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Pivoting neuromuscular control and proprioception in females and males

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European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Purpose

Noncontact ACL injuries occur most commonly in pivoting sports and are much more frequent in females than in males. However, information on sex differences in proprioceptive acuity under weight-bearing and leg neuromuscular control in pivoting is scarce. The objective of this study was to investigate sex differences in pivoting neuromuscular control during strenuous stepping tasks and proprioceptive acuity under weight-bearing.

Methods

21 male and 22 female subjects were recruited to evaluate pivoting proprioceptive acuity under weight-bearing, and pivoting neuromuscular control (in terms of leg pivoting instability, stiffness, maximum internal and external pivoting angles, and entropy of time-to-peak EMG in lower limb muscles) during strenuous stepping tasks performed on a novel offaxis elliptical trainer.

Results

Compared to males, females had significantly lower proprioceptive acuity under weight-bearing in both internal and external pivoting directions, higher pivoting instability, larger maximum internal pivoting angle, lower leg pivoting stiffness, and higher entropy of time-to-peak EMG in the gastrocnemius muscles during strenuous stepping tasks with internal and external pivoting perturbations.

Conclusions

Results of this study may help us better understand factors contributing to ACL injuries in females and males, develop training strategies to improve pivoting neuromuscular control and proprioceptive acuity, and potentially reduce ACL and lower-limb musculoskeletal injuries.

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Abbreviations

ACL:

Anterior cruciate ligament

BF:

Biceps femoris

EMG:

Electromyography

EP:

External pivoting

ET:

Elliptical trainer

FPT:

Free pivoting task

FRF:

Frequency response function

Glmax:

Gluteus maximus

Glmed:

Gluteus medius

IP:

Internal pivoting

LG:

Lateral gastrocnemius

MEPT:

Motor external perturbation task

MG:

Medial gastrocnemius

MIPT:

Motor internal perturbation task

Q angle:

Quadriceps angle

RST:

Regular stepping task

SD:

Standard deviation

ST:

Semitendinosus

VL:

Vastus lateralis

VMO:

Vastus medialis oblique

References

  • Aglietti P, Insall JN, Cerulli G (1983) Patellar pain and incongruence. I: measurements of incongruence. Clin Orthop Relat Res 176:217–224

    PubMed  Google Scholar 

  • Bendat JS, Piersol AG (2010) Random data: analysis and measurement procedures, 4th edn. Wiley, Hoboken

    Book  Google Scholar 

  • Beynnon BD, Johnson RJ, Abate JA, Fleming BC, Nichols CE (2005) Treatment of anterior cruciate ligament injuries, part I. Am J Sports Med 33(10):1579–1602

    Article  PubMed  Google Scholar 

  • Blickhan R (1989) The spring-mass model for running and hopping. J Biomech 22(11–12):1217–1227

    Article  CAS  PubMed  Google Scholar 

  • Boden BP, Dean GS, Feagin JA Jr, Garrett WE Jr (2000) Mechanisms of anterior cruciate ligament injury. Orthopedics 23(6):573–578

    CAS  PubMed  Google Scholar 

  • Burnfield JM, Shu Y, Buster T, Taylor A (2010) Similarity of joint kinematics and muscle demands between elliptical training and walking: implications for practice. Phys Ther 90(2):289–305

    Article  PubMed  Google Scholar 

  • Cavanaugh JT, Guskiewicz KM, Stergiou N (2005) A nonlinear dynamic approach for evaluating postural control: new directions for the management of sport-related cerebral concussion. Sports Med 35(11):935–950

    Article  PubMed  Google Scholar 

  • Chaitow L, DeLany JW (2000) The pelvis, vol 2. Clinical application of neuromuscular techniques: the lower body. Churchill Livingstone, New York

    Google Scholar 

  • Chang PH, Kang SH (2010) Stochastic estimation of human arm impedance under nonlinear friction in robot joints: a model study. J Neurosci Methods 189(1):97–112

    Article  PubMed  Google Scholar 

  • Chang AH, Lee SJ, Zhao H, Ren Y, Zhang LQ (2014) Impaired varus–valgus proprioception and neuromuscular stabilization in medial knee osteoarthritis. J Biomech 47(2):360–366

    Article  PubMed Central  PubMed  Google Scholar 

  • Clark FJ, Burgess RC, Chapin JW, Lipscomb WT (1985) Role of intramuscular receptors in the awareness of limb position. J Neurophysiol 54(6):1529–1540

