Adding Stiffness to the Foot Modulates Soleus Force-Velocity Behaviour during Human Walking

Kota Z Takahashi, Michael T Gross, Herman van Werkhoven, Stephen J Piazza, Gregory S Sawicki, Kota Z Takahashi, Michael T Gross, Herman van Werkhoven, Stephen J Piazza, Gregory S Sawicki

Abstract

Previous studies of human locomotion indicate that foot and ankle structures can interact in complex ways. The structure of the foot defines the input and output lever arms that influences the force-generating capacity of the ankle plantar flexors during push-off. At the same time, deformation of the foot may dissipate some of the mechanical energy generated by the plantar flexors during push-off. We investigated this foot-ankle interplay during walking by adding stiffness to the foot through shoes and insoles, and characterized the resulting changes in in vivo soleus muscle-tendon mechanics using ultrasonography. Added stiffness decreased energy dissipation at the foot (p < 0.001) and increased the gear ratio (i.e., ratio of ground reaction force and plantar flexor muscle lever arms) (p < 0.001). Added foot stiffness also altered soleus muscle behaviour, leading to greater peak force (p < 0.001) and reduced fascicle shortening speed (p < 0.001). Despite this shift in force-velocity behaviour, the whole-body metabolic cost during walking increased with added foot stiffness (p < 0.001). This increased metabolic cost is likely due to the added force demand on the plantar flexors, as walking on a more rigid foot/shoe surface compromises the plantar flexors' mechanical advantage.

Figures

Figure 1. Adding stiffness to the foot…
Figure 1. Adding stiffness to the foot altered the centre-of-pressure propagation during stance, and decreased net mechanical work due to foot deformation.
(a) The centre-of-pressure (COP) during stance was expressed in the foot’s sagittal plane (N = 20). Each circle corresponds to averaged COP data for one percent of stance. The position of the ankle joint in the foot’s reference is denoted by the diamonds. A vertical projection of the metatarsal-phalangeal joint in the foot’s reference frame is denoted by the dashed vertical grey lines. (b) The foot deformation power was time-normalized to the stride cycle (N = 20). Three distinct phases of power were evident: negative power immediately after heel strike, negative power during ~30–60 percent of stride, and positive power before toe-off. (c) Total positive work, negative work, and net work were quantified during stride (N = 20, means ± s.e.m). With added foot stiffness (ΔK), there was an increase in total positive work (p < 0.001), decrease in magnitude of negative work (p < 0.001), and decrease in magnitude of net work (p < 0.001). P-values indicate the main effect of added foot stiffness. **denotes significant pair-wise difference with respect to each of the other conditions. Square brackets show additional significant pair-wise comparisons.
Figure 2. Adding stiffness to the foot…
Figure 2. Adding stiffness to the foot increased the gear ratio during stance.
(a) Lever arm of the ground reaction force (GRF) relative to the ankle, and moment arm of the plantar flexor during stance were time-normalized to percentage of stance (N = 20). (b) The gear ratio was estimated as the ratio of GRF lever arm to plantar flexor moment arm during stance (N = 20). The vertical lines define 5 and 95% of stance. (c) The peak gear ratio and the average gear ratio were computed during 5–95% of stance (N = 20, mean ± s.e.m). With added foot stiffness (ΔK), there were increases in the peak gear ratio (p < 0.001) and the average gear ratio during stance (p < 0.001). P-values indicate the main effect of added foot stiffness. **denotes significant pair-wise difference with respect to each of the other conditions. Square brackets show additional significant pair-wise comparisons.
Figure 3. Adding stiffness to the foot…
Figure 3. Adding stiffness to the foot increased soleus activation and force, and decreased fascicle shortening velocity.
