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Department of Integrative Physiology, University of Colorado, Boulder, Colorado
Submitted 17 May 2004 ; accepted in final form 28 January 2005
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ABSTRACT |
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20% of the net cost of normal running. Even with the greatest ESA, mean electromyograph (mEMG) of the medial gastrocnemius and soleus muscles during later portions of stance phase did not change significantly compared with normal running, indicating that these muscles are not responsible for the initiation of leg swing. However, with ESA, rectus femoris mEMG during the early portions of swing phase was as much as 74% less than during normal running, confirming that it is responsible for the propagation of leg swing. biomechanics; locomotion; electromyography; energetic cost
Energetics.
Several mechanical functions are thought to determine the energetic cost of level running, including support of body weight, horizontal propulsion, and leg swing. The most significant is the production of vertical force to support body weight (18). Additionally, horizontal propulsion accounts for 40% of the net energetic cost of running (8). However, the portion of the energetic cost of running due to leg swing remains controversial (19, 33). Leg swing in running is a combination of active and passive mechanics (2, 6). In addition to initiating and propagating leg swing, muscle actions are also needed for maintaining flexed knee and ankle joint positions during swing and arresting leg motion at the end of the swing phase.
A diverse array of studies has creatively but indirectly investigated the energetic cost of leg swing in running and found it to be negligible. Torso loading (30) and simulated reduced gravity (13, 27) experiments have found direct proportionality between the vertical force needed to support weight and the energetic cost of running, implying that leg swing does not comprise a substantial fraction of the cost of running. If leg swing costs were substantial, then such loading and unloading procedures would cause changes in cost that are less than proportional. Thus Taylor et al. (30) surmised that leg swing does not exact a significant metabolic cost. A comparison of gazelles and cheetahs, animals with the same body weight but with light vs. massive limbs, found the metabolic cost of locomotion to be indistinguishable. This evidence also suggests that the cost of leg swing is small (31). Overall, these studies indicate that leg swing comprises a negligible fraction of the energetic cost of running.
Results from limb-loading studies, biomechanical analyses, and blood flow experiments support the opposite view. Whereas adding 1% of body weight to the torso causes a 1% increase in metabolic rate, adding 1% of body weight to the feet causes as much as a 9% increase in running humans (9, 17, 21, 25). This evidence suggests that the cost of leg swing is more substantial than the cost of supporting body weight. Furthermore, loads placed on the feet cause a greater increase in metabolic rate than loads placed more proximally on the leg (21). This suggests that the moment of inertia of leg segments about proximal leg joints determines the energetic cost of leg swing. Limb loading experiments on other species also indicate a significant cost of leg swing (29). Classically, Hill (15) and more recently van Ingen Schenau et al. (33) have reasoned that the mechanical work involved in leg swing accounts for the vast majority of the metabolic cost of running. Most recently, Marsh et al. (19, 20), quantified leg muscle blood flow in running birds and concluded that leg swing comprises 26% of the net cost of normal running. Overall, these studies indicate that leg swing is a substantial determinant of the energetic cost of running.
Our first aim was to quantify the energetic cost of initiating and propagating leg swing in running. We applied external swing assist (ESA) forces to accelerate the swing leg forward at the end of stance phase. We hypothesized that the energetic cost of running would decrease when ESA was provided. We suggest that a decrease in energy consumption with the optimal ESA would indicate the normal cost of initiating and propagating leg swing.
Muscle activity. Remarkably, we do not have a definitive understanding of which muscles are responsible for initiating and propagating leg swing in running. In walking, ankle plantar flexor muscle(s) contributes to swing phase initiation (16, 23, 26). In running, these muscles are active during the second half of stance phase (22), suggesting that they could contribute to leg swing initiation. The hip flexor muscles, i.e., rectus femoris (RF), iliacus (IL), and psoas (PS), are active just before and during early leg swing and thus are thought to contribute to leg swing initiation and propagation (1, 22, 24, 28). However, these inferences are based on temporal correlation rather than clear cause and effect. During the swing phase of running, the hamstring muscles are active to maintain a flexed knee, and the anterior tibialis (AT) presumably acts to maintain a dorsiflexed ankle. At the end of swing phase, muscles such as the biceps femoris (BF) are active, presumably to arrest leg motion via eccentric actions.
Our second aim was to more definitively understand which muscles are responsible for leg swing initiation and propagation in running. We recorded electromyographic (EMG) signals from key leg muscles during normal running and with ESA. We hypothesized that medial gastrocnemius (MG), soleus (Sol), and RF EMG would be reduced during late stance and/or early swing phases when ESA was provided. We suggest that a decrease in the activation of these muscles would indicate how much they normally contribute to leg swing.
