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4D Phase Contrast MRI detects heterogeneous strain rate patterns along the length of the Tibialis Anterior muscle during dynamic contractions1Radiology, Leiden University Medical Center, Leiden, Netherlands, 2Biomedical Engineering & Physics, Amsterdam Movement Sciences, Amsterdam University Medical Center, Location AMC, Amsterdam, Netherlands, 3Radiology, Stanford University, Stanford, CA, United States, 4Rehabilitation Medicine, Leiden University Medical Center, Leiden, Netherlands, 5Radiology and Nuclear Medicine, Amsterdam Movement Sciences, Amsterdam University Medical Center, Location AMC, Amsterdam, Netherlands, 6Duchenne Center Netherlands, Veenendaal, Netherlands
Synopsis
We assessed strain rate distributions within the Tibialis Anterior muscle by acquiring whole lower leg 4D PC-MRI during dynamic exercise, with and without load. Our data revealed a spatially heterogeneous strain rate pattern along the length of the Tibialis Anterior muscle during movement cycle. During dorsiflexion, the smallest negative strain rates were observed (in first approximation) along the fiber in the most proximal segment and the largest positive strain rates (in first approximation) across the fiber in the most distal segment, while plantarflexion showed the expected opposite. No effect of load was detected on strain rates.
Introduction
It is known that muscles do not uniformly shorten along their longitudinal axis1 and therefore strains during contraction and relaxation are likely heterogeneously distributed within the muscle. This notion is supported by the finding that muscle damage after heavy eccentric exercise is not uniformly distributed within muscles2,3. However, the few studies that assessed strain heterogeneity within muscles reported contrasting results, including homogeneous distributions and higher strain rates distally4,5. A limitation in these studies was that primarily 2D imaging techniques with limited coverage or single slice assessments were used in combination with small ROIs6,7. Consequently, 3D information with high spatial resolution, needed to assess the hypothesized complex strain distributions within muscle, was not available. In addition, these studies used primarily isometric contractions and passive joint motions which are not reflective for daily-life activities whereas dynamic contraction against load would be more reflective. We used an in-house developed accelerated time-resolved 3D Phase Contrast (PC)-MRI protocol with sufficient spatial-temporal resolution to facilitate a 3D assessment of strain rate distributions in the Tibialis Anterior (TA) muscle during dynamic exercise, under two different load conditions.Methods
MR datasets were acquired in the right lower leg of 12 healthy volunteers (age: 31.6±15.9 years; 50% m) with a 3T Philips Ingenia system (Best, Netherlands) and 16-channel receive coil with the ankle in neutral position. The MR examination consisted of a Dixon acquisition (TR/TE/∆TE/FA 7.8/1.27/1.1/3; voxel size 1x1x3mm3) for muscle segmentation, diffusion-weighted acquisition (fat-suppressed SE-EPI; TR/TE 6123/48ms; b-values: 0(4), 400(19) s/mm2; voxel size 3x3x6mm3) to assess principal fiber directions and two 4D PC-MRI acquisitions to retrieve velocity information during dorsi-/plantarflexion movement (starting in plantarflexion), with and without load (VENC=10 cm/s; 20 time-points, voxel size 3x3x6mm3; scan duration of 432 seconds corresponding to 216 motion task repetitions) covering the lower leg (FOV 192x192x390mm3). 4D PC-MRI data were acquired by incoherently undersampling k-space based on a pseudo-spiral pattern (R=9.1)8,9. The applied load was 7.5% of maximum voluntary contraction force (MVC-force). MVC-force was measured as the highest value of three contractions for dorsi-flexor muscles prior to the scan examination using a handheld dynamometer. A schematic representation of the exercise set-up is shown in Figure 1.Data-analysis
PC-MRI data was reconstructed using a Compressed Sensing pipeline9 using BART10. The infinitesimal strain rate tensor was calculated and diagonalized to obtain the principal eigenvectors and -values. Volumes of interest (VOIs) were drawn on the muscle border along the full length of the TA using scanner reconstructed water images of the Dixon. These images were subsequently registered to individual time-points of the PC-MRI data (magnitude images) using 3D-Demons11, and the deformation matrices were used to deform the VOIs. Full segmented muscle volumes were divided into five equal segments based on normalized muscle length (distal 0-100% proximal). Strain rate eigenvalues are reported as weighted mean and standard deviation for each of the individual segments and over the full volume for maximum dorsi-/plantarflexion position. Two-Way Repeated Measures ANOVAs with Bonferonni correction (p-value≤0.0125) was used to assess the effect of load and proximodistal location on strain rates.Results
Representative velocity images and strain rate maps are shown for one subject during maximal dorsiflexion velocity with load (Figure 2). A consistent temporal pattern was found for strain rate eigenvalues during both load conditions, consisting of a large negative eigenvalue (local contraction, 1st-eigenvalue), large positive eigenvalue (local expansion, 2nd-eigenvalue) and one approximately zero eigenvalue (3rd-eigenvalue) (Figure 3). A main effect was found for proximodistal location for negative and positive strain rate eigenvalues during dorsi- and plantarflexion (Table 1; Figure 3). Post-hoc analysis showed that during dorsiflexion the smallest negative strain rates (contraction) (in first approximation) along the fiber were detected in the most proximal segment and the largest positive strain rates (expansion) (in first approximation) across the fiber in the most distal segment. During plantarflexion, the smallest positive strain rates (expansion) were detected in the most proximal segment (in first approximation) along the fiber and the largest negative strain rates in the most distal segment (in first approximation) across the fiber. No load effect was detected on strain rates (Figure 3-4).Discussion
This study revealed spatially heterogeneous strain rate patterns along the length of the TA muscle during dynamic dorsi-/plantarflexion contractions with and without load, with the smallest and largest strain rates in most proximal and distal segment, respectively. Observed strain rate eigenvalues agreed with both magnitude and temporal patterns reported in previous studies1,8. The observed spatial pattern is consistent with part of the 2D strain rate measurements in other muscles, where higher strain rates distally were attributed to the smaller CSA5,13. Other likely factors which may contribute to heterogeneity in strain rates are variations in fascicle lengths and curvature, extracellular matrix, motor unit activation and neural control14-17. No differences in principal strain rates were detected between the two load conditions. This is probably related to the relatively low load levels and fixed timing of the movement cycle13,18. We aim to combine strain rate eigenvectors with the acquired DTI data to improve our understanding of muscle contractile function.Conclusion
Spatially heterogeneous strain rates were detected along the length of the TA muscle indicating that 3D assessments are required for better understanding of muscle contractile function.Acknowledgements
This work was supported by the Netherlands Organization for Scientific Research (NWO), under research program VIDI, project "Similar but not thesame", number 917.164.90, and the Dutch Technology Foundation TTW (DIMASK #15500).References
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