Daniel E. Lieberman1, Madhusudhan Venkadesan1,2,8, William A. Werbel3,8, Adam I. Daoud1,8, Susan D’Andrea4, Irene S. Davis5, Robert Ojiambo Mang’Eni6,7 & Yannis Pitsiladis6,7

  1. Department of Human Evolutionary Biology, 11 Divinity Avenue,
  2. School of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts 02138, USA
  3. University of Michigan Medical School, Ann Arbor, Michigan 48109, USA
  4. Center for Restorative and Regenerative Medicine, Providence Veterans Affairs Medical Center, Providence, Rhode Island 02906, USA
  5. Department of Physical Therapy, University of Delaware, Newark, Delaware 19716, USA
  6. Department of Medical Physiology, Moi University Medical School, PO Box 4606, 30100 Eldoret, Kenya
  7. Faculty of Biomedical & Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK
  8. These authors contributed equally to this work.
Correspondence to: Daniel E. Lieberman1 Correspondence and requests for materials should be addressed to D.E.L. (Email: danlieb@fas.harvard.edu).


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Abstract

Humans have engaged in endurance running for millions of years1, but the modern running shoe was not invented until the 1970s. For most of human evolutionary history, runners were either barefoot or wore minimal footwear such as sandals or moccasins with smaller heels and little cushioning relative to modern running shoes. We wondered how runners coped with the impact caused by the foot colliding with the ground before the invention of the modern shoe. Here we show that habitually barefoot endurance runners often land on the fore-foot (fore-foot strike) before bringing down the heel, but they sometimes land with a flat foot (mid-foot strike) or, less often, on the heel (rear-foot strike). In contrast, habitually shod runners mostly rear-foot strike, facilitated by the elevated and cushioned heel of the modern running shoe. Kinematic and kinetic analyses show that even on hard surfaces, barefoot runners who fore-foot strike generate smaller collision forces than shod rear-foot strikers. This difference results primarily from a more plantarflexed foot at landing and more ankle compliance during impact, decreasing the effective mass of the body that collides with the ground. Fore-foot- and mid-foot-strike gaits were probably more common when humans ran barefoot or in minimal shoes, and may protect the feet and lower limbs from some of the impact-related injuries now experienced by a high percentage of runners.
Running can be most injurious at the moment the foot collides with the ground. This collision can occur in three ways: a rear-foot strike (RFS), in which the heel lands first; a mid-foot strike (MFS), in which the heel and ball of the foot land simultaneously; and a fore-foot strike (FFS), in which the ball of the foot lands before the heel comes down. Sprinters often FFS, but 75–80% of contemporary shod endurance runners RFS2, 3. RFS runners must repeatedly cope with the impact transient of the vertical ground reaction force, an abrupt collision force of approximately 1.5–3 times body weight, within the first 50 ms of stance (Fig. 1a). The time integral of this force, the impulse, is equal to the change in the body’s momentum during this period as parts of the body’s mass decelerate suddenly while others decelerate gradually4. This pattern of deceleration is equivalent to some proportion of the body’s mass (Meff, the effective mass) stopping abruptly along with the point of impact on the foot5. The relation between the impulse, the body’s momentum and Meff is expressed as
Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, or to obtain a text description, please contact npg@nature.com
where Fz(t) is the time-varying vertical ground reaction force, 0- is the instant of time before impact, T is the duration of the impact transient, Mbody is the body mass, vcom is the vertical speed of the centre of mass, vfoot is the vertical speed of the foot just before impact and g is the acceleration due to gravity at the Earth’s surface.


FIGURE 1. Vertical ground reaction forces and foot kinematics for three foot strikes at 3.5 m s-1 in the same runner.






