Therefore, as
for the older adults vs young adults, it can be suggested that the
proprioceptive feed-back information from repeated practice is the mediator of
predictive feed-forward motor commands.
Duty factor, ground contact duration, average vertical force and rate of
force generation were not different between runners and non-active subjects
(Fig. 9). Because the anterior
COM displacement during ground contact was lower for active runners we
expected force generation per meter distance to be different between runners
and non-active individuals. However, no significant (P=0.299)
differences in the force generation per meter distance were noted between
activity groups (Fig. 9). The
intra-individual differences within groups might be too high and the effect of
the reduced anterior COM displacement during ground contact too low to detect
significant differences in the force generation per meter distance between
runners and non-active subjects. However, endurance runners showed a lower
horizontal impulse during deceleration and acceleration phase compared to the
non-active subjects. Thus, besides the higher mechanical advantage at the knee
joint during the initial part of the ground contact phase, the lower
horizontal forces (deceleration and acceleration phase) in the experienced
runners group is a further indicator of an improvement in running mechanics
(Chang and Kram, 1999).
Conclusions
In conclusion, our results show that the capacities of the TS and QF MTUs
were reduced during aging. Further, the results suggest that chronic
endurance-running exercise did not prevent this age-related degeneration nor
provoke any further adaptational effects on the mechanical (tendon stiffness,
muscle strength) or morphological (pennation angle, fascicle length, muscle
thickness) properties of the high-load bearing MTUs studied in the young
adults. However, running experience increases the mechanical advantage for the
QF MTU (lower gear ratio at the knee joint) while running even at old age.
Older adults react to the reduced capacity of their MTUs by increasing safety
during running (higher duty factor, lower flight time) and benefit from a
mechanical advantage for the TS MTU (lower gear ratio at the ankle joint),
lower rate of force generation and force generation per meter distance. We
suppose that the improvement in running mechanics in the older adults happens
because of a perceptual motor recalibration and a feed-forward adaptation of
the motor task aimed at decreasing the disparity between the reduced capacity
of the MTUs and the running effort.
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List of abbreviations |
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Acknowledgments |
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References |
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---|
Aagaard, P., Andersen, J. L., Dyhre-Poulsen, P., Leffers, A. M.,
Wagner, A., Magnusson, S. P., Halkjaer-Kristensen, J. and Simonsen, E.
B. (2001). A mechanism for increased contractile strength of
human pennate muscle in response to strength training: changes in muscle
architecture. J. Physiol.
534,613
-623.
Abeele, S. and Bock, O. (2003). Transfer of sensorimotor adaptation between different movement categories. Exp. Brain Res. 148,128 -132.[CrossRef][Medline]
Arampatzis, A., Brüggemann, G.-P. and Metzler, V. (1999). The effect of speed on leg stiffness and joint kinetics in human running. J. Biomech. 32,1349 -1353.[CrossRef][Medline]
Arampatzis, A., Karamanidis, K., DeMonte, D., Stafilidis, S., Morey-Klapsing, G. and Brüggemann, G.-P. (2004). Differences between measured and resultant joint moments during voluntary and artificially elicited isometric knee extension contractions. Clin. Biomech. 19,277 -283.[CrossRef]
Arampatzis, A., Morey-Klapsing, G., Karamanidis, K., DeMonte, D., Stafilidis, S. and Brüggemann, G.-P. (2005a). Differences between measured and resultant joint moments during isometric contractions at the ankle joint. J. Biomech. 38,885 -892.[CrossRef][Medline]
Arampatzis, A., Stafilidis, S., DeMonte, G., Karamanidis, K., Morey-Klapsing, G. and Brüggemann, G.-P. (2005b). Strain and elongation of the human gastrocnemius tendon and aponeurosis during maximal plantarflexion effort. J. Biomech. 38,833 -841.[CrossRef][Medline]
Baratta, R., Solomonow, M., Zhou, B. H., Letson, D., Chuinard, R. and D'Ambrosia, R. (1988). Muscular coactivation. The role of the antagonist musculature in maintaining knee stability. Am. J. Sports Med. 16,113 -122.[Abstract]
Biewener, A. A. and Roberts, T. J. (2000). Muscle and tendon contributions to force, work, and elastic energy savings: a comparative perspective. Exerc. Sport Sci. Rev. 28, 99-107.[Medline]
Biewener, A. A., Farley, C. T., Roberts, T. J. and Temaner,
M. (2004). Muscle mechanical advantage of human walking and
running: implications for energy cost. J. Appl.
