Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
Title: Achilles tendon length changes during walking in long-term diabetes patients
Neil J. Cronin PhD1,2, Jussi Peltonen MSc2, Masaki Ishikawa PhD3, Paavo V. Komi PhD2,
Janne Avela PhD2, Thomas Sinkjaer PhD1 & Michael Voigt PhD1
1
Center for Sensory-Motor Interaction, Department of Health Science and Technology, Aalborg
University, Denmark;
2
Neuromuscular Research Centre, Department of Biology of Physical Activity, University of
Jyväskylä, Finland;
3
Department of Health and Sport management, Osaka University of Health and Sport Sciences,
Osaka, Japan
Running head: Diabetic tendon behaviour during walking
Address for correspondence:
Neil J. Cronin
Fredrik Bajers Vej 7 E1-121,
Aalborg East,
DK-9220,
Denmark.
njcronin@hst.aau.dk
Phone: +45 9940 8775
Fax: +45 9815 4008
Abstract word count: 238
Main text word count: 3950
Number of figures and tables: 4 figures, 2 tables
1
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
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Abstract
2
3
Background: Diabetes leads to numerous side effects, including an increased density of collagen
4
fibrils and thickening of the Achilles tendon. This may increase tissue stiffness and could affect
5
stretch distribution between muscle and tendinous tissues during walking. The primary aim of this
6
study was to examine stretch distribution between muscle and tendinous tissues in the medial
7
gastrocnemius muscle-tendon unit in long-term diabetes patients and control subjects during
8
walking.
9
Methods: Achilles tendon length changes were investigated in 13 non-neuropathic diabetes patients
10
and 12 controls, whilst walking at a self selected speed across a 10m force platform.
11
Electromyographic activity was recorded in the medial gastrocnemius, soleus and tibialis anterior
12
muscles, goniometers were used to detect joint angle changes, and ultrasound was used to estimate
13
tendon length changes.
14
Findings: Achilles tendon length changes were attenuated in diabetes patients compared to controls,
15
and were inversely correlated with diabetes duration (r = -0.628; P<0.05), as was ankle range of
16
motion (r = -0.693; P<0.01). Tendon length changes were also independent of walking speed (r = -
17
0.299; P = 0.224) and age (r = 0.115; P = 0.721) in the diabetic group.
18
Interpretation: Stretch distribution between muscle and tendon during walking is altered in diabetic
19
patients, which could decrease walking efficiency, a factor that may be exacerbated with increasing
20
diabetes duration. Diabetes-induced changes in mechanical tendon properties may be at least partly
21
responsible for attenuated tendon length changes during walking in this patient group.
22
23
24
25
26
27
Keywords: Diabetes mellitus, tendon, stretch reflex, muscle-tendon interaction, human walking
2
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
1
Introduction
2
3
Diabetes mellitus (DM) can lead to numerous side effects that have functional consequences for
4
movement, such as deterioration in the function of large afferent nerve fibres (e.g. Muller et al.,
5
2008), particularly the type Ia and II afferents originating in the muscle spindles (Nardone and
6
Schieppati, 2007; Nielsen et al., 2004). As afferent receptors from muscle spindles are thought to
7
contribute to the ongoing muscle activity during walking (e.g. af Klint et al., 2008; Sinkjaer et al.,
8
2000), changes in their morphology due to diabetes could affect motor control during walking (e.g.
9
Muller et al., 2008). Furthermore, as DM patients generally exhibit a decreased ability to rapidly
10
produce force (Nielsen et al., 2004), the ability to recover from a balance disturbance during gait
11
may be compromised, thus contributing to the increased fall risk reported in DM patients (e.g.
12
Morley, 2007).