Impact transients associated with RFS running are sudden forces with high rates and magnitudes of loading that travel rapidly up the body and thus may contribute to the high incidence of running-related injuries, especially tibial stress fractures and plantar fasciitis6, 7, 8. Modern running shoes are designed to make RFS running comfortable and less injurious by using elastic materials in a large heel to absorb some of the transient force and spread the impulse over more time9 (Fig. 1b). The human heel pad also cushions impact transients, but to a lesser extent5, 10, 11, raising the question of how runners struck the ground before the invention of modern running shoes. Previous studies have found that habitually shod runners tend to adopt a flatter foot placement when barefoot than when shod, thus reducing stresses on the foot12, 13, 14, 15, but there have been no detailed studies of foot kinematics and impact transients in long-term habitually barefoot runners.
We compared foot strike kinematics on tracks at preferred endurance running speeds (4–6 m s-1) among five groups controlled for age and habitual footwear usage (Methods and Supplementary Data 2). Adults were sampled from three groups of individuals who run a minimum of 20 km per week: (1) habitually shod athletes from the USA; (2) athletes from the Rift Valley Province of Kenya (famed for endurance running16), most of whom grew up barefoot but now wear cushioned shoes when running; and (3) US runners who grew up shod but now habitually run barefoot or in minimal footwear. We also compared adolescents from two schools in the Rift Valley Province: one group (4) who have never worn shoes; and another group (5) who have been habitually shod most of their lives. Speed, age and distance run per week were not correlated significantly with strike type or foot and ankle angles within or among groups. However, because the preferred speed was approximately 1 m s-1 slower in indoor trials than in outdoor trials, we made statistical comparisons of kinematic and kinetic data only between groups 1 and 3 (Table 1).


Strike patterns vary within subjects and groups, but these trials (Table 1 andSupplementary Data 6) confirm reports2, 3, 9 that habitually shod runners who grew up wearing shoes (groups 1 and 5) mostly RFS when shod; these runners also predominantly RFS when barefoot on the same hard surfaces, but adopt flatter foot placements by dorsiflexing approximately 7–10° less (analysis of variance, P < 0.05). In contrast, runners who grew up barefoot or switched to barefoot running (groups 2 and 4) most often used FFS landings followed by heel contact (toe–heel–toe running) in both barefoot and shod conditions. MFS landings were sometimes used in barefoot conditions (group 4) and shod conditions (group 2), but RFS landings were infrequent during barefoot running in both groups. A major factor contributing to the predominance of RFS landings in shod runners is the cushioned sole of most modern running shoes, which is thickest below the heel, orienting the sole of the foot so as to have about 5° less dorsiflexion than does the sole of the shoe, and allowing a runner to RFS comfortably (Fig. 1). Thus, RFS runners who dorsiflex the ankle at impact have shoe soles that are more dorsiflexed relative to the ground, and FFS runners who plantarflex the ankle at impact have shoe soles that are flatter (less plantarflexed) relative to the ground, even when knee and ankle angles are not different (Table 1). These data indicate that habitually unshod runners RFS less frequently, and that shoes with elevated, cushioned heels facilitate RFS running (Supplementary Data 3).
Kinematic differences among foot strikes generate markedly different collision forces at the ground, which we compared in habitually shod and barefoot adult runners from the USA during RFS and FFS running (Methods and Supplementary Data 2). Whereas RFS landings cause large impact transients in shod runners and even larger transients in unshod runners (Fig. 1a, b), FFS impacts during toe–heel–toe gaits typically generate ground reaction forces lacking a distinct transient (Fig. 1c), even on a stiff steel force plate4, 17, 18, 19. At similar speeds, magnitudes of peak vertical force during the impact period (6.2 ± 3.7% (all uncertainties are s.d. unless otherwise indicated) of stance for RFS runners) are approximately three times lower in habitual barefoot runners who FFS than in habitually shod runners who RFS either barefoot or in shoes (Fig. 2a). Also, over the same percentage of stance the average rate of loading in FFS runners when barefoot is seven times lower than in habitually shod runners who RFS when barefoot, and is similar to the rate of loading of shod RFS runners (Fig. 2b). Further, in the majority of barefoot FFS runners, rates of loading were approximately half those of shod RFS runners.

FIGURE 2. Variation in impact transients.

Modelling the foot and leg as an L-shaped double pendulum that collides with the ground (Fig. 3a) identifies two biomechanical factors, namely the initial point of contact and ankle stiffness, that decrease Meff and, hence, the magnitude of the impact transient (equation (1) and Supplementary Data 4). A RFS impact typically occurs just below the ankle, under the centre of mass of the foot plus leg, and with variable plantarflexion (Fig. 3b). Therefore, the ankle converts little translational energy into rotational energy and most of the translational kinetic energy is lost in the collision, leading to an increase in Meff(ref. 20). In contrast, a FFS impact occurs towards the front of the foot (Fig. 3a), and the ankle dorsiflexes as the heel drops under control of the triceps surae muscles and the Achilles tendon (Fig. 3b). The ground reaction force in a FFS therefore torques the foot around the ankle, which reduces Meff by converting part of the lower limb’s translational kinetic energy into rotational kinetic energy, especially in FFS landings with low ankle stiffness (Fig. 3a). We note that MFS landings with intermediate contact points are predicted to generate intermediate Meff values.