Physiol. 97,2266
-2274.
Birch, H. L., McLaughlin, L., Amith, R. K. and Goodship, A. E. (1999). Treadmill exercise-induced tendon hypertrophy: assessment of tendons with different mechanical functions. Equine Vet. J. Suppl. 30,222 -226.
Blevins, F. T., Hecker, A. T., Bigler, G. T., Boland, A. L. and Hayes, W. C. (1994). The effects of donor age and strain rate on the biomechanical properties of bone-patellar tendon-bone allografts. Am. J. Sports Med. 22,328 -333.[Abstract]
Bobbert, M. F. (2001). Dependence of human
squat jump performance on the series elastic compliance of the triceps surae:
a simulation study. J. Exp. Biol.
204,533
-542.
Bock, O. (2005). Components of sensorimotor adaptation in young and elderly subjects. Exp. Brain Res. 160,259 -263.[CrossRef][Medline]
Bojsen-Møller, J., Hansen, P., Aagaard, P., Kjaer, M. and Magnusson, S. P. (2003). Measuring mechanical properties of the vastus lateralis tendon-aponeurose complex in vivo by ultrasound imaging. Scand. J. Med. Sci. Sports 13,259 -265.[CrossRef][Medline]
Buch, E. R., Young, S. and Contreras-Vidal, J. L.
(2003). Visuomotor adaptation in normal aging. Learn.
Mem. 10,55
-63.
Carrier, D. R., Heglund, N. C. and Earls, K. D. (1994). Variable gearing during locomotion in the human musculoskeletal system. Science 265,651 -653.[Medline]
Chang, Y. H. and Kram, R. (1999). Metabolic
cost of generating horizontal forces during human running. J. Appl.
Physiol. 86,1657
-1662.
Criswell, D. S., Powers, S. K., Herb, R. A. and Dodd, S. L. (1997). Mechanism of specific force deficit in the senescent rat diaphragm. Respir. Physiol. 107,149 -155.[CrossRef][Medline]
Curwin, S. L., Vailas, A. C. and Wood, J.
(1988). Immature tendon adaptation to strenuous exercise.
J. Appl. Physiol. 65,2297
-2301.
D'Antona, G., Pellegrino, M. A., Adami, R., Rossi, R., Carlizzi,
C. N., Canepari, M., Saltin, B. and Bottinelli, R.
(2003). The effect of aging and immobilization on structure and
function of human skeletal muscle fibers. J. Physiol.
552,499
-511.
De Haan, A., de Jong, J., van Doorn, J. E., Huijing, P. A., Woittiez, R. D. and Westra, H. G. (1986). Muscle economy of isometric contractions as a function of stimulation time and relative muscle length. Pflugers Arch. 407,445 -450.[CrossRef][Medline]
Demster, W. T., Gabel, W. C. and Felts, W. J. (1959). The anthropometry of the manual work space for the seated subject. Am. J. Phys. Anthropol. 17,289 -317.[CrossRef][Medline]
DeVita, P. (1994). The selection of standard convention for analyzing gait data based on the analysis of relevant biomechanical factors. J. Biomech. 27,501 -508.[CrossRef][Medline]
DeVita, P. and Hortobagyi, T. (2000). Age
causes a redistribution of joint torques and powers during gait. J.
Appl. Physiol. 88,1804
-1811.
DeVita, P., Blankenship-Hunter, P. and Skelly, W. A. (1992). Effects of functional knee brace on the biomechanics of running. Med. Sci. Sports Exerc. 24,797 -806.[Medline]
Erni, T. and Dietz, V. (2001). Obstacle
avoidance during human walking: learning rate and cross-modal transfer.
J. Physiol. 534,303
-312.
Ettema, G. J. (1996). Mechanical efficiency and
efficiency of storage and release of series elastic energy in skeletal muscle
during stretchshorten cycles. J. Exp. Biol.
199,1983
-1997.
Fernandez-Ruiz, J., Hall, C., Vergara, P. and Diiaz, R. (2000). Prism adaptation in normal aging: slower adaptation rate and larger aftereffect. Cogn. Brain Res. 9, 223-226.[CrossRef][Medline]
Frontera, W. R., Hughes, V. A., Lutz, K. J. and Evans, W. J.
(1991). A cross-sectional study of muscle strength and mass in
45- to 78-yr-old men and women. J. Appl. Physiol.
71,644
-650.
