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ARTICLE IN PRESS
Journal of Biomechanics 36 (2003) 1761–1769
Muscle activity reduces soft-tissue resonance at
heel-strike during walking
James M. Wakelinga,*, Anna-Maria Liphardta,b, Benno M. Nigga
a
b
Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, Calgary, Alberta Canada T2N 1N4
Institute for Training and Movement Science, German Sport University, Cologne, Carl-Diem-Weg 6, 50933 Koln,
. Germany
Accepted 28 May 2003
Abstract
Muscle activity has previously been suggested to minimize soft-tissue resonance which occurs at heel-strike during walking and
running. If this concept were true then the greatest vibration damping would occur when the input force was closest to the resonant
frequency of the soft-tissues at heel-strike. However, this idea has not been tested. The purpose of this study was to test whether
muscle activity in the lower extremity is used to damp soft-tissue resonance which occurs at heel-strike during walking. Hard and
soft shoe conditions were tested in a randomized block design. Ground reaction forces, soft-tissue accelerations and myoelectric
activity were measured during walking for 40 subjects. Soft-tissue mass was estimated from anthropologic measurements, allowing
inertial forces in the soft-tissues to be calculated. The force transfer from the ground to the tissues was compared with changes in the
muscle activity. The soft condition resulted in relative frequencies (input/tissue) to be closer to resonance for the main soft-tissue
groups. However, no increase in force transmission was observed. Therefore, the vibration damping in the tissues must have
increased. This increase concurred with increases in the muscle activity for the biceps femoris and lateral gastrocnemius. The
evidence supports the proposal that muscle activity damps soft-tissue resonance at heel-strike. Muscles generate forces which act
across the joints and, therefore, shoe design may be used to modify muscle activity and thus joint loading during walking
and running.
r 2003 Elsevier Ltd. All rights reserved.
Keywords: Vibration; EMG; Joint loading
1. Introduction
Ground reaction forces act between the ground and
the foot of a person during walking and running.
Ground reaction forces typically have an impact peak
after heel-strike due to the collision of the foot with the
ground. The impact force occurs within 50 ms after first
contact and causes shock waves to travel through both
the soft-tissues and skeletal components of the body.
The impact force should be expected to cause oscillations in the wobbling structures of the body, and the
tissues may resonante if their natural frequencies are
close to the frequency of the input force.
It has been proposed that lower extremity muscle
activity adapts to the impact force which occurs during
*Corresponding author. Tel.: +1-403-220-7004; fax: +1-403-2843553.
E-mail address: [email protected] (J.M. Wakeling).
0021-9290/03/$ – see front matter r 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0021-9290(03)00216-1
heel-strike in order to minimize soft-tissue resonance
(Nigg et al., 1995). If such a situation occurs then it may
be possible to use shoe materials to modify the impact
force and thus vibration load on the body in order to
cause specific alterations in the muscle activity and thus
joint loading. Previous studies have shown that the
hardness of a shoe midsole causes changes in the time to
peak impact force at heel-strike (Light et al., 1980;
Frederick et al., 1984; Nigg et al., 1987; Lafortune et al.,
1996). This time and the associated loading rate are a
correlate of the major frequency content of the impact
force (typically 10–20 Hz for running) and thus indicate
that different shoes will result in different vibration
loads on the tissues. The natural frequencies of the softtissues in the lower extremity range between 10 and
50 Hz (Wakeling and Nigg, 2001a), and so may
potentially resonate due to the heel-strike impacts.
However, both the natural frequency and damping
coefficients of the soft-tissues of the lower extremity
ARTICLE IN PRESS
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J.M. Wakeling et al. / Journal of Biomechanics 36 (2003) 1761–1769
change with altered muscle activity (Wakeling and Nigg,
2001a), indicating that muscle has the capability to alter
the vibration response of the soft-tissues and the
potential to minimize the soft-tissue resonance. During
controlled vibration experiments, it was shown that
muscle activity was used to increase vibration damping
when an input frequency approached the resonance
frequency of the tissue (Wakeling et al., 2002a). It has
been shown that lower extremity muscle activity does
adapt to the altered impact forces during running with
different shoe midsole materials (Wakeling et al., 2001b,
2002b). However, it has not been shown that the muscle
adaptation which occurs in response to the impact force
during walking and running is related to the soft-tissue
vibration frequencies.
The purpose of this experiment was to measure
changes in the muscle activity and soft-tissue vibrations
which occurred during walking with different shoe
conditions. The hypothesis to be tested was that when
the input frequency of the ground reaction force
approached the vibration frequency of the soft-tissues
then the muscle activity within those tissues would
increase in order to minimize the vibrations.
