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Delayed	onset	of	vastii	muscle	activity	in
response	to	rapid	postural	perturbations
following	eccentric	exercise:	A...
Article		in		British	Journal	of	Sports	Medicine	·	August	2013
DOI:	10.1136/bjsports-2012-092015	·	Source:	PubMed
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Delayed onset of vastii muscle activity in response
to rapid postural perturbations following eccentric
exercise: a mechanism that underpins knee pain
after eccentric exercise?
Nosratollah Hedayatpour,1,2
Deborah Falla3,4
1
Department of Physical
Education and Sport Science,
University of Bojnord, Bojnord,
Iran
2
Department of Health Science
and Technology, Centre for
Sensory-Motor Interaction
(SMI), Aalborg University,
Aalborg, Denmark
3
Department of
Neurorehabilitation
Engineering, Bernstein Center
for Computational
Neuroscience, University
Medical Center Göttingen,
Georg-August University,
Göttingen, Germany
4
Pain Clinic, Center for
Anesthesiology, Emergency and
Intensive Care Medicine,
University Hospital Göttingen,
Göttingen, Germany
Correspondence to
Dr Deborah Falla,
Department of
Neurorehabilitation
Engineering, Bernstein Center
for Computational
Neuroscience, University
Medical Center Göttingen,
Georg-August University,
Von-Siebold-Str. 4, Göttingen
37075, Germany;
deborah.falla@bccn.uni-
goettingen.de
Received 21 November 2012
Revised 5 April 2013
Accepted 17 June 2013
To cite: Hedayatpour N,
Falla D. Br J Sports Med
Published Online First:
[please include Day Month
Year] doi:10.1136/bjsports-
2012-092015
ABSTRACT
Background Appropriate timing of activity of the
vastus medialis obliqus (VMO) and vastus lateralis (VL)
muscles is a key factor for proper tracking of the patella
in the trochlear groove during knee extension. This study
investigates the relative timing of activation of the VMO
and VL muscles during unexpected perturbations
performed before and after eccentric exercise.
Methods Surface electromyography signals were
recorded from the VMO and VL muscles of the right leg
in 11 healthy men during rapid postural perturbations
performed at baseline, immediately after eccentric
exercise of the quadriceps, and at 24 and 48 h after
exercise. Participants stood on a moveable platform
during which eight randomised postural perturbations
were performed (4 repetitions of 2 perturbation types:
8 cm forward slides, 8 cm backward slides).
Results Before the eccentric exercise, the onset of VMO
activity was significantly earlier than the VL muscle
(average for both forward and backward perturbations:
VMO 39.0±7.1 ms; VL 43.7±7.9 ms). However, the onset
of VMO activity was significantly later compared with VL
muscle immediately after eccentric exercise and this
remained 24 and 48 h after eccentric exercise (average
across all postexercise sessions and perturbation directions:
VMO 72.3±11.1 ms; VL 56.0±8.2 ms; p<0.05).
Conclusions The onset of VMO–VL activity in response
to rapid destabilising perturbations is altered immediately
after eccentric exercise and during eccentric exercise-
induced muscle soreness up to 48 h later. These
observations may help explain the high prevalence of knee
disorders after high intensity eccentric exercise.
INTRODUCTION
The ability of the quadriceps femoris to rapidly sta-
bilise the patella during an unexpected knee per-
turbation is dependent on the onset and amplitude
of muscle activation.1 2
The onset of vastus media-
lis obliqus (VMO) activity typically occurs earlier
than that of the vastus lateralis (VL) or at least syn-
chronously during the postural perturbations,3
stair-stepping4
and patella tendon reflex reac-
tions.2 5 6
Consequently, delayed onset of the
VMO compared with VL activity has frequently
been reported as a potential cause for patellar mal-
tracking and development of pain.7
From an anatomical perspective, the appropriate
timing of VMO activation relative to the VL
muscle is necessary to compensate for the strong
lateral pull of the VL muscle during knee exten-
sion. It has been hypothesised that changes in the
onset of VMO activation may contribute to an
imbalance in muscle forces and, as a consequence,
lead to lateral maltracking of the patella.8 6
An
excessive lateral tracking of the patella could induce
localised stresses that are transmitted through the
cartilage with the potential to excite nociceptors in
the subchondral bone, which in turn can result in
patellofemoral pain syndrome (PFPS).9
PFPS is a common complaint in the sporting and
general populations, especially when repetitive lower
limb eccentric loading is frequently performed.10 11
Muscles subjected to eccentric loading become stiff
and sore 24 h after exercise because of the patho-
physiological changes and inflammation at the
injured sites.12 13
Furthermore, in the injured muscle,
neuromuscular responses can be impaired most likely
due to pain,13 14
remodelling of the neuromuscular
junction,15
changes in the proprioceptive function16
and alteration in the muscle fibre membrane proper-
ties.14 17 18
Thus, it may be expected that eccentric
exercise of the quadriceps contributes to a change in
the onset of activation of the VMO and VL muscles
to stabilise the patella during perturbations to the
knee. This knowledge may be relevant for
exercise-related patella disorders that develop follow-
ing unaccustomed exercise. Therefore, in the current
study, we analysed the relative timing of activation of
the VMO and VL muscles during unexpected knee
perturbations performed before and after eccentric
exercise. The type of perturbation used resembles
perturbations that might commonly be encountered
during sport activities.
METHODS
Subjects
Eleven healthy men (age, mean±SD, 24.1±4.1 years,
body mass 73.5±11.2 kg, height 1.77±0.05 m) with
no history of knee injury participated in the study. All
participants were right leg dominant and were not
involved in regular exercise of their knee extensor
muscles for at least 6 months before the experiment.
The study was conducted in accordance with the
Declaration of Helsinki and approved by the Ethics
committee of Nordjylland, Denmark (N 20070019).
All measures were performed at the Center for
Sensory Motor-Interaction, Aalborg University,
Denmark. Participants provided informed written
consent before participation in the study.
Eccentric exercise
Participants performed eccentric exercise on a
KinCom Isokinetic Dynamometer (Chattanooga
Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015 1
Original article
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Group, Tennessee, USA). The exercise protocol consisted of 4
bouts of 25 maximum voluntary eccentric knee extension con-
tractions at a speed of 60°/s between 90° and 170° of knee
extension, with 3 min of rest between each set. During the exer-
cise, visual feedback of force was provided on a screen posi-
tioned in front of the subject, and the subject was encouraged to
maintain maximal force. A load equal to twice the maximal vol-
untary contraction of knee extension was applied during the
eccentric contractions.14
Maximal voluntary contraction (MVC)
of the knee extensors, subjective pain intensity ratings, muscle
circumference, time to task failure for a 50% MVC sustained
isometric knee extension contraction and EMG onset and amp-
litude of the VMO and VL muscles during rapid postural per-
turbations were recorded before, immediately after, and at 24 h
and 48 h after eccentric exercise.
Assessment of muscle pain intensity and thigh
circumference
A 10 cm visual analogue scale (VAS), labelled with end points
on the left (no pain) and right (worst pain imaginable), was
used to assess the perceived pain intensity 24 and 48 h after
exercise. Participants were asked to rate their average pain inten-
sity corresponding to their level of soreness experienced during
daily activities (eg, climbing stairs) since their last visit to
the laboratory (over the last 24 h). If any soreness was indicated,
the subject was asked whether the discomfort was more pro-
nounced in the inner, middle or outer region of the quadriceps.
Thigh circumference was measured using a tape-measure around
the distal portion of the thigh at 10% of the distance between
the superior border of the patella and the anterior superior
iliac spine.
Maximum and sustained knee extension contractions
Participants were asked to perform three maximal isometric
knee extensions on the right (3–5 s in duration) using the
KinCom Isokinetic Dynamometer with the knee and hip in 90°
of flexion with 2 min of rest in between repetitions. Participants
were supported by straps over the right thigh, pelvis and trunk.
Visual feedback of force was provided on a screen positioned in
front of the subject and verbal encouragement to exceed the
previous force level was given. Participants also performed an
isometric knee extension contraction at 50% MVC sustained
until task failure on the KinCom Dynamometer, with the par-
ticipant in the same position as in the maximal voluntary con-
tractions. The submaximal force was relative to the highest
MVC measured on the same day of the test. Task failure was
defined as a drop in torque >5% MVC for more than 5 s after
strong verbal encouragement to the subject to maintain the
target torque. A rest period of ∼20 min was given prior to start-
ing the perturbations.
Postural perturbations
Participants stood with their feet shoulder width apart, with
their right lower limb on a moveable force platform and left
foot on the ground. An oscilloscope connected to a force plat-
form was positioned in front of the participant to monitor
weight bearing. A positioning actuator19
translated the platform
either 8 cm forwards or backwards over 150 ms. Hip joint
motion was restricted by a strap secured around the pelvis and
greater trochanter that was bolted firmly to the wall. The
subject stood comfortably with equal weight on each limb using
the visual feedback on weight bearing. In each direction (for-
wards and backwards), four 3 s trials were collected in which
the plate was triggered to move at a random interval within 3 s.
Participants were unaware of when the plate would be triggered
to move. The order of the direction of platform movement
(forward and backward) was randomised. Surface EMG data
were collected from the VL and VMO muscles during the
perturbations.
