Ankle stiffness has been known as one of the most important components contributing to the maintenance of lower body stability during postural balance and locomotion. It has been repeatedly shown that women have lower stability and increased risk of injury when compared to men participating in similar sports activities, yet sex differences in neuromuscular control of the ankle, including the modulation of ankle stiffness, and their contribution to stability remain unknown. To identify sex differences in human ankle stiffness, this study quantified multi-dimensional ankle stiffness in 20 young, healthy men and 20 young, healthy women over a range of ankle muscle contractions, from relaxed to 20% of maximum voluntary co-contraction of ankle muscles. A wearable ankle robot and a system identification method were used to reliably quantify ankle stiffness in a 2-dimensional space spanning the sagittal plane and the frontal plane. In all muscle activation levels, significant sex differences in ankle stiffness were identified in both the sagittal and frontal planes. In the given experimental conditions, ankle stiffness in males was higher than females up to 15.1 and 8.3 Nm/rad in the sagittal plane and the frontal plane, respectively. In addition, sex differences in the spatial structure of ankle stiffness were investigated by quantifying three parameters defining the stiffness ellipse of the ankle: area, aspect ratio, and orientation. In all muscle activation levels, a significant sex difference was identified in the area of stiffness ellipse as expected from the sex difference in the sagittal and frontal planes. However, no statistical sex difference was observed in the aspect ratio and orientation, which would be due to little differences in major anatomical configurations of the ankle joint between sexes. This study, in combination with future studies investigating sex differences during dynamic tasks (e.g. postural balance and locomotion) would serve as a basis to develop a risk assessment tool and sex-specific training programs for efficient ankle injury prevention or rehabilitation.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Almeida, S. A., D. W. Trone, D. M. Leone, R. A. Shaffer, S. L. Patheal, and K. Long. Gender differences in musculoskeletal injury rates: a function of symptom reporting? Med. Sci. Sports Exerc. 31(12):1807–1812, 1999.
Bendat, J., and A. Piersol. Random Data: Analysis and Measurement Process (4th ed.). New York: Wiley, 2010.
Beynnon, B. D., I. M. Bernstein, A. Belisle, B. Brattbakk, P. Devanny, R. Risinger, and D. Durant. The effect of estradiol and progesterone on knee and ankle joint laxity. Am. J. Sports Med. 33(9):1298–1304, 2005.
Beynnon, B. D., P. A. Renstrom, D. M. Alosa, J. F. Baumhauer, and P. M. Vacek. Ankle ligament injury risk factors: a prospective study of college athletes. J. Orthop. Res. 19(2):213–220, 2001.
Burdet, E., R. Osu, D. W. Franklin, T. E. Milner, and M. Kawato. The central nervous system stabilizes unstable dynamics by learning optimal impedance. Nature 414(6862):446–449, 2001.
Casadio, M., P. G. Morasso, and V. Sanguineti. Direct measurement of ankle stiffness during quiet standing: implications for control modelling and clinical application. Gait Posture 21(4):410–424, 2005.
Council, N. R. Musculoskeletal disorders and the workplace. Washington, DC: National Academy Press, 2001.
Elias, S. R. 10-year trend in USA Cup soccer injuries: 1988-1997. Med. Sci. Sports Exerc. 33(3):359–367, 2001.
Ficanha, E. M., G. Ribeiro, and M. A. Rastgaar. Design and evaluation of a 2-DOF instrumented platform for estimation of the ankle mechanical impedance in the sagittal and frontal planes. IEEE/ASME Trans. Mechatron. 21(5):2531–2542, 2016.
Franklin, D. W., G. Liaw, T. E. Milner, R. Osu, E. Burdet, and M. Kawato. Endpoint stiffness of the arm is directionally tuned to instability in the environment. J. Neurosci. 27(29):7705–7716, 2007.
Gatev, P., S. Thomas, T. Kepple, and M. Hallett. Feedforward ankle strategy of balance during quiet stance in adults. J. Physiol. 514(Pt 3):915–928, 1999.
Glenmark, B., M. Nilsson, H. Gao, J. A. Gustafsson, K. Dahlman-Wright, and H. Westerblad. Difference in skeletal muscle function in males vs. females: role of estrogen receptor-beta. Am. J. Physiol. Endocrinol. Metab. 287(6):E1125–E1131, 2004.
Granata, K. P., D. A. Padua, and S. E. Wilson. Gender differences in active musculoskeletal stiffness. Part II. Quantification of leg stiffness during functional hopping tasks. J. Electromyogr. Kinesiol. 12(2):127–135, 2002.
