Sex Differences in Lower Limb Proprioception and Mechanical Function Among Healthy Adults

in Motor Control
View More View Less
  • 1 Shanghai University of Sport
  • 2 University of Ottawa
Restricted access

Purchase article

USD  $24.95

Student 1 year online subscription

USD  $77.00

1 year online subscription

USD  $103.00

Student 2 year online subscription

USD  $147.00

2 year online subscription

USD  $195.00

Twenty-four healthy adults, including 12 females and 12 males, participated in the study. Each female participant completed three trials in three different phases of one menstrual cycle, which included follicular, ovulatory, and luteal phases. The study aimed to investigate whether there is any difference in joint kinetic sense, neuromuscular coordination, and isokinetic muscle strength (a) between healthy males and females at different phases of the menstrual cycle and (b) between females at different phases of the menstrual cycle. The outcome measures included the number of jumps in the square-hop test and ankle and knee proprioception, which were assessed by an electric-driven movable frame rotated at 0.4 deg/s and isokinetic muscle strength measured by a computerized dynamometer (Biodex). For the square-hop test (p = .006), ankle dorsiflexion/plantar flexion (p < .05), knee flexion/extension (p < .05), the relative peak torque of the isokinetic muscle strength at the 60° and 180° knee flexion/extension (p < .001), and the 30° and 120° ankle plantar flexion/dorsiflexion (p < .05) between females and males showed significant differences. For the females at different phases of the menstrual cycle, significant differences were found on ankle dorsiflexion (p = .003), plantar flexion (p = .023), knee extension (p = .029), the square-hop test (p = .036), and relative peak torque of isokinetic muscle strength at 180° knee flexion (p = .029). This study demonstrated that there are sex differences in lower limb proprioception and mechanical function. Females at ovulatory and luteal phases have better lower limb proprioception than at the follicular phase.

Hu and Wang are with the School of Kinesiology, Shanghai University of Sport, Shanghai, China. Li is with the School of Human Kinetics, University of Ottawa, Ottawa, Ontario, Canada.

Wang (wanglin@sus.edu.cn) is corresponding author.
  • Abt, J.P., Sell, T.C., Laudner, K.G., McCrory, J.L., Loucks, T.L., Berga, S.L., & Lephart, S.M. (2007). Neuromuscular and biomechanical characteristics do not vary across the menstrual cycle. Knee Surgery, Sports Traumatology, Arthroscopy, 15(7), 901907. PubMed ID: 17364205 doi:10.1007/s00167-007-0302-3

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Adachi, N., Nawata, K., Maeta, M., & Kurozawa, Y. (2008). Relationship of the menstrual cycle phase to anterior cruciate ligament injuries in teenaged female athletes. Archives of Orthopaedic and Trauma Surgery, 128(5), 473478. PubMed ID: 17909824 doi:10.1007/s00402-007-0461-1

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Alexander, A., Irving, A.J., & Harvey, J. (2017). Emerging roles for the novel estrogen-sensing receptor GPER1 in the CNS. Neuropharmacology, 113(Pt B), 652660. PubMed ID: 27392633 doi:10.1016/j.neuropharm.2016.07.003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Aydoğ, S.T., Hasçelik, Z., Demirel, H.A., Tetik, O., Aydoğ, E., & Doral, M.N. (2005). The effects of menstrual cycle on the knee joint position sense: Preliminary study. Knee Surgery, Sports Traumatology, Arthroscopy, 13(8), 649653. PubMed ID: 15871012 doi:10.1007/s00167-004-0604-7

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Baker, M.L., Epari, D.R., Lorenzetti, S., Sayers, M., Boutellier, U., & Taylor, W.R. (2017). Risk factors for knee injury in golf: A systematic review. Sports Medicine, 47(12), 26212639. PubMed ID: 28884352 doi:10.1007/s40279-017-0780-5

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Balachandar, V., Marciniak, J.L., Wall, O., & Balachandar, C. (2017). Effects of the menstrual cycle on lower-limb biomechanics, neuromuscular control, and anterior cruciate ligament injury risk: A systematic review. Muscles, Ligaments and Tendons Journal, 7(1), 136. PubMed ID: 28717621 doi:10.11138/mltj/2017.7.1.136