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METHODS |
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Subjects. Ten recreational distance runners (5 men, 5 women; age: 26.1 ± 3.3 yr; mass: 65.7 ± 10.0 kg; height 1.74 ± 0.08; mean ± SD) volunteered to participate. Subjects regularly ran at least 2 h/wk. They were in good health and free of musculoskeletal injury. The experimental protocol was approved by the University of Colorado Human Research Committee. All subjects gave written, informed consent.
Protocol. The experiment commenced with a standing metabolic rate trial and a 10-min control (normal running) trial without the external swing assist (ESA 0%). All subjects were familiar with treadmill running before data collection. Subjects ran on a Quinton 18-60 treadmill at 3.0 m/s. The experimental trials consisted of four randomly ordered, 7-min ESA trials (ESA 1, 2, 3, and 4% body weight). A second 10-min ESA 0% trial concluded each experimental session. Subjects rested for at least seven min between running trials.
ESA. The ESA device applied an independent anterior force to each shoe, above the distal dorsum of the foot, during the swing phase (Fig. 1). During the stance phase, as the foot moved backward, the treadmill motor acted to stretch the rubber tubing. At the onset of swing phase, the device pulled the foot and leg anteriorly. Shortly after midswing position, the cable clamp on the nylon cord reached the stopper plate and the ESA force dropped to zero. Thus, beyond midswing, the leg naturally followed through the remainder of swing phase. In pilot experiments without the stopper plate, ESA forces >4% caused delayed onset knee flexor muscle soreness presumably due to eccentric muscle actions during the swing phase. So, for safety reasons and to minimize eccentric muscle actions, we employed the stopper plate and limited the ESA setting to 4% body weight during the experimental trials.
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1% of body weight greater than the specified force level. During the swing phase, as the rubber tubing shortened, the ESA force decreased to the specified force, at which point the cable clamp met the stopper plate and the ESA force immediately dropped to zero (i.e., the nylon cord went slack).
Energetics.
We measured rates of oxygen consumption (
O2) and carbon dioxide production (CO2) using an open-circuit respirometry system (Physio-Dyne Instrument, Quogue, NY). We measured standing metabolic rate before the running trials. For the control and experimental running trials, we allowed 7 and 4 min, respectively, for the subjects to reach steady state, and then we calculated the average O2 (ml O2/s) and CO2 (ml CO2/s) for the subsequent 2 min. We monitored mean respiratory exchange ratios to verify steady-state aerobic metabolism (mean respiratory exchange ratio < 1.0). We calculated metabolic rate, i.e., metabolic power (Pmet; W/kg), using the subjects' body mass and a standard equation (5):
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Stride temporal variables and EMG. To determine when stance and swing phases occurred, we detected foot-strike and toe-off events with foot switches (B & L Engineering, Tustin, CA). We calculated swing time, contact time, and stride frequency from the foot-switch data.
We measured EMG signals using a telemetered amplifier system (Noraxon, Scottsdale, AZ). Before electrode placement, we shaved and prepared the skin with fine sandpaper and alcohol. We placed bipolar surface electrodes (1-cm diameter; silver-silver chloride), 2 cm apart (center to center) on the skin over five muscles (MG, Sol, RF, long head of the BF, and AT) of the right leg according to the guidelines of Cram and Kasman (11). Before the experiment, subjects performed a series of contractions to ensure cross talk was negligible (34). The electrodes remained in place throughout the experimental protocol without being removed or replaced.
We sampled EMG signals at a frequency of 1,000 Hz and applied a recursive second-order Butterworth band-pass digital filter (20–500 Hz). We performed two separate analyses on the EMG signals: temporal patterns and amplitude. We examined the temporal characteristics of each muscle's EMG for normal running to define when in the stride cycle we should evaluate the amplitude. For the temporal analyses, we full-wave rectified the data, and then we used a second-order Butterworth low-pass digital filter (7 Hz) to yield a linear envelope. With foot-strike and toe-off information, we synchronized the EMG signals to the gait events. Through visual inspection of each muscle's normal running EMG data, we determined the time in a gait cycle that a quiescent baseline consistently occurred in all subjects. We calculated the means and standard deviations (SDs) of the baseline data and defined a muscle as active if the EMG linear envelope exceeded a threshold of the baseline plus a certain number of SDs for at least 100 ms. For the different muscles, the number of SDs ranged from two to six, depending on the noise level of the baseline. For each muscle, the same number of SDs was used for all subjects. To calculate mean EMG (mEMG) amplitude, we full-wave rectified the band-pass-filtered data, and then we calculated mEMG on the basis of the temporal EMG characteristics of normal running.
