Journal of Applied Biomechanics, 2013, 29, 481-489 © 2013 Human Kinetics, Inc. An Official Journal of ISB www.JAB-Journal.com ORIGINAL RESEARCH Changes in Kinematics, Metabolic Cost, and External Work During Walking With a Forward Assistive Force Christopher A. Zirker, Bradford C. Bennett, and Mark F. Abel University of Virginia We examined how the application of a forward horizontal force applied at the waist alters the metabolic cost, kinematics, and external work of gait. Horizontal assist forces of 4%, 8% and 12% of a subject’s body weight were applied via our testing apparatus while subjects walked at comfortable walking speed on a level treadmill. Kinematic and metabolic parameters were measured using motion capture and ergospirometry respectively on a group of 10 healthy male subjects. Changes in kinematic and metabolic parameters were quantified and found similar to walking downhill at varying grades. A horizontal assist force of 8% resulted in the greatest reduction of metabolic cost. Changes in recovery factor, external work, and center of mass (COM) movement did not correlate with changes in metabolic rate and therefore were not driving the observed reductions in cost. The assist force may have performed external work by providing propulsion as well as raising the COM as it pivots over the stance leg. Assist forces may decrease metabolic cost by reducing the concentric work required for propulsion while increasing the eccentric work of braking. These findings on the effects of assist forces suggest novel mobility aids for individuals with gait disorders and training strategies for athletes. Keywords: gait, treadmill walking, energy, kinematics During walking, the body adapts to maintain stability and efficiency under a variety of circumstances. There is an expanding body of research examining the energy required for locomotion under different environmental conditions and the underlying biomechanical adaptations. Changes in energy requirements during locomotion have been studied extensively on different surfaces such as grass and sand,1,2 uphill and downhill gradients,3–5 and at different speeds.6 One interesting walking condition occurs when an external force is applied in the horizontal direction such that the propulsion required for locomotion is reduced. Prior work found that an assistive horizontal force could reduce metabolic energy consumption during walking by up to 47% when 10% of a subject’s body weight pulled forward at the waist.7 Such reductions suggest that this type of assistance could be helpful in assistive devices for individuals such as those with cerebral palsy where the high metabolic cost of ambulation limits their participation in society. However, to date there is no research into the kinematics or mechanical work of Christopher A. Zirker (Corresponding Author) is with the Department of Mechanical and Aerospace Engineering, University of Virginia, Charlottesville, VA. Bradford C. Bennett is with the Department of Mechanical and Aerospace Engineering, and with the Department of Orthopaedic Surgery, University of Virginia, Charlottesville, VA. Mark F. Abel is with the Department of Orthopaedic Surgery, University of Virginia, Charlottesville, VA. walking with a horizontal assist force that would aid in understanding the reduction in metabolic energy use and inform us as to whether a device (eg, a powered walker) would be an appropriate aid. Other groups have examined the relationship between gait and energy during normal walking but not during assisted walking. An inverted pendulum model can describe the energy exchange between kinetic energy and gravitational potential energy of the body center of mass (COM) and how this can reduce cost during level walking.8 Expanding upon this model, one can calculate the external work performed on the COM and the energy exchange between kinetic and potential energy can be quantified.9 The mechanical work for step-to-step transitions is an important determinant of metabolic cost10 and the energetic cost of raising the COM during this transition is significant.11 However, it has been shown that healthy human subjects do not demonstrate a reduction in metabolic cost when movement of the COM is reduced12 and that changes in mechanical work do not explain higher metabolic costs in the young13 or elderly.14 Therefore external work and metabolic cost are not always covariant, and the causes of changes in the metabolic cost of gait are unclear. Studying the kinematics, work, and energy of human locomotion with an assistive force may add further insights into the relationship between the mechanics and energetics of walking. We hypothesized that a horizontal assist force (HAF) in the direction of walking will result in a decrease in metabolic cost and that an optimal assist force exists to create 481 482 Zirker, Bennett, and Abel the greatest reduction in cost. Secondly, since external work and metabolic cost are positively correlated in both healthy15 and disabled populations16 we hypothesized that some of the