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Beynnon, B.D., Johnson, R.J., Braun, S., Sargent, M., Bernstein, I.M., Skelly, J.M., & Vacek, P.M. (2006). The relationship between menstrual cycle phase and anterior cruciate ligament injury: A case-control study of recreational alpine skiers. The American Journal of Sports Medicine, 34(5), 757764. PubMed ID: 16436538 doi:10.1177/0363546505282624

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Birch, K., & Reilly, T. (2002). The diurnal rhythm in isometric muscular performance differs with eumenorrheic menstrual cycle phase. Chronobiology International, 19(4), 731742. PubMed ID: 12182500 doi:10.1081/CBI-120006083

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bonetti, L.V., Grisa, N.C., Demeda, C.S., Finger, A.L.T., De Marchi, T., & Tadiello, G.S. (2018). Isokinetic performance of knee extensor and flexor musculature in adolescent female handball players. Archivos de Medicina del Deporte, 35(3), 157161.

    • Search Google Scholar
    • Export Citation
  • Burris, T.P., Solt, L.A., Wang, Y., Crumbley, C., Banerjee, S., Griffett, K., Kojetin, D.J. (2013). Nuclear receptors and their selective pharmacologic modulators. Pharmacological Reviews, 65(2), 710778. PubMed ID: 23457206 doi:10.1124/pr.112.006833

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Centers for Disease Control and Prevention. (2002). CDC injury research agenda. Atlanta, GA: National Center for Injury Prevention and Control.

    • Search Google Scholar
    • Export Citation
  • Chappell, J.D., Yu, B., Kirkendall, D.T., & Garrett, W.E. (2002). A comparison of knee kinetics between male and female recreational athletes in stop-jump tasks. The American Journal of Sports Medicine, 30(2), 261267. PubMed ID: 11912098 doi:10.1177/03635465020300021901

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Dargo, L., Robinson, K.J., & Games, K.E. (2017). Prevention of knee and anterior cruciate ligament injuries through the use of neuromuscular and proprioceptive training: An evidence-based review. Journal of Athletic Training, 52(12), 11711172. PubMed ID: 29172648 doi:10.4085/1062-6050-52.12.21

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Deitch, J.R., Starkey, C., Walters, S.L., & Moseley, J.B. (2006). Injury risk in professional basketball players: A comparison of Women’s National Basketball Association and National Basketball Association athletes. The American Journal of Sports Medicine, 34(7), 10771083. doi:10.1177/0363546505285383

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Eiling, E., Bryant, A., Petersen, W., Murphy, A., & Hohmann, E. (2007). Effects of menstrual-cycle hormone fluctuations on musculotendinous stiffness and knee joint laxity. Knee Surgery, Sports Traumatology, Arthroscopy, 15(2), 126132. PubMed ID: 16821077 doi:10.1007/s00167-006-0143-5

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Fernandez, W.G., Yard, E.E., & Comstock, R.D. (2007). Epidemiology of lower extremity injuries among U.S. high school athletes. Academic Emergency Medicine, 14(7), 641645. PubMed ID: 17513688 doi:10.1197/j.aem.2007.03.1354

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ferri, A., Scaglioni, G., Pousson, M., Capodaglio, P., Van Hoecke, J., & Narici, M. (2003). Strength and power changes of the human plantar flexors and knee extensors in response to resistance training in old age. Acta Physiologica Scandinavica, 177(1), 6978. PubMed ID: 12492780 doi:10.1046/j.1365-201X.2003.01050.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Fridén, C., Hirschberg, A.L., Saartok, T., & Renström, P. (2006). Knee joint kinaesthesia and neuromuscular coordination during three phases of the menstrual cycle in moderately active women. Knee Surgery, Sports Traumatology, Arthroscopy, 14(4), 383389. PubMed ID: 15942744 doi:10.1007/s00167-005-0663-4.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Friden, C., Saartok, T., Bäckström, C., Leanderson, J., & Renström, P. (2003). The influence of premenstrual symptoms on postural balance and kinesthesia during the menstrual cycle. Gynecological Endocrinology, 17(6), 433440. PubMed ID: 14992161

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Fukaya, K., Kawamori, A., Osada, Y., Kitazawa, M., & Ishiguro, M. (2017). The forecasting of menstruation based on a state‐space modeling of basal body temperature time series. Statistics in Medicine, 36(21), 33613379. PubMed ID: 28543214 doi:10.1002/sim.7345