Time-normalized data (stride cycle) of (a) soleus activation (N = 19, left limb), (b) soleus force (N = 20, right limb), (c) fascicle length (N = 20, right limb), and (d) fascicle velocity (N = 20, right limb). Stance phase is highlighted in grey. With added foot stiffness (ΔK), there was an increase in peak soleus activation (p = 0.020), increase in integrated soleus activation during stance (p = 0.013), increase in soleus peak force (p < 0.001), and increase in soleus integrated force during stance (p < 0.001). In addition, added foot stiffness decreased soleus fascicle velocity at peak force (p < 0.001) and decreased the average fascicle shortening velocity during stance (p < 0.001) but had no significant effect on fascicle length at peak force (p = 0.182) and the average fascicle length during stance (p = 0.408). P-values indicate the main effect of added foot stiffness. **denotes significant pair-wise difference with respect to each of the other conditions. Square brackets show additional significant pair-wise comparisons.
Figure 4. Slower fascicle shortening speed contributed…
Figure 4. Slower fascicle shortening speed contributed to enhanced soleus force production.
(a) Soleus peak force was plotted against fascicle velocity at the time of peak force (N = 20, mean ± s.e.m). With added foot stiffness (ΔK), there was a shift towards slower fascicle velocity at the time of peak plantar flexor force. At the greatest stiffness (ΔK = 65.6 N/mm), the soleus fascicle was actually lengthening during peak force production. P-values indicate the main effect of added foot stiffness, and significant pair-wise comparisons are denoted by the square brackets. (b) Force per unit activation was quantified as the ratio of integrated soleus force and integrated soleus activation during stance (N = 19, mean ± s.e.m). Added foot stiffness increased the force per unit activation (p = 0.010). The greatest added foot stiffness condition (ΔK = 65.6 N/mm) had greater force per unit activation compared to ΔK = 14.8 N/mm and ΔK = 28.7 N/mm (denoted by the square brackets).
Figure 5. Whole-body net metabolic power was…
Figure 5. Whole-body net metabolic power was increased at the greatest added foot stiffness.
Net metabolic power was quantified using indirect calorimetry (N = 20, mean ± s.e.m). P-value indicate the main effect of added foot stiffness. At the greatest added foot stiffness (ΔK = 65.6 N/mm), the net metabolic power was greater than each of the other conditions (denoted by**).
Figure 6. Experimental protocol.
Figure 6. Experimental protocol.
Each subject walked on an instrumented treadmill at 1.25 m/s under 5 conditions in a randomized order: barefoot, shod, and shod with three levels of added insole thickness. Data collection was separated in two testing sessions separated by approximately 24 hours: one day for metabolic energy analysis, and another day for lower limb mechanics including ultrasound and electromyography. The order of the days was randomized. Rate of whole-body metabolic energy expenditure was analysed using indirect calorimetry. B-mode ultrasound images were acquired from the right soleus muscle, while electromyography sensors were placed on the ankle muscles of the left limb including lateral and medial gastrocnemius, soleus, and tibialis anterior.

References

    1. Cunningham C. B., Schilling N., Anders C. & Carrier D. R. The influence of foot posture on the cost of transport in humans. J Exp Biol 213, 790–797, doi: 10.1242/jeb.038984 (2010).
    1. Usherwood J. R., Channon A. J., Myatt J. P., Rankin J. W. & Hubel T. Y. The human foot and heel-sole-toe walking strategy: a mechanism enabling an inverted pendular gait with low isometric muscle force? J R Soc Interface 9, 2396–2402, doi: 10.1098/rsif.2012.0179 (2012).
    1. Hansen A. H., Childress D. S. & Knox E. H. Roll-over shapes of human locomotor systems: effects of walking speed. Clin Biomech (Bristol, Avon) 19, 407–414, doi: 10.1016/j.clinbiomech.2003.12.001 (2004).
    1. Carrier D. R., Heglund N. C. & Earls K. D. Variable gearing during locomotion in the human musculoskeletal system. Science 265, 651–653 (1994).
    1. Erdemir A. & Piazza S. J. Rotational foot placement specifies the lever arm of the ground reaction force during the push-off phase of walking initiation. Gait Posture 15, 212–219 (2002).
