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Tam 2018
Tam 2018
Authors: Nicholas Tam1,2, Ross Tucker3, Jordan Santos-Concejero4, Danielle Prins1, and
Robert P. Lamberts1,5
DOI: https://doi.org/10.1123/ijspp.2018-0151
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
Original investigation
Lamberts1,5.
1
– Division of Exercise Science and Sports Medicine, Department of Human Biology,
Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa.
2
– Department of Physiology, Faculty of Medicine and Nursing, University of the Basque
Country UPV/EHU, Leioa, Spain.
3
- World Rugby, Dublin, Ireland
4
– Department of Physical Education and Sport, Faculty of Education and Sport, University
of the Basque Country UPV/EHU, Vitoria-Gasteiz, Spain
5
– Institute of Sport and Exercise Medicine, Division of Orthopaedic Surgery, Department of
Surgery, Faculty of Medicine and Health Sciences, Stellenbosch University, Tygerberg,
South Africa.
Abstract
It is debated whether running biomechanics make good predictors of running economy, with
little known information about the neuromuscular and joint stiffness contributions to
economical running gait. Purpose: The aim of this study was to understand the relationship
running set at 3.3 ms-1, where oxygen consumption was assessed. Overground running trials
were also performed at 3.3 ms-1 to assess kinematics, kinetics and muscle activity.
Spatiotemporal gait variables, joint stiffness, pre-activation and stance phase muscle activity
(gluteus medius; rectus femoris (RF); biceps femoris(BF); peroneus longus (PL); tibialis
anterior (TA); gastrocnemius lateralis and medius (LG and MG) were variables of specific
presented with short ground contact times (r=0.639, p<0.001) and greater strides frequencies
(r=-0.630, p<0.001). Lower ankle and greater knee stiffness were associated with lower
oxygen consumption (r=0.527, p=0.007 & r=0.384, p=0.043, respectively). Only LG:TA co-
activation during stance were associated with lower oxygen cost of transport (r=0.672,
p<0.0001). Conclusions: Greater muscle pre-activation and bi-articular muscle activity during
stance were associated with more economical runners. Consequently, trained runners who
exhibit greater neuromuscular activation prior to and during ground contact, in turn optimise
spatiotemporal variables and joint stiffness, will be the most economical runners.
Introduction:
Running economy, defined as the oxygen or energy cost of transport, has been found
neuromuscular control are of interest to coaches and applied sports scientists as they are
Recently, Moore (2016) published a review article clarifying the current understanding
of the relationship between a range of modifiable biomechanical factors and running economy
4
. These relationships were classified as either beneficial, conflicting or limited/unknown. Most
from beneficial, e.g. self-selected stride length, to conflicting, such as ground contact time and
4,7,10
swing time . Other biomechanical factors which may influence running economy were
discussed. Examples of these include ground reaction forces, swing phase characteristics,
joint stiffness and footstrike pattern. These too were noted to have a conflicting and/or under
10–13
investigated relationship with running economy , while the alignment of the ground
reaction force resultant vector and the leg axis during stance, leg stiffness, stride angles did
movement initiation and regulation, such as muscle activation during propulsion and agonist-
antagonist co-activation are also believed to influence running economy, though fewer studies
15
have explored this relationship to date . Interestingly, research participants involved in
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
5,8
studying these relationships vary from novice runners to elite runners and it is well-
described that with running training, physiological and biomechanical changes take place.
