Gender differences in active musculoskeletal stiffness. Part I.: Quantification in controlled measurements of knee joint dynamics

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Abstract

Active females demonstrate increased risk for musculoskeletal injuries relative to equivalently-trained males. Although gender differences in factors such as passive laxity, skeletal geometry and kinematics have been examined, the effect of gender on active muscle stiffness has not been reported. Stiffness of the active quadriceps and hamstrings musculature were recorded during isometric knee flexion and extension exertions from twelve male and eleven female subjects. A second-order biomechanical model of joint dynamics was used to quantify stiffness from the transient motion response to an angular perturbation of the lower-leg. Female subjects demonstrated reduced active stiffness relative to male subjects at all torque levels, with levels 56–73% of the males. Effective stiffness increased linearly with the torque load, with stiffness increasing at a rate of 3.3 Nm/rad per unit of knee moment in knee flexion exertions (hamstrings) and 6.6 Nm/rad per unit of knee moment extension exertions (quadriceps). To account for gender differences in applied moment associated with leg mass, regressions analyses were completed that demonstrated a gender difference in the slope of stiffness-versus-knee moment relation. Further research is necessary to identify the cause of the observed biomechanical difference and implications for controlling injury.

Introduction

Females have an increased risk of musculoskeletal injuries relative to equivalently trained males. Regional studies illustrate that female high school basketball players suffer 3.8 times the risk of injury than male counterparts [1]. Female collegiate soccer and basketball players demonstrate more than twice the risk of ACL and cartilage injury of the knee compared to their male counterparts [2], [3]. This gender bias has yet to be explained.

Potential contributing factors to the gender bias in musculoskeletal injury rate include differences in mechanical properties of the ligaments, joint kinematics, and skeletal alignment [4], [5], [6], [7]. These factors all represent passive characteristics of the joint. Passive resistance to anterior tibial distraction at the knee is correlated with the risk of musculoskeletal injury [8], [9] and is reduced in females compared to equivalently-trained males [10]. However, during functional activities joint loads go well beyond the capacity of the passive elements and require assistance from active muscles to stabilize the joint. Hence, muscles serve as the primary active stabilizers of the knee during functional loading conditions, protecting against injury [11], [12], [13].

A potential factor that has been overlooked is the gender difference in joint stability from active muscle stiffness. Stiffness of active muscle is proportional to the myoelectric activation and force generated by the muscle [14], [15], [16]. Similarly, the rotational stiffness of a joint is linearly proportional to the active joint moment and muscle recruitment [17], [18], [19]. This active joint stiffness can be voluntarily controlled through muscle recruitment [20], [21], [22]. Stability of the knee requires active muscle stiffness [23], [24]. Specifically, the hamstring muscles can restrain anterior translation of the knee joint thereby reducing the biomechanical risk of strain injury [25], [26]. When the two components of knee joint stiffness are compared, i.e. stiffness from active muscle recruitment and stiffness from passive joint structures, the active muscles are the dominant component in total joint stiffness during functional conditions [11], [27] Wojtys [28], [29] applied a distraction force to the knee and demonstrated that active muscle co-contraction successfully reduced the resulting anterior tibial distraction by 473% in men compared to 217% in women. The influence of muscle activation on this force-versus-displacement ratio suggests potential gender differences in the muscle stiffness of the recruited muscles. Recognizing the importance of muscle stiffness on joint stability [23], gender differences in active muscle stiffness may contribute to the gender bias in injury risk. Unfortunately, there are no reported measures examining gender differences in active muscle stiffness.

We hypothesized that active stiffness characteristics of the knee are reduced in females. Active muscle stiffness is also proportional to the myoelectric activation and force generated by the muscle [15]. Thus, we expected that in-vivo active muscle stiffness must increase with knee moment. Recognizing that active joint stiffness is proportional to the applied moment, the slope of the stiffness-versus-moment relation is an important factor in stability [30]. This slope will be referred to as the stiffness gradient. In addition to quantifying gender differences in stiffness we also investigated whether the stiffness gradient differs between men and women. This effort represents part of an ongoing investigation to quantify potential gender differences in musculoskeletal stability.

Section snippets

Materials and methods

Twelve male and eleven female volunteers with no known knee abnormalities or recent musculoskeletal injuries participated in this study. Informed consent approved by the Human Investigations Committee of the university was obtained from all subjects. Subjects ranged in age from 21 to 33 years with no significant age difference between genders (Table 1).

The experimental protocol included measurement of inertial properties of the leg and measurement of effective joint stiffness from perturbation

Results

Subjects exhibited significant gender differences in height, tibial lengths and lower leg inertia but demonstrated no significant difference in age or weight (Table 1, Table 2). The second-order model of leg motion response explained 78±6% of the data variability in the accelerometer data with RMS error less than 4.6±0.8 % of the baseline acceleration of gravity. Thus, the model appeared to be a reasonable representation of the biomechanical performance and the computed parameters of damping

Discussion

Active muscle stiffness contributes to musculoskeletal behavior and is essential for the maintenance of joint stability [38], [39]. Muscles serve as the primary active stabilizers during functional loading conditions, protecting against musculoskeletal injury [11], [13], [27]. Although research has demonstrated gender differences in passive joint stiffness [10] it was necessary to establish the influence of gender on active muscle stiffness.

Results confirm that effective stiffness was affected

Conclusion

Gender differences exist in active joint stiffness. The mechanism to explain that difference remains unknown. Active muscles serve as the primary stabilizers of the knee during functional loading conditions and protect against musculoskeletal injury. Reduced effective stiffness may contribute to the gender bias in risk of musculoskeletal instability. Fortunately, neuromotor recruitment of agonist and antagonist activity can be used to modify effective joint stiffness during locomotor function

Acknowledgements

This research was supported in part by a grant R01 AR46111-02 from NIAMS of the National Institutes of Health. The authors thank A. Massimini for her assistance in these analyses. Preliminary results have been presented in part the year 2000 annual conference for the Gait and Clinical Movement Analysis Society and the 2000 American Society of Biomechanics conference [59], [60].

Kevin Granata received a MS in physics from Purdue University and a Ph.D. in biomechanics from The Ohio State University. He serves as the Research and Engineering Director of the Motion Analysis and Motor Performance Laboratory at the University of Virginia where he is an Assistant Professor in the departments of Orthopaedic Surgery and Biomedical Engineering. His research focuses on neuromotor control and modeling of movement with specific interests in musculoskeletal stability and associated

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    Kevin Granata received a MS in physics from Purdue University and a Ph.D. in biomechanics from The Ohio State University. He serves as the Research and Engineering Director of the Motion Analysis and Motor Performance Laboratory at the University of Virginia where he is an Assistant Professor in the departments of Orthopaedic Surgery and Biomedical Engineering. His research focuses on neuromotor control and modeling of movement with specific interests in musculoskeletal stability and associated injury mechanisms.

    Sara Wilson received a M.S. and Ph.D. in mechanical engineering and medical engineering respectively from the Massachusetts Institute of Technology. She joined the Motion Analysis and Motor Performance Laboratory at the University of Virginia to study muscle mechanics and spinal kinematics associated with dynamics of low-back stability and clinical evaluation. She s currently an Assistant Professor with the Department of Mechanical Engineering at the University of Kansas.

    Darin Padua received an M.S. in athletic training from the University of North Carolina and Ph.D. sports medicine and biomechanics with the Motion Analysis and Motor Performance Laboratory at the University of Virginia. His re arch interests focus on gender factors influencing muscular recruitment of functional performance and musculoskeletal injury risk. He is currently an Assistant Professor with the Department of Exercise and Sport Science at the University of North Carolina.

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