reduction in metabolic cost with assist force is due to a decrease in external work due to an increase in recovery factor. Finally, since walking downhill creates a forward force similar to a HAF, we hypothesized that kinematics changes of the lower extremities would resemble those of downhill walking. Methods Subjects Kinematic and metabolic data were collected and analyzed in a convenience sample of 10 healthy adult males without known musculoskeletal, neurological, cardiac, or pulmonary pathology [age = 32.8 ± 13.2, height = 1.8 ± .07 m, mass = 77.5 ± 12.0 kg]. All tests were conducted in the Motion Analysis and Motor Performance Laboratory at the University of Virginia. Subject consent was approved by the University of Virginia’s Human Investigation Committee and was obtained for all subjects. Protocol Throughout this protocol, subjects walked at a selfselected comfortable walking speed. Subject walking speed was determined in two steps. First, the treadmill was started at a slow “barely walking” speed then accelerated by the investigators in increments of 0.2 km/hr as requested by the subject until the subject indicated it was the desired speed. Next, the treadmill speed was increased to a rapid “close to running” pace and decelerated in a similar method until the subject again indicated the desired speed. The two indicated speeds were averaged to determine walking speed; mean walking speed was 1.29 ± 0.08 m/s. Testing began with subjects sitting at rest until two minutes of baseline resting steady state metabolic rate was recorded. Subjects rested while seated rather than standing because subtracting the standing from the total rates tends to underestimate the total effort of walking.17 In addition, this allowed the protocol to be repeated in future studies by individuals with disabilities that use assistive devices and have difficulty standing as has been done in other studies.18–20 Next, subjects performed a “warm up” baseline walking trial on the treadmill without any assist force until two minutes after steady state was achieved. This cycle of sitting and walking was repeated with a HAF of 4%, 8%, and 12% of the subject’s body weight. These assist forces were chosen to bracket the 10% HAF that produced the maximum metabolic reduction in the work of Gottschall and Kram7 with a lower 4% assist force for use in future studies including subjects with disabilities who struggle with higher forces. This required at least seven minutes of walking but no more than eleven minutes of walking per condition. Trial order was randomized for assist force trials. After a rest period, subjects completed a fifth “cool down” repeated baseline trial with no assist force. Subjects were then asked to fill out a brief questionnaire providing a qualitative description of their experiences of walking with an assist force. Assistive Force Apparatus A constant HAF was applied through a belt strapped around each subject’s waist and the desired load was applied via hanging weights on a pulley system (Figure 1). A spring was used to filter the motion artifacts between the subject and the weights. A spring stiffness of 2.8 N/ cm was used so that the natural frequency of the springmass system was different from gait cadence to avoid resonance. No damping was added to the system. The length of the horizontal section of the pulley system was maintained at greater than 60 cm resulting in a variation from the horizontal of the assist force vector was less than less than 2° for all trials. Forces between the subject and the spring were recorded using a load cell and were maintained on average within 8.0 ± 1.4% for 4% HAF, 6.0 ± 0.9% for 8% HAF and 5.3 ± 1.0% for 12% HAF of the desired force, which is a variation of less than 10 N for even the highest assist forces measured. Variations in the assist force were oscillatory and did not produce a systematic bias toward greater or weaker assist forces. The assist force apparatus did not interfere with subject movement and allowed unrestricted treadmill walking. Data Collection After 4 minutes of walking steady state metabolic rate was confirmed by monitoring real-time VO2/kg consumption visually. All resting and walking trials were conducted until two minutes of steady state metabolic data were recorded. Three-dimensional kinematic data were collected using an eight camera Vicon Motion Analysis System (Oxford Metric; Oxford, UK) at 120 Hz. A full-body Vicon Plug-in Gait set of 37 markers21 and Figure 1 — Schematic of the experimental setup. A rope was attached to a waist belt worn by the subject and connected in series to a load cell, spring, rope, and weights. The subject wore a set of 38 markers and an oxygen consumption measuring device which included a vest and mask (not shown). Walking with a Forward Assistive Force 483 the Oxycon Mobile apparatus (Viasys Healthcare; San Diego, CA) were attached to the subjects after anthropometric measurements were taken. For each walking task, kinematic data were collected for at least five trials of ten complete