    1. Rubenson J., Pires N. J., Loi H. O., Pinniger G. J. & Shannon D. G. On the ascent: the soleus operating length is conserved to the ascending limb of the force-length curve across gait mechanics in humans. J Exp Biol 215, 3539–3551, doi: 10.1242/jeb.070466 (2012).
    1. Ishikawa M., Komi P. V., Grey M. J., Lepola V. & Bruggemann G. P. Muscle-tendon interaction and elastic energy usage in human walking. J Appl Physiol (1985) 99, 603–608, doi: 10.1152/japplphysiol.00189.2005 (2005).
    1. Farris D. J. & Sawicki G. S. Human medial gastrocnemius force-velocity behavior shifts with locomotion speed and gait. Proc Natl Acad Sci USA 109, 977–982, doi: 10.1073/pnas.1107972109 (2012).
    1. Lai A. et al.. In vivo behavior of the human soleus muscle with increasing walking and running speeds. J Appl Physiol (1985) 118, 1266–1275, doi: 10.1152/japplphysiol.00128.2015 (2015).
    1. DeVita P., Helseth J. & Hortobagyi T. Muscles do more positive than negative work in human locomotion. J Exp Biol 210, 3361–3373, doi: 10.1242/jeb.003970 (2007).
    1. Farris D. J. & Sawicki G. S. The mechanics and energetics of human walking and running: a joint level perspective. J R Soc Interface 9, 110–118, doi: 10.1098/rsif.2011.0182 (2012).
    1. Neptune R. R., Kautz S. A. & Zajac F. E. Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking. J Biomech 34, 1387–1398 (2001).
    1. Zelik K. E., Takahashi K. Z. & Sawicki G. S. Six degree-of-freedom analysis of hip, knee, ankle and foot provides updated understanding of biomechanical work during human walking. J Exp Biol 218, 876–886, doi: 10.1242/jeb.115451 (2015).
    1. Siegel K. L., Kepple T. M. & Caldwell G. E. Improved agreement of foot segmental power and rate of energy change during gait: inclusion of distal power terms and use of three-dimensional models. J Biomech 29, 823–827 (1996).
    1. Takahashi K. Z. & Kepple T. M. & Stanhope, S. J. A unified deformable (UD) segment model for quantifying total power of anatomical and prosthetic below-knee structures during stance in gait. J Biomech 45, 2662–2667, doi: 10.1016/j.jbiomech.2012.08.017 (2012).
    1. MacWilliams B. A., Cowley M. & Nicholson D. E. Foot kinematics and kinetics during adolescent gait. Gait Posture 17, 214–224 (2003).
    1. Rolian C., Lieberman D. E., Hamill J., Scott J. W. & Werbel W. Walking, running and the evolution of short toes in humans. J Exp Biol 212, 713–721, doi: 10.1242/jeb.019885 (2009).
    1. Bruening D. A., Cooney K. M. & Buczek F. L. Analysis of a kinetic multi-segment foot model part II: kinetics and clinical implications. Gait Posture 35, 535–540, doi: 10.1016/j.gaitpost.2011.11.012 (2012).
    1. Takahashi K. Z. & Stanhope S. J. Mechanical energy profiles of the combined ankle-foot system in normal gait: insights for prosthetic designs. Gait Posture 38, 818–823, doi: 10.1016/j.gaitpost.2013.04.002 (2013).
    1. Roy J. P. & Stefanyshyn D. J. Shoe midsole longitudinal bending stiffness and running economy, joint energy, and EMG. Med Sci Sports Exerc 38, 562–569, doi: 10.1249/01.mss.0000193562.22001.e8 (2006).
    1. Willwacher S., König M., Potthast W. & Brüggemann G. P. Does specific footwear facilitate energy storage and return at the metatarsophalangeal joint in running? J Appl Biomech 29, 583–592 (2013).
    1. Willwacher S., König M., Braunstein B., Goldmann J. P. & Brüggemann G. P. The gearing function of running shoe longitudinal bending stiffness. Gait Posture 40, 386–390, doi: 10.1016/j.gaitpost.2014.05.005 (2014).