13
14
During walking, DM patients exhibit biomechanical deficits compared to age-matched healthy
15
subjects. For example, slower walking speeds, shorter strides and greater co-contraction of agonist
16
and antagonist muscles at the ankle and knee joints have all been reported in DM patients and
17
patients with peripheral neuropathy, a nervous disorder often associated with DM (Kwon et al.,
18
2003; Mueller et al., 1994). Although the kinematics and kinetics of diabetic gait are well
19
documented, very little is known about the mechanical behaviour of muscle and tendinous tissues
20
during gait in DM patients. Structural abnormalities have been observed in the Achilles tendon of
21
DM patients, including an increased density of collagen fibrils, as well as thickening and
22
vascularisation of the Achilles tendon (Giacomozzi et al., 2005; Grant et al., 1997; Ji et al., 2009).
23
This may lead to increased tissue stiffness, and thus contribute to a loss of joint mobility. During the
24
stance phase of human walking, muscle-tendon units (MTU) of the lower limb are naturally
25
stretched (e.g. Ishikawa et al., 2005; Lichtwark and Wilson, 2006). This stretch is distributed
3
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
1
between muscle and tendinous tissues depending on their relative stiffnesses (Rack and Westbury,
2
1984). Consequently, an increase in tendon stiffness may increase the stretch transferred to the
3
muscle fibres during walking, which may in turn decrease movement efficiency by decreasing
4
tendon elastic energy storage. As tendon disorganisation has been suggested to progressively
5
increase with increasing diabetes duration (Batista et al., 2008), movement efficiency may also
6
progressively decrease with increasing diabetes duration.
7
8
Based on the aforementioned neural and mechanical deficits observed in DM patients, one would
9
expect tendon lengthening to be decreased during gait when compared to control subjects. This
10
would change the pattern of stretch distribution within the MTU, and could have important
11
functional consequences for muscle force production, afferent feedback and movement efficiency.
12
The primary purpose of this study was to examine stretch distribution between muscle and
13
tendinous tissues in the medial gastrocnemius (MG) MTU in long-term DM patients and control
14
subjects during walking. An additional aim was to examine whether associations existed between
15
diabetes duration and specific stretch, torque and gait parameters. It was hypothesised that DM
16
patients would exhibit decreased rate of torque development and short latency stretch reflex (SLR)
17
responses, as observed previously (Nielsen et al., 2004). During walking, it was anticipated that DM
18
patients would exhibit attenuated tendon stretch responses compared to control subjects, and that
19
this would be exacerbated as the duration of diabetes increased.
20
21
Methods
22
23
Subjects
24
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Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
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To recruit DM patients, an advertisement was placed in a local publication. In total, 26 patients
2
volunteered, 10 of whom did not meet the patient criteria. Three others withdrew from the
3
measurements due to illness or injury, resulting in the collection of data from 13 patients (Table 1).
4
Criteria for patient selection were: ability to comfortably walk 10 metres approximately 10 times
5
with intermittent rest; diagnosis of DM; ability to walk independently without an assistive device;
6
ability to lie supine; a minimum ankle range of motion of 40° (combined dorsi- and plantar flexion,
7
which was determined prior to the measurements); unimpaired vision and hearing; and diabetes
8
duration >10 years. Subjects were excluded if they had severe orthopedic abnormalities, severe
9
neurological disorders, previous cerebrovascular accident, a history of plantar ulceration or previous
10
lower extremity amputation. The mean duration of diabetes in the DM group was 31±12 years
11
(range 15-54). Patients with a long duration of diabetes were recruited to ensure a high frequency of
12
late diabetic complications. The level of neuropathy was assessed using the neuropathy disability
13
score (NDS; Young et al., 1993) and neuropathy was defined as NDS > 5. All DM patients included
14
in the study had an NDS score of ≤ 4. To recruit control subjects, an advertisement was placed in a
15
local newspaper. In total, 32 subjects volunteered, and 12 were selected to enable age, height and
16
body mass to be matched as closely as possible between groups (Table 1). Control subjects had no
17
history of neuromuscular or skeletal disorders that could have influenced gait. A brief questionnaire
18
was used to obtain medical and demographic data from all subjects. Patients and control subjects
19
were all routinely active but did not regularly participate in sports. Prior to testing, the procedures
20
were explained thoroughly, and all subjects provided written informed consent. All procedures
21
conformed with the declaration of Helsinki, and the experiments were approved by the local ethics
22
committees of the University of Jyväskylä and the Central Hospital of Central Finland, respectively.