strides each. Trials were collected at least one minute apart after the first two minutes of walking during each task. Assist force data were collected by a single degree of freedom load cell (ATI Industrial Automation; Apex, North Carolina) at 1080 Hz through Vicon. Data Processing For each assist force level, the normalized net metabolic rate was calculated by subtracting the average resting steady state VO2 L∙min–1 from the average walking steady state VO2 L∙min-1. This value was then divided by the subjects mass to obtain VO2 L∙min–1∙kg–1. Metabolic cost, VO2 L∙m–1∙kg–1, was obtained by dividing the rate by the walking velocity. Marker trajectory data were exported from Vicon and processed using MATLAB (Mathworks; Natick, Massachusetts). Gait events were determined using validated methods22 and used to calculate average stride length and duration of swing phase and stance. Joint kinematics of the ankle, knee, and hip were determined using the Vicon Plug-in Gait model. Previously described energy and work measures23 were calculated based on the COM position found using a validated full-body kinematic model.23 COM position data were then filtered using a bidirectional low-pass second order Butterworth filter with a cutoff frequency of 8 Hz to remove signal noise without introducing a phase shift. Work and energy values calculated include the kinetic and gravitational potential energy of the COM, external work (Wext), external work assuming no energy exchange (Wne), recovery factor (R), and the relative phase angle between kinetic and potential energy curves. Recovery factor is the percentage of mechanical energy recovered through energy exchange between the kinetic and potential energy of the movement of the COM. Subject Questionnaire After testing, subjects were asked to fill out a brief questionnaire. The questionnaire asked the subjects to rank the trials by effort required, inquired if walking during the assist force trials “felt natural,” and requested for subjects to provide their own qualitative comments about the experiment and walking with an assist force. All subjects responded to the questionnaire in full. Comparison with Downhill Walking When walking downhill there exists a component of force normal to the ground and a component parallel to the ground (ie, direction of travel); this force is what allows passive dynamic walking robots to walk down a slight grade.24 The component parallel to the direction of travel can be found as the sine of the angle of inclination times downward force or body weight. Thus the angle that creates a desired force parallel to the ground can be computed. Slopes of 2.3°, 4.6°, and 6.9° create forces parallel to the ground that are 4%, 8%, and 12% of body weight, respectively. Statistics Differences between variables were determined using repeated-measures ANOVA with Tukey’s post hoc test. Significance was determined at P < .05. Because no significant differences were found between the “warm-up” and “cool-down” baseline trials for any measure, data from the two were averaged to create “normal” or “0% HAF” condition. Correlations were determined using a Pearson correlation. Results Application of a HAF reduced metabolic cost such that the lowest cost was observed at 8% HAF (P < .001). The metabolic costs differed with assist level (P < .001) with all three levels of assist force resulting in a reduction in metabolic cost relative to normal walking (P < .001). During assisted trials, the metabolic cost of walking at comfortable walking speed was shown to reduce by 23.7 ± 6.3% of normal walking for 4% HAF, 34.7 ± 6.9% for 8% HAF, and 19.1 ± 12.8% for 12% HAF (Figure 2). Eight of the ten subjects demonstrated the pattern shown while the remaining two had the lowest metabolic cost at 12% HAF followed by 8%, then 4% while the highest cost was always measured during normal walking. When asked to rank the trials in order of preference, subjects preferred the unassisted “warm up” condition followed by 4% HAF, unassisted “cool down,” 8% HAF, and lastly 12% HAF. Eight out of ten subjects rated the 12% HAF trial as requiring the most effort. All subjects stated that walking with an assist force “felt unnatural” especially at the higher force levels, although the 4% HAF trial was generally regarded as “easy” or “tolerable.” Many subjects, either verbally or in writing, commented that the sensation of walking with an assist force was similar to walking downhill. Recovery factor did not necessarily increase nor did external work decrease with an assist force (Table 1). Wext differed from the normal condition only at 12% assist where it was 33% larger (P < .02). Wne increased with every assist level (P < .005). The recovery factor increased with the 4% HAF (P < .04) but was not different from the normal condition at the higher assist levels. The recovery factor for normal walking of 64.7 changed to 72.0 for 4%, (P < .03), 70.5 for 8% (P < .11) and 64.4 for 12% HAF (P < .99). The relative phase increased at each assist level (P < .001), nearly 180° out of phase at 4% HAF, but increasing at 8% and 12% HAF. There were significant changes in all dependent measures except the ratio of potential to kinetic energy (Figure 3). The main effects for the relative phase, Wext, Wne, and excursions of the potential and kinetic energies were at the P < .001 level, while the recovery factor had a level of P < .005. 