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Fulstone, D., Chandran, A., Barron, M., & DiPietro, L. (2016). Continued sex-differences in the rate and severity of knee injuries among collegiate soccer players: The NCAA injury surveillance system, 2004–2009. International Journal of Sports Medicine, 37(14), 11501153. PubMed ID: 27706548 doi:10.1055/s-0042-112590

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Goble, D.J. (2010). Proprioceptive acuity assessment via joint position matching: From basic science to general practice. Physical Therapy, 90(8), 11761184. PubMed ID: 20522675 doi:10.2522/ptj.20090399

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Han, J., Anson, J., Waddington, G., Adams, R., & Liu, Y. (2015). The role of ankle proprioception for balance control in relation to sports performance and injury. Biomed Research International, 2015, 842804. PubMed ID: 26583139 doi:10.1155/2015/842804

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Han, J., Waddington, G., Adams, R., Anson, J., & Liu, Y. (2016). Assessing proprioception: A critical review of methods. Journal of Sport and Health Science, 5(1), 8090. PubMed ID: 30356896 doi:10.1016/j.jshs.2014.10.004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hertel, J., Williams, N. I., Olmsted-Kramer, L.C., Leidy, H.J., & Putukian, M. (2006). Neuromuscular performance and knee laxity do not change across the menstrual cycle in female athletes. Knee Surgery, Sports Traumatology, Arthroscopy, 14(9), 817822. PubMed ID: 16470385 doi:10.1007/s00167-006-0047-4

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hewett, T.E. (2000). Neuromuscular and hormonal factors associated with knee injuries in female athletes. Sports Medicine, 29(5), 313327. PubMed ID: 10840866 doi:10.2165/00007256-200029050-00003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hill, E.C., Housh, T.J., Smith, C.M., Schmidt, R.J., & Johnson, G.O. (2018). Gender-and muscle-specific responses during fatiguing exercise. The Journal of Strength & Conditioning Research, 32(5), 14711478. PubMed ID: 29334581 doi:10.1519/JSC.0000000000001996

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hoffman, M., Harter, R.A., Hayes, B.T., Wojtys, E.M., & Murtaugh, P. (2008). The interrelationships among sex hormone concentrations, motoneuron excitability, and anterior tibial displacement in women and men. Journal of Athletic Training, 43(4), 364372. PubMed ID: 18668169 doi:10.4085/1062-6050-43.4.364

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Jorgensen, M.G., Laessoe, U., Hendriksen, C., Nielsen, O.B.F., & Aagaard, P. (2013). Efficacy of Nintendo Wii training on mechanical leg muscle function and postural balance in community-dwelling older adults: A randomized controlled trial. Journals of Gerontology Series A: Biomedical Sciences and Medical Sciences, 68(7), 845852. doi:10.1093/gerona/gls222

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Konopka, J.A., Hsue, L., Chang, W., Thio, T., & Dragoo, J.L. (2019). The effect of oral contraceptive hormones on anterior cruciate ligament strength. The American Journal of Sports Medicine, 48(1), 8592. PubMed ID: 31765227 doi:10.1177/0363546519887167

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kubo, K., Miyamoto, M., Tanaka, S., Maki, A., Tsunoda, N., & Kanehisa, H. (2009). Muscle and tendon properties during menstrual cycle. International Journal of Sports Medicine, 30(2), 139143. doi:10.1055/s-0028-1104573

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lambers, K., Ootes, D., & Ring, D. (2012). Incidence of patients with lower extremity injuries presenting to US emergency departments by anatomic region, disease category, and age. Clinical Orthopaedics and Related Research®, 470(1), 284290. doi:10.1007/s11999-011-1982-z

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Laver, L., Luig, P., Achenbach, L., Myklebust, G., & Karlsson, J. (2018). Handball injuries: Epidemiology and injury characterization: Part 1. In Handball sports medicine (pp. 141153). Springer.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Legerlotz, K., Bey, M.E., Götz, S., & Böhlke, N. (2018). Constant performance in balance and proprioception tests across the menstrual cycle—A pilot study in well trained female ice hockey players on hormonal contraception. Health Science Reports, 1(1), e18. PubMed ID: 30623036 doi:10.1002/hsr2.18