23
24
Study protocol
25
5
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
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Prior to the measurements, resting Achilles tendon length was determined in the right leg of all
2
subjects. For this procedure, subjects lay supine with a fully extended knee and an ankle angle of
3
90° (neutral position). The point at which the muscle and outer tendon converged was visually
4
identified using ultrasound, and marked on the skin. The distance between this point and the distal
5
insertion point (also confirmed by ultrasound) was defined as resting tendon length.
6
7
In all testing conditions, electromyographic (EMG) activity was recorded in the MG, soleus (SOL)
8
and tibialis anterior (TA) muscles of the right leg using bipolar surface electrodes (720, AMBU,
9
Denmark) with a diameter of 5mm and an inter-electrode distance of 2 cm. Before electrode
10
placement, the skin was shaved, abraded and cleaned with alcohol to maximise EMG signal quality.
11
The electrodes were positioned as close to the respective muscle mid-belly as possible without
12
interfering with the ultrasound probe position (see below).
13
14
Stretch and maximum torque trials
15
16
In patients exhibiting signs of neurological impairment, stretch reflex amplitude and latency have
17
been shown to be smaller and longer, respectively, compared to control subjects (Nielsen et al.,
18
2004). To determine whether this was also the case for the present subject group, all of whom were
19
classified as non-neuropathic, a series of rapid dorsiflexion stretches were performed. Subjects were
20
seated in an ankle dynamometer, with the hip (120°), knee (180°) and ankle (90°) angles fixed (see
21
Figure 1). Two straps were used to attach the foot to the dynamometer pedal, and the thigh was
22
strapped to the seat to minimise leg movement. The upper body was also strapped to the upper part
23
of the seat. Ten passive dorsiflexion stretches were induced (3°; 120°/s), with a minimum of 15s
24
between consecutive trials. Throughout these trials, subjects completely relaxed the muscles of their
6
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
1
right leg, and EMG activity was continuously monitored. Any trials showing deviation from the
2
baseline EMG in any of the examined muscles prior to stretch were rejected.
3
4
Maximal voluntary contractions (MVC) were performed with the ankle plantar- and dorsiflexors. In
5
all trials, subjects were instructed to develop maximum torque as quickly as possible. At least three
6
contractions were performed for each muscle group in a random order, with rest periods of 2-3
7
minutes between trials. Each trial required the maximal moment to be maintained for 2-3s. The trial
8
exhibiting the highest peak moment value was selected as the MVC. Prior to all stretch and MVC
9
trials, the ankle axis of rotation was carefully aligned with that of the ankle dynamometer. The order
10
of the stretch and MVC trials was randomised.