2. Methods
2.1. Subjects
Twenty male (age 26.971.0 yr; mass 78.2473.20 kg;
mean7SEM) and 20 female (age 25.871.1 yr; mass
67.6171.60 kg) subjects were tested. The subjects were
students at the University of Calgary. Subjects gave
their informed, written, consent to participate in
accordance with the University of Calgary’s Conjoint
Health Research Ethics Board policy on research using
human subjects.
Muscle and soft-tissue masses within the lower
extremity were estimated from a series of length, breadth
and skin fold measurements using methods previously
described (Wakeling et al., 2002a).
2.2. Protocol
Subjects were instructed to walk at a brisk pace along
a 20 m indoor track. A force plate (Kistler AG,
Winterthur, Switzerland) was placed in the centre of
the track, level with the ground. Initial trials determined
the starting position, which would result in the fifth step
of the right foot striking the force plate. During the
experiment, subjects were requested not to focus on the
position of the force plate. Timing lights, spanning
the force plate, were used to measure the walking
velocity. The timing of heel-strike was determined by an
accelerometer attached to the heel-cup of the right shoe.
The control condition was a hard-soled leather shoe
(Asker Shore C 77, 320 g). A soft (Asker Shore C 28)
heel-cup insert was used as the insert condition. This
insert had mass 26.2 g, and a maximum thickness of
4.5 mm which compressed to approximately 1.5 mm
with body weight. The starting condition was randomized. Each condition was tested in blocks of 10
consecutive trials. The blocks were tested in the order
ABBAAB, where A and B represent the two different
conditions. This block design was used to minimize bias
in the results due to muscle fatigue. For each trial, data
were collected from a standing posture for 2 s, a
subsequent walk of 10 double paces, and a final 2 s
stand. Data were analysed for the middle eight steps
from each trial.
2.3. Outcome measures
The ground reaction force, the myoelectric signals
from the lower extremity muscles and the soft-tissue
accelerations were recorded at 2400 Hz using a 12-bit
data acquisition system. Soft-tissue vibrations were
measured from the muscle bellies of the vastus lateralis,
biceps femoris (long head), tibialis anterior and lateral
gastrocnemius using skin-mounted tri-axial accelerometers (EGAX accelerometer, nominal frequency
response 0–600 Hz; Entran devices). The axes were
orientated to be parallel to the long axis of the segment,
normal to the skin, and medio-lateral. Accelerometers
(o5 g) were attached to the skin surface, 1 cm distal to
the EMG electrode, using Hollister medical adhesive
glue, and a stretch adhesive bandage preloaded the
accelerometer to improve the congruence of motion with
the soft-tissues (Wakeling and Nigg, 2001a, b). Myoelectric activity was recorded from the rectus femoris,
biceps femoris (long head), tibialis anterior and lateral
gastrocnemius muscles. Myoelectric activity was measured from the muscle bellies using round bipolar
surface electrodes (Ag/AgCl) after removal of the hair
and cleaning of the skin with isopropyl wipes. Each
electrode was 10 mm in diameter and had an interelectrode spacing of 22 mm and was placed midway between
the motor end plate and distal myotendinous junction.
A ground electrode was placed on the lateral condyle of
the knee. EMGs were preamplified at source (Biovision,
Wehrheim, Germany).
2.4. Analysis
Initial analysis showed high frequency oscillations
(>300 Hz) in the vertical ground reaction forces. These
oscillations were removed by a 100 Hz low-pass filter,
and the mean ground reaction force calculated from the
30 trials for each subject-condition combination
and the vertical impact force was quantified for
each trial by its maximum loading rate, F’GRF;max ; and
ARTICLE IN PRESS
J.M. Wakeling et al. / Journal of Biomechanics 36 (2003) 1761–1769
Table 1
Coefficients for the wavelets used to analyze high- and low-frequency
components from the myoelectric signal
Frequency
fc (Hz)
s
t (ms)
Frequency band (Hz)
High
Low
30.91
150.95
0.0997
0.0302
2.1
7.1
12–63
71–274
Center-frequency fc ; scale s; time resolution t:
its peak value, FGRF;max : An effective input frequency,
fGRF , was estimated from four times the period
between the maximum loading rate and the peak
impact force.