Frontera, W. R., Suh, D., Krivickas, L. S., Hughes, V. A., Goldstein, R. and Roubenoff, R. (2000). Skeletal muscle fiber quality in older men and women. Am. J. Physiol. 279,C611 -C618.
Fujie, H., Yamamoto, N., Murakami, T. and Hayashi, K. (2000). Effects of growth on the response of the rabbit patellar tendon to stress shielding: a biomechanical study. Clin. Biomech. 15,370 -378.[CrossRef]
Gans, C. and Gaunt, A. S. (1991). Muscle architecture in relation to function. J. Biomech. 24, 53-65.[CrossRef][Medline]
Griffin, T. M., Roberts, T. J. and Kram, R.
(2003). Metabolic cost of generating muscular force in human
walking: insights from load-carrying and speed experiments. J.
Appl. Physiol. 95,172
-183.
Hansen, P., Aagaard, P., Kjaer, M., Larsson, B. and Magnusson,
S. P. (2003). Effect of habitual running on human Achilles
tendon load-deformation properties and cross-sectional area. J.
Appl. Physiol. 95,2375
-2380.
Hayashi, K. (1996). Biomechanical studies of the remodeling of knee joint tendons and ligaments. J. Biomech. 29,707 -716.[CrossRef][Medline]
Herzog, W. (1987). Determination of muscle model parameters using an optimization technique. Biomechanics X-B, 1175-1179.
Herzog, W. and Read, L. J. (1993). Lines of action and moment arms of the major force-carrying structures crossing the human knee joint. J. Anat. 182,213 -230.[Medline]
Herzog, W., Hasler, E. and Abrahamse, S. K. (1991). A comparison of knee extensor strength curves obtained theoretically and experimentally. Med. Sci. Sports Exerc. 23,108 -114.[Medline]
Hof, A. L., Van Zandwijk, J. P. and Bobbert, M. F. (2002). Mechanics of human triceps surae muscle in walking, running and jumping. Acta Physiol. Scand. 174, 17-30.[CrossRef][Medline]
Hortobagyi, T., Mizelle, C., Beam, S. and DeVita, P. (2003). Old adults perform activities of daily living near their maximal capabilities. J. Gerontol. 58,M453 -M460.
Kagerer, F. A., Contreras-Vidal, J. L. and Stelmach, G. E. (1997). Adaptation to gradual as compared with sudden visuo-motor distortions. Exp. Brain Res. 115,557 -561.[Medline]
Karamanidis, K., Arampatzis, A. and Brüggemann, G.-P. (2003). Symmetry and reproducibility of kinematic parameters during various running techniques. Med. Sci. Sports Exerc. 35,1009 -1016.[Medline]
Karamanidis, K., Arampatzis, A. and Brüggemann, G.-P. (2004). Reproducibility of electromyography and ground reaction force during various running techniques. Gait Posture. 19,115 -123.[CrossRef][Medline]
Karpakka, J., Väänänen, K., Virtanen, P., Savolainen, J., Orava, S. and Takala, T. E. S. (1990). The effects of remobilization and exercise on collagen biosynthesis in rat tendon. Acta Physiol. Scand. 139,139 -145.[Medline]
Ker, R. F., Alexander, R. McN. and Bennett, M. B. (1988). Why are mammalian tendons so thick? J. Zool. Lond. 216,309 -324.
Kiiskinen, D. (1977). Physical training and connective tissues in young mice-physical properties of Achilles tendons and long bones. Growth 41,123 -137.[Medline]
Kjaer, M. (2004). Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol. Rev. 84,694 -698.
Klitgaard, H., Mantoni, M., Schiaffino, S., Ausoni, S., Gorza, L., Laurent-Winter, C., Schnohr, P. and Saltin, B. (1990). Function, morphology and protein expression of ageing skeletal muscle: a cross-sectional study of elderly men with different training background. Acta Physiol. Scand. 140, 41-54.[Medline]
Komatsu, K., Shibata, T., Shimada, A., Viidik, A. and Chiba, M. (2004). Age-related and regional differences in the stress-strain and stress-relaxation behaviors of the rat incisor periodontal ligament. J. Biomech. 37,1097 -1106.[CrossRef][Medline]
Kram, R. and Taylor, C. R. (1990). Energetics of running: a new perspective. Nature 346,265 -267.[CrossRef][Medline]
Kubo, K., Kanehisa, H., Azuma, K., Ishuzu, M., Kuno, S.-Y., Okada, M. and Fukunaga, T. (2003a). Muscle architecture characteristics in young and elderly men and women. Int. J. Sports Med. 24,125 -130.[CrossRef][Medline]
Kubo, K., Kanehisa, H., Azuma, K., Ishuzu, M., Kuno, S.-Y. A., Okada, M. and Fukunaga, T. (2003b). Muscle architectural characteristics in women aged 0-79 years. Med. Sci. Sports Exerc. 35,39 -44.[CrossRef][Medline]
Kubo, K., Kanehisa, H., Miyatani, M., Tachi, M. and Fukunaga, T. (2003c). Effect of low-load resistance training on the tendon properties in middle-aged and elderly women. Acta Physiol. Scand. 178,25 -32.[CrossRef][Medline]
Kubo, K., Akima, H., Ushiyama, J., Tabata, I., Fukuoka, H.,
Kanehisa, H. and Fukunaga, T. (2004). Effects of 20
days of bed rest on the viscoelastic properties of tendon structures in lower
limb muscles. Br. J. Sports Med.