Electromyography
Surface electrodes (Ag–AgCl surface electrodes, Ambu
Neuroline, conductive area: 28 mm2
) were placed in bipolar
configuration (interelectrode distance: 2 cm) at a position equal
to 10% of the distance between the medial border (VMO) and
lateral border (VL) of the patella and anterior superior iliac
spine. A reference electrode was placed around the right ankle.
The positions of the electrodes were marked on the skin during
the first session (day 1) so that the locations could be replicated
24 and 48 h after exercise. Surface EMG signals were amplified
(EMG amplifier, EMG-128, OT Bioelettronica, Torino, Italy,
bandwidth 10–500 Hz), sampled at 2048 Hz and stored after
12-bit A/D conversion.
For the submaximal contraction, the average rectified value
(ARV) was calculated for epochs of 1 s during the contraction,
which was sustained until task failure. The values obtained from
the 1 s long epochs in intervals of 10% of the time to task
failure were averaged to obtain one representative value for each
10% interval. For each session, the per cent change in ARV over
time was calculated by subtracting the final value from the initial
value of ARV and dividing by the initial value.
To assess the onset of muscle activity during the postural per-
turbations, surface EMG data were full-wave rectified and band-
pass filtered at 10–350 Hz. Muscle activation onset was defined
based on a threshold that was 3 SDs greater than the baseline,
within a time window of 45 ms after platform movement.
Moreover, the EMG ARV of each muscle was calculated over a
fixed window, which was 200 ms after the onset of plate move-
ment. For each perturbation direction, the muscle activation
onset and ARV obtained over the four trials were averaged to
obtain a representative value. The per cent change in the VMO:
VL onset time was calculated as the difference between the VL
and VMO onset times divided by the VMO onset time. A posi-
tive per cent change in the VMO:VL onset time indicated acti-
vation of the VMO muscle later than the VL muscle. The per
cent change in the VMO:VL activation ratio was also calculated
as the difference between the VL and VMO EMG ARV divided
by the VMO EMG ARV. A negative per cent change in the
VMO:VL activation ratio indicated a lower EMG amplitude of
the VMO muscle compared with the VL muscle.
Statistical analysis
A one-way repeated-measures analysis of variance (ANOVA) was
applied to analyse MVC, time to task failure and thigh circum-
ference with time as the repeated measure. Two-way repeated-
measures ANOVA was used to assess the per cent change of
ARV across the sustained contraction at 50% MVC (per cent
change from the first to the last epoch), with session and muscle
as dependent factors. A three-way ANOVA was applied to assess
changes in muscle onset time from the pre-exercise session
(baseline) to postexercise sessions (immediately after, and at 24
and 48 h) with time, muscle and perturbation direction (back-
ward and forward) as dependent factors. Moreover, a three-way
ANOVA was used to evaluate the change of ARV from baseline
to postexercise (immediately after, and at 24 and 48 h), with
time, muscle and perturbation direction (backward and
forward) as dependent factors.
2 Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015
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Two-way ANOVAs were applied to assess the per cent change
in VMO:VL onset and per cent change in the VMO:VL ampli-
tude ratio from baseline (pre-exercise) to the postexercise ses-
sions with time and perturbation direction as dependent factors.
Finally, a Pearson correlation coefficient was obtained to assess
the relationship between the per cent change in EMG amplitude
and the per cent change in muscle onset across testing
sessions. Pairwise comparisons were performed with the
Student-Newman-Keuls post hoc test when ANOVA was signifi-
cant. The significance level was set at p<0.05 for all statistical
procedures. Results are reported as the mean and SD in the text
and SE in the figures.
RESULTS
One-way repeated-measure ANOVA revealed a significant reduc-
tion in maximum voluntary knee extension force (F=10.5,
p<0.0001) and time to task failure (F=9.7, p<0.0001) after
eccentric exercise. MVC and time to task failure were not signifi-
cantly different between the three postexercise sessions (immedi-
ately after, and at 24 and 48 h, p>0.05). Moreover, pain
intensity increased and pain become more pronounced in the
inner region of the thigh (over the vastus medialis muscle), as
self-reported by the participants at 24 h (5.5±0.7) and 48 h post-
exercise (5.8±0.9). No difference in pain intensity was observed
between 24 and 48 h postexercise. The thigh circumference mea-
sured during the postexercise sessions was also significantly
larger compared with the pre-exercise session measure (p<0.05).
A two-way repeated-measures ANOVA showed a greater per-
centage of decrease in ARV of the EMG (in the final epoch with
respect to the initial epoch) during the postexercise sustained
isometric contractions compared with the pre-exercise condition
(F=7.5, p<0.0001). In all sessions, the VMO muscle showed a
greater reduction in ARV compared with the VL muscle
(F=2.9, p<0.05). The mean and SD of all performance para-
meters are reported in table 1.
Postural perturbations
A three-way repeated-measures ANOVA revealed an interaction
between muscle and time (F=12.4, p<0.001) which showed that
the onset of VMO was significantly earlier than VL muscle in
response to the perturbations performed during the baseline con-
dition (p<0.05). However, the onset of VMO activity was sig-
nificantly later than VL activity immediately after, and at 24 and
48 h after eccentric exercise (p<0.001). This observation was
consistent for both the forward and backward perturbations
(p>0.05). An example of the surface EMG signals detected from
the distal portion of VMO and VL muscles 200 ms after platform
movement is illustrated in figure 1. The per cent change in
VMO:VL onset also showed that the onset of VMO activity
occurred significantly later than VL activity during all postexer-
cise sessions (p<0.01) but not during the pre-exercise condition
(figure 2).
A three-way repeated-measures ANOVA also showed that in
all conditions (before, immediately after, and at 24 and 48 h
after eccentric exercise), the VL muscle displayed greater values
of ARV in response to the postural perturbations compared with
the VMO muscle (F=20.4, p<0.0001). Furthermore, the per
cent change in VMO:VL activation in response to the perturba-
tions performed in the postexercise sessions were significantly
larger than the per cent change in VMO:VL activation observed
in the pre-exercise session (p<0.05; figure 3).
However, the per cent change in VMO:VL activation was not
significantly different between postexercise sessions (p>0.05) or
between the forward and backward perturbations (p>0.05).
Correlation between EMG onset and amplitude
The per cent change in the EMG onset time (average for the VL
and VMO muscles) from the pre-exercise session to the postex-
ercise sessions (average for all postexercise sessions) was com-
pared with the per cent change in EMG ARV (average for the
VL and VMO muscles) from the pre-exercise session to the
postexercise sessions (average for all postexercise sessions). Per
cent change in EMG onset and per cent change in EMG ARV
were negatively correlated (R=−0.23, p<0.05, figure 4), indi-
cating that the increased EMG onset time postexercise was par-
tially associated with decreased muscle activation.
DISCUSSION
An earlier activation of the VMO muscle relative to the VL
muscle has been observed for healthy individuals in normal con-
ditions. This priority of VMO activation may be of particular
importance to optimally track the patella due to the smaller
cross-sectional area of VMO muscle and the predominantly lat-
erally directed force of the VL muscle. This study demonstrates
that the onset of VMO activation was later than that of the VL
during destabilising knee perturbations performed immediately
after, and at 24 and 48 h after eccentric exercise. The results
indicate that eccentric exercise alters the sequence of VMO:VL
onset, which may result in an imbalance of the quadriceps
forces contributing to stabilisation of the patella. Over time, this
may potentially contribute to lateral maltracking of the patella.
Muscle performance
In the current study, participants reported that their quadriceps
muscle was sore 24 and 48 h after eccentric exercise, which
might be related to damage of the contractile elements and con-
nective tissue.20
Signs and symptoms of pain may result from
pathophysiological changes in the muscle fibres. After muscle
fibre injury, phagocyte cell infiltration results in progressive
Table 1 Mean±SD (n=11) for maximal voluntary contraction (MVC), time to task failure, thigh circumference and average rectified value (ARV)
rate of reduction over the sustained contraction at 50% MVC for the VMO and VL muscles
Pre-exercise Immediately after At 24 h postexercise At 48 h postexercise
MVC (N m) 595±45 460±29* 470±31* 475±33*
Task failure (s) 85.5±23.6 40.7±14.5* 45.8±19.2* 44.2±16.8*
Thigh circumference (cm) 41.3±2.9 42.1±3.2* 42.3±3.1* 42.2±2.9*
VMO ARV (mV) 7.2±10.3% −35.±14.8%* −38.7±15.5%* −40.6±17.5%*
VL ARV (mV) 5.8±8.9% −28.2±11.8%* −30.1±13.5%* −31.2±14.5%*
*p<0.05.
Values for all performance parameters at all postexercise sessions were significantly different compared with baseline.
Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015 3
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necrosis of the contractile elements and inflammation,12 20 21
which in turn sensitises the intramyofibril group IV afferents.21
In the current study, the average pain intensity reported by par-
ticipants was 5.5±0.7 and 5.8±0.9 at 24 and 48 h, respectively.