    1. Baxter J. R., Novack T. A., Van Werkhoven H., Pennell D. R. & Piazza S. J. Ankle joint mechanics and foot proportions differ between human sprinters and non-sprinters. Proc Biol Sci 279, 2018–2024, doi: 10.1098/rspb.2011.2358 (2012).
    1. Lin S. C. et al.. Changes in windlass effect in response to different shoe and insole designs during walking. Gait Posture 37, 235–241, doi: 10.1016/j.gaitpost.2012.07.010 (2013).
    1. Bojsen-Møller F. & Lamoreux L. Significance of free-dorsiflexion of the toes in walking. Acta Orthop Scand 50, 471–479 (1979).
    1. Cronin N. J., Avela J., Finni T. & Peltonen J. Differences in contractile behaviour between the soleus and medial gastrocnemius muscles during human walking. J Exp Biol 216, 909–914, doi: 10.1242/jeb.078196 (2013).
    1. Lee S. S. & Piazza S. J. Built for speed: musculoskeletal structure and sprinting ability. J Exp Biol 212, 3700–3707, doi: 10.1242/jeb.031096 (2009).
    1. Browning R. C., Modica J. R., Kram R. & Goswami A. The effects of adding mass to the legs on the energetics and biomechanics of walking. Med Sci Sports Exerc 39, 515–525, doi: 10.1249/mss.0b013e31802b3562 (2007).
    1. Griffin T. M., Roberts T. J. & Kram R. Metabolic cost of generating muscular force in human walking: insights from load-carrying and speed experiments. J Appl Physiol (1985) 95, 172–183, doi: 10.1152/japplphysiol.00944.2002 ( 2003).
    1. Kram R., Arellano C. J. & Franz J. R. The metabolic cost of locomotion; muscle by muscle. Exerc Sport Sci Rev 39, 57–58, doi: 10.1097/JES.0b013e31820f905b (2011).
    1. Farris D. J., Robertson B. D. & Sawicki G. S. Elastic ankle exoskeletons reduce soleus muscle force but not work in human hopping. J Appl Physiol (1985) 115, 579–585, doi: 10.1152/japplphysiol.00253.2013 (2013).
    1. Collins S. H., Wiggin M. B. & Sawicki G. S. Reducing the energy cost of human walking using an unpowered exoskeleton. Nature 522, 212–215, doi: 10.1038/nature14288 (2015).
    1. Baxter J. R. & Piazza S. J. Plantar flexor moment arm and muscle volume predict torque-generating capacity in young men. J Appl Physiol (1985) 116, 538–544, doi: 10.1152/japplphysiol.01140.2013 (2014).
    1. Hillstrom H. J. et al.. Foot type biomechanics part 1: structure and function of the asymptomatic foot. Gait Posture 37, 445–451, doi: 10.1016/j.gaitpost.2012.09.007 (2013).
    1. Mootanah R. et al.. Foot Type Biomechanics Part 2: are structure and anthropometrics related to function? Gait Posture 37, 452–456, doi: 10.1016/j.gaitpost.2012.09.008 (2013).
    1. Angin S., Crofts G., Mickle K. J. & Nester C. J. Ultrasound evaluation of foot muscles and plantar fascia in pes planus. Gait Posture 40, 48–52, doi: 10.1016/j.gaitpost.2014.02.008 (2014).
    1. Stefanyshyn D. & Fusco C. Increased shoe bending stiffness increases sprint performance. Sports Biomech 3, 55–66, doi: 10.1080/14763140408522830 (2004).
    1. Stefanyshyn D. J. & Nigg B. M. Influence of midsole bending stiffness on joint energy and jump height performance. Med Sci Sports Exerc 32, 471–476 (2000).
    1. Cavagna G. A. & Kaneko M. Mechanical work and efficiency in level walking and running. J Physiol 268, 467–481 (1977).
    1. Umberger B. R. & Martin P. E. Mechanical power and efficiency of level walking with different stride rates. J Exp Biol 210, 3255–3265, doi: 10.1242/jeb.000950 (2007).