FIGURE 3. Differences during impact between shod RFS runners (group 1) and barefoot FFS runners (group 3) at approximately 4 m s-1.


The conservation of angular impulse momentum during a rigid plastic collision can be used to predict Meff as a function of the location of the centre of pressure at impact for ankles with zero and infinite joint stiffnesses (Supplementary Data 4). Figure 3 shows model values of Meff for an average foot and shank comprising 1.4% and 4.5% Mbody, respectively, where the shank is 1.53 times longer than the foot21Meff can be calculated, using experimental data from equation (1), as
Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, or to obtain a text description, please contact npg@nature.com
Using equation (2) with kinematic and kinetic data from groups 1 and 3 (Methods), we find that Meff averages 4.49 ± 2.24 kg for RFS runners in the barefoot condition and 1.37 ± 0.42 kg for habitual barefoot runners who FFS (Fig. 3a). Normalized to Mbody, the average Meff is 6.8 ± 3.0% for barefoot RFS runners and 1.7 ± 0.4% for barefoot FFS runners. For all RFS landings, these values are not significantly different from the predicted Meff values for a rigid ankle (5.5–5.9% Mbody) or a compliant ankle (3.4–5.9% Mbody), indicating that ankle compliance has little effect and that there is some contribution from mass above the knee, which is very extended in these runners (Fig. 3b). For FFS landings, Meff values are smaller than the predicted values for a rigid ankle (2.7–4.1% Mbody) and are insignificantly greater than those predicted for a compliant ankle (0.45–1.1% Mbody), suggesting low levels of ankle stiffness. These results therefore support the prediction that FFS running generates collisions with a much lower Meff than does RFS running. Furthermore, MFS running is predicted to generate intermediate Meff values with a strong dependence on the centre of pressure at impact and on ankle stiffness.
How runners strike the ground also affects vertical leg compliance, defined as the drop in the body’s centre of mass relative to the vertical force during the period of impact. Vertical compliance is greater in FFS running than in RFS running, leading to a lower rate of loading (Fig. 3c). More compliance during the impact period in FFS runners is partly explained by a 74% greater drop in the centre of mass (t-test, P < 0.009), resulting, in part, from ankle dorsiflexion and knee flexion (Fig. 3b). In addition, like shod runners, barefoot runners adjust leg stiffness depending on surface hardness22. As a result, we found no significant differences in rates or magnitudes of impact loading in barefoot runners on hard surfaces relative to cushioned surfaces (Supplementary Data 5).
Differences between RFS and FFS running make sense from an evolutionary perspective. If endurance running was an important behaviour before the invention of modern shoes, then natural selection is expected to have operated to lower the risk of injury and discomfort when barefoot or in minimal footwear. Most shod runners today land on their heels almost exclusively. In contrast, runners who cannot or prefer not to use cushioned shoes with elevated heels often avoid RFS landings and thus experience lower impact transients than do most shod runners today, even on very stiff surfaces (Fig. 2). Early bipedal hominins such as Australopithecus afarensis had enlarged calcaneal tubers and probably walked with a RFS23. However, they lacked some derived features of the modern human foot, such as a strong longitudinal arch1, 24 that functionally improves the mass–spring mechanics of running by storing and releasing elastic energy25. We do not know whether early hominins ran with a RFS, a MFS or a FFS gait. However, the evolution of a strong longitudinal arch in genus Homowould increase performance more for non-RFS landings because the arch stretches passively during the entire first half of stance in FFS and MFS gaits. In contrast, the arch can stretch passively only later in stance during RFS running, when both the fore-foot and the rear-foot are on the ground. This difference may account for the lower cost of barefoot running relative to shod running15, 26.
Evidence that barefoot and minimally shod runners avoid RFS strikes with high-impact collisions may have public health implications. The average runner strikes the ground 600 times per kilometre, making runners prone to repetitive stress injuries6, 7, 8. The incidence of such injuries has remained considerable for 30 years despite technological advancements that provide more cushioning and motion control in shoes designed for heel–toe running27, 28, 29. Although cushioned, high-heeled running shoes are comfortable, they limit proprioception and make it easier for runners to land on their heels. Furthermore, many running shoes have arch supports and stiffened soles that may lead to weaker foot muscles, reducing arch strength. This weakness contributes to excessive pronation and places greater demands on the plantar fascia, which may cause plantar fasciitis. Although there are anecdotal reports of reduced injuries in barefoot populations30, controlled prospective studies are needed to test the hypothesis that individuals who do not predominantly RFS either barefoot or in minimal footwear, as the foot apparently evolved to do, have reduced injury rates.
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Methods Summary