38,324
-330.
Lam, T. and Dietz, V. (2004). Transfer of motor
performance in an obstacle avoidance task to different walking conditions.
J. Neurophysiol. 92,2010
-2016.
Lieber, R. L. and Friden, J. (2000). Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 23,1647 -1666.[CrossRef][Medline]
Mademli, L., Arampatzis, A., Morey-Klapsing, G. and Brügemann, G.-P. (2004). Effect of ankle joint position and electrode placement on the estimation of the antagonistic moment during maximal plantarflexion. J. Electromyogr. Kinesiol. 14,591 -597.[CrossRef][Medline]
Maganaris, C. N., Baltzopoulos, V. and Sargeant, A. J.
(1998). Changes in Achilles tendon moment arm from rest to
maximum isometric plantarflexion: in vivo observations in man. J.
Physiol. 510,977
-985.
Magnusson, S. P., Aagaard, P., Rosager, S., Dyhre-Poulsen, P.
and Kjaer, M. (2001). Load-displacement properties of
the human triceps surae aponeurosis in vivo. J.
Physiol. 531,277
-288.
McMahon, T. A. (1985). The role of compliance in mammalian running gaits. J. Exp. Biol. 115,263 -282.[Abstract]
McNay, E. C. and Willingham, D. B. (1998). Deficit in learning of a motor skill requiring strategy, but not of perceptuomotor recalibration, with aging. Learn. Mem. 4, 411-420.[Abstract]
Messier, S. P., Davis, S. E., Curl, W. W., Lowery, R. B. and Pack, R. J. (1991). Etiologic factors associated with patellofemoral pain in runners. Med. Sci. Sports Exerc. 23,1008 -1015.[Medline]
Mulder, T., Zijlstra, W. and Geurts, A. (2002). Assessment of motor recovery and decline. Gait Posture 16,198 -210.[CrossRef][Medline]
Muramatsu, T., Muraoka, T., Takeshita, D., Kawakami, Y., Hirano,
Y. and Fukunaga, T. (2001). Mechanical properties of tendon
and aponeurosis of human gastrocnemius muscle in vivo. J. Appl.
Physiol. 90,1671
-1678.
Narici, M. V., Maganaris, C. N., Reeves, N. D. and Capodaglio,
P. (2003). Effect of aging on human muscle architecture.
J. Appl. Physiol. 95,2229
-2234.
Nigg, B. M., Cole, G. K. and Nachbauer, W. (1993). Effects of arch height of the foot on angular motion of the lower extremities in running. J. Biomech. 26,909 -916.[CrossRef][Medline]
Noyes, F. R. and Grood, E. S. (1976). The strength of the anterior cruciate ligament in humans are rhesus monkeys. Age-related and species related changes. J. Bone Jt Surg. 58,1074 -1082.[Abstract]
Out, L., Vrijkotte, T. G., van Soest, A. J. and Bobbert, M. F. (1996). Influence of the parameters of a human triceps surae muscle model on the isometric torque-angle relationship. J. Biomech. Eng. 118,17 -25.[Medline]
Pai, Y. C., Wening, J. D., Runtz, E. F., Iqbal, K. and Pavol, M.
J. (2003). Role of feedforward control of movement stability
in reducing slip-related balance loss and falls among older adults.
J. Neurophysiol. 90,755
-762.
Pavol, M. J., Runtz, E. F., Edwards, B. J. and Pai, Y. C. (2002). Age influences the outcome of a slipping perturbation during initial but not repeated exposures. J. Gerontol. 57,M496 -M503.