To our knowledge, no study has explored the effect of muscle activation and
hypothesized that better runners would display a lower oxygen cost of transport, and would
present with shorter ground contact times, higher stride frequencies and muscle-activation
Methods:
Thirty trained male runners (age: 25.8 ± 5.0 years; body mass: 66.0 ± 13.3 kg; height:
175.2 ± 7.5 cm) participated in this study and were able to run 10-km in < 45 minutes
(Supplementary Figure 1). All runners were free of injury six months prior to participating in
this study and wore their preferred running shoes throughout the study. Before participating
all runners signed an informed consent, while ethical approval for the study was granted by
Runners completed a constant-speed running set of 6 minutes at 3.3 ms-1, with the
treadmill incline set at 1% 16. This running speed was chosen as being representative of their
self-reported easy training pace, this is equivalent to a 50-min 10-km run. During the test, gas
(COSMED Quark CPET, Rome, Italy), which was calibrated before each session according to
the instructions of the manufacturer. To ensure VO2 steady-state measurements, the speed
selected was slower than the individual lactate threshold of each athlete (further confirmed
during the test by respiratory exchange ratios being below 1.0 during the whole running bout
for all athletes at each speed). VO2 (mlO2·kg−1·min−1) values collected during the last 30 s of
the running bout were averaged and designated as steady-state oxygen cost of transport
were conducted on a 60-m indoor synthetic running track. Participants completed six clean
MX motion analysis system (Oxford Metrics Ltd, UK), sampling at 250 Hz using a modified
Helen-Hayes marker set. Ground reaction force (GRF) data were collected using two 900 ×
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600 mm force platform (AMTI, USA), sampling at 2000 Hz, synchronised with the motion
capture system. Surface electromyography (EMG) was measured on seven right lower limb
muscles, namely gluteus medius (GM), rectus femoris (RF), biceps femoris (BF), peroneus
longus, tibialis anterior (TA) and gastrocnemius lateralis and medius (LG and MG,
respectively). Prior to placement, the skin areas were prepared and two surface electrodes
17
placed on the muscle location according to SENIAM guidelines . Leads and pre-amplifiers
connected to the electrodes were secured with medical grade tape to avoid artefacts from
lower limb movement during running. The transmitter unit was secured in a harness strapped
to the participant’s back and data sampled at 2000 Hz (Noraxon 2400T G2, Noraxon, USA).
After completing running trials at the designated speeds, the runners then completed three
Marker trajectory and kinetic data were filtered using a low-pass fourth-order
Butterworth filter with a cut-off frequency of 8 and 60 Hz, respectively. For each trial, one
complete gait cycle was analysed. The lower body PlugInGait model calculated three-
dimensional lower extremity joint angles and net resultant joint moments using a Newton-Euler
inverse dynamics approach using this data. Joint angles were de-scribed using the joint
coordinate system 18. Three-dimensional joint moments were expressed as external moments
Knee and ankle joint angles and moments were extracted for each participant’s right
limb and were averaged over the 6 trials. Stance phase was the time over which a vertical
force exceeded one standard deviation (SD) above baseline force platform noise and
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
continued to elevate until toe-off (vertical force <1 SD baseline). Further, peak vertical ground
reaction force (in body weight (BW) units) extracted and vertical initial rate loading rate (BW·s-
1
) quantified between 200 N and 90% of the impact transient peak (first peak prior to
maximum). When no distinct impact transient was present, the same parameters were
measured using the average percentage of stance ±1 SD as determined for each condition in
19
trials with an impact transient . Sagittal plane knee and ankle stiffness (quasi-torsional
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stiffness) were calculated for load acceptance phase according previous published methods
20
. Specifically, the load acceptance phase is the point at which the joint angle reached
maximum flexion in mid-stance of the ground contact phase. The angular distance from initial
touchdown to maximum flexion angle in mid-stance was determined and the magnitude of the
moment at the same points. A linear fit of the torque-angle was determined as the magnitude
of joint stiffness
The raw digital EMG signal of both sub-maximal and sprint trials were rectified and root
21
mean squared (RMS) analysis performed at 50 Hz to smooth the data . Average EMG
amplitude was calculated for pre-activation and stance phase, reported as a percentage of
maximal sprint. Pre-activation was defined as the EMG activity 100 ms before ground contact.
Further, RF:BF, RF:GM and LG:TA agonist-antagonist muscle co-activation ratios were
22
computed for each phase . Agonist: antagonist EMG ratios of 1.0 indicate equal activation
of the two antagonistic muscles, whereas co-activation ratios greater than 1.0 indicate
increased agonist (RF or LG) activation compared with the antagonist (BF, GM or TA)
muscles. Ratios less than 1 indicate greater activity of the antagonist relative to the agonist
muscle 22.