    CAS  PubMed  Google Scholar 

  • Coplan JA (1989) Rotational motion of the knee: a comparison of normal and pronating subjects. J Orthop Sports Phys Ther 10(9):366–369

    Article  CAS  PubMed  Google Scholar 

  • Cug M, Ak E, Ozdemir RA, Korkusuz F, Behm DG (2012) The effect of instability training on knee joint proprioception and core strength. J Sport Sci Med 11(3):468–474

    Google Scholar 

  • Delp SL, Hess WE, Hungerford DS, Jones LC (1999) Variation of rotation moment arms with hip flexion. J Biomech 32(5):493–501

    Article  CAS  PubMed  Google Scholar 

  • Demirbüken I, Yurdalan SU, Savelberg H, Meijer K (2009) Gender specific strategies in demanding hopping conditions. J Sports Sci Med 8:265–270

    PubMed Central  PubMed  Google Scholar 

  • Eils E, Schroter R, Schroder M, Gerss J, Rosenbaum D (2010) Multistation proprioceptive exercise program prevents ankle injuries in basketball. Med Sci Sport Exer 42(11):2098–2105

    Article  Google Scholar 

  • Farley CT, Houdijk HH, Van Strien C, Louie M (1998) Mechanism of leg stiffness adjustment for hopping on surfaces of different stiffnesses. J Appl Physiol 85(3):1044–1055

    CAS  PubMed  Google Scholar 

  • Fleming BC, Renstrom PA, Ohlen G, Johnson RJ, Peura GD, Beynnon BD, Badger GJ (2001) The gastrocnemius muscle is an antagonist of the anterior cruciate ligament. J Orthop Res 19(6):1178–1184

    Article  CAS  PubMed  Google Scholar 

  • Granata KP, Padua DA, Wilson SE (2002a) Gender differences in active musculoskeletal stiffness. Part II. Quantification of leg stiffness during functional hopping tasks. J Electromyogr Kinesiol 12(2):127–135

    Article  CAS  PubMed  Google Scholar 

  • Granata KP, Wilson SE, Padua DA (2002b) Gender differences in active musculoskeletal stiffness. Part I. Quantification in controlled measurements of knee joint dynamics. J Electromyogr Kinesiol 12(2):119–126

    Article  PubMed  Google Scholar 

  • Griffin LY, Agel J, Albohm MJ, Arendt EA, Dick RW, Garrett WE, Garrick JG, Hewett TE, Huston L, Ireland ML, Johnson RJ, Kibler WB, Lephart S, Lewis JL, Lindenfeld TN, Mandelbaum BR, Marchak P, Teitz CC, Wojtys EM (2000) Noncontact anterior cruciate ligament injuries: risk factors and prevention strategies. J Am Acad Orthop Surg 8(3):141–150

    CAS  PubMed  Google Scholar 

  • Herrington L (2005) Knee-joint position sense: the relationship between open and closed kinetic chain tests. J Sport Rehabil 14:356–362

    Google Scholar 

  • Hewett TE, Paterno MV, Myer GD (2002) Strategies for enhancing proprioception and neuromuscular control of the knee. Clin Orthop Relat Res 402:76–94

    Article  PubMed  Google Scholar 

  • Hewett TE, Shultz SJ, Griffin LY, American Orthopaedic Society for Sports Medicine (2007) Understanding and preventing noncontact ACL injuries. Human Kinetics, Champaign

    Google Scholar 

  • Hootman JM, Dick R, Agel J (2007) Epidemiology of collegiate injuries for 15 sports: summary and recommendations for injury prevention initiatives. J Athl Train 42(2):311–319

    PubMed Central  PubMed  Google Scholar 

  • Horak FB (2006) Postural orientation and equilibrium: what do we need to know about neural control of balance to prevent falls? Age Ageing 35(Suppl 2):ii7–ii11

    PubMed  Google Scholar 

  • Horton MG, Hall TL (1989) Quadriceps femoris muscle angle: normal values and relationships with gender and selected skeletal measures. Phys Ther 69(11):897–901

    CAS  PubMed  Google Scholar 

  • Jarque CM, Bera AK (1987) A test for normality of observations and regression residuals. Int Stat Rev 55:163–172

    Article  Google Scholar 

  • Kearney RE, Hunter IW (1990) System identification of human joint dynamics. Crit Rev Biomed Eng 18(1):55–87

