Physiological insights into medial gastrocnemius function during eccentric contraction in normal and in acute atrophy – Quantification of 2D strain rate indices from Velocity Encoded Phase Contrast MR Imaging.
Usha Sinha1, Vadim Malis2, Robert Csapo3, and Shantanu Sinha3

1Physics, San Diego State University, San Diego, CA, United States, 2Physics, University of California at San Diego, San Diego, CA, United States, 3Radiology, University of California at San Diego, San Diego, CA, United States

Synopsis

In-vivo studies of muscle function under different motion paradigms can elucidate the physiology of acute atrophy. This study maps the 2D strain rate tensor in subjects performing eccentric contractions before and after Unilateral Limb Suspension induced acute atrophy. As expected, strain rate values are smaller during eccentric compared to isometric contractions, since in the eccentric mode, muscle contraction occurs under lengthening conditions resulting in a net smaller local elongation. Changes of SR indices with atrophy are negligible possibly due to a balance of force loss from atrophy and greater force generation from a potentially stiffer matrix.

Purpose

Eccentric contractions are of interest since many physiological functions occur when the muscle is actively lengthening. Further, eccentric contractions have been shown to be most effective for muscle strengthening.1 This study focuses on effect of atrophy, induced by unilateral limb suspension (ULLS), on muscle strain rate (SR) tensor indices during eccentric contractions of the Medial Gastrocnemius (MG) derived from velocity encoded phase contrast (VE-PC) images.

Methods

Acute atrophy was induced by the ULLS model2 (4 weeks of chronic unloading of the dominant leg using crutches and a raised shoe for the non-dominant leg) in six subjects with IRB approval. Dynamic imaging was performed pre- and post-ULLS during eccentric contractions at 60% Maximum Voluntary Contraction (MVC). A computer controlled foot pedal device rotated the foot during eccentric contraction, with visual feedback guidance enabling consistent force generation.3 The parameters of the gated, 3-directionally encoded VE-PC sequence were: 7-8 oblique-sagittal slices (1.7x1.7x5 mm) to cover the MG and 22 temporal phases. Muscle fascicles were manually contoured from water suppressed FSE images acquired in the same orientation and tracked through the dynamic cycle for fiber orientation. The 2D SR tensor (symmetric part of the spatial gradient of the velocity) of the MG was calculated from the VE-PC images to extract: (i) positive and negative eigenvalues, (ii) the out-of-plane component calculated as the negative of the (sum of the in-plane) eigenvalues, (iii) SR-muscle fiber angles corresponding to the angle between the eigenvector corresponding to the positive eigenvalue and the muscle fiber. Statistical analysis compared pre- to post-ULLS cohorts based on SR indices at the force value corresponding to the post-ULLS for each subject.

Results

The eigenvalues extracted at each voxel were sorted into negative and positive eigenvalue images (Figure 1). During isometric contraction, the local deformation is negative and thus the negative eigenvalue image extracted at peak contraction is denoted as strain rate along the muscle fiber. In eccentric contraction, the dynamic cycle starts with the foot in a plantarflexed position and pushed to the dorsiflexed position by the pedal while the foot is exerting a resisting force (phases 1-12 in Fig. 2) with the latter half of the cycle (12-24) being passive plantarflexion with the foot following the pedal. Since the net deformation is active lengthening in the first half of the cycle, the positive eigenvalue (local elongation) is denoted as the SR along the muscle fiber (Fig. 1). The average SR indices (positive, negative, sum eigenvalues and SR-muscle fiber angles) as a function of the dynamic cycle are shown in Figure 2. No significant changes were seen in any of the SR values between the pre- and post-ULLS subjects.

Discussion

Overall, SR values are much lower for eccentric contractions compared to our findings on isometric contractions for the same level of MVC. The lower values of SR arise from the fact the muscles are contracting while there is an active lengthening during dorsiflexion caused by external force from the foot pedal. The net result is a smaller extent of tissue deformation due to simultaneous local contraction and elongation. The net deformation is lengthening as the foot is pushed to the dorsiflexed position (Fig. 2, 2nd column). The local elongation of tissue is also confirmed by the low values of the SR-fiber angle where the SR eigenvector corresponds to the positive eigenvalue (SR-fiber angles: pre-ULLS: -200 and post-ULLS: -300; the negative sign indicates that the SR is rotated distally compared to the muscle fiber). Surprisingly, there are no significant differences in the SR indices between pre- and post-ULLS cohorts. This is in contrast to our findings on SR indices during isometric contractions which showed significant differences in SR-fiber angles and in fiber cross section SR. A potential explanation for minimal changes in SR with acute atrophy in eccentric contraction comes from our modeling studies simulating extracellular matrix (ECM) material stiffness. Modeling predicts that during eccentric contraction, the muscle tissue with stiffer ECM (as may occur in atrophy) generates more force, as the ECM is in strained state tending to enhance force generation (Figure 3). But atrophy induced reduction in specific muscle fiber force will reduce the force generation. The balance between loss of muscle force due to reduced specific force and increase in force due to increase in matrix ECM stiffness may account for minimal changes in SR in eccentric contractions between pre- and post-ULLS subjects.

Conclusion

Dynamic studies using eccentric contraction may provide physiological insights into acute atrophy reflecting changes in both contractile elements and ECM material properties.

Acknowledgements

This work was supported by the National Institute of Arthritis and Musculoskeletal and Skin Diseases Grant 5RO1-AR-053343-08.

References

1. Lieber RL, Fridén J. Mechanisms of muscle injury after eccentric contraction. J Sci Med Sport. 1999;2(3):253-65.

2. Shin D, Finni T, Ahn S, et al. Effect of Chronic Unloading and Rehabilitation on Human Achilles Tendon Properties: a Velocity-Encoded Phase-Contrast MRI Study. J Appl Physiol 2008;105(4):1179–86.

3. Sinha S, Shin D, Hodgson JA, et al. Computer-Controlled, MR-Compatible Foot-Pedal Device to Study Dynamics of the Muscle Tendon Complex Under Isometric, Concentric, and Eccentric Contractions. J Magn Reson Imaging. 2012;36(2):498–504.

Figures

Figure 1. 2D SR indices extracted from pre- and post-ULLS imaging on one subject during peak of the eccentric contraction. SRfiber is the strain rate along a direction closest to the muscle fiber direction and for eccentric contraction corresponds to the positive eigenvalue (local elongation: ( middle column); The SR values are small and relatively minor changes are seen between the pre- and post-ULLS data.

Figure 2. SR indices (negative eigenvalue (1st column), positive eigenvalue (2nd column), sum-eigenvalues (3rd column), SR-fiber angle (4th column) averaged over ROIs, slices and subjects over the dynamic cycle. The change in SR-fiber angle at frame 11 is when the motion changes from contraction to relaxation. The angle is calculated between the positive eigenvector and the fiber, as the former principal strain is closest in orientation to the muscle fiber.

Figure 3. Schematic of a single muscle fiber and extracellular matrix showing the forces during isometric and eccentric contraction. Potential changes in post-ULLS are a lower specific force and an increase in tissue stiffness. In compressive state (IC, top row) the ECM resists the muscle force and in tensile state (EC, lower row) the ECM adds to the muscle force; these factors account for a lower force in IC and a minimal change in force in EC with acute atrophy.



Proc. Intl. Soc. Mag. Reson. Med. 24 (2016)
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