11
12
Walking trials
13
14
During walking, an ultrasonographic device (Alpha-10; 7.5 MHz probes; Aloka, Japan) operating at
15
100 frames per second was used to measure the displacement of the MG muscle-tendon junction
16
(MTJ), which was combined with the estimated displacement of the distal Achilles tendon to give
17
an estimate of Achilles tendon length change. To position the probe accurately over the MTJ, the
18
medial and lateral borders of the MG muscle were identified, and the midpoint between the two
19
borders was marked on the skin. Sagittal-plane scans were then taken at the insertion point of the
20
Achilles tendon, which was also marked on the skin. A straight line was drawn between the two
21
points, and this line was assumed to be the operating axis of the muscle–tendon unit (MTU). The
22
MTJ was identified as the intersection between the most distal part of the MG muscle and the outer
23
tendon along the MTU operating axis. The probe was secured over the skin surface with a custom-
24
made support device to minimise any probe movement relative to the skin. Echoabsorptive markers
25
were also positioned between the probe and the skin within view of the ultrasound image to confirm
7
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
1
that the probe did not move relative to the skin. The total additional weight due to the ultrasound
2
probe was approximately 150g. The reliability of the ultrasound method of estimating MTJ
3
displacement was determined by calculating the coefficient of variation between three different
4
trials for each subject during walking. The mean value was 4±2%, which is similar to values
5
reported previously during walking (Cronin et al., 2009a, 2009b). Goniometers (University of
6
Jyväskylä, Finland) were attached to the lateral side of the ankle and knee joints in order to monitor
7
joint angle changes during gait. Subjects were instructed to walk at a self selected speed across a
8
10m walkway, which was instrumented with two rows of force platforms capable of detecting
9
ground reaction forces from both feet along the entire length of the walkway (Figure 2). All subjects
10
wore low-heeled (less than 2.5 cm) shoes with a non-rockered sole. Each subject had several
11
practice trials. Subsequently, joint angle, ground reaction force (GRF), EMG and ultrasound data
12
were recorded from 8-12 trials per subject. A digital pulse was used to synchronise the kinetic,
13
kinematic, EMG and ultrasound data. Subjects were allowed to rest as needed between trials. The
14
order of the two broad test conditions (stretch/MVC and walking) was randomised, and all data
15
were collected by the same two investigators.
16
17
Data acquisition and analysis
18
19
For all conditions, EMG signals were amplified, band-pass filtered (10-1000 Hz), rectified and then
20
low-pass filtered at 40 Hz. All EMG, goniometer and torque/GRF signals were sampled at 2 kHz
21
and stored for later analysis. For the stretch trials, data from 10 trials were averaged for each
22
subject, and SLR amplitude and latency were determined from the averaged EMG traces for each
23
subject and for SOL and MG. To detect the onset latency of the SLR response, a window was
24
defined from 20 to 60 ms after the stretch onset, which incorporates the physiological range for the
25
onset of the SLR (e.g. Grey et al., 2004). Within this window, the onset of the SLR was determined
8
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
1
as the moment at which the EMG signal exceeded 2 standard deviations of the mean pre-stimulus
2
background EMG activity, averaged over 1 s. The amplitude of the SLR was then measured by
3
subtracting mean pre-stimulus EMG from the peak EMG value within a 30 ms window starting at
4
the SLR onset. As the medium latency component of the stretch reflex was not always clearly
5
identifiable, this component was not analysed. Maximal torque in response to stretch was
6
determined from the averaged torque trace.
7
8
For the MVC trials, maximal torque was calculated from the stable portion of the torque curve over
9
a 1s epoch from the trial exhibiting the highest torque value. In the same 1s epoch, the mean
10
processed EMG amplitude was calculated, and used to normalise the EMG data obtained during
11
walking (MG and SOL were normalised to plantar flexion MVC, and TA was normalised to
12
dorsiflexion MVC). This method of normalization was chosen to provide a crude estimate of the
13
degree of muscle activation required during gait (Burden et al., 2003), enabling a group comparison
14
to be made for each muscle. Similarly, SLR amplitudes in MG and SOL were normalised to plantar
15
flexion MVC.
16
17
For the walking trials, joint angle, GRF and EMG data were averaged for 50-60 steps per subject,
18
and GRF and EMG signals were then normalised to body mass and MVC, respectively. For the
19
ultrasound analysis, data from three trials were analysed and averaged. To select the trials to be
20
analysed, the three trials where the ankle range of motion throughout the stance phase was closest to
21
that of the mean ankle range of motion were selected, to ensure that these trials were representative
22
of the mean response. In each ultrasound image, the MTJ was identified, and this point was tracked
23
continuously throughout the stance phase. As this method only provides information about the
24
movement of the proximal end of the tendon, Achilles tendon moment arms based on previous data
25
during walking (Rugg et al., 1990) were combined with measured ankle joint angle changes to
9
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
1
determine the rotation of the distal tendon, thus enabling the actual tendon length change to be
2
estimated. Tendon length change was normalised to the length at the point of ground contact.