This is in agreement with the level of pain reported postec-
centric exercise of the quadriceps in previous studies.13
Furthermore, an altered VMO/VL timing during stair climbing
was observed in patients with patellofemoral pain with a pain
intensity of 4.9±2.3.22
Maximal voluntary knee extension force, time to task failure
during a sustained knee extension contraction and associated
EMG activity were significantly decreased with respect to base-
line, most likely due to the high accumulation of metabolites
within the skeletal muscle23
and/or an inhibitory effect mediated
by nociception at the cortical and spinal levels,24
which in turn
reduces the neural drive to the muscle fibres.25
The EMG amplitude of the VMO and VL muscles did not
change significantly over time during the sustained contraction
performed before the eccentric exercise. The lack of reduction
in ARV at baseline can be explained by the increasing motor
unit recruitment and/or discharge rate required to compensate
for contractile failure caused by fatigue.26
However, a greater
Figure 1 Example of surface electromyography signals detected from
the distal portion of the right vastus medialis obliqus (VMO) and vastus
lateralis muscles of one subject during a backward perturbation
performed before the eccentric exercise (A), immediately after (B), and
at 24 h (C) and 48 h after the eccentric exercise (D). The dashed
vertical line indicates the first onset of muscle activity detected. Note
that the VMO muscle is activated first at baseline; however, this
response is delayed immediately after (B), and at 24 h (C) and 48 h
after the eccentric exercise.
Figure 3 Per cent change in the vastus medialis obliqus:vastus
lateralis (VMO:VL) activation ratio (mean±SE, n=11) during postural
perturbations performed before the eccentric exercise (baseline),
immediately after, and at 24 and 48 h after eccentric exercise. A
negative per cent change indicates lower activation of the VMO muscle
compared with the VL muscle. *Represents a significant difference in
the per cent change relative to baseline for the forward and backward
perturbations (p<0.05).
Figure 2 Per cent change in vastus medialis obliqus:vastus lateralis
(VMO:VL) onset (mean±SE, n=11) during postural perturbations
performed before the eccentric exercise (baseline), immediately after,
and at 24 and 48 h after the eccentric exercise. A positive per cent
change indicates later activation of the VMO muscle compared with the
VL muscle. *Represents a significant difference in the per cent change
relative to baseline for the forward and backward perturbations
(p<0.05).
4 Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015
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percentage decrease in ARV of the EMG was observed during
the postexercise sustained isometric contractions compared with
the pre-exercise condition. Accordingly, previous studies have
reported a larger decrease in the EMG amplitude during sus-
tained contractions after eccentric exercise-induced muscle fibre
damage.13 27
The VMO muscle showed a larger reduction in
EMG ARV over the postexercise sustained contraction compared
with the VL muscle, most likely due to the greater muscle fibre
injury within this muscle. Thigh circumference measured imme-
diately after and at 24 and 48 h after exercise was larger than at
baseline possibly due to muscle inflammation.12 21
VMO:VL onset prior to eccentric exercise
Prior to performing the eccentric exercise, the EMG onset of
VMO was significantly earlier than the VL muscle in response to
rapid destabilising knee perturbations in both the forward and
backward directions, which is in agreement with previous find-
ings during postural perturbations,3
stair-stepping4
patella
tendon reflex reactions5 6 2
and walking.28
An earlier activation
of the VMO muscle relative to the VL muscle has been attributed
to a ‘feed-forward’ mechanism in which the VMO receives a
‘feed-forward’ enhancement in excitation (relative to that of the
VL) to optimally track the patella.5 29
This mechanism has been
proposed because of the larger cross-sectional area and velocity-
producing properties of the VL, which are predicted to result in a
dominance of laterally directed patellar motion.5
VMO:VL onset after eccentric exercise
After eccentric exercise, pain manifested and the onset of VMO
activity was significantly later than that of the VL muscle during
the postural perturbations performed immediately after eccen-
tric exercise, and this change in activation remained 24 and
48 h after exercise.
Moreover, a greater reduction of the VMO EMG amplitude
was observed during the postural perturbations performed post-
exercise compared with the VL muscle.
The current study is the first to assess changes in the onset of
activation of the VMO and VL muscles during postural pertur-
bations performed after eccentric exercise and during delayed
onset muscle soreness. The altered timing of activation of the
VMO:VL muscles after eccentric exercise may be related to the
pathophysiological changes and/or pain within the skeletal
muscle. Changes in the onset and EMG amplitude, which were
observed immediately after eccentric exercise, are most likely
explained by a combination of muscle fibre damage and metab-
olite accumulation within the muscle, whereas the presence of
pain within the quadriceps muscle, which was present 24 and
48 h postexercise, can contribute to delayed or inhibited neuro-
muscular responses at the injured site13 30
by inhibition at the
cortical and spinal levels.24
A muscular imbalance between the
VMO and VL muscles and improper timing of activation
between the two muscles are also reported in patients with
patellofemoral pain syndrome.2
Furthermore, higher pain inten-
sity rated by patients with patellofemoral pain syndrome during
the week prior to a stair-stepping task was associated with a sig-
nificantly delayed onset time of the VMO muscle relative to the
VL muscle during the task.22
Deficits in the timing of muscle
activity have been identified in other musculoskeletal pain con-
ditions such as neck pain31
low back pain32
and long-standing
groin pain.33
Pain is common after high-intensity eccentric exercise, most
likely due to fibre injury within the skeletal muscle.20
In the
current study, the participants described the greatest pain inten-
sity over their inner thigh (vastus medialis muscle), which con-
firms previous findings that reported a lower pressure pain
threshold and higher pain scores for the VMO muscle up to
72 h after eccentric exercise of the quadriceps muscle.13 30 34
Greater soreness over the medial aspect of the quadriceps
muscle has also been reported to be associated with a larger
reduction of muscle activity and signal conduction velocity for
the VMO muscle,13 14 30 35
which may contribute to the
delayed onset of VMO activity observed in the current study.
For example, studies investigating muscle fibre conduction vel-
ocity have shown that after high-intensity exercise of the quadri-
ceps muscle, a greater reduction in conduction velocity is
observed for the VMO muscle, and the recovery of conduction
velocity in the VMO muscle occurs later than for other muscles
of the quadriceps.14 30
The highest intensity of pain rated over
the VMO muscle and the larger reduction in conduction vel-
ocity of the VMO suggests that the VMO muscle is more sus-
ceptible to fibre injury during eccentric exercise, most probably
due to high force production in this area to stabilise the patella
during high load leg exercise. Accordingly, VMO muscle weak-
ness has been shown to be one of the most common muscular
imbalances in athletes with knee pain. For example, Grana and
Kriegshauser36
reported that in the presence of knee injury the
VMO muscle is the first to atrophy and the last to respond to
rehabilitation. Gerber et al37
also reported greater atrophy of
the VMO compared with other quadriceps components in ath-
letes suffering from a traumatic knee injury.
The altered onset of VMO:VL activity after eccentric exercise
could also be explained by remodelling of the neuromuscular
junction,38
changes in proprioceptive function39
and an alter-
ation in muscle fibre membrane properties at the injured sites.18
There is evidence of membrane depolarisation as a result of
remoulding of the neuromuscular junction and/or fibre mem-
brane disruption after eccentric exercise, which may have
Figure 4 Scatter plot of the per cent change in electromyography
(EMG) onset (average for the vastus medialis obliqus (VMO) and vastus
lateralis (VL) muscles) versus the per cent change in EMG average
rectified value (average for the VMO and VL muscles) during postural
perturbations performed at baseline compared with the postexercise
sessions (average for all postexercise sessions). Data from all
participants and all muscles are pooled together. The negative
correlation indicates that the increased EMG onset time at the
postexercise sessions is partially associated with the decreased muscle
activation observed during that session.
Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015 5
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impaired conduction of action potentials along the muscle
fibre.14 15 17 18
Additionally, the slowing of reflex muscle activ-
ity could also be due to the loss of proprioceptive input from
the injured site as reported in previous studies.16
Methodological considerations
Sustained contraction until task failure performed before a per-
turbation may influence muscle onset. However, in the current
study, the participants were given 20 min to rest and recover
from muscle fatigue. Accordingly, a greater difference in VMO:
VL onset observed following eccentric exercise, with respect to
the baseline condition, suggests that the change in VMO:VL
onset across testing sessions was the result of muscle damage
and not simply due to fatigue.
CONCLUSION
The onset of the VMO muscle is significantly later than that of
the VL muscle during rapid destabilising perturbations of the
leg following eccentric exercise, most likely due to muscle fibre
damage and pain. This finding suggests that eccentric exercise of
the quadriceps can delay reflex activity of the vastii muscles and
may compromise patella stabilisation, thereby leaving the knee
complex more vulnerable to injury. Further studies are needed
to determine how long after eccentric exercise the VMO:VL
timing will return to normal. This knowledge may be useful to
prevent patellofemoral disorders after high-intensity eccentric
exercise.
What are the new findings?
▸ Muscles subjected to eccentric loading become stiff and sore
24 h after exercise and neuromuscular control of the injured
muscle may be altered.
▸ Previous studies, however, have typically examined the effect
of eccentric exercise on muscle activity during non-functional
activities.
▸ This study shows that eccentric exercise of the quadriceps
alters the onset of activation of the vastii muscles to
stabilise the patella during rapid, unexpected perturbations
to the knee.
▸ The type of perturbation used resembles perturbations that
might commonly be encountered during sport activities.