484 Zirker, Bennett, and Abel Figure 2 — Measured metabolic rates as a percentage of normal unassisted walking (mean ± standard deviation). The curve is a second-order polynomial least squares fit, y = 9.8x2 – 55.9x + 146.8, R2 = .98. Table 1 Summary of data Average Value % Reduction in Metabolic Cost Normal 4% 8% 12% 0 23.7* 34.7* 19.1* Stride Length (cm) 143 138* 135* 130* Stride Duration (s) 1.1 1.06* 1.04* 1.00* % of Stride in Double Support 18.5 17.5* 16.7* 16.0* Max Hip Flexion (deg) 33.1 30.8* 29.2* 29.5* Max Hip Extension (deg) –14.5 –12.7 –11.2* –6.0* Max Knee Flexion (deg) 66.9 68.2 69.8* 71.6* Max Knee Extension (deg) 0.1 –1.4* –1.7* –0.9 Max Dorsiflexion (deg) 10.7 10.1 11.3 12.8* Max Plantar Flexion (deg) –21.4 –19.4 –15.4* –12.2* Hip Excursion (deg) 47.6 43.5* 40.4* 35.5* Knee Excursion (deg) 66.8 69.6* 71.5* 72.5* Ankle Excursion (deg) 32.1 29.5* 26.7* 25.0* Relative Phase (deg) 159 181* 197* 213* Recovery Factor 64.7 72.0* 70.5 64.4 Wext (J∙kg–1∙m–1) 0.64 0.56 0.66 0.85* Wne (J∙kg–1∙m–1) 1.80 2.01* 2.23* 2.36* Kinetic Energy Excursion (J∙kg–1∙m–1) 0.224 0.250 0.278* 0.294* Potential Energy Excursion (J∙kg–1∙m–1) 0.238 0.256 0.287* 0.300* Potential Energy / Kinetic Energy 1.16 1.12 1.11 1.09 *Indicates P < .05 compared with normal. Walking with a Forward Assistive Force 485 Figure 3 — Demeaned kinetic and potential energies of the center of mass over half a stride, where 0% is the maximum kinetic energy. Shifting peaks of the potential energy curves show the changing relative phase while varying amplitudes correspond with changes in external work. As with changing downhill grades, changes in assist force resulted in changes in gait kinematics (Table 1). There were main effects for maximum hip and knee flexions, hip extension, and ankle dorsiflexion, and all angle excursions (P < .001) as well as for maximum knee extension and ankle plantar flexion (P < .01). Maximum hip flexion and extension decreased. In addition, maximum knee flexion in stance increased and ankle plantar flexion decreased with increasing HAF. Excursions of the hip and ankle decreased while knee excursion increased. Stride length shortened with increasing assistance (P < .001) and all values differed from each other (P < .02). For stride duration there was also a main effect (P < .001) and all assist values were shorter than the normal condition but did not differ from each other. The relative percentage of time of each stride spent in double support decreased with increasing assist force (P < .01); normal to 4%: P < .04, normal to 8% and normal to 12%: P < .001. This reduced time in double support can be seen in the altered phasing of joint angles of the lower extremities between assist force levels (Figure 4). Discussion The metabolic results supported our hypothesis that an assist force would reduce the cost of walking in healthy adults. However, we reject our hypothesis that this reduction in metabolic cost is the result of a reduction of external work performed as the same trend was not seen in Wext and Wne. In fact, there was a significant increase in Wne with increasing assist force. This increase in Wne was the result of increases in excursions of both the potential and kinetic energies. While there was an increase in the recovery factor at 4% HAF reflecting improved phasing of the energies, this could not overcome the increases in the energy excursions to decrease the overall Wext performed. Therefore our hypothesis that the reduced metabolic consumption would be accompanied by reduced mechanical work and improved energy recovery was not substantiated. Our measured reductions in metabolic cost are lower in magnitude but with a similar trend as the data of Gottschall and Kram7 and both sets of data suggest the maximum reduction in metabolic cost occurs between 8% and 10% HAF. The different percentages in reductions found in the two studies is most likely due to their use of standing for the resting metabolic state instead of the sitting values used in this study; subtracting a larger “resting” value results in any changes being a larger percentage of the unassisted data. As mentioned previously, we chose sitting as our rest condition to be consistent when working with populations that have difficulty standing. In addition, some researchers believe using standing resting values tends to underestimate the cost of walking as it removes the effort to stand.17 Recent work measured a standing metabolic rate as 16% greater than sitting,17 but other researchers have found greater differences in the cost of maintaining a standing posture.25 Another difference between the two studies was that subjects in the present work walked at their