Characterization of passive elastic properties of the human medial gastrocnemius muscle belly using supersonic shear imaging
Introduction
There is substantial evidence in the literature that the assessment of muscle mechanical properties allows a better understanding of muscle function and of the mechanisms responsible for muscle adaptations following acute or chronic interventions (e.g., Goubel and Lensel-Corbeil, 2003, Caiozzo, 2002). The passive mechanical properties are an important component of muscle function because they are related to the muscle extensibility (Gajdosik, 2001). In human experiments, passive torque–angle curves are classically characterized (e.g., Gajdosik, 2001, McNair et al., 2002, Magnusson et al., 1998, Nordez et al., 2008, Nordez et al., 2009). However, several synergistic muscles, tissues (e.g., aponeurosis, tendon), and articular structures (Riemann et al., 2001) contribute to the passive torque. Thus, assessment of individual muscle mechanical properties in vivo remains challenging.
In that framework, Hoang et al. (2005) recently proposed an elegant method to estimate the passive force–length relationship of the human gastrocnemius muscle–tendon units (GMTU). This method consists of measuring passive ankle torques at a range of knee angles. Based on the reasonable assumption that the GMTU constitute the only structure that crosses both ankle and knee joints that it produces a significant passive torque during the ankle motion, an optimization is used to identify parameters of the force-length curve from the torque–angle data (Hoang et al., 2005, Nordez et al., 2010). However, this method is valid for multi-joint muscles and necessitates passive experiments at various different knee angles, which may limit its use in clinical practice and its applicability for other muscles.
In addition, this method has led to contradictory results, where the GMTU were slack over about one-quarter of its physiological range (Hoang et al., 2007), while other studies showed that they are slack over more than half of this range (Riener and Edrich, 1999, Muraoka et al., 2004, Muraoka et al., 2005). Therefore, the estimation of muscle slack length, which usually corresponds to the length beyond which the muscle begins to develop passive elastic force, remains a topic of continued interest for researchers. Thus, an alternative method of evaluating passive muscle mechanical properties would provide fundamental information on muscle behavior in vivo.
Elastographic methods were recently used to quantify in vivo muscle mechanical properties by measuring the propagation velocity of shear waves by imaging techniques. Using transient elastography, recent experiments showed that the shear elastic modulus of gastrocnemius muscle is partly related to ankle torque during a passive stretching (0.69<R²<0.93), but with low reliability (Nordez et al., 2008). This lack of reliability could be explained by some limitations of transient elastography (Nordez et al., 2008), which seem to be overcome with the supersonic shear imaging (SSI) technique (Bercoff et al., 2004, Gennisson et al., 2010). For instance, using SSI, Nordez and Hug (2010) reported a reliable linear relationship between the biceps brachii shear elastic modulus and its electromyographic (EMG) activity level during incremental isometric contractions. Thus, it seems that SSI may be a valuable tool for measuring the muscle shear elastic modulus during passive stretching. Muscle–tendon structures are characterized by a non-linear stress–strain relationship. Thus, Young modulus (its first derivative) increases with lengthening. Since muscle elastic modulii are increased when the tension or the stretching levels are increased (e.g., Fung, 1993, Nordez et al., 2008), it can be hypothesized that the shear elastic modulus measured using SSI could provide an indirect estimation of passive muscle tension.
Therefore, the present study was designed to assess the relationship between muscle shear elastic modulus measured using SSI and muscle length of the gastrocnemius muscle–tendon units. This relationship was used to provide an estimation of muscle slack length and stiffness and compared to the force–length relationship obtained using the Hoang model (Hoang et al., 2005). In addition, the reliability of one simple measure of likely clinical relevance was calculated with the knee fully extended.
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Subjects
Seven sedentary healthy men (age: 27±6 yr; height: 177±6 cm; weight: 74±10 kg) volunteered to participate in this study. They were given detailed information about the purpose and methods used in the present experimentation, and gave written consent. This study was conducted according to the Helsinki Statement, and has been approved by the local ethics committee.
Passive torque–angle relationships
An isokinetic dynamometer (Biodex 3 medical, Shirley, NY, USA) was used to measure ankle angle, joint angular velocity, and torque
Muscle shear elastic modulus–length relationship during passive stretches
The shear elastic modulus–length relationship obtained at the knee fully extended (R²=0.996±0.005, ranged from 0.980 to 1.000, Fig. 3), or for all knee joint angles (R²=0.977±0.019, ranged from 0.944 to 0.995) was very well fitted by the exponential model.
Parameters of the normalized shear elastic modulus–length relationship at 0° of knee flexion (α=136.7±18.1 m−1 and l0=0.443±0.021 m) were not significantly different to those obtained at all knee joint configurations (α=139.2±16.4 m−1 and l0=
Discussion
First, the present study shows that, in comparison to the previous transient elastographic technique (Nordez et al., 2008), the Supersonic Shear Imaging method enables researchers and clinicians to greatly improve the reliability of muscle shear elastic modulus measurement during passive stretching of the plantar flexors (Fig. 2). Indeed, the repeatability of both α and l0 was improved in the present study (CV<7.5%), compared to the results previously reported (CV=60%; Nordez et al., 2008). In
Conflict of interest statement
All authors disclose any financial and personal relationships with other people or organizations that could inappropriately influence this work.
Acknowledgments
This work was supported by the Association Française contre les Myopathies (AFM-contract no. 14597), the Région des Pays de la Loire (contract no. 2010_11120) and the Fond Européen de Développement Régional (FEDER). Lilian Lacourpaille and Alexandre Fouré are thanks for their help during the experiments and helpful discussions.
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