We studied five subject groups (Table 1 and Supplementary Data 1), both barefoot and in running shoes. Habitually shod and barefoot US subjects ran over a force plate embedded 80% of the way along a 20–25-m-long indoor track. We quantified joint angles using a three-dimensional infrared kinematic system (Qualysis) at 240 Hz and a 500-Hz video camera (Fastec InLine 500M). African subjects were recorded on a 20–25-m outdoor track of hard dirt using a 500-Hz video camera. All subjects ran at preferred speeds with several habituation trials before each condition, and were recorded for five to seven trials per condition. We taped kinematic markers on joints and segments in all subjects. Video frames were analysed using IMAGEJ (http://rsb.info.nih.gov/nih-image/) to measure the angle of the plantar surface of the foot relative to earth horizontal (plantar foot angle), as well as ankle, knee and hip angles (Methods). We recorded the vertical ground reaction force (Fz) in US subjects at 4,800 Hz using AMTI force plates (BP400600 Biomechanics Force Platform), and normalized the results to body weight. The impact-transient magnitude and percentage of stance were measured at peak, and the rate of loading was quantified between 200 N and 90% of peak (following ref. 18). When there was no distinct impact transient, the same parameters were measured at the same percentage of stance plus/minus 1 s.d. as determined for each condition in trials with an impact transient. The effective mass (Meff) in RFS runners was calculated using the integral of Fz (equation (2)) between the time when Fzexceeded 4 s.d. above baseline noise and the time when the transient peak was reached as measured in RFS runners; the impulse over the same percentage of stance (6.2 ± 3.7%) was used to calculated Meff in FFS runners. Vertical foot and leg speed were calculated using a central difference method and the three-dimensional kinematic data.
Full methods accompany this paper.
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References