3
4
Statistics
5
6
Prior to analysis, data were tested for normality based on a Q-Q plot. To assess group differences,
7
independent samples t-tests (normal distribution) or Mann-Whitney U tests (abnormal distribution)
8
were used. To determine correlations between variables, Pearson’s (normal distribution) or
9
Spearman’s (abnormal distribution) rank correlation coefficients were used. For all statistical tests,
10
the level of significance was set at P < 0.05. Results are presented as means (SD).
11
12
Results
13
14
In 3 of the DM patients, it was not possible to elicit clear SLR responses in MG or SOL. As
15
hypothesised, normalised SLR amplitudes were lower in DM patients compared to controls.
16
Furthermore, in response to rapid stretches with no muscle pre-activation, as well as during MVC,
17
DM patients showed a decreased rate of torque development. SLR and MVC data for both groups
18
are shown in Table 2.
19
20
In the walking trials, the inter-trial coefficient of variation for walking speed was 3.4% in the
21
controls and 5.3% in the DM group. The controls walked significantly faster than the patients (1.27
22
(0.18) m/s vs. 1.06 (0.24) m/s; Independent t; P < 0.05), and exhibited a shorter mean stride
23
duration (1.00 (0.10) s vs. 1.12 (0.12) s; Independent t; P < 0.05). Stance phase duration did not
24
differ statistically between groups (722 (83) ms for controls vs. 800 (103) ms for patients;
25
Independent t; P = 0.413), but the stance phase occupied a larger proportion of the total stride in the
10
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
1
patients (63 (4) % vs. 60 (2) %; Independent t; P < 0.05). Between group differences in gait related
2
parameters throughout the stance phase are shown in Figure 3. Peak tendon length change (relative
3
to the length at ground contact) in the stance phase was not associated with walking speed in the
4
controls (Pearson; r = -0.056, P = 0.862) or the patients (Pearson; r = -0.299, P = 0.224), nor was it
5
associated with the range of ankle rotation during stance in either group (Spearman; r = -0.209, P =
6
0.537 and r = 0.305, P = 0.335 in controls and patients, respectively).
7
8
In the patient group, the duration of diabetes did not significantly correlate with normalised SLR
9
amplitude (MG: Spearman; r = 0.257, P = 0.623; SOL: Pearson; r = 0.019, P = 0.923) or latency
10
(MG: Spearman; r = -0.305, P = 0.248; SOL: Spearman; r = -0.396, P = 0.125). Similarly, no
11
correlation was observed between diabetes duration and MVC or stretch-induced torque parameters
12
(Pearson; r values between 0.171 and 0.410, P > 0.05). During walking, diabetes duration was
13
inversely correlated with peak tendon length change (Pearson; r = -0.628, P < 0.05), showing that
14
increased diabetes duration was associated with greater decrements in tendon lengthening (Figure
15
4). Diabetes duration was negatively correlated with the range of ankle joint rotation during stance
16
(Pearson; r = -0.693, P < 0.01), but was not correlated with the range of knee joint rotation
17
(Pearson; r = -0.083, P = 0.798). Neither the duration of diabetes (Pearson; r = -0.117, P = 0.703)
18
nor the range of ankle joint rotation (Pearson; r = 0.272, P = 0.369) correlated with walking speed.
19
Diabetes duration was also unrelated to age (Pearson; r = 0.115, P = 0.721).