How might it impact on clinical practice in the near
future?
▸ Patellofemoral pain syndrome is a common complaint in the
sporting and general populations, especially when repetitive
lower limb eccentric loading is frequently performed.
▸ The knowledge gained from this study may be relevant for
the understanding and prevention of exercise-related patella
disorders which develop following unaccustomed exercise.
Acknowledgements The authors are grateful to Professor Lars Arendt-Nielsen for
his support.
Contributors NH was responsible for the concept development and study design,
data collection, analysis and interpretation of the data and writing of the
manuscript. DF was responsible for the concept development and study design,
analysis and interpretation of the data, and writing of the manuscript.
Funding This research received no specific grant from any funding agency in the
public, commercial or not-for-profit sectors.
Competing interests None.
Ethics approval The Ethics committee of Nordjylland, Denmark (N 20070019).
Provenance and peer review Not commissioned; externally peer reviewed.
Data sharing statement The data from the study are included in this manuscript.
REFERENCES
1 Hedayatpour N, Hassanlouei H, Arendt-Nielsen L, et al. Delayed-onset muscle
soreness alters the response to postural perturbations. Med Sci Sports Exerc
2011;43:1010–16.
2 Witvrouw E, Sneyers C, Lysens R, et al. Reflex response times of vastus medialis
oblique and vastus lateralis in normal subjects and in subjects with patellofemoral
pain syndrome. J Orthop Sports Phys Ther 1996;24:160–5.
3 Ng EC, Chui MP, Siu AY, et al. Ankle positioning and knee perturbation affect
temporal recruitment of the vastii muscles in people with patellofemoral pain.
Physiotherapy 2011;97:65–70.
4 Cavazzuti L, Merlo A, Orlandi F, et al. Delayed onset of electromyographic activity
of vastus medialis obliquus relative to vastus lateralis in subjects with patellofemoral
pain syndrome. Gait Posture 2010;32:290–5.
5 Grabiner MD, Koh TJ, Draganich LF. Neuromechanics of the patellofemoral joint.
Med Sci Sports Exerc 1994;26:10–21.
6 Voight ML, Wieder DL. Comparative reflex response times of vastus medialis obliquus
and vastus lateralis in normal subjects and subjects with extensor mechanism
dysfunction. An electromyographic study. Am J Sports Med 1991;19:131–7.
7 Fulkerson JP, Shea KP. Current concepts review: disorder of patellofemoral
alignment. J Bone Joint Surg Am 1990;72:1424–9.
8 Insall J. Current concepts review: patellar pain. J Bone Joint Surg Am 1982;64:147–52.
9 Fulkerson JP, Shea KP. Mechanical basis for patellofemoral pain and cartilage
breakdown. In: Ewing JW, ed. Articular cartilage and knee joint function: basic
science and arthroscopy. New York, NY: Raven Press, 1990:93–101.
10 DeHaven KE, Dolan WA, Mayer PJ. Chondromalacia in athletes. Am J Sports Med
1979;7:5–11.
11 Holmes SW, Clancy WG. Clinical classification of patellofemoral pain and
dysfunction. J Orthop Sports Phys Ther 1998;28:299–306.
12 Bobbert MF, Hollander AP, Huijing PA. Factors in delayed onset muscular soreness
of man. Med Sci Sports Exerc 1986;18:75–81.
13 Hedayatpour N, Falla D, Arendt-Nielsen L, et al. Sensory and electromyographic
mapping during delayed-onset muscle soreness. Med Sci Sports Exerc 2008;40:326–34.
14 Hedayatpour N, Falla D, Arendt-Nielsen L, et al. Motor unit conduction velocity
during sustained contraction after eccentric exercise. Med Sci Sports Exer
2009;41:1927–33.
15 Chen YW, Hubal MJ, Hoffman EP, et al. Molecular responses of human muscle to
eccentric exercise. J Appl Physiol 2003;95:2485–94.
16 Jennings AG, Seedhom BB. Proprioception in the knee and reflex hamstring
contraction latency. J Bone Joint Surg Br 1994;76:491–4.
17 Clarkson PM, Byrnes WC, McCormick K, et al. Muscle soreness and serum creatine
kinase activity following isometric, eccentric, and concentric exercise. Int J Sports
Med 1986;7:152–5.
18 McBride TA, Gorin FA, Carlsen RC. Membrane depolarization following high
resistance eccentric exercise in rat tibialis anterior. FASEB J 1994;8:A307.
19 Van Doornik J, Sinkjaer T. Robotic platform for human gait analysis. IEEE Trans
Biomed Eng 2007;54:1696–702.
20 Newham DJ, Jones DA, Clarkson PM. Repeated high-force eccentric exercise: effects
on muscle pain and damage. J Appl Physiol 1987;63:1381–6.
21 Smith LL. Acute inflammation: the underlying mechanism in delayed onset muscle
soreness? Med Sci Sports Exerc 1991;23:542–51.
22 Boling MC, Bolgla LA, Mattacola CG, et al. Outcomes of a weight-bearing
rehabilitation program for patients diagnosed with patellofemoral pain syndrome.
Arch Phys Med Rehabil 2006;87:1428–35.
23 Babault N, Desbrosses K, Fabre MS, et al. Neuromuscular fatigue development
during maximal concentric and isometric knee extensions. J Appl Physiol
2006;100:780–5.
24 Le Pera D, Graven-Nielsen T, Valeriani M, et al. Inhibition of motor system
excitability at cortical and spinal level by tonic muscle pain. Clin Neurophysiol
2001;112:1633–41.
25 Kaufman MP, Hayes SG, Adreani CM, et al. Discharge properties of group III and IV
muscle afferents. Adv Exp Med Biol 2002;508:25–32.
26 Kirsch RF, Rymer WZ. Neural compensation for fatigue-induced changes in muscle
stiffness during perturbations of elbow angle in human. J Neurophysiol 1992;68:449–70.
27 Hortobagyi T, Houmard J, Fraser D, et al.. Normal forces and myofibril disruption
after repeated eccentric exercise. J Appl Physiol 1998;84:492–8.
6 Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015
Original article
group.bmj.comon August 21, 2013 - Published bybjsm.bmj.comDownloaded from
28 Pal S, Besier TF, Draper CE, et al. Patellar tilt correlates with vastus lateralis: vastus
medialis activation ratio in maltracking patellofemoral pain patients. J Orthop Res
2012;30:927–33.
29 Cowan SM, Bennell KL, Hodges PW, et al. Simultaneous feed forward recruitment
of the vasti in untrained postural tasks can be restored by physical therapy. J Orthop
Res 2003;21:553–8.
30 Hedayatpour N, Falla D, Arendt-Nielsen L, et al. Effect of delayed-onset muscle
soreness on muscle recovery after a fatiguing isometric contraction. Scand J Med Sci
Sports 2010;20:145–53.
31 Falla D, Jull G, Hodges PW. Feedforward activity of the cervical flexor muscles
during voluntary arm movements is delayed in chronic neck pain. Exp Brain Res
2004;157:43–8.
32 Hodges PW, Richardson CA. Delayed postural contraction of transversus abdominis
in low back pain associated with movement of the lower limb. J Spinal Disord
1998;11:46–56.
33 Cowan SM, Schache AG, Brukner P, et al. Delayed onset of transversus abdominus
in long-standing groin pain. Med Sci Sports Exerc 2004;36:2040–5.
34 Newham DJ, Mills KR, Quigley BM, et al. Pain and fatigue after concentric and
eccentric muscle contractions. Clin Sci 1983;64:55–62.
35 Hedayatpour N, Falla D. Non-uniform muscle adaptations to eccentric exercise and
the implications for training and sport. J Electromyogr Kinesiol 2012;22:329–33.
36 Grana WA, Kriegshauser LA. Scientific basis of extensor mechanism disorders. Clin
Sports Med 1985;4:247–57.
37 Gerber C, Hoppeler H, Claassen H, et al. The lower-extremity musculature in chronic
symptomatic instability of the anterior cruciate ligament. J Bone Joint Surg Am
1985;67:1034–43.
38 Warren GL, Angels CP, Shah SJ, et al. Uncoupling of in vivo torque production from
EMG in mouse muscles injured by eccentric contractions. J Physiol 1999;515:609–19.
39 Weerakkody NS, Whitehead NP, Canny BJ, et al. Large-fiber mechanoreceptors
contribute to muscle soreness after eccentric exercise. J Pain 2001;2:209–19.
Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015 7
Original article
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doi: 10.1136/bjsports-2012-092015
published online August 19, 2013Br J Sports Med
Nosratollah Hedayatpour and Deborah Falla
exercise?
that underpins knee pain after eccentric
following eccentric exercise: a mechanism
response to rapid postural perturbations
Delayed onset of vastii muscle activity in
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Delayed onset of vastii muscle activity in response to rapid postural perturbations following eccentric exercise: a mechanism that underpins knee pain after eccentric exercise

  • 1. See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/255985728 Delayed onset of vastii muscle activity in response to rapid postural perturbations following eccentric exercise: A... Article in British Journal of Sports Medicine · August 2013 DOI: 10.1136/bjsports-2012-092015 · Source: PubMed CITATIONS 6 READS 193 2 authors: Some of the authors of this publication are also working on these related projects: Thoracic dysfunction in whiplash associated disorders View project Nosratollah Hedayatpour 47 PUBLICATIONS 170 CITATIONS SEE PROFILE Deborah Falla University of Birmingham 217 PUBLICATIONS 4,513 CITATIONS SEE PROFILE All content following this page was uploaded by Nosratollah Hedayatpour on 23 June 2017. The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document and are linked to publications on ResearchGate, letting you access and read them immediately.