own comfortable walking speed 486 Zirker, Bennett, and Abel Figure 4 — Joint kinematics of the lower extremities for various levels of assist forces. Flexion at the hip and knee and dorsiflexion of the ankle are defined as positive. Heel strike occurs at 0% of the stride. rather than a uniform speed. Since comfortable walking speed typically results in the most efficient gait, subjects walking at an arbitrary speed may have higher costs that allow for a greater reduction with assist force. Despite observing the highest recovery factor, most energetically efficient relative phase, and lowest Wext at 4% HAF, the greatest reduction of metabolic cost was seen at 8% HAF. This result indicates that while changes in recovery factor, total external work and COM motion can contribute to reduction of metabolic cost, they are not the sole cause and other mechanisms must be considered. Although the assist force was only applied in the horizontal direction, it may have been able to contribute to elevating the COM. Considering gait as an inverted pendulum, the forward leg acts as a pivot which guides the COM through its trajectory.8 Between toe off and midstance of the contralateral foot, the COM rises as it moves in the forward direction, increasing its potential energy. During unassisted walking, this energy comes from either metabolic expenditure or transfer from kinetic energy, but during assisted walking it may be provided by the assist force as the COM is pulled forward while it travels upwards to its peak height during midstance. Walking with a Forward Assistive Force 487 While the inverted pendulum model may provide a simple and insightful means of analyzing mechanical energy during walking, it is not the only relevant tool for explaining the associated metabolic cost. In addition to both recovery factor and relative phase showing the greatest improvement at 4% HAF instead of 8% HAF, Wne increased as assist force increased. This discrepancy between the work performed by the subject, work performed by the assist force device, and the overall metabolic cost indicates that additional factors may need to be considered when comparing mechanical and metabolic energy costs of walking. During normal walking, forward speed is not constant and involves propulsion by the trailing leg during toe off and braking by the lead leg during heel strike. This individual limb work during double support has been shown to be an important determinant of metabolic cost.10 The peak anterior/posterior ground reaction force for propulsion during normal walking at comfortable walking speed is around 2 N/kg and supplies up to 85% of the power in walking.26 For our conditions, this would result in a nominal impulse of 0.6 Ns/kg per stride. The percentage of this impulse provided by a 4%, 8% and 12% HAF is 67%, 133% and 200%, respectively, reducing the work requirements for forward propulsion but increasing the requirements of braking. This can also be viewed from the perspective of the work performed. The virtual work values of the assist forces relative to the treadmill belt on the subjects are 68%, 110% and 140% of the Wext at 4%, 8% and 12% HAF, respectively. Once the required propulsion and work is supplied, any additional energy must be dissipated. Thus it may be natural that the greatest reduction in metabolic cost occurs at a point where the added impulse and virtual work are close to the no assist values. While the combined leg work computed here is less than would be computed using the individual limb method,10 we still see an increased Wext and metabolic cost at 12% HAF relative to 8% HAF where the added impulse and work were beyond what was needed for propulsion. For lower assist levels, the fact that negative (eccentric) work is more metabolically efficient than positive (concentric) work27 results in reduced cost despite the increase in braking force for lower assist levels. Several changes in the kinematics of the lower extremities were noteworthy. At the hip joint, flexion during heel strike and extension during toe off are both reduced significantly (Figure 4, Table 1) as assist force increased reflecting the shortened stride. Our data also suggests that the source of the increased COM and potential energy excursion was increased flexion of the knee during stance. The maximum flexion of the knee during stance increased with assist force most likely because of the increased braking during double support7 similar to what is seen in walking downhill. This braking could also contribute to the increase in kinetic energy variation. There is also a significant decrease in plantar flexion accompanying toe off. This suggests that one effect of the HAF was to reduce the power requirements at the ankle, an effect suggested in earlier work by decreased EMG activity in the medial gastrocnemius.7 Because the plantar flexors are responsible for the majority of the propulsive work at the ankle during toe off,28 it is intuitive that plantar flexion angles should decrease dramatically as assist force increases. This