20
21
Discussion
22
23
The main findings of this study were that Achilles tendon length changes during walking were
24
attenuated in long-term diabetic patients compared to control subjects. Although DM patients
25
walked slower than control subjects, no differences were observed in mean ankle or knee
11
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
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trajectories during the stance phase. As there were no differences between groups in shank length
2
(41 (4) versus 40 (3) cm) or resting tendon length (18.4 (3) versus 19 (3) cm), the data suggest that
3
MTU length changes during stance were similar between groups. Therefore, the smaller tendon
4
length changes observed in the DM group may be at least partly attributable to changes in tendon
5
properties, as previously reported (Giacomozzi et al., 2005). Peak tendon lengthening also
6
decreased with increasing diabetes duration. Therefore, changes in tissue properties due to diabetes
7
may be progressive (Batista et al., 2008), even in the absence of peripheral neuropathy. Similar
8
MTU length changes but smaller tendon length changes imply a greater stretch of the muscle
9
fascicles and aponeurosis in the DM group. These changes in stretch distribution could decrease
10
elastic energy storage in the tendon, and increase the amount of work performed by the muscle
11
fibres, which would decrease walking efficiency in this population (e.g. Sawicki et al., 2009). The
12
hypothesis that the muscle fibres are required to perform more work may be supported by the
13
finding that relative muscle activation was higher in TA and similar in MG and SOL in the DM
14
group compared to controls. As the patients walked slower, they actually required greater relative
15
activation of all muscles to achieve a given walking speed.
16
17
Within the DM group, ankle joint rotation during the stance phase decreased as diabetes duration
18
increased. This finding may support the hypothesis that changes in structural tissue properties
19
related to DM contribute to decreased joint mobility (Delbridge et al., 1985, 1988; Hajrasouliha et
20
al., 2005). However, as no differences were observed in mean ankle or knee trajectories between
21
groups, it seems that joint mobility may only be compromised in very long term diabetes patients.
22
Nonetheless, these data clearly show that increased diabetes duration is associated with decreased
23
tendon lengthening during walking. Previous studies have shown that in healthy individuals, the
24
Achilles tendon is stretched during stance, storing elastic energy, and then rapidly recoils (and
25
returns elastic energy) during pushoff, and this helps humans to move efficiently (e.g. Alexander
12
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
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and Bennet-Clark, 1977; Ishikawa et al., 2005). Data from the present study suggest that in DM
2
patients, this mechanism is less effective, particularly in the terminal stance phase (70-100%),
3
where ankle strength and mobility have their greatest effect (Mueller et al., 1994).
4
5
In the present study, DM patients showed lower SLR amplitudes and a lower amplitude and slope
6
of the torque response to stretch in the plantar- and dorsiflexors. Maximal voluntary torque
7
amplitude did not differ between the groups, but the slope of the torque response was lower in the
8
patients. Similar observations have been reported previously after electrically evoked contractions
9
of the soleus muscle (Nielsen et al., 2004). The latter study also reported longer SLR latencies in the
10
SOL muscle of DM patients, which was not observed here, although there was a trend towards
11
longer latencies in MG and SOL. As DM patients generally walk slower than control subjects, a
12
decreased ability to produce force quickly may not be a major limitation during normal undisturbed
13
gait. However, in response to balance disturbances during gait, an increase in the time taken for
14
force production in the plantar- and dorsiflexors could induce a delay in the mechanical response,
15
which in combination with decreased function of large afferents, could decrease the ability to
16
compensate for balance disturbances (e.g. Dingwell et al., 1999; Gutierrez et al., 2001), particularly
17
as large afferents are thought to contribute to recovery from such disturbances (e.g. Sinkjaer et al.,
18
2000). These factors are likely to contribute to increased fall risk in DM patients. No clear
19
relationships were observed between diabetes duration and stretch or torque responses, suggesting
20
that changes in these parameters may be independent of diabetes duration. However, the possibility
21
cannot be excluded that the relatively small sample size in this study prevented a clear relationship
22
from emerging.