  • 2. Delayed onset of vastii muscle activity in response to rapid postural perturbations following eccentric exercise: a mechanism that underpins knee pain after eccentric exercise? Nosratollah Hedayatpour,1,2 Deborah Falla3,4 1 Department of Physical Education and Sport Science, University of Bojnord, Bojnord, Iran 2 Department of Health Science and Technology, Centre for Sensory-Motor Interaction (SMI), Aalborg University, Aalborg, Denmark 3 Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, University Medical Center Göttingen, Georg-August University, Göttingen, Germany 4 Pain Clinic, Center for Anesthesiology, Emergency and Intensive Care Medicine, University Hospital Göttingen, Göttingen, Germany Correspondence to Dr Deborah Falla, Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, University Medical Center Göttingen, Georg-August University, Von-Siebold-Str. 4, Göttingen 37075, Germany; deborah.falla@bccn.uni- goettingen.de Received 21 November 2012 Revised 5 April 2013 Accepted 17 June 2013 To cite: Hedayatpour N, Falla D. Br J Sports Med Published Online First: [please include Day Month Year] doi:10.1136/bjsports- 2012-092015 ABSTRACT Background Appropriate timing of activity of the vastus medialis obliqus (VMO) and vastus lateralis (VL) muscles is a key factor for proper tracking of the patella in the trochlear groove during knee extension. This study investigates the relative timing of activation of the VMO and VL muscles during unexpected perturbations performed before and after eccentric exercise. Methods Surface electromyography signals were recorded from the VMO and VL muscles of the right leg in 11 healthy men during rapid postural perturbations performed at baseline, immediately after eccentric exercise of the quadriceps, and at 24 and 48 h after exercise. Participants stood on a moveable platform during which eight randomised postural perturbations were performed (4 repetitions of 2 perturbation types: 8 cm forward slides, 8 cm backward slides). Results Before the eccentric exercise, the onset of VMO activity was significantly earlier than the VL muscle (average for both forward and backward perturbations: VMO 39.0±7.1 ms; VL 43.7±7.9 ms). However, the onset of VMO activity was significantly later compared with VL muscle immediately after eccentric exercise and this remained 24 and 48 h after eccentric exercise (average across all postexercise sessions and perturbation directions: VMO 72.3±11.1 ms; VL 56.0±8.2 ms; p<0.05). Conclusions The onset of VMO–VL activity in response to rapid destabilising perturbations is altered immediately after eccentric exercise and during eccentric exercise- induced muscle soreness up to 48 h later. These observations may help explain the high prevalence of knee disorders after high intensity eccentric exercise. INTRODUCTION The ability of the quadriceps femoris to rapidly sta- bilise the patella during an unexpected knee per- turbation is dependent on the onset and amplitude of muscle activation.1 2 The onset of vastus media- lis obliqus (VMO) activity typically occurs earlier than that of the vastus lateralis (VL) or at least syn- chronously during the postural perturbations,3 stair-stepping4 and patella tendon reflex reac- tions.2 5 6 Consequently, delayed onset of the VMO compared with VL activity has frequently been reported as a potential cause for patellar mal- tracking and development of pain.7 From an anatomical perspective, the appropriate timing of VMO activation relative to the VL muscle is necessary to compensate for the strong lateral pull of the VL muscle during knee exten- sion. It has been hypothesised that changes in the onset of VMO activation may contribute to an imbalance in muscle forces and, as a consequence, lead to lateral maltracking of the patella.8 6 An excessive lateral tracking of the patella could induce localised stresses that are transmitted through the cartilage with the potential to excite nociceptors in the subchondral bone, which in turn can result in patellofemoral pain syndrome (PFPS).9 PFPS is a common complaint in the sporting and general populations, especially when repetitive lower limb eccentric loading is frequently performed.10 11 Muscles subjected to eccentric loading become stiff and sore 24 h after exercise because of the patho- physiological changes and inflammation at the injured sites.12 13 Furthermore, in the injured muscle, neuromuscular responses can be impaired most likely due to pain,13 14 remodelling of the neuromuscular junction,15 changes in the proprioceptive function16 and alteration in the muscle fibre membrane proper- ties.14 17 18 Thus, it may be expected that eccentric exercise of the quadriceps contributes to a change in the onset of activation of the VMO and VL muscles to stabilise the patella during perturbations to the knee. This knowledge may be relevant for exercise-related patella disorders that develop follow- ing unaccustomed exercise. Therefore, in the current study, we analysed the relative timing of activation of the VMO and VL muscles during unexpected knee perturbations performed before and after eccentric exercise. The type of perturbation used resembles perturbations that might commonly be encountered during sport activities. METHODS Subjects Eleven healthy men (age, mean±SD, 24.1±4.1 years, body mass 73.5±11.2 kg, height 1.77±0.05 m) with no history of knee injury participated in the study. All participants were right leg dominant and were not involved in regular exercise of their knee extensor muscles for at least 6 months before the experiment. The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics committee of Nordjylland, Denmark (N 20070019). All measures were performed at the Center for Sensory Motor-Interaction, Aalborg University, Denmark. Participants provided informed written consent before participation in the study. Eccentric exercise Participants performed eccentric exercise on a KinCom Isokinetic Dynamometer (Chattanooga Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015 1 Original article BJSM Online First, published on August 19, 2013 as 10.1136/bjsports-2012-092015 Copyright Article author (or their employer) 2013. Produced by BMJ Publishing Group Ltd under licence. group.bmj.comon August 21, 2013 - Published bybjsm.bmj.comDownloaded from
  • 3. Group, Tennessee, USA). The exercise protocol consisted of 4 bouts of 25 maximum voluntary eccentric knee extension con- tractions at a speed of 60°/s between 90° and 170° of knee extension, with 3 min of rest between each set. During the exer- cise, visual feedback of force was provided on a screen posi- tioned in front of the subject, and the subject was encouraged to maintain maximal force. A load equal to twice the maximal vol- untary contraction of knee extension was applied during the eccentric contractions.14 Maximal voluntary contraction (MVC) of the knee extensors, subjective pain intensity ratings, muscle circumference, time to task failure for a 50% MVC sustained isometric knee extension contraction and EMG onset and amp- litude of the VMO and VL muscles during rapid postural per- turbations were recorded before, immediately after, and at 24 h and 48 h after eccentric exercise. Assessment of muscle pain intensity and thigh circumference A 10 cm visual analogue scale (VAS), labelled with end points on the left (no pain) and right (worst pain imaginable), was used to assess the perceived pain intensity 24 and 48 h after exercise. Participants were asked to rate their average pain inten- sity corresponding to their level of soreness experienced during daily activities (eg, climbing stairs) since their last visit to the laboratory (over the last 24 h). If any soreness was indicated, the subject was asked whether the discomfort was more pro- nounced in the inner, middle or outer region of the quadriceps. Thigh circumference was measured using a tape-measure around the distal portion of the thigh at 10% of the distance between the superior border of the patella and the anterior superior iliac spine. Maximum and sustained knee extension contractions Participants were asked to perform three maximal isometric knee extensions on the right (3–5 s in duration) using the KinCom Isokinetic Dynamometer with the knee and hip in 90° of flexion with 2 min of rest in between repetitions. Participants were supported by straps over the right thigh, pelvis and trunk. Visual feedback of force was provided on a screen positioned in front of the subject and verbal encouragement to exceed the previous force level was given. Participants also performed an isometric knee extension contraction at 50% MVC sustained until task failure on the KinCom Dynamometer, with the par- ticipant in the same position as in the maximal voluntary con- tractions. The submaximal force was relative to the highest MVC measured on the same day of the test. Task failure was defined as a drop in torque >5% MVC for more than 5 s after strong verbal encouragement to the subject to maintain the target torque. A rest period of ∼20 min was given prior to start- ing the perturbations. Postural perturbations Participants stood with their feet shoulder width apart, with their right lower limb on a moveable force platform and left foot on the ground. An oscilloscope connected to a force plat- form was positioned in front of the participant to monitor weight bearing. A positioning actuator19 translated the platform either 8 cm forwards or backwards over 150 ms. Hip joint motion was restricted by a strap secured around the pelvis and greater trochanter that was bolted firmly to the wall. The subject stood comfortably with equal weight on each limb using the visual feedback on weight bearing. In each direction (for- wards and backwards), four 3 s trials were collected in which the plate was triggered to move at a random interval within 3 s. Participants were unaware of when the plate would be triggered to move. The order of the direction of platform movement (forward and backward) was randomised. Surface EMG data were collected from the VL and VMO muscles during the perturbations. Electromyography Surface electrodes (Ag–AgCl surface electrodes, Ambu Neuroline, conductive