The mean tissue acceleration during the 2 s static
standing period prior to each walking trial was
subtracted from the acceleration records, to reference
the accelerations to a vertical standing posture. The
mean acceleration traces were calculated from
the 240 steps from each subject-muscle-axis-condition
combination. Inertial tissue forces were calculated for
each direction from the product of the mean referenced
acceleration in that direction and the soft-tissue
mass. Inertial forces were quantified by their maximum
absolute loading rate after heel-strike, the maximum and
minimum peak forces surrounding the maximum
inertial loading rate. The vibration frequency was
estimated from twice the period between the maximum
and minimum forces.
Myoelectric signals were resolved into their intensities
in time-frequency space using EMG specific wavelet
techniques (von Tscharner, 2000). The intensity
is the power of the EMG signal contained within a
particular frequency band. The total intensity over the
frequency band 11–432 Hz was calculated using a filterbank of 11 wavelets with time resolutions from 45 to
12 ms. The intensity was also calculated for specific high
and low-frequency bands using two wavelets W ðf Þ
which were defined as the following function of
frequency, f :
fc s
f
W ðf Þ ¼
e fc sðf =fc þ1Þ ;
fc
ð1Þ
where fc is the centre frequency of the wavelet, and s is a
scaling factor. Parameters defining these two wavelets
are given in Table 1. The intensities at the high and lowfrequency bands were calculated in the same manner as
the intensity for each wavelet from the previously
reported filter-bank (von Tscharner, 2000).
The mean intensity trace was calculated for the 240
steps from each subject-muscle-condition combination,
and was calculated for 50 ms time windows before and
after heel-strike for the total intensity, and for 10 ms
time windows spanning 50 ms before to 50 ms after heelstrike for the high- and low-frequency bands.
1763
2.5. Statistics
The effects of the shoe condition on the measures of
the GRF, vibration and EMG were determined using
multifactorial analyses of variance. In each test the
subject identity and the shoe condition were used as
factors. Relative changes in parameters between the
shoe conditions were calculated as the difference
between the insert and control relative to the control
value. All tests were considered significant at the a ¼
0:05 level. Mean values are presented with the standard
error of sample mean (SEM).
3. Results
The subjects walked at a velocity of 2.1070.01 m s 1
(mean7SEM) with a stance duration of 54972 ms.
Analysis of variance showed that there were significant
differences in both the walking velocity and stance
duration between subjects, however, there were no
significant effects of the shoe condition on these
parameters.
3.1. Ground reaction forces
The vertical ground reaction force showed an impact
peak at 22 ms, and this impact peak was followed by a
second peak at 50 ms for 35 of the 40 subjects (Fig. 1A).
The ground reaction forces then showed large and broad
peaks which are characteristic of walking. Superimposed
on this characteristic pattern there were oscillations of
small magnitude and high frequency (>300 Hz). Parameters quantifying the impact peak were calculated after
these high-frequency oscillations were filtered and are
shown in Table 2.
Analysis of variance of the GRF parameters showed
that there were significant effects of the shoe condition
on the loading rate (15.9% decrease for the insert
condition), and the effective input frequency (9.4%
decrease), however there were no significant effects of
the shoe condition on the magnitude of the impact peak.
3.2. Soft-tissue vibrations
Transient peaks of inertial force occurred in all softtissue groups after heel-strike (e.g. Figs. 2 and 3). The
magnitude of the peak forces (Table 3) varied with their
direction relative to the leg segment. When walking with
the control condition, the mean vibration frequencies
weighted by the magnitude of the peak inertial forces
were 26.1371.02, 24.2671.28, 38.5471.16 and
28.6271.03 Hz (N ¼ 40) for the quadriceps, hamstrings,
tibialis anterior and triceps surae soft-tissue groups,
respectively.
ARTICLE IN PRESS
J.M. Wakeling et al. / Journal of Biomechanics 36 (2003) 1761–1769
1764
There were significant effects of the insert condition
on the maximum inertial loading rate for 10 of the
possible 12 tissue-direction combinations (Table 3) with
a reduction in the maximum inertial loading rate with
the insert condition (e.g. 23.3% for the axial direction in
the tibialis anterior). There were significant effects of the
insert condition on the maximum inertial force for five
of the possible 12 tissue-direction combinations (reduction for the insert condition; greatest reduction of 19.5%
for the axial direction in the tibialis anterior). There
were significant effects of the insert condition on the
vibration frequency for four of the possible 12 tissuedirection combinations (reduction for the insert condition; greatest reduction of 16.2% for the axial direction
in the hamstrings).
GRF [kN]
3.3. Myoelectric activity
0
200
GRF [kN]
400
600
Time [ms]
(A)
1
0
50
Time [ms]
(B)
GRF [kN]
The insert condition resulted in changes to the
myoelectric activity for all four muscles tested (Fig. 4).