    CAS  PubMed  Google Scholar 

  • Kobayashi H, Kanamura T, Koshida S, Miyashita K, Okado T, Shimizu T, Yokoe K (2010) Mechanisms of the anterior cruciate ligament injury in sports activities: a twenty-year clinical research of 1,700 athletes. J Sports Sci Med 9(4):669–675

    PubMed Central  PubMed  Google Scholar 

  • Kurz MJ, Stergiou N (2003) The aging human neuromuscular system expresses less certainty for selecting joint kinematics during gait. Neurosci Lett 348(3):155–158

    Article  CAS  PubMed  Google Scholar 

  • Landry SC, McKean KA, Hubley-Kozey CL, Stanish WD, Deluzio KJ (2007) Neuromuscular and lower limb biomechanical differences exist between male and female elite adolescent soccer players during an unanticipated side-cut maneuver. Am J Sports Med 35(11):1888–1900

    Article  PubMed  Google Scholar 

  • Lee SJ, Hidler J (2008) Biomechanics of overground vs treadmill walking in healthy individuals. J Appl Physiol 104(3):747–755

    Article  PubMed  Google Scholar 

  • Lee SJ, Ren Y, Geiger F, Chang AH, Press JM, Zhang L-Q (2011) Offaxis neuromuscular training of knee injuries using an offaxis robotic elliptical trainer. In: Proceedings of the 33rd annual international conference of the IEEE engineering in medicine and biology society, Aug 31-September 4, Boston

  • Lee SJ, Ren Y, Geiger F, Zhang LQ (2013) Gender differences in offaxis neuromuscular control during stepping under a slippery condition. Eur J Appl Physiol 113(11):2857–2866

    Article  PubMed  Google Scholar 

  • Lee SJ, Ren Y, Chang AH, Geiger F, Zhang LQ (2014) Effects of pivoting neuromuscular training on pivoting control and proprioception. Med Sci Sports Exerc 46(7):1400–1409

    Article  PubMed  Google Scholar 

  • Lephart SM, Pincivero DM, Rozzi SL (1998) Proprioception of the ankle and knee. Sports Med 25(3):149–155

    Article  CAS  PubMed  Google Scholar 

  • Loudon JK, Jenkins W, Loudon KL (1996) The relationship between static posture and ACL injury in female athletes. J Orthop Sports Phys Ther 24(2):91–97

    Article  CAS  PubMed  Google Scholar 

  • McMahon TA, Valiant G, Frederick EC (1987) Groucho running. J Appl Physiol 62(6):2326–2337

    CAS  PubMed  Google Scholar 

  • Micheo W, Hernandez L, Seda C (2010) Evaluation, management, rehabilitation, and prevention of anterior cruciate ligament injury: current concepts. PMR 2(10):935–944

    Article  Google Scholar 

  • Nagai T, Sell TC, Abt JP, Lephart SM (2012) Reliability, precision, and gender differences in knee internal/external rotation proprioception measurements. Phys Ther Sport 13(4):233–237

    Article  PubMed  Google Scholar 

  • O’Connor JJ (1993) Can muscle co-contraction protect knee ligaments after injury or repair? J Bone Jt Surg Br 75(1):41–48

    Google Scholar 

  • Olsen OE, Myklebust G, Engebretsen L, Bahr R (2004) Injury mechanisms for anterior cruciate ligament injuries in team handball: a systematic video analysis. Am J Sports Med 32(4):1002–1012

    Article  PubMed  Google Scholar 

  • Pai YC, Rymer WZ, Chang RW, Sharma L (1997) Effect of age and osteoarthritis on knee proprioception. Arthritis Rheum 40(12):2260–2265

    Article  CAS  PubMed  Google Scholar 

  • Park H-S, Wilson NA, Zhang L-Q (2008) Gender differences in passive knee biomechanical properties in tibial rotation. J Orthop Res 26(7):937–944

    Article  PubMed  Google Scholar 

  • Quatman CE, Hewett TE (2009) The anterior cruciate ligament injury controversy: is valgus collapse a sex-specific mechanism? Br J Sports Med 43(5):328–335

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Quatman CE, Quatman-Yates CC, Hewett TE (2010) A plane explanation of anterior cruciate ligament injury mechanisms: a systematic review. Sports Med 40(9):729–746