finding is in agreement with previous findings of decreased horizontal ground reaction forces during the propulsive phase when walking with an assist force.7 Walking with a horizontal assist force can be compared with downhill walking where a component of gravity acts parallel to the walking surfaces. Unsurprisingly, many of the kinematic and energetic changes observed with a HAF are similar to those reported in downhill walking studies and could explain why some subjects noted the similarities between the two activities. While studies have found a reduction in stride duration at slopes with grades of 10% and 15%,29 we found a reduction at all levels of assist. The increased knee flexion during stance with increased assist force is qualitatively similar to the increases in knee flexion angles seen in walking down a ramp.30 Decreased stride length with increased assist force may result from the increased shear ground reaction forces required for braking as is seen in downhill walking,30 but was only found for slopes greater than 17%. As we observed in assisted walking, metabolic cost decreases with slope angle to a point then increases again.31 The greatest metabolic reductions happen roughly around a –9% grade,31,32 which converts to a 9% HAF. Our findings suggest a strong biomechanical link between walking with a HAF and downhill walking. There are several limitations to this study. First, we report only the external work (the work done on the COM) and not the internal work that is done by the limbs relative to the COM. However, the nature of the kinematic changes suggest there was little change in the internal work done relative to the COM. While kinematic changes are identified in the lower extremity with increasing HAF, it is not clear what specific aspects of these changes contribute to changes in metabolic cost, recovery factor and relative phase. Furthermore, while this study demonstrates that the relationship between energetic and metabolic cost are not directly related, it does not explain why. This shortcoming could be addressed by incorporating dynamics to study reduction in joint moments during gait or estimating muscle activation to show reduced muscular effort. This study implies possible training routines for athletes such as hikers and mountaineers who navigate slopes who may be able to incorporate assisted treadmill walking into their training routines if walking downhill is not available. Because the majority of injuries incurred during hiking occur during descent,33 simulating downhill walking using an assist force may provide a manner of training to strengthen leg muscles and reduce the risk of injury. Perhaps more importantly these findings may have important therapeutic implications for both rehabilitation and the development of assistive devices. When treating patients with disorders that cause them to fatigue rapidly, 488 Zirker, Bennett, and Abel usage of an assist force during treadmill exercises could increase the time patients remain active during therapy sessions. The development of an intelligent powered walker may be of benefit to many patients. Individuals with conditions such as cerebral palsy often demonstrate gait patterns with a significantly higher cost of walking34 and have reduced strength in their plantar flexors. A powered walker which senses user feedback and intelligently provides a forward force at appropriate times (ie, push-off and not during foot contact when negative work is performed) may enable walker users to travel greater distances without rest thus increasing independence and quality of life. This study is the first to show how work, lower limb kinematics, and motion of the COM change with the application of a forward horizontal assist force. The greatest reductions in metabolic cost were seen at 8% HAF. Changes in metabolic cost, walking temporal parameters and kinematics of the hip and knee were similar to what is seen in downhill walking at slopes equivalent to the assist force levels. Indeed recent work has shown that in walking on slopes, the joints of the lower limbs are tuned together and only a selected property is tuned to adapt in response to the slope.35 Despite shorter stride length and duration, shorter periods of double support, shifting of the phase of the energies, and increases in energy excursions with increasing HAF, the ratio of potential energy to kinetic energy never changes and it is only at 12% HAF that the external work increases. Future work should include collection of force data that would allow the computation of individual leg work to provide better understanding of the reductions in metabolic cost. In addition, further study is needed to fully understand our adaptation to assist forces in walking. This data sheds light on the basic organization of walking and adds to the body of work23,36,37 that suggests that the “organization” of the gait with respect to the COM remains an important feature of walking under various conditions. 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