Statistical analyses. Energetic, kinematic, and mEMG data from this study were analyzed across all conditions using a repeated-measure single-factor ANOVA. When warranted, we performed a Tukey's honestly significant difference post hoc test to analyze differences between each ESA level. Significance was defined as P < 0.05.
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RESULTS |
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BF activity patterns were less consistent between subjects than the other muscles studied. All subjects activated the BF in midswing phase (average of 69% of stride cycle), and in 9 of the 10 subjects the BF activity ceased at an average of 129% (late stance phase). Two subjects had brief periods of inactivity from 100 to 116% of the stride cycle. One subject only briefly activated the BF (70–87%). Thus, to evaluate the effect of ESA on the BF during swing phase, we analyzed mEMG from 69 to 100% of the stride cycle for the other nine subjects. To evaluate the effect of ESA on the BF during stance phase, we analyzed mEMG from 16 to 29% of the stride cycle for 9 of 10 subjects; one subject was excluded due to the absence of activation during stance phase.
Nine of 10 subjects maintained activation of the AT from 42 to 106% of the stride cycle (most of swing and early stance). To evaluate the effect of ESA on the AT during swing phase, we analyzed mEMG from 42 to 100% of the stride cycle.
Effect of ESA on EMG amplitude. Decreases in mEMG with ESA indicate that a particular muscle contributes to swing initiation and/or propagation during normal running. We did not detect a significant change during late stance phase in MG (P = 0.38) or Sol (P = 0.76) mEMG (Fig. 5). During the swing phase, however, mEMG of the RF dramatically decreased by 38%, 63%, and 74% (P < 0.0001) in response to the 2, 3, and 4% ESA conditions, respectively (Fig. 5).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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20% of the net cost of running at 3.0 m/s. Although we hypothesized that we would find an energetically optimum ESA force, we did not find such a minimum below the 4% body weight ESA force. The actual total cost of swing may be more or less than 20%. If we had applied greater ESA forces, metabolic cost may have further decreased, but we did not apply forces >4% body weight to avoid injuring our subjects. Another factor to consider is the metabolic cost of arresting leg swing before foot strike. Our ESA device applied a forward pulling force to the feet that might have increased the cost of arresting leg swing and thus counteracted the reduction in swing initiation and propagation costs. However, our EMG data for the BF, a hip extensor and knee flexor muscle, did not show increased activation with ESA in late swing phase. This suggests that the cost of arresting leg swing did not increase due to ESA. However, we did not eliminate the basic cost of arresting leg motion, which properly should be considered part of the total cost of leg swing. AT muscle activity was present during the swing phase and invariant with ESA. The metabolic cost of AT activity must have some, although probably small, metabolic cost. Because we did not reduce, let alone eliminate, BF or AT activity with ESA, our estimate of 20% could be an underestimate of the total cost of leg swing.
On the other hand, the actual cost of swing may be <20% if there is some interaction between leg swing and forward propulsion. The ESA device pulls each leg anteriorly during the first portion of swing phase. Although ESA primarily reduces the body's need to perform work required for leg swing, it also applies a forward propulsive impulse to the whole body. Chang and Kram (8) estimated that forward propulsion comprises 40% of the net metabolic cost of running. Our observed decrease in metabolic cost with ESA probably reflects both a decreased cost of leg swing and a decreased cost of propulsion. Thus we believe that our estimate of leg swing cost of 20% of the net cost of running is a moderate overestimate, but further investigation is needed to consider the interactions of propulsion and swing.
If the cost of leg swing comprises 20% of the net metabolic cost of running, how have whole body loading and unloading studies surmised that it is negligible (13, 30)? Recall that if leg swing costs are substantial, then whole body loading procedures should cause less than proportional increases in cost. Taylor et al. (30) added loads of 20% body weight and found a proportional increase in metabolic cost, but they used only two human subjects in their experimental design. Thus their statistical resolving power may not have been robust enough to detect a small cost of leg swing. Another limitation is that their subjects carried the loads in backpacks, which probably required additional recruitment of abdominal and back postural muscles (3). The metabolic demand of such postural muscles could have inflated the apparent cost of supporting the additional weight and obscured the cost of leg swing. Furthermore, Taylor et al. (30) compared loaded and unloaded gross metabolic cost. We calculated that net metabolic cost and believe that this value gives better insight into the cost of running itself, although that philosophy is controversial (7). More recent studies of loaded running energetics have found less than proportional increases in net metabolic cost due to small (10% body weight) additions of mass balanced around the torso. Cureton and Sparling (12) found a 6.8% increase with an average load of 7.5% body weight. Thorstensson (32) reported a 7.5% increase in response to a 10% body weight load. Bourdin et al. (4) observed a 4.7% increase for a 9.3% body weight load. Cooke et al. (10) found a statistically insignificant 3.3% increase with a 10% body weight load. Obviously, parsing out the small changes in metabolic rate due to only 10% body weight extra loads pushes the limits of accuracy in these measurements. But overall, there is a less than proportional increase in the net metabolic rate when loads are carried around the torso during running. However, Farley and McMahon (13) unweighted their subjects (by 25, 50, and 75%) and found almost exactly proportional decreases in net metabolic cost. It remains unclear why reduced-gravity running experiments suggest that swing cost is negligible, yet several loading experiments suggest that there is some cost of swing.