    Article  PubMed  Google Scholar 

  • Ren Y, Lee SJ, Park HS, Zhang LQ (2013) A pivoting elliptical training system for improving pivoting neuromuscular control and rehabilitating musculoskeletal injuries. IEEE Trans Neural Syst Rehabil Eng 21(5):860–868

    Article  PubMed  Google Scholar 

  • Riemann BL, Lephart SM (2002) The sensorimotor system, part II: the role of proprioception in motor control and functional joint stability. J Athl Train 37(1):80–84

    PubMed Central  PubMed  Google Scholar 

  • Roos EM, Herzog W, Block JA, Bennell KL (2011) Muscle weakness, afferent sensory dysfunction and exercise in knee osteoarthritis. Nat Rev Rheumatol 7(1):57–63

    Article  PubMed  Google Scholar 

  • Rozzi SL, Lephart SM, Gear WS, Fu FH (1999) Knee joint laxity and neuromuscular characteristics of male and female soccer and basketball players. Am J Sports Med 27(3):312–319

    CAS  PubMed  Google Scholar 

  • Shultz SJ, Pye ML, Montgomery MM, Schmitz RJ (2012) Associations between lower extremity muscle mass and multiplanar knee laxity and stiffness: a potential explanation for sex differences in frontal and transverse plane knee laxity. Am J Sports Med 40(12):2836–2844

    Article  PubMed  Google Scholar 

  • Wojtys EM, Huston LJ, Schock HJ, Boylan JP, Ashton-Miller JA (2003) Gender differences in muscular protection of the knee in torsion in size-matched athletes. J Bone Joint Surg Am 85-A(5):782–789

    PubMed  Google Scholar 

  • Zazulak BT, Hewett TE, Reeves NP, Goldberg B, Cholewicki J (2007a) Deficits in neuromuscular control of the trunk predict knee injury risk: a prospective biomechanical-epidemiologic study. Am J Sports Med 35(7):1123–1130

    Article  PubMed  Google Scholar 

  • Zazulak BT, Hewett TE, Reeves NP, Goldberg B, Cholewicki J (2007b) The effects of core proprioception on knee injury: a prospective biomechanical-epidemiological study. Am J Sports Med 35(3):368–373

    Article  PubMed  Google Scholar 

  • Zhang L-Q, Wang G (2001) Dynamic and static control of the human knee joint in abduction-adduction. J Biomech 34(9):1107–1115

    Article  CAS  PubMed  Google Scholar 

  • Zhang L-Q, Nuber GW, Butler JP, Bowen MK, Rymer WZ (1998) In vivo human knee joint dynamic properties as functions of muscle contraction and joint position. J Biomech 31(1):71–76

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors acknowledge the grant support of the National Institutes of Health, National Science Foundation, and National Institute on Disability and Rehabilitation Research.

Conflict of interest

Li-Qun Zhang and Yupeng Ren hold equity positions in Rehabtek LLC, which received National Science Foundation funding in developing the multi-axis robotic elliptical trainer in this study.

Ethical standards

All participants gave their written informed consent to participate in the study that was approved by the Institute of Review Board at Northwestern University.

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Authors and Affiliations

  1. Sensory-Motor Performance Program, Rehabilitation Institute of Chicago, Suite 1406, 345 E. Superior Street, Chicago, IL, 60611, USA

    Song Joo Lee, Yupeng Ren, Sang Hoon Kang, François Geiger & Li-Qun Zhang

  2. Department of Biomedical Engineering, Northwestern University, Chicago, IL, 60611, USA

    Song Joo Lee & Li-Qun Zhang

  3. Department of Physical Medicine and Rehabilitation, Northwestern University, Chicago, IL, 60611, USA

    Song Joo Lee, Sang Hoon Kang & Li-Qun Zhang

  4. Department of Orthopaedic Surgery, Northwestern University, Chicago, IL, 60611, USA

    Li-Qun Zhang

Authors
  1. Song Joo Lee
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  2. Yupeng Ren
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  3. Sang Hoon Kang
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  4. François Geiger
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  5. Li-Qun Zhang
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Corresponding author

Correspondence to Li-Qun Zhang.

Additional information

Communicated by Dick F. Stegeman.

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Lee, S.J., Ren, Y., Kang, S.H. et al. Pivoting neuromuscular control and proprioception in females and males. Eur J Appl Physiol 115, 775–784 (2015). https://doi.org/10.1007/s00421-014-3062-z

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  • DOI: https://doi.org/10.1007/s00421-014-3062-z

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