Statistical analysis:
Data were screened for normality of distribution using a Shapiro-Wilk Normality Test.
Effect sizes (ES) were calculated using a Cohen's d and assessed according to the scale
23
proposed by Hopkins et al (2009) . Relationships between EMG and metabolic, kinematic
and kinetic variables were assessed with Pearson’s correlations for data that were parametric
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
or Spearman’s Rho correlations for non-parametric data. 95% confidence intervals (CI) were
calculated for the correlations. Differences were deemed statistically significant at p<0.05.
Statistical analyses were performed using SPSS version 22 (IBM Corporation, USA) and
Results:
Descriptive characteristics of the runners are presented in Table 1, with the runners’
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10-km time ranging from 28.10 – 44.82 minutes. Across the whole group, reduced oxygen
cost of transport was associated with shorter ground contact times (r=0.639, p<0.001, large
effect) and greater stride frequency (r=-0.630, p<0.001, large effect) (Figure 1A & B,
respectively). Stride duration, length and swing time were not associated with oxygen cost of
Oxygen cost of transport was related to measures of both knee and ankle joint stiffness
(Figure 2). As ankle stiffness increased, oxygen cost of transport increased (r=0.527, p=0.007,
large effect) (Figure 2A), whereas higher knee stiffness was associated with a lower oxygen
cost of transport (r=0.384, p=0.043, moderate effect) (Figure 2B). With regards muscle co-
relatively greater LG activation), oxygen cost of transport increased (r=0.672, p<0.0001, large
For pre-activation of the lower limb, oxygen cost of transport was unaffected by tibialis
both medial and lateral gastrocnemius increased (r=-0.661, p<0.0001, large effect and r=-
0.535, p=0.003, large effect respectively) (Table 2). In addition, higher peroneus longus pre-
activation was associated with reduced oxygen cost of transport (r=-0.518, p=0.004).
Oxygen cost of transport was negatively associated with biceps femoris and gluteus
medius pre-activation (r=-0.431, p=0.019, moderate effect and r=-0.442, p=0.016, moderate
effect, respectively), as well as rectus femoris pre-activation (r=-0.373, p=0.046) (Table 2).
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
During ground contact, fewer relationships between muscle activation and running
economy were found. However, both higher medial gastrocnemius activation and higher
rectus femoris during ground contact time were associated with a lower oxygen cost of
Discussion:
The aim of this study was to investigate the influence of muscle activation and
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spatiotemporal gait parameters on oxygen cost of transport in runners ranging in ability from
elite to merely trained. In particular, we wished to address previous studies conflicting findings
relationship between spatiotemporal factors and oxygen cost of transport and wished to further
A novel and important aspect of this study was the wide range of running abilities, and
running economies, of participants in the study – the oxygen cost of transport ranged from
174.93 to 242.73 mlkg-1km-1. This is important because many previous studies in trained
runners have assessed more homogenous groups 7, including other studies on elite Kenyan
runners spanning a range of running abilities, the present study was better able to discern how
The first important findings of this study were the observed relationships between
greater pre-activation of the lower limb posterior musculature and improved running economy.
This suggests that greater pre-activation reduces the metabolic demand of running, and thus
lower the oxygen cost of transport. This emphasises the importance of neuromuscular pre-
activation in the biomechanical preparation for ground contact to optimizing joint stiffness and
stability for efficient running 15. The mechanism for this reduction in oxygen cost as a result of
increased pre-activation may be that pre-emptive neuromuscular control of the joint decreases
the need for corrective muscle activation at and after ground contract where loading forces
are applied to joints. The ability for the muscles to anticipate the magnitude of force they are
required to tune to or attenuate may optimize joint stabilisation as well as cost-effective energy
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
25
transfer for forward motion . The latter agrees with Hamner et al., 2010, who found that the
posterior musculature contributed to about half of the peak vertical support after initial contact
26
. Thus, the ability for muscles to tune or pre-activate prior to ground contact may enable
runners to efficiently transfer energy during the braking phase towards propulsion.
biceps femoris and gastrocnemius during ground contact while running at 5 ms-1. In the
present study, we find no such relationship, either at ground contact or during pre-activation
when running at 3.3 ms-1. This may be because the pre-activation serves to reduce the need
for muscle activity during ground contact, as described, or may be the result of different
running speeds 9.