Recent studies have found similar quantitative results similar to ours using dramatically different and innovative methodology. Marsh et al. (19, 20) measured the rate of blood flow to leg swing and stance muscles in running birds (guinea fowl). They found a direct relationship between cardiac output and systemic O2, so they were able to estimate local oxygen demand using local blood flow. Whereas stance muscles demand the vast majority of the leg blood flow (74%) during running, leg swing muscles demand the remaining 26% of the leg blood flow. Although these measurements are not from human runners, it is intriguing that our estimate of the cost of leg swing is so similar to that of Marsh et al.
EMG. We reject the hypothesis that activation of ankle plantar flexors would decrease with ESA. We did not find changes in mEMG of the MG and Sol muscles with ESA in the second half of stance phase. These results suggest that the plantar flexor muscle group is not responsible for leg swing initiation in running. This finding is in contrast to the idea raised in several walking studies that the ankle plantar flexor(s) initiate leg swing (16, 23, 26). We attribute the activation of the ankle plantar flexor muscles in late stance to the functions of forward propulsion and supporting body weight. Further defining the function of this muscle group is warranted.
We reject the hypothesis that RF activation decreases during late stance phase with ESA. However, as hypothesized, RF activation decreased during the first half of swing phase with ESA. The RF was not characteristically active during normal running in the later portion of stance phase, suggesting that RF does not contribute to leg swing initiation. However, the mEMG of the RF during 40–60% of the stride cycle, decreased progressively and dramatically with ESA. Thus our EMG results show directly that RF muscle activation is responsible for leg swing propagation but not leg swing initiation. Through the elegant use of indwelling fine wire EMG electrodes, Andersson et al. (1) were able to demonstrate that in late stance phase two other major hip flexors, IL and PS, are activated before RF activation. Thus we can still only infer from their study that EMG timing and joint kinematics that IL and/or PS initiate leg swing in running.
Limitations and future study. Our ESA device is simple, is inexpensive, and appears to nearly eliminate the need for active leg swing initiation and propagation during running. However, the force pattern of our ESA is not necessarily energetically optimal, and an actively controlled ESA device might be superior. An ideal ESA device might be activated and deactivated at exact points in the stride cycle and with programmable force magnitudes. An ideal ESA device might also apply separate forces to each leg segment; however, our goal was to begin with a simple device and a simple experimental design. Pulling on multiple leg segments might cause undesirable intersegmental interactions and cocontractions. Finally, an ESA device might somehow eliminate the need for the muscle actions during swing to maintain knee flexion and/or ankle dorsiflexion.
It is likely that the treadmill motor exclusively loaded the elastic cords of the ESA device. We attempted to confirm this by measuring BF muscle activation during stance phase. BF muscle activation during late stance phase (16–29% of stride cycle) actually decreased in response to ESA. In a future ESA study, it would be helpful to collect EMG data from the gluteus maximus muscle during stance phase to further quantify the role of the treadmill motor in loading the ESA device during stance phase. Moreover, because we observed substantial decreases in metabolic cost, the results suggest that the runners did not expend much, if any, additional energy to load the ESA elastic cords.
Our experiment gave insight into the leg swing functions of MG, Sol, and RF, but EMG measurements of other hip flexor muscles such as the IL and PS would provide further information. Another useful experiment would examine the possible increases in activity of these muscles in response to ankle weights that make leg swing more difficult. Moreover, a study investigating the interaction between horizontal propulsion and leg swing is needed to clarify our energetics findings. Specifically, an experiment that combines an applied horizontal force at the waist for center of mass propulsion (8) and ESA would reveal the interaction between horizontal propulsion and leg swing mechanics in running. If the individual effects of each device do not sum when combined, this would indicate that the cost of leg swing initiation and propagation is less than the 20% we found here. We also plan to study the effects of ESA for a range of running speeds because many have argued that leg swing is more costly at faster speeds (14, 15). ESA could also be used to evaluate the cost of leg swing in walking. Finally, we are exploring potential clinical uses of ESA for treadmill walking rehabilitation.
In conclusion, we find that leg swing requires 20% of the net energy consumed in running. Neither MG, Sol, nor RF muscles contribute to leg swing initiation; however, RF does play a significant role in leg swing propagation.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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