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Malinzak, R.A., Colby, S.M., Kirkendall, D.T., Yu, B., & Garrett, W.E. (2001). A comparison of knee joint motion patterns between men and women in selected athletic tasks. Clinical Biomechanics, 16(5), 438445. PubMed ID: 11390052 doi:10.1016/S0268-0033(01)00019-5

    • Crossref
    • Search Google Scholar
    • Export Citation
  • McGuine, T.A., Post, E.G., Hetzel, S.J., Brooks, M.A., Trigsted, S., & Bell, D.R. (2017). A prospective study on the effect of sport specialization on lower extremity injury rates in high school athletes. The American Journal of Sports Medicine, 45(12), 27062712. PubMed ID: 28735552 doi:10.1177/0363546517710213

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Montgomery, M.M., & Shultz, S.J. (2010). Isometric knee-extension and knee-flexion torque production during early follicular and postovulatory phases in recreationally active women. Journal of Athletic Training, 45(6), 586593. PubMed ID: 21062182 doi:10.4085/1062-6050-45.6.586

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Muaidi, Q.I. (2017). Does gender make a difference in knee rotation proprioception and range of motion in healthy subjects? Journal of Back and Musculoskeletal Rehabilitation, 30(6), 12371243. PubMed ID: 28800303 doi:10.3233/BMR-169613

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Murphy, D.F., Connolly, D.A.J., & Beynnon, B.D. (2003). Risk factors for lower extremity injury: A review of the literature. British Journal of Sports Medicine, 37(1), 13. PubMed ID: 12547739 doi:10.1136/bjsm.37.1.13

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nagai, T., Sell, T.C., Abt, J.P., & Lephart, S.M. (2012). Reliability, precision, and gender differences in knee internal/external rotation proprioception measurements. Physical Therapy in Sport, 13(4), 233237. PubMed ID: 23068898 doi:10.1016/j.ptsp.2011.11.004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nelson, M.E., Fiatarone, M.A., Morganti, C.M., Trice, I., Greenberg, R.A., & Evans, W.J. (1994). Effects of high-intensity strength training on multiple risk factors for osteoporotic fractures: A randomized controlled trial. JAMA, 272(24), 19091914. PubMed ID: 7990242 doi:10.1001/jama.1994.03520240037038

    • Crossref
    • Search Google Scholar
    • Export Citation
  • O’ Connor, P.J., Poudevigne, M.S., & Pasley, J.D. (2002). Perceived exertion responses to novel elbow flexor eccentric action in women and men. Medicine & Science in Sports & Exercise, 34(5), 862868. PubMed ID: 11984307

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Okamoto, T., Kobayashi, R., & Sakamaki-Sunaga, M. (2017). Effect of resistance exercise on arterial stiffness during the follicular and luteal phases of the menstrual cycle. International Journal of Sports Medicine, 38(5), 347352. doi:10.1055/s-0043-101377

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Östenberg, A., Roos, E., Ekdah, C., & Roos, H. (1998). Isokinetic knee extensor strength and functional performance in healthy female soccer players. Scandinavian Journal of Medicine & Science in Sports, 8(5), 257264. doi:10.1111/j.1600-0838.1998.tb00480.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Pincivero, D.M., Coelho, A.J., & Campy, R.M. (2003). Perceived exertion and maximal quadriceps femoris muscle strength during dynamic knee extension exercise in young adult males and females. European Journal of Applied Physiology, 89(2), 150156. PubMed ID: 12665978 doi:10.1007/s00421-002-0768-0

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Pincivero, D.M., Coelho, A.J., Campy, R.M., Salfetnikov, Y., & Bright, A. (2001). The effects of voluntary contraction intensity and gender on perceived exertion during isokinetic quadriceps exercise. European Journal of Applied Physiology, 84(3), 221226. PubMed ID: 11320639 doi:10.1007/s004210170008

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Pincivero, D.M., Coelho, A., & Erikson, W. (2000). Perceived exertion during isometric quadriceps contraction: A comparison between men and women. Journal of Sports Medicine and Physical Fitness, 40(4), 319. PubMed ID: 11297002

    • Search Google Scholar
    • Export Citation
  • Ravara, B., Gobbo, V., Incendi, D., Porzionato, A., Macchi, V., De Caro, R., Patruno, M. (2018). Revisiting the peculiar regional distribution of muscle fiber types in rat Sternomastoid Muscle. European Journal of Translational Myology, 28(1), 7302. PubMed ID: 29686819 doi:10.4081/ejtm.2018.7302

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Reed, B.G., & Carr, B.R. (2018). The normal menstrual cycle and the control of ovulation. In Endotext [Internet]South Dartmouth, MA: MDText. com, Inc.