23
24
Based on the methodology employed, the muscle-tendon junction was assumed to only shift in the
25
scanning plane. Medio-lateral and/or antero-posterior displacement would thus result in minor
13
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
1
measurement errors. Moment arm lengths were also estimated based on previous data obtained from
2
younger subjects (Rugg et al., 1990), which could introduce some errors in tendon length
3
estimation. Since Achilles tendon moment arms do not differ between young and elderly subjects
4
(Morse et al., 2005), this error is likely to have been minimal. Nonetheless, as changes in muscle
5
thickness during contraction can affect moment arm lengths (Maganaris et al., 1998), and muscle
6
thickness was not measured in this study, the possibility cannot be excluded that this parameter
7
influenced our data. It should also be noted that tendon length was not directly measured. Although
8
direct methods have been used to study muscle-tendon interaction in animals (e.g. Daley et al.,
9
2009), this method is highly invasive and has not been successfully applied in humans. Similarly,
10
structural properties of the Achilles tendon were not measured in this study. However, tendon
11
disorganisation has been reported to be present in diabetic individuals and absent in age-matched
12
controls (Batista et al., 2008). The fact that the right leg was measured for all subjects may be a
13
limitation, as leg dominance differed between subjects. Due to the cable attached to the ultrasound
14
probe, which could have inhibited natural walking if attached to the left leg, this was unavoidable. It
15
could also be argued that it is difficult to compare groups walking at different speeds. However,
16
since DM patients naturally walk slower than controls, any efforts to match walking speeds would
17
require one subject group to walk at an unnatural speed, which could alter various parameters
18
including balance, patterns of muscle activation and muscle-tendon length changes (see Cronin et
19
al., 2009b). Such changes would render a comparison between groups inappropriate. Furthermore,
20
knee and ankle joint kinematics were similar between groups, as were shank lengths, suggesting
21
that MTU length changes were also similar. As one aim of this study was to examine MTU stretch
22
distribution, these findings validate the use of unmatched walking speeds in this study. Finally, the
23
small sample size in this study is also a limitation, albeit unavoidable due to the specificity of the
24
inclusion criteria.
25
14
Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
1
Conclusions
2
3
In the human lower limb, Achilles tendon length changes during walking are attenuated in long-
4
term diabetic patients compared to control subjects. This difference cannot solely be attributed to
5
differences in walking speed or joint kinematics between the groups, and appears to be exacerbated
6
by increased diabetes duration. These changes are likely to decrease the capacity of the tendon to
7
store elastic energy, and result in a larger stretch of the muscle fascicles and/or aponeurosis.
8
Movement efficiency may thus be compromised in this population, and this may worsen as the
9
duration of diabetes increases. As DM patients also exhibited a decreased ability to rapidly produce
10
force, and impaired short latency stretch reflexes, the ability to overcome unexpected balance
11
disturbances during gait may be compromised in DM patients, even in the absence of peripheral
12
neuropathy.
13
14
Acknowledgements
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This study was financially support by an International Travel grant from the International Society of
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Biomechanics. The authors gratefully acknowledge the financial support of The Obel Family
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Foundation and The Spar Nord Foundation, as well as the administrative assistance of Katja
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Pylkkänen.
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Figure legends
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Journal: Clinical Biomechanics, vol. 25 No. 5, June 2010 (476-482) DOI: 10.1016/j.clinbiomech.2010.01.018
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Figure 1. Experimental setup for the stretch and MVC trials. A: Schematic of the subjects’ joint
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configurations whilst sitting in the ankle dynamometer. B: A fully instrumented subject seated in
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the ankle dynamometer.
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Figure 2. Experimental setup for the walking trials. A: One subject from the DM group. The
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ultrasound device was placed on a carriage and pushed alongside the subject while they walked
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along the force platform. B: Schematic of the equipment used during the walking trials.
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Figure 3. Changes in gait parameters throughout the entire stance phase. A: GRF normalised to
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body mass (Vertical force: thin traces; Antero-posterior force: thick traces); B: Ankle trajectory; C:
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Knee trajectory; D: MG EMG; E: TA EMG; F: Achilles tendon length relative to length at ground
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contact. In all cases, data were averaged from 13 patients and 12 controls. * and ** denote a
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significant difference between groups across the entire stance phase at P < 0.05 and P < 0.01,
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respectively. Soleus EMG is not shown since no differences were observed in relative activation
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between groups in this muscle.
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Figure 4. Correlations between diabetes duration and specific gait parameters. A: Peak Achilles
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tendon lengthening throughout the entire stance phase. B: Mean walking speed. C: Range of ankle
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joint rotation during the stance phase. In all cases, n = 13.
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