  1. Bramble, D. M. & Lieberman, D. E. Endurance running and the evolution ofHomoNature 432, 345–352 (2004) | Article | PubMed | ISI | ChemPort |
  2. Kerr, B. A., Beauchamp, L., Fisher, V. & Neil, R. in Proc. Int. Symp. Biomech. Aspects Sports Shoes Playing Surf. (eds Nigg, B. M. & Kerr, B. A.) 135–142 (Calgary Univ. Press, 1983)
  3. Hasegawa, H., Yamauchi, T. & Kraemer, W. J. Foot strike patterns of runners at 15-km point during an elite-level half marathonJ. Strength Cond. Res. 21, 888–893 (2007) | Article | PubMed
  4. Bobbert, M. F., Schamhardt, H. C. & Nigg, B. M. Calculation of vertical ground reaction force estimates during running from positional dataJ. Biomech. 24, 1095–1105 (1991) | Article | PubMed | ChemPort |
  5. Chi, K. J. & Schmitt, D. Mechanical energy and effective foot mass during impact loading of walking and runningJ. Biomech. 38, 1387–1395 (2005) | Article | PubMed
  6. Milner, C. E., Ferber, R., Pollard, C. D., Hamill, J. & Davis, I. S.Biomechanical factors associated with tibial stress fractures in female runnersMed. Sci. Sports Exerc. 38, 323–328 (2006) | Article | PubMed
  7. Pohl, M. B., Hamill, J. & Davis, I. S. Biomechanical and anatomical factors associated with a history of plantar fasciitis in female runnersClin. J. Sport Med. 19, 372–376 (2009) | Article | PubMed
  8. van Gent, R. N. et al. Incidence and determinants of lower extremity running injuries in long distance runners: a systematic reviewBr. J. Sports Med. 41, 469–480 (2007) | Article | PubMed | ChemPort |
  9. Nigg, B. R. The Biomechanics of Running Shoes (Human Kinetics, 1986)
  10. Ker, R. F., Bennett, M. B., Alexander, R. M. & Kester, R. C. Foot strike and the properties of the human heel padProc. Inst. Mech. Eng. H 203, 191–196 (1989) | Article | PubMed | ChemPort |
  11. De Clercq, D., Aerts, P. & Kunnen, M. The mechanical characteristics of the human heel pad during foot strike in running: an in vivocineradiographic studyJ. Biomech. 27, 1213–1222 (1994) | Article | PubMed | ChemPort |
  12. De Wit, B., De Clercq, D. & Aerts, P. Biomechanical analysis of the stance phase during barefoot and shod runningJ. Biomech. 33, 269–278 (2000) | Article | PubMed | ChemPort |
  13. Divert, C., Mornieux, G., Baur, H., Mayer, F. & Belli, A. Mechanical comparison of barefoot and shod runningInt. J. Sports Med. 26, 593–598 (2005) | Article | PubMed | ChemPort |
  14. Eslami, M., Begon, M., Farahpour, N. & Allard, P. Forefoot-rearfoot coupling patterns and tibial internal rotation during stance phase of barefoot versus shod runningClin. Biomech. (Bristol, Avon) 22, 74–80 (2007) | Article | PubMed
  15. Squadrone, R. & Gallozi, C. Biomechanical and physiological comparison of barefoot and two shod conditions in experienced barefoot runnersJ. Sports Med. Phys. Fitness 49, 6–13 (2009) | PubMed | ChemPort |
  16. Onywera, V. O., Scott, R. A., Boit, M. K. & Pitsiladis, Y. P. Demographic characteristics of elite Kenyan runnersJ. Sports Sci. 24, 415–422 (2006) | Article | PubMed
  17. Dickinson, J. A., Cook, S. D. & Leinhardt, T. M. The measurement of shock waves following heel strike while runningJ. Biomech. 18, 415–422 (1985) | Article | PubMed | ChemPort |
  18. Williams, D. S., McClay, I. S. & Manal, K. T. Lower extremity mechanics in runners with a converted forefoot strike patternJ. Appl. Biomech. 16, 210–218 (2000)
  19. Laughton, C. A., Davis, I. & Hamill, J. Effect of strike pattern and orthotic intervention on tibial shock during runningJ. Appl. Biomech. 19, 153–168 (2003)
  20. Chatterjee, A. & Garcia, M. Small slope implies low speed for McGeers’ passive walking machinesDyn. Syst. 15, 139–157 (2000)
  21. Dempster, W. T. Space Requirements of the Seated Operator: Geometrical, Kinematic, and Mechanical Aspects of the Body, with Special Reference to the Limbs. WADC Technical Report 55-159 (United States Air Force, 1955)
  22. Dixon, S. J., Collop, A. C. & Batt, M. E. Surface effects on ground reaction forces and lower extremity kinematics in runningMed. Sci. Sports Exerc. 32, 1919–1926 (2000) | Article | PubMed | ChemPort |
  23. Latimer, B. & Lovejoy, C. O. The calcaneus of Australopithecus afarensisand its implications for the evolution of bipedalityAm. J. Phys. Anthropol.78, 369–386 (1989) | Article | PubMed | ISI | ChemPort |
  24. Jungers, W. L. et al. The foot of Homo floresiensisNature 459, 81–84 (2009) | Article | PubMed | ChemPort |
  25. Ker, R. F., Bennett, M. B., Bibby, S. R., Kester, R. C. & Alexander, R. M.The spring in the arch of the human footNature 325, 147–149 (1987) | Article | PubMed | ChemPort |
  26. Divert, C. et al. Barefoot-shod running differences: shoe or mass effect.Int. J. Sports Med. 29, 512–518 (2008) | Article | PubMed | ChemPort |
  27. Marti, B. in The Shoe in Sport (ed. Segesser, B.) 256–265 (Yearbook Medical, 1989)
  28. Richards, C. E., Magin, P. J. & Calister, R. Is your prescription of distance running shoes evidence-based? Br. J. Sports Med. 43, 159–162 (2009) | Article | PubMed | ChemPort |
  29. van Mechelen, W. Running injuries: a review of the epidemiological literatureSports Med. 14, 320–335 (1992) | Article | PubMed | ChemPort |
  30. Robbins, S. E. & Hanna, A. M. Running-related injury prevention through barefoot adaptationsMed. Sci. Sports Exerc. 19, 148–156 (1987) | PubMed | ChemPort |