    • Search Google Scholar
    • Export Citation
  • Rogers, L.M., & Dhaher, Y.Y. (2017). Female sex hormones modulate the response to low-frequency rTMS in the human motor cortex. Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation, 10(4), 850852. doi:10.1016/j.brs.2017.02.010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Romani, W., Patrie, J., Curl, L.A., & Flaws, J.A. (2003). The correlations between estradiol, estrone, estriol, progesterone, and sex hormone-binding globulin and anterior cruciate ligament stiffness in healthy, active females. Journal of Women’s Health (Larchmt), 12(3), 287298. doi:10.1089/154099903321667627

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ros, A.G., Holm, S.E., Fridén, C., & Annette, I.-L.H. (2013). Responsiveness of the one-leg hop test and the square hop test to fatiguing intermittent aerobic work and subsequent recovery. The Journal of Strength & Conditioning Research, 27(4), 988994. PubMed ID: 22706574 doi:10.1519/JSC.0b013e31825feb5b

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rozzi, S.L., Lephart, S.M., Gear, W.S., & Fu, F.H. (1999). Knee joint laxity and neuromuscular characteristics of male and female soccer and basketball players. The American Journal of Sports Medicine, 27(3), 312319. PubMed ID: 10352766 doi:10.1177/03635465990270030801

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ruedl, G., Ploner, P., Linortner, I., Schranz, A., Fink, C., Sommersacher, R., Burtscher, M. (2009). Are oral contraceptive use and menstrual cycle phase related to anterior cruciate ligament injury risk in female recreational skiers? Knee Surgery, Sports Traumatology, Arthroscopy, 17(9), 10651069. PubMed ID: 19333573 doi:10.1007/s00167-009-0786-0

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Salem, H.S., Varzhapetyan, V., Patel, N., Dodson, C.C., Tjoumakaris, F.P., & Freedman, K.B. (2019). Anterior cruciate ligament reconstruction in young female athletes: Patellar versus hamstring tendon autografts. The American Journal of Sports Medicine, 47(9), 20862092. PubMed ID: 31233335 doi:10.1177/0363546519854762

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sugimoto, D., Myer, G.D., Barber Foss, K.D., Pepin, M.J., Micheli, L.J., & Hewett, T.E. (2016). Critical components of neuromuscular training to reduce ACL injury risk in female athletes: Meta-regression analysis. British Journal of Sports Medicine, 50(20), 12591266. PubMed ID: 27251898 doi:10.1136/bjsports-2015-095596

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sung, E., Han, A., Hinrichs, T., Vorgerd, M., Manchado, C., & Platen, P. (2014). Effects of follicular versus luteal phase-based strength training in young women. Springerplus, 3(1), 668. doi:10.1186/2193-1801-3-668

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tenan, M.S., Hackney, A.C., & Griffin, L. (2016). Maximal force and tremor changes across the menstrual cycle. European Journal of Applied Physiology, 116(1), 153160. PubMed ID: 26365403 doi:10.1007/s00421-015-3258-x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Warden, S.J., Saxon, L.K., Castillo, A.B., & Turner, C.H. (2006). Knee ligament mechanical properties are not influenced by estrogen or its receptors. American Journal of Physiology—Endocrinol and Metabolism, 290(5), E1034E1040. doi:10.1152/ajpendo.00367.2005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wojtys, E.M., Huston, L.J., Boynton, M.D., Spindler, K.P., & Lindenfeld, T.N. (2002). The effect of the menstrual cycle on anterior cruciate ligament injuries in women as determined by hormone levels. The American Journal of Sports Medicine, 30(2), 182188. PubMed ID: 11912085 doi:10.1177/03635465020300020601

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Xu, D., Hong, Y., Li, J., & Chan, K. (2004). Effect of tai chi exercise on proprioception of ankle and knee joints in old people. British Journal of Sports Medicine, 38(1), 5054. PubMed ID: 14751946 doi:10.1136/bjsm.2002.003335

    • Crossref
    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 458 458 150
Full Text Views 15 15 2
PDF Downloads 9 9 2