Interestingly, the effect sizes of the pre-activation correlations and oxygen cost of
transport reported in this study appear to be larger at the distal end of the lower limb with
smaller effects proximally. The only anterior muscle found to correlate with running economy
was rectus femoris, although it only bore a small effect. Collectively, these findings suggest
the importance of muscle pre-activation in regulating leg stiffness especially from the distal
28
lower limb that makes first contact with the ground . In addition, this finding supports the
small contribution of tibialis anterior pre-activation on both stiffness and running economy.
Another notable finding was that greater rectus femoris and medial gastrocnemius
activation during ground contact was associated with reduced oxygen cost of transport. These
observations may support the findings of Heise et al. who described an improved oxygen cost
of transport with longer activation of bi-articular muscles during swing 29. However, in contrast
to Heise et al, our findings relate to the ground contact phase rather than swing phase. These
findings further suggest that the most economical runners rely on greater bi-articular muscle
activation, like rectus femoris to perform the dual role of hip flexion and knee extension.
Similarly, the medial gastrocnemius acts to perform both knee flexion and plantarflexion. In
contrast to mono-articular muscles that may require substantially greater energy to perform
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
30
singular functions . As such, bi-articular muscles appear energy efficient as they span two
joints and simultaneously work to provide optimal stability of multiple joints and efficiently
A further finding of this study was that lower oxygen cost of transport was associated
with lower lateral gastrocnemius – tibialis anterior co-activation during ground contact. This
observation suggests that excessive lateral gastrocnemius activity, relative to tibialis anterior
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activity, is costly to oxygen cost of transport. In addition, a large co-activation ratio may not
just be inefficient and metabolically costly, it may not allow the joint to actively attenuate the
load through movement but instead through muscle tuning during the ground contact phase
25
.
We found that oxygen cost was positively correlated with ankle stiffness. This finding
supports the previous finding on lateral gastrocnemius – tibialis anterior co-activation ratio
during ground contact and running economy, since increasing lateral gastrocnemius activity,
which we found increases oxygen cost, may increase the stiffness of the ankle. In addition,
balanced or equitable activity of the shank muscles may be favourable metabolically, as the
gastrocnemius is a bi-articular muscle that would provide efficient joint stabilization across to
Interestingly, oxygen cost of transport was inversely associated with knee stiffness.
This suggests that knee joint stability is important for running performance, and whether or not
this stiffness maybe harmful for joint health remains to be elucidated. Previous research has
associated greater agonist-antagonist muscle co-activation ratio of the thigh with increased
15
knee stiffness during ground contact . Collectively, we are able to further understand the
metabolic cost were reduced ground contact time and increased stride frequency during
running at 3.3 ms-1. Both these spatiotemporal factors combine to attain optimal metabolic
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
efficiency when running at 3.3 ms-1, inferring that successful runners are those that are able
to minimise their ground contact time whilst increasing their stride frequency. Black et al.
(2017) suggested that the optimum speed for economical running would fall within 70% of an
athlete’s lactate turn point, which was found to be 3.61 ms-1 in their cohort 32. Collectively, the
data from this current study and that of previous research 7,32 illustrate that when running at a
comfortable self-selected speed, the optimal associated biomechanics will involve shorter
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Mechanistically, shorter ground contact times may reduce the duration of the braking
phase during stance. This is usually associated with greater pre-activation of the shank
muscles, which has been proposed to increase the sensitivity of the muscle spindle
economy 33. Regarding stride frequency, our results also agree with previous literature 34.