area: 28 mm2 ) were placed in bipolar configuration (interelectrode distance: 2 cm) at a position equal to 10% of the distance between the medial border (VMO) and lateral border (VL) of the patella and anterior superior iliac spine. A reference electrode was placed around the right ankle. The positions of the electrodes were marked on the skin during the first session (day 1) so that the locations could be replicated 24 and 48 h after exercise. Surface EMG signals were amplified (EMG amplifier, EMG-128, OT Bioelettronica, Torino, Italy, bandwidth 10–500 Hz), sampled at 2048 Hz and stored after 12-bit A/D conversion. For the submaximal contraction, the average rectified value (ARV) was calculated for epochs of 1 s during the contraction, which was sustained until task failure. The values obtained from the 1 s long epochs in intervals of 10% of the time to task failure were averaged to obtain one representative value for each 10% interval. For each session, the per cent change in ARV over time was calculated by subtracting the final value from the initial value of ARV and dividing by the initial value. To assess the onset of muscle activity during the postural per- turbations, surface EMG data were full-wave rectified and band- pass filtered at 10–350 Hz. Muscle activation onset was defined based on a threshold that was 3 SDs greater than the baseline, within a time window of 45 ms after platform movement. Moreover, the EMG ARV of each muscle was calculated over a fixed window, which was 200 ms after the onset of plate move- ment. For each perturbation direction, the muscle activation onset and ARV obtained over the four trials were averaged to obtain a representative value. The per cent change in the VMO: VL onset time was calculated as the difference between the VL and VMO onset times divided by the VMO onset time. A posi- tive per cent change in the VMO:VL onset time indicated acti- vation of the VMO muscle later than the VL muscle. The per cent change in the VMO:VL activation ratio was also calculated as the difference between the VL and VMO EMG ARV divided by the VMO EMG ARV. A negative per cent change in the VMO:VL activation ratio indicated a lower EMG amplitude of the VMO muscle compared with the VL muscle. Statistical analysis A one-way repeated-measures analysis of variance (ANOVA) was applied to analyse MVC, time to task failure and thigh circum- ference with time as the repeated measure. Two-way repeated- measures ANOVA was used to assess the per cent change of ARV across the sustained contraction at 50% MVC (per cent change from the first to the last epoch), with session and muscle as dependent factors. A three-way ANOVA was applied to assess changes in muscle onset time from the pre-exercise session (baseline) to postexercise sessions (immediately after, and at 24 and 48 h) with time, muscle and perturbation direction (back- ward and forward) as dependent factors. Moreover, a three-way ANOVA was used to evaluate the change of ARV from baseline to postexercise (immediately after, and at 24 and 48 h), with time, muscle and perturbation direction (backward and forward) as dependent factors. 2 Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015 Original article group.bmj.comon August 21, 2013 - Published bybjsm.bmj.comDownloaded from
  • 4. Two-way ANOVAs were applied to assess the per cent change in VMO:VL onset and per cent change in the VMO:VL ampli- tude ratio from baseline (pre-exercise) to the postexercise ses- sions with time and perturbation direction as dependent factors. Finally, a Pearson correlation coefficient was obtained to assess the relationship between the per cent change in EMG amplitude and the per cent change in muscle onset across testing sessions. Pairwise comparisons were performed with the Student-Newman-Keuls post hoc test when ANOVA was signifi- cant. The significance level was set at p<0.05 for all statistical procedures. Results are reported as the mean and SD in the text and SE in the figures. RESULTS One-way repeated-measure ANOVA revealed a significant reduc- tion in maximum voluntary knee extension force (F=10.5, p<0.0001) and time to task failure (F=9.7, p<0.0001) after eccentric exercise. MVC and time to task failure were not signifi- cantly different between the three postexercise sessions (immedi- ately after, and at 24 and 48 h, p>0.05). Moreover, pain intensity increased and pain become more pronounced in the inner region of the thigh (over the vastus medialis muscle), as self-reported by the participants at 24 h (5.5±0.7) and 48 h post- exercise (5.8±0.9). No difference in pain intensity was observed between 24 and 48 h postexercise. The thigh circumference mea- sured during the postexercise sessions was also significantly larger compared with the pre-exercise session measure (p<0.05). A two-way repeated-measures ANOVA showed a greater per- centage of decrease in ARV of the EMG (in the final epoch with respect to the initial epoch) during the postexercise sustained isometric contractions compared with the pre-exercise condition (F=7.5, p<0.0001). In all sessions, the VMO muscle showed a greater reduction in ARV compared with the VL muscle (F=2.9, p<0.05). The mean and SD of all performance para- meters are reported in table 1. Postural perturbations A three-way repeated-measures ANOVA revealed an interaction between muscle and time (F=12.4, p<0.001) which showed that the onset of VMO was significantly earlier than VL muscle in response to the perturbations performed during the baseline con- dition (p<0.05). However, the onset of VMO activity was sig- nificantly later than VL activity immediately after, and at 24 and 48 h after eccentric exercise (p<0.001). This observation was consistent for both the forward and backward perturbations (p>0.05). An example of the surface EMG signals detected from the distal portion of VMO and VL muscles 200 ms after platform movement is illustrated in figure 1. The per cent change in VMO:VL onset also showed that the onset of VMO activity occurred significantly later than VL activity during all postexer- cise sessions (p<0.01) but not during the pre-exercise condition (figure 2). A three-way repeated-measures ANOVA also showed that in all conditions (before, immediately after, and at 24 and 48 h after eccentric exercise), the VL muscle displayed greater values of ARV in response to the postural perturbations compared with the VMO muscle (F=20.4, p<0.0001). Furthermore, the per cent change in VMO:VL activation in response to the perturba- tions performed in the postexercise sessions were significantly larger than the per cent change in VMO:VL activation observed in the pre-exercise session (p<0.05; figure 3). However, the per cent change in VMO:VL activation was not significantly different between postexercise sessions (p>0.05) or between the forward and backward perturbations (p>0.05). Correlation between EMG onset and amplitude The per cent change in the EMG onset time (average for the VL and VMO muscles) from the pre-exercise session to the postex- ercise sessions (average for all postexercise sessions) was com- pared with the per cent change in EMG ARV (average for the VL and VMO muscles) from the pre-exercise session to the postexercise sessions (average for all postexercise sessions). Per cent change in EMG onset and per cent change in EMG ARV were negatively correlated (R=−0.23, p<0.05, figure 4), indi- cating that the increased EMG onset time postexercise was par- tially associated with decreased muscle activation. DISCUSSION An earlier activation of the VMO muscle relative to the VL muscle has been observed for healthy individuals in normal con- ditions. This priority of VMO activation may be of particular importance to optimally track the patella due to the smaller cross-sectional area of VMO muscle and the predominantly lat- erally directed force of the VL muscle. This study demonstrates that the onset of VMO activation was later than that of the VL during destabilising knee perturbations performed immediately after, and at 24 and 48 h after eccentric exercise. The results indicate that eccentric exercise alters the sequence of VMO:VL onset, which may result in an imbalance of the quadriceps forces contributing to stabilisation of the patella. Over time, this may potentially contribute to lateral maltracking of the patella. Muscle performance In the current study, participants reported that their quadriceps muscle was sore 24 and 48 h after eccentric exercise, which might be related to damage of the contractile elements and con- nective tissue.20 Signs and symptoms of pain may result from pathophysiological changes in the muscle fibres. After muscle fibre injury, phagocyte cell infiltration results in progressive Table 1 Mean±SD (n=11) for maximal voluntary contraction (MVC), time to task failure, thigh circumference and average rectified value (ARV) rate of reduction over the sustained contraction at 50% MVC for the VMO and VL muscles Pre-exercise Immediately after At 24 h postexercise At 48 h postexercise MVC (N m) 595±45 460±29* 470±31* 475±33* Task failure (s) 85.5±23.6 40.7±14.5* 45.8±19.2* 44.2±16.8* Thigh circumference (cm) 41.3±2.9 42.1±3.2* 42.3±3.1* 42.2±2.9* VMO ARV (mV) 7.2±10.3% −35.±14.8%* −38.7±15.5%* −40.6±17.5%* VL ARV (mV) 5.8±8.9% −28.2±11.8%* −30.1±13.5%* −31.2±14.5%* *p<0.05. Values for all performance parameters at all postexercise sessions were significantly different compared with baseline. Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015 3 Original article group.bmj.comon August 21, 2013 - Published bybjsm.bmj.comDownloaded from