Granata, K. P., S. E. Wilson, and D. A. Padua. Gender differences in active musculoskeletal stiffness. Part I. Quantification in controlled measurements of knee joint dynamics. J. Electromyogr. Kinesiol. 12(2):119–126, 2002.
Hansen, A. H., D. S. Childress, S. C. Miff, S. A. Gard, and K. P. Mesplay. The human ankle during walking: implications for design of biomimetic ankle prostheses. J. Biomech. 37(10):1467–1474, 2004.
Heitz, N. A., P. A. Eisenman, C. L. Beck, and J. A. Walker. Hormonal changes throughout the menstrual cycle and increased anterior cruciate ligament laxity in females. J. Athl. Train. 34(2):144–149, 1999.
Hewett, T. E. Neuromuscular and hormonal factors associated with knee injuries in female athletes. Strategies for intervention. Sports Med. 29(5):313–327, 2000.
Hill, D. W., and J. C. Smith. Gender difference in anaerobic capacity: role of aerobic contribution. Br. J. Sports Med. 27(1):45–48, 1993.
Hogan, N. Adaptive-control of mechanical impedance by coactivation of antagonist muscles. IEEE Trans. Autom. Control 29(8):681–690, 1984.
Hosea, T. M., C. C. Carey, and M. F. Harrer. The gender issue: epidemiology of ankle injuries in athletes who participate in basketball. Clin. Orthop. Relat. Res. 372:45–49, 2000.
Hunter, I. W., and R. E. Kearney. Dynamics of human ankle stiffness—variation with mean ankle torque. J. Biomech. 15(10):747–752, 1982.
Huston, L. J., and E. M. Wojtys. Neuromuscular performance characteristics in elite female athletes. Am. J. Sports Med. 24(4):427–436, 1996.
Janssen, I., S. B. Heymsfield, Z. M. Wang, and R. Ross. Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J. Appl. Physiol. (1985) 89(1):81–88, 2000.
Kearney, R. E., R. B. Stein, and L. Parameswaran. Identification of intrinsic and reflex contributions to human ankle stiffness dynamics. IEEE Trans. Biomed. Eng. 44(6):493–504, 1997.
Kent-Braun, J. A., and A. V. Ng. Specific strength and voluntary muscle activation in young and elderly women and men. J. Appl. Physiol. (1985) 87(1):22–29, 1999.
Kerrigan, D., M. Todd, and C. U. Della. Gender differences in joint biomechanics during walking: normative study in young adults. Am. J. Med. Rehabil. 77(1):2–7, 1998.
Kubo, K., H. Kanehisa, and T. Fukunaga. Gender differences in the viscoelastic properties of tendon structures. Eur. J. Appl. Physiol. 88(6):520–526, 2003.
Latash, M. L., and V. M. Zatsiorsky. Joint stiffness—myth or reality. Human Mov. Sci. 12(6):653–692, 1993.
Lee, H., P. Ho, M. Rastgaar, H. I. Krebs, and N. Hogan. Multivariable static ankle mechanical impedance with active muscles. IEEE Trans. Neural Syst. Rehabil. Eng. 22(1):44–52, 2014.
Lee, H., and N. Hogan. Time-varying ankle mechanical impedance during human locomotion. IEEE Trans. Neural Syst. Rehabil. Eng. 23(5):755–764, 2015.
Lee, H., H. I. Krebs, and N. Hogan. Multivariable dynamic ankle mechanical impedance with active muscles. IEEE Trans. Neural Syst. Rehabil. 22(5):971–981, 2014.
Lee, H., H. I. Krebs, and N. Hogan. Multivariable dynamic ankle mechanical impedance with relaxed muscles. IEEE Trans. Neural Syst. Rehabil. Eng. 22(6):1104–1114, 2014.
Lee, H., E. Rouse, and H. I. Krebs. Summary of human ankle mechanical impedance during walking. IEEE J. Transl. Eng. Health Med. 4:1–7, 2016.
Loram, I. D., and M. Lakie. Direct measurement of human ankle stiffness during quiet standing: the intrinsic mechanical stiffness is insufficient for stability. J. Physiol. Lond. 545(3):1041–1053, 2002.
Miller, A. E., J. D. MacDougall, M. A. Tarnopolsky, and D. G. Sale. Gender differences in strength and muscle fiber characteristics. Eur. J. Appl. Physiol. Occup. Physiol. 66(3):254–262, 1993.