Prince, F., Corriveau, H., Hébert, R. and Winter, D. A. (1997). Gait in the elderly. Gait Posture 5,128 -135.[CrossRef]
Reeves, N. D., Maganaris, C. N. and Narici, M. V.
(2003). Effect of strength training on human patella tendon
mechanical properties of older individuals. J.
Physiol. 548,971
-981.
Reeves, N. D., Narici, M. V. and Maganaris, C. N.
(2004). In vivo human muscle structure and function: adaptations
to resistance training in old age. Exp. Physiol.
89,675
-689.
Riener, R. and Edrich, T. (1999). Identification of passive elastic joint moments in the lower extremities. J. Biomech. 32,539 -544.[CrossRef][Medline]
Roberts, T. J. and Marsh, R. L. (2003). Probing
the limits to muscle-powered accelerations: lessons from jumping
bullfrogs. J. Exp. Biol.
206,2567
-2580.
Roberts, T. J., Kram, R., Weyand, P. G. and Taylor, C. R.
(1998). Energetics of bipedal running. I. Metabolic cost of
generating force. J. Exp. Biol.
201,2745
-2751.
Rosager, S., Aagaard, P., Dyhre-Poulsen, P., Neergaard, K., Kjaer, M. and Magnusson, S. P. (2002). Load-displacement properties of the human triceps aponeurosis and tendon in runners and non-runners. Scand. J. Med. Sci. Sports 12, 90-98.[CrossRef][Medline]
Savelberg, H. H. and Meijer, K. (2004). The effect of age and joint angle on the proportionality of extensor and flexor strength at the knee joint. J. Gerontol. 59,1120 -1128.
Schultz, A. B. (1992). Mobility impairment in the elderly: challenges for biomechanics research. J. Biomech. 25,519 -528.[CrossRef][Medline]
Shadmehr, R. (2004). Generalization as a behavioral window to the neural mechanisms of learning internal models. Hum. Mov. Sci. 23,543 -568.[CrossRef][Medline]
Stafilidis, S., Karamanidis, K., Morey-Klapsing, G., DeMonte, G., Brüggemann, G. P. and Arampatzis, A. (2005). Strain and elongation of the vastus lateralis aponeurosis and tendon in vivo during maximal isometric contraction. Eur. J. Appl. Physiol. 94,317 -322.[CrossRef][Medline]
Trappe, S., Gallagher, P., Harber, M., Carrithers, J., Fluckey,
J. and Trappe, T. (2003). Single muscle fibre
contractile properties in young and old men and women. J.
Physiol. 552,47
-58.
van Hedel, H. J., Biedermann, M., Erni, T. and Dietz, V.
(2002). Obstacle avoidance during human walking: transfer of
motor skill from one leg to the other. J. Physiol.
543,709
-717.
Viidik, A. (1969). Tensile strength properties of Achilles tendon system in trained and untrained rabbits. Acta. Orthop. Scand. 40,261 -272.[Medline]
Vogel, H. G. (1980). Influence of maturation and aging on mechanical and biomechanical properties of connective tissue in rats. Mech. Ageing Dev. 14,283 -292.[CrossRef][Medline]
Wang, J. H.-C. (2005). Mechanobiology of tendon. J. Biomech. doi: 10.1016/j.jbiomech.2005.05.011[CrossRef]
Wojcik, L. A., Thelen, D. G., Schultz, A. B., Ashton-Miller, J. A. and Alexander, N. B. (2001). Age and gender differences in peak lower extremity joint torques and ranges of motion used during single-step balance recovery from a forward fall. J. Biomech. 34,67 -73.
Wolpert, D. M., Ghahramani, Z. and Jordan, M. I. (1995). An internal model for sensorimotor integration. Science 269,1880 -1882.
Woltring, H. J. (1986). A FORTRAN package for generalized, cross-validatory spline smoothing and differentiation. Adv. Eng. Software 8,104 -113
Woo, S. L.-Y., Gomez, M. A., Amiel, D., Ritter, M. A., Gelberman, R. H. and Akeson, W. H. (1981). The effects of exercise on the biomechanical and biochemical properties of swine digital flexor tendons. J. Biomech. Eng. 103, 51-56.
Wright, S. and Weyand, P. G. (2001). The application of ground force explains the energetic cost of running backward and forward. J. Exp. Biol. 204,1805 -1815.
Zuurbier, C. J. and Huijing, P. A. (1992). Influence of muscle geometry on shortening speed of fibre, aponeurosis and muscle. J. Biomech. 25,1017 -1026.