  • 5. necrosis of the contractile elements and inflammation,12 20 21 which in turn sensitises the intramyofibril group IV afferents.21 In the current study, the average pain intensity reported by par- ticipants was 5.5±0.7 and 5.8±0.9 at 24 and 48 h, respectively. This is in agreement with the level of pain reported postec- centric exercise of the quadriceps in previous studies.13 Furthermore, an altered VMO/VL timing during stair climbing was observed in patients with patellofemoral pain with a pain intensity of 4.9±2.3.22 Maximal voluntary knee extension force, time to task failure during a sustained knee extension contraction and associated EMG activity were significantly decreased with respect to base- line, most likely due to the high accumulation of metabolites within the skeletal muscle23 and/or an inhibitory effect mediated by nociception at the cortical and spinal levels,24 which in turn reduces the neural drive to the muscle fibres.25 The EMG amplitude of the VMO and VL muscles did not change significantly over time during the sustained contraction performed before the eccentric exercise. The lack of reduction in ARV at baseline can be explained by the increasing motor unit recruitment and/or discharge rate required to compensate for contractile failure caused by fatigue.26 However, a greater Figure 1 Example of surface electromyography signals detected from the distal portion of the right vastus medialis obliqus (VMO) and vastus lateralis muscles of one subject during a backward perturbation performed before the eccentric exercise (A), immediately after (B), and at 24 h (C) and 48 h after the eccentric exercise (D). The dashed vertical line indicates the first onset of muscle activity detected. Note that the VMO muscle is activated first at baseline; however, this response is delayed immediately after (B), and at 24 h (C) and 48 h after the eccentric exercise. Figure 3 Per cent change in the vastus medialis obliqus:vastus lateralis (VMO:VL) activation ratio (mean±SE, n=11) during postural perturbations performed before the eccentric exercise (baseline), immediately after, and at 24 and 48 h after eccentric exercise. A negative per cent change indicates lower activation of the VMO muscle compared with the VL muscle. *Represents a significant difference in the per cent change relative to baseline for the forward and backward perturbations (p<0.05). Figure 2 Per cent change in vastus medialis obliqus:vastus lateralis (VMO:VL) onset (mean±SE, n=11) during postural perturbations performed before the eccentric exercise (baseline), immediately after, and at 24 and 48 h after the eccentric exercise. A positive per cent change indicates later activation of the VMO muscle compared with the VL muscle. *Represents a significant difference in the per cent change relative to baseline for the forward and backward perturbations (p<0.05). 4 Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015 Original article group.bmj.comon August 21, 2013 - Published bybjsm.bmj.comDownloaded from
  • 6. percentage decrease in ARV of the EMG was observed during the postexercise sustained isometric contractions compared with the pre-exercise condition. Accordingly, previous studies have reported a larger decrease in the EMG amplitude during sus- tained contractions after eccentric exercise-induced muscle fibre damage.13 27 The VMO muscle showed a larger reduction in EMG ARV over the postexercise sustained contraction compared with the VL muscle, most likely due to the greater muscle fibre injury within this muscle. Thigh circumference measured imme- diately after and at 24 and 48 h after exercise was larger than at baseline possibly due to muscle inflammation.12 21 VMO:VL onset prior to eccentric exercise Prior to performing the eccentric exercise, the EMG onset of VMO was significantly earlier than the VL muscle in response to rapid destabilising knee perturbations in both the forward and backward directions, which is in agreement with previous find- ings during postural perturbations,3 stair-stepping4 patella tendon reflex reactions5 6 2 and walking.28 An earlier activation of the VMO muscle relative to the VL muscle has been attributed to a ‘feed-forward’ mechanism in which the VMO receives a ‘feed-forward’ enhancement in excitation (relative to that of the VL) to optimally track the patella.5 29 This mechanism has been proposed because of the larger cross-sectional area and velocity- producing properties of the VL, which are predicted to result in a dominance of laterally directed patellar motion.5 VMO:VL onset after eccentric exercise After eccentric exercise, pain manifested and the onset of VMO activity was significantly later than that of the VL muscle during the postural perturbations performed immediately after eccen- tric exercise, and this change in activation remained 24 and 48 h after exercise. Moreover, a greater reduction of the VMO EMG amplitude was observed during the postural perturbations performed post- exercise compared with the VL muscle. The current study is the first to assess changes in the onset of activation of the VMO and VL muscles during postural pertur- bations performed after eccentric exercise and during delayed onset muscle soreness. The altered timing of activation of the VMO:VL muscles after eccentric exercise may be related to the pathophysiological changes and/or pain within the skeletal muscle. Changes in the onset and EMG amplitude, which were observed immediately after eccentric exercise, are most likely explained by a combination of muscle fibre damage and metab- olite accumulation within the muscle, whereas the presence of pain within the quadriceps muscle, which was present 24 and 48 h postexercise, can contribute to delayed or inhibited neuro- muscular responses at the injured site13 30 by inhibition at the cortical and spinal levels.24 A muscular imbalance between the VMO and VL muscles and improper timing of activation between the two muscles are also reported in patients with patellofemoral pain syndrome.2 Furthermore, higher pain inten- sity rated by patients with patellofemoral pain syndrome during the week prior to a stair-stepping task was associated with a sig- nificantly delayed onset time of the VMO muscle relative to the VL muscle during the task.22 Deficits in the timing of muscle activity have been identified in other musculoskeletal pain con- ditions such as neck pain31 low back pain32 and long-standing groin pain.33 Pain is common after high-intensity eccentric exercise, most likely due to fibre injury within the skeletal muscle.20 In the current study, the participants described the greatest pain inten- sity over their inner thigh (vastus medialis muscle), which con- firms previous findings that reported a lower pressure pain threshold and higher pain scores for the VMO muscle up to 72 h after eccentric exercise of the quadriceps muscle.13 30 34 Greater soreness over the medial aspect of the quadriceps muscle has also been reported to be associated with a larger reduction of muscle activity and signal conduction velocity for the VMO muscle,13 14 30 35 which may contribute to the delayed onset of VMO activity observed in the current study. For example, studies investigating muscle fibre conduction vel- ocity have shown that after high-intensity exercise of the quadri- ceps muscle, a greater reduction in conduction velocity is observed for the VMO muscle, and the recovery of conduction velocity in the VMO muscle occurs later than for other muscles of the quadriceps.14 30 The highest intensity of pain rated over the VMO muscle and the larger reduction in conduction vel- ocity of the VMO suggests that the VMO muscle is more sus- ceptible to fibre injury during eccentric exercise, most probably due to high force production in this area to stabilise the patella during high load leg exercise. Accordingly, VMO muscle weak- ness has been shown to be one of the most common muscular imbalances in athletes with knee pain. For example, Grana and Kriegshauser36 reported that in the presence of knee injury the VMO muscle is the first to atrophy and the last to respond to rehabilitation. Gerber et al37 also reported greater atrophy of the VMO compared with other quadriceps components in ath- letes suffering from a traumatic knee injury. The altered onset of VMO:VL activity after eccentric exercise could also be explained by remodelling of the neuromuscular junction,38 changes in proprioceptive function39 and an alter- ation in muscle fibre membrane properties at the injured sites.18 There is evidence of membrane depolarisation as a result of remoulding of the neuromuscular junction and/or fibre mem- brane disruption after eccentric exercise, which may have Figure 4 Scatter plot of the per cent change in electromyography (EMG) onset (average for the vastus medialis obliqus (VMO) and vastus lateralis (VL) muscles) versus the per cent change in EMG average rectified value (average for the VMO and VL muscles) during postural perturbations performed at baseline compared with the postexercise sessions (average for all postexercise sessions). Data from all participants and all muscles are pooled together. The negative correlation indicates that the increased EMG onset time at the postexercise sessions is partially associated with the decreased muscle activation observed during that session. Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015 5 Original article group.bmj.comon August 21, 2013 - Published bybjsm.bmj.comDownloaded from