Analysis of variance showed that there was no
significant effect of the shoe condition for the total
intensity for the rectus femoris in both the 50 ms
windows before and after heel-strike. Significant effects
of the shoe condition were observed for the total
intensity for the biceps femoris, tibialis anterior and
lateral gastrocnemius (increases in the total intensity
with the insert condition; Fig. 4).
1
100
1
0
200
400
600
Time [ms]
(C)
Fig. 1. Vertical ground reaction force (GRF) during one stance phase
of walking (A). The time around heel-strike is shown at a larger scale
in B. Mean and standard error of sample mean of the vertical GRFs
for 30 trials (C). Raw traces are shown in A and B, and filtered traces
are used for B and C.
Fig. 2. Inertial forces in the hamstrings for a 57 kg subject. Traces are
shown for the control condition (black lines) and insert condition (grey
lines), as mean7SEM (N ¼ 240). Heel-strike occurred at a time of 0.
Table 2
Parameters describing the impact peak of the vertical ground reaction force
Condition
Loading rate, F’GRF;max (kN s 1)
Impact force, FGRF;max (kN s 1)
Time to peak force tGRF (ms)
Input frequency, fGRF (Hz)
Control
Insert
63.8570.67
53.7070.57
1.03670.005
1.03670.005
22.2370.16
22.7070.19
34.8370.21
31.5770.21
Values are given as mean 7SEM (N ¼ 1192).
ARTICLE IN PRESS
J.M. Wakeling et al. / Journal of Biomechanics 36 (2003) 1761–1769
Fig. 3. Inertial forces in the triceps surae for a 57 kg subject. Traces are
shown for the control condition (black lines) and insert condition (grey
lines), as mean7SEM (N ¼ 240). Heel-strike occurred at a time of 0.
ANOVA results showed the only significant decreases
in the high-frequency myoelectric activity to occur at
40 to 30 ms and 10 to 0 ms for the rectus femoris,
and for 50 to 30 ms for the tibialis anterior (Fig. 4).
All other significant effects of shoe condition on the
myoelectric frequency at the high- and low-frequency
bands were for increases with the insert condition. The
greatest changes in myoelectric activity occurred for the
lateral gastrocnemius muscle (24% increase extending
from 50 to +50 ms). The biceps femoris showed
significant shoe increases in myoelectric activity which
reached 15% for the interval 20 to +20 ms. The
tibialis anterior showed a gradation from decreased
activity before heel-strike to increased activity after heelstrike, with the change from decreasing to increasing
intensity occurring approximately 20 ms later for the
high- than for the low-frequency band. The shoe
condition showed little significant effect on the myoelectric activity from the rectus femoris.
4. Discussion
4.1. Limitations to the experimental design
Muscle force production during walking changes
throughout a stride. The frequency and damping
1765
coefficients of the soft-tissues change with muscle force
(Wakeling and Nigg, 2001a) and, therefore, will also be
expected to change throughout the stride. If dynamic
muscle force cannot be accurately predicted from
myoelectric activity, then so too the frequency and
damping coefficients cannot be accurately modelled
throughout a stride. The purpose of this study was to
investigate the soft-tissue vibrations immediately following heel-strike and so the soft-tissue vibrations were
characterized by their inertial loading rate, peak inertial
force and effective frequency. These measures are taken
directly from the acceleration traces, and therefore can
be made without invoking assumptions about the
muscle-force-dependent changes in the vibrations which
would have to be made for more complex modelling.
The high- and low-frequency bands used for myoelectric analysis in this study (Table 1) were developed to
have short time resolutions (o10 ms), and to resolve the
frequency bands where distinct myoelectric signals have
previously been observed in man (Wakeling et al.,
2001a). The short time resolutions were necessary to
minimize the effects of movement artefacts related to the
heel-strike impact from the measured myoelectric
activity. We can be confident that the resolved signal
before heel-strike using the two-frequency band approach is independent of impact related artefacts. The
presented results were similar to myoelectric intensities
calculated using pooled high- and low-frequency bands
(wavelets 2–3 and 6–8 from the filter-bank of 11
wavelets; time resolutions o40 ms), but confirm that
changes in muscle pre-activation are a real effect.
4.2. Soft-tissue resonance
The lower extremities experienced oscillating input
forces (the ground reaction force) during walking
(Fig. 1). The high-frequency oscillations measured in
the ground reaction force (>300 Hz) are likely due to
the resonance of the force plate and had frequencies an
order of magnitude hi …
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