Mirbagheri, M. M., H. Barbeau, and R. E. Kearney. Intrinsic and reflex contributions to human ankle stiffness: variation with activation level and position. Exp. Brain Res. 135(4):423–436, 2000.
Montgomery, J., and D. Avers. Daniels and Worthingham’s Muscle Testing: Techniques of Manual Examination (8th ed.). Philadelphia: Saunders, 2007.
Nalam, V., H. Lee. Design and validation of a multi-axis robotic platform for the characterization of ankle neuromechanics. In: Proceedings of the IEEE International Conference on Robotics and Automation 2017 (ICRA 2017); Singapore.
Nalam, V., H. Lee. A new robotic approach to characterize mechanical impedance and energetic passivity of the human ankle during standing. Paper presented at: In: Proceedings of the 39th Annual International Conference of IEEE Engineering Medicine and Biology Society, South Korea, 2017.
Neptune, R. R., S. A. Kautz, and F. E. Zajac. Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking. J. Biomech. 34(11):1387–1398, 2001.
Perry, J. Gait Analysis: Normal and Pathologic Functions. New Jersey: Slack Inc., 1992.
Quatman, C. E., K. R. Ford, G. D. Myer, M. V. Paterno, and T. E. Hewett. The effects of gender and pubertal status on generalized joint laxity in young athletes. J. Sci. Med. Sport. 11(3):257–263, 2008.
Ristolainen, L., A. Heinonen, B. Waller, U. M. Kujala, and J. A. Kettunen. Gender differences in sport injury risk and types of inju-ries: a retrospective twelve-month study on cross-country skiers, swimmers, long-distance runners and soccer players. J. Sports Sci. Med. 8(3):443–451, 2009.
Robertson, D. G., and D. A. Winter. Mechanical energy generation, absorption and transfer amongst segments during walking. J. Biomech. 13(10):845–854, 1980.
Rouse, E. J., R. D. Gregg, L. J. Hargrove, and J. W. Sensinger. The difference between stiffness and quasi-stiffness in the context of biomechanical modeling. IEEE Trans. Biomed. Eng. 60(2):562–568, 2013.
Rouse, E. J., L. J. Hargrove, E. J. Perreault, and T. A. Kuiken. Estimation of human ankle impedance during the stance phase of walking. IEEE Trans. Neural Syst. Rehabil. Eng. 22(4):870–878, 2014.
Shamaei, K., G. S. Sawicki, and A. M. Dollar. Estimation of quasi-stiffness and propulsive work of the human ankle in the stance phase of walking. PLoS ONE 8(3):e59935, 2013.
Slauterbeck, J., C. Clevenger, W. Lundberg, and D. M. Burchfield. Estrogen level alters the failure load of the rabbit anterior cruciate ligament. J. Orthop. Res. 17(3):405–408, 1999.
Stefanyshyn, D. J., and B. M. Nigg. Dynamic angular stiffness of the ankle joint during running and sprinting. J. Appl. Biomech. 14(3):292–299, 1998.
Wilkerson, R. D., and M. A. Mason. Differences in men’s and women’s mean ankle ligamentous laxity. Iowa Orthop. J. 20:46–48, 2000.
Winter, D. A. Human balance and posture control during standing and walking. Gait Posture 3:193–214, 1995.
Winter, D. A., A. E. Patla, S. Rietdyk, and M. G. Ishac. Ankle muscle stiffness in the control of balance during quiet standing. J. Neurophysiol. 85(6):2630–2633, 2001.
Zeller, B. L., J. L. McCrory, W. B. Kibler, and T. L. Uhl. Differences in kinematics and electromyographic activity between men and women during the single-legged squat. Am. J. Sports Med. 31(3):449–456, 2003.
This study was completed by a support of Virginia G. Piper Foundation, adidas-ASU Global Sport Alliance, and Ira A. Fulton Schools of Engineering at the Arizona State University.
Conflict of interest
The authors declare that there is no conflict of interest in this study.
Associate Editor Sean S. Kohles oversaw the review of this article.
About this article
Cite this article
Trevino, J., Lee, H. Sex Differences in 2-DOF Human Ankle Stiffness in Relaxed and Contracted Muscles. Ann Biomed Eng 46, 2048–2056 (2018). https://doi.org/10.1007/s10439-018-2092-9
- Human ankle
- Ankle stiffness
- Ankle injury
- Gender difference
- Sex difference