    1. Sawicki G. S., Lewis C. L. & Ferris D. P. It pays to have a spring in your step. Exerc Sport Sci Rev 37, 130–138, doi: 10.1097/JES.0b013e31819c2df6 (2009).
    1. Neptune R. R. & Sasaki K. Ankle plantar flexor force production is an important determinant of the preferred walk-to-run transition speed. J Exp Biol 208, 799–808, doi: 10.1242/jeb.01435 (2005).
    1. Franz J. R., Wierzbinski C. M. & Kram R. Metabolic cost of running barefoot versus shod: is lighter better? Med Sci Sports Exerc 44, 1519–1525, doi: 10.1249/MSS.0b013e3182514a88 (2012).
    1. Brockway J. M. Derivation of formulae used to calculate energy expenditure in man. Hum Nutr Clin Nutr 41, 463–471 (1987).
    1. Holden J. P. & Chou G. & Stanhope, S. J. Changes in knee joint function over a wide range of walking speeds. Clin Biomech (Bristol, Avon) 12, 375–382 (1997).
    1. Zelik K. E., La Scaleia V., Ivanenko Y. P. & Lacquaniti F. Coordination of intrinsic and extrinsic foot muscles during walking. Eur J Appl Physiol 115, 691–701, doi: 10.1007/s00421-014-3056-x (2015).
    1. Kelly L. A., Lichtwark G. & Cresswell A. G. Active regulation of longitudinal arch compression and recoil during walking and running. J R Soc Interface 12, 20141076 (2015).
    1. Takahashi K. Z. & Horne J. R. & Stanhope, S. J. Comparison of mechanical energy profiles of passive and active below-knee prostheses: a case study. Prosthet Orthot Int 39, 150–156, doi: 10.1177/0309364613513298 (2015).
    1. Gruber A. Mechanics and energetics of footfall patterns in running Doctor of Philosophy thesis, University of Massachusetts Amherst, (2012).
    1. Maganaris C. N., Baltzopoulos V. & Sargeant A. J. In vivo measurement-based estimations of the human Achilles tendon moment arm. Eur J Appl Physiol 83, 363–369 (2000).
    1. Aggeloussis N., Giannakou E., Albracht K. & Arampatzis A. Reproducibility of fascicle length and pennation angle of gastrocnemius medialis in human gait in vivo. Gait Posture 31, 73–77, doi: 10.1016/j.gaitpost.2009.08.249 (2010).
    1. Finni T. Structural and functional features of human muscle-tendon unit. Scand J Med Sci Sports 16, 147–158, doi: 10.1111/j.1600-0838.2005.00494.x (2006).
    1. Reeves N. D., Maganaris C. N. & Narici M. V. Ultrasonographic assessment of human skeletal muscle size. Eur J Appl Physiol 91, 116–118, doi: 10.1007/s00421-003-0961-9 (2004).
    1. Cronin N. J., Carty C. P., Barrett R. S. & Lichtwark G. Automatic tracking of medial gastrocnemius fascicle length during human locomotion. J Appl Physiol (1985) 111, 1491–1496, doi: 10.1152/japplphysiol.00530.2011 (2011).
    1. Gillett J. G., Barrett R. S. & Lichtwark G. A. Reliability and accuracy of an automated tracking algorithm to measure controlled passive and active muscle fascicle length changes from ultrasound. Comput Methods Biomech Biomed Engin 16, 678–687, doi: 10.1080/10255842.2011.633516 (2013).
    1. Farris D. J. & Lichtwark G. A. UltraTrack: Software for semi-automated tracking of muscle fascicles in sequences of B-mode ultrasound images. Comput Methods Programs Biomed 128, 111–118, doi: 10.1016/j.cmpb.2016.02.016 (2016).
    1. Fukunaga T. et al.. Physiological cross-sectional area of human leg muscles based on magnetic resonance imaging. J Orthop Res 10, 928–934, doi: 10.1002/jor.1100100623 (1992).

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