  • 7. impaired conduction of action potentials along the muscle fibre.14 15 17 18 Additionally, the slowing of reflex muscle activ- ity could also be due to the loss of proprioceptive input from the injured site as reported in previous studies.16 Methodological considerations Sustained contraction until task failure performed before a per- turbation may influence muscle onset. However, in the current study, the participants were given 20 min to rest and recover from muscle fatigue. Accordingly, a greater difference in VMO: VL onset observed following eccentric exercise, with respect to the baseline condition, suggests that the change in VMO:VL onset across testing sessions was the result of muscle damage and not simply due to fatigue. CONCLUSION The onset of the VMO muscle is significantly later than that of the VL muscle during rapid destabilising perturbations of the leg following eccentric exercise, most likely due to muscle fibre damage and pain. This finding suggests that eccentric exercise of the quadriceps can delay reflex activity of the vastii muscles and may compromise patella stabilisation, thereby leaving the knee complex more vulnerable to injury. Further studies are needed to determine how long after eccentric exercise the VMO:VL timing will return to normal. This knowledge may be useful to prevent patellofemoral disorders after high-intensity eccentric exercise. What are the new findings? ▸ Muscles subjected to eccentric loading become stiff and sore 24 h after exercise and neuromuscular control of the injured muscle may be altered. ▸ Previous studies, however, have typically examined the effect of eccentric exercise on muscle activity during non-functional activities. ▸ This study shows that eccentric exercise of the quadriceps alters the onset of activation of the vastii muscles to stabilise the patella during rapid, unexpected perturbations to the knee. ▸ The type of perturbation used resembles perturbations that might commonly be encountered during sport activities. How might it impact on clinical practice in the near future? ▸ Patellofemoral pain syndrome is a common complaint in the sporting and general populations, especially when repetitive lower limb eccentric loading is frequently performed. ▸ The knowledge gained from this study may be relevant for the understanding and prevention of exercise-related patella disorders which develop following unaccustomed exercise. Acknowledgements The authors are grateful to Professor Lars Arendt-Nielsen for his support. Contributors NH was responsible for the concept development and study design, data collection, analysis and interpretation of the data and writing of the manuscript. DF was responsible for the concept development and study design, analysis and interpretation of the data, and writing of the manuscript. Funding This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors. Competing interests None. Ethics approval The Ethics committee of Nordjylland, Denmark (N 20070019). Provenance and peer review Not commissioned; externally peer reviewed. Data sharing statement The data from the study are included in this manuscript. REFERENCES 1 Hedayatpour N, Hassanlouei H, Arendt-Nielsen L, et al. Delayed-onset muscle soreness alters the response to postural perturbations. Med Sci Sports Exerc 2011;43:1010–16. 2 Witvrouw E, Sneyers C, Lysens R, et al. Reflex response times of vastus medialis oblique and vastus lateralis in normal subjects and in subjects with patellofemoral pain syndrome. J Orthop Sports Phys Ther 1996;24:160–5. 3 Ng EC, Chui MP, Siu AY, et al. Ankle positioning and knee perturbation affect temporal recruitment of the vastii muscles in people with patellofemoral pain. Physiotherapy 2011;97:65–70. 4 Cavazzuti L, Merlo A, Orlandi F, et al. Delayed onset of electromyographic activity of vastus medialis obliquus relative to vastus lateralis in subjects with patellofemoral pain syndrome. Gait Posture 2010;32:290–5. 5 Grabiner MD, Koh TJ, Draganich LF. Neuromechanics of the patellofemoral joint. Med Sci Sports Exerc 1994;26:10–21. 6 Voight ML, Wieder DL. Comparative reflex response times of vastus medialis obliquus and vastus lateralis in normal subjects and subjects with extensor mechanism dysfunction. An electromyographic study. Am J Sports Med 1991;19:131–7. 7 Fulkerson JP, Shea KP. Current concepts review: disorder of patellofemoral alignment. J Bone Joint Surg Am 1990;72:1424–9. 8 Insall J. Current concepts review: patellar pain. J Bone Joint Surg Am 1982;64:147–52. 9 Fulkerson JP, Shea KP. Mechanical basis for patellofemoral pain and cartilage breakdown. In: Ewing JW, ed. Articular cartilage and knee joint function: basic science and arthroscopy. New York, NY: Raven Press, 1990:93–101. 10 DeHaven KE, Dolan WA, Mayer PJ. Chondromalacia in athletes. Am J Sports Med 1979;7:5–11. 11 Holmes SW, Clancy WG. Clinical classification of patellofemoral pain and dysfunction. J Orthop Sports Phys Ther 1998;28:299–306. 12 Bobbert MF, Hollander AP, Huijing PA. Factors in delayed onset muscular soreness of man. Med Sci Sports Exerc 1986;18:75–81. 13 Hedayatpour N, Falla D, Arendt-Nielsen L, et al. Sensory and electromyographic mapping during delayed-onset muscle soreness. Med Sci Sports Exerc 2008;40:326–34. 14 Hedayatpour N, Falla D, Arendt-Nielsen L, et al. Motor unit conduction velocity during sustained contraction after eccentric exercise. Med Sci Sports Exer 2009;41:1927–33. 15 Chen YW, Hubal MJ, Hoffman EP, et al. Molecular responses of human muscle to eccentric exercise. J Appl Physiol 2003;95:2485–94. 16 Jennings AG, Seedhom BB. Proprioception in the knee and reflex hamstring contraction latency. J Bone Joint Surg Br 1994;76:491–4. 17 Clarkson PM, Byrnes WC, McCormick K, et al. Muscle soreness and serum creatine kinase activity following isometric, eccentric, and concentric exercise. Int J Sports Med 1986;7:152–5. 18 McBride TA, Gorin FA, Carlsen RC. Membrane depolarization following high resistance eccentric exercise in rat tibialis anterior. FASEB J 1994;8:A307. 19 Van Doornik J, Sinkjaer T. Robotic platform for human gait analysis. IEEE Trans Biomed Eng 2007;54:1696–702. 20 Newham DJ, Jones DA, Clarkson PM. Repeated high-force eccentric exercise: effects on muscle pain and damage. J Appl Physiol 1987;63:1381–6. 21 Smith LL. Acute inflammation: the underlying mechanism in delayed onset muscle soreness? Med Sci Sports Exerc 1991;23:542–51. 22 Boling MC, Bolgla LA, Mattacola CG, et al. Outcomes of a weight-bearing rehabilitation program for patients diagnosed with patellofemoral pain syndrome. Arch Phys Med Rehabil 2006;87:1428–35. 23 Babault N, Desbrosses K, Fabre MS, et al. Neuromuscular fatigue development during maximal concentric and isometric knee extensions. J Appl Physiol 2006;100:780–5. 24 Le Pera D, Graven-Nielsen T, Valeriani M, et al. Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain. Clin Neurophysiol 2001;112:1633–41. 25 Kaufman MP, Hayes SG, Adreani CM, et al. Discharge properties of group III and IV muscle afferents. Adv Exp Med Biol 2002;508:25–32. 26 Kirsch RF, Rymer WZ. Neural compensation for fatigue-induced changes in muscle stiffness during perturbations of elbow angle in human. J Neurophysiol 1992;68:449–70. 27 Hortobagyi T, Houmard J, Fraser D, et al.. Normal forces and myofibril disruption after repeated eccentric exercise. J Appl Physiol 1998;84:492–8. 6 Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015 Original article group.bmj.comon August 21, 2013 - Published bybjsm.bmj.comDownloaded from
  • 8. 28 Pal S, Besier TF, Draper CE, et al. Patellar tilt correlates with vastus lateralis: vastus medialis activation ratio in maltracking patellofemoral pain patients. J Orthop Res 2012;30:927–33. 29 Cowan SM, Bennell KL, Hodges PW, et al. Simultaneous feed forward recruitment of the vasti in untrained postural tasks can be restored by physical therapy. J Orthop Res 2003;21:553–8. 30 Hedayatpour N, Falla D, Arendt-Nielsen L, et al. Effect of delayed-onset muscle soreness on muscle recovery after a fatiguing isometric contraction. Scand J Med Sci Sports 2010;20:145–53. 31 Falla D, Jull G, Hodges PW. Feedforward activity of the cervical flexor muscles during voluntary arm movements is delayed in chronic neck pain. Exp Brain Res 2004;157:43–8. 32 Hodges PW, Richardson CA. Delayed postural contraction of transversus abdominis in low back pain associated with movement of the lower limb. J Spinal Disord 1998;11:46–56. 33 Cowan SM, Schache AG, Brukner P, et al. Delayed onset of transversus abdominus in long-standing groin pain. Med Sci Sports Exerc 2004;36:2040–5. 34 Newham DJ, Mills KR, Quigley BM, et al. Pain and fatigue after concentric and eccentric muscle contractions. Clin Sci 1983;64:55–62. 35 Hedayatpour N, Falla D. Non-uniform muscle adaptations to eccentric exercise and the implications for training and sport. J Electromyogr Kinesiol 2012;22:329–33. 36 Grana WA, Kriegshauser LA. Scientific basis of extensor mechanism disorders. Clin Sports Med 1985;4:247–57. 37 Gerber C, Hoppeler H, Claassen H, et al. The lower-extremity musculature in chronic symptomatic instability of the anterior cruciate ligament. J Bone Joint Surg Am 1985;67:1034–43. 38 Warren GL, Angels CP, Shah SJ, et al. Uncoupling of in vivo torque production from EMG in mouse muscles injured by eccentric contractions. J Physiol 1999;515:609–19. 39 Weerakkody NS, Whitehead NP, Canny BJ, et al. Large-fiber mechanoreceptors contribute to muscle soreness after eccentric exercise. J Pain 2001;2:209–19. Hedayatpour N, et al. Br J Sports Med 2013;0:1–7. doi:10.1136/bjsports-2012-092015 7 Original article group.bmj.comon August 21, 2013 - Published bybjsm.bmj.comDownloaded from
  • 9. doi: 10.1136/bjsports-2012-092015 published online August 19, 2013Br J Sports Med Nosratollah Hedayatpour and Deborah Falla exercise? that underpins knee pain after eccentric following eccentric exercise: a mechanism response to rapid postural perturbations Delayed onset of vastii muscle activity in http://bjsm.bmj.com/content/early/2013/08/19/bjsports-2012-092015.full.html Updated information and services can be found at: These include: References http://bjsm.bmj.com/content/early/2013/08/19/bjsports-2012-092015.full.html#ref-list-1 This article cites 37 articles, 8 of which can be accessed free at: P<P Published online August 19, 2013 in advance of the print journal. service Email alerting the box at the top right corner of the online article. Receive free email alerts when new articles cite this article. Sign up in Collections Topic (343 articles)Musculoskeletal syndromes (178 articles)Degenerative joint disease Articles on similar topics can be found in the following collections (DOIs) and date of initial publication. publication. Citations to Advance online articles must include the digital object identifier citable and establish publication priority; they are indexed by PubMed from initial typeset, but have not not yet appeared in the paper journal. Advance online articles are Advance online articles have been peer reviewed, accepted for publication, edited and http://group.bmj.com/group/rights-licensing/permissions To request permissions go to: http://journals.bmj.com/cgi/reprintform To order reprints go to: http://group.bmj.com/subscribe/ To subscribe to BMJ go to: group.bmj.comon August 21, 2013 - Published bybjsm.bmj.comDownloaded from
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