An important reason why this relationship between these spatiotemporal variables and
4,7,10
running economy remains conflicted may be athlete training status and the subsequent
32
running speed selected for assessment as discussed by Black et al. . In this respect, we
emphasize that the relationships we describe in this study are present in a group of trained
runners of wide-ranging abilities and running economies. We suggest that this highlights the
relationships in very homogenous groups very difficult. Previous studies have often concluded
that no relationship exists between running economy and these variables, when in fact they
may simply be observing a phenomenon across too narrow a range of the outcome variable
(oxygen cost of transport, in this case), and the predictor variable (spatiotemporal variables).
It must be acknowledged that the speed assessed in this study represents a relatively
low intensity for the elite runners than for the trained group, relative to their 10-km race time.
However, we ensured that no athlete was running beyond their threshold intensity using an
RER of 1.0 as a cut-off, and so believe the values to be valid. However, we cannot discount
that biomechanical changes at relatively slower speeds for the elite runners may make the
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
comparison with trained runners at relatively higher speeds an imperfect one. Finally, a
limitation of this study is that oxygen cost was assessed on a treadmill, whereas
spatiotemporal factors and muscle activation were measured during overground running at a
different time. However, running speeds were ensured to be well replicated between trials.
Practical Applications:
identify and stratify athletes with great potential and has been known to be especially good at
doing this in athletes with very similar VO2 values. With this in mind, it is much debated about
the ability of various biomechanical and neuromuscular variables associated with a lower
oxygen cost of transport (running economy). This study has found that in general trained
runners with broad running abilities (< 45 min 10-km time) that shorter ground contact times
and greater stride frequencies are desirable. In addition, the ability to exhibit greater muscular
pre-activation is beneficial in lower the oxygen cost of transport. Thus, trained runners may
find it beneficial to included exercises that improve gait technique and neuromuscular
determine whether indeed, the factors are modifiable or not in one’s gait pattern.
Conclusion:
Trained runners able to run 10-km in < 45 minutes (3.7 ms-1) when running at 3.3 ms-
1
are most economical when running with shorter ground contact times and increased stride
frequency. More economical runners also exhibit lower ankle but greater knee stiffness. This
is associated with greater muscle pre-activation prior to ground contact and greater bi-articular
muscle activation (rectus femoris and medial gastrocnemius) during ground contact. Lastly,
balanced or equal lateral gastrocnemius – tibialis anterior muscle activation during ground
contact was also found to be more economical. The findings from this study show that the
most economical runners exhibit refined neuromuscular control prior to and during ground
contact that facilitate optimal spatiotemporal running biomechanics such as shorter ground
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
contact times and higher stride frequencies when running at 3.33 ms-1. Further studies should
determine whether these factors are indeed modifiable to improve running performance.
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“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
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© 2018 Human Kinetics, Inc.
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International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
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“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
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Figure 1: Correlations between oxygen cost of transport (running economy) and (A) ground
contact time; (B) stride frequency; (C) stride duration; (D) swing time; € stride length in trained
runners, running at 3.3 m s-1. Dotted lines represent 95% confidence intervals.
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
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Figure 2: Correlations between oxygen cost of transport (running economy) at 3.3 m s -1 and
(A) ankle and (B) knee joint stiffness and (C) lateral gastrocnemius – tibialis anterior (LG:TA)
co-activation during ground contact. Dotted lines represent 95% confidence intervals.
“Running Economy: Neuromuscular and Joint Stiffness Contributions in Trained Runners” by Tam N et al.
International Journal of Sports Physiology and Performance
© 2018 Human Kinetics, Inc.
Group
n 30
age (years) 25.76 ± 4.99
body mass (kg) 66.00 ± 13.33
height (m) 175.19 ± 7.52
Running economy (mlkg-1km-1) 206.03 ± 19.02
10-km time (min) 36.03 ± 7.46
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Table 2: The relationship between muscle activity during pre-activation or ground contact (%
max sprint) and oxygen cost of transport (ml.kg-1∙km-1).