In this study, we use magnetic resonance elastography (MRE) to examine the effects of a season of collegiate hockey on brain biomechanics to better understand the neurological impact of traumatic brain injury. We scanned 13 collegiate-level hockey players at four time points over the course over year using MRE to quantify the possible changes to the viscoelastic mechanical properties caused by repeated head impacts. We discovered that both stiffness and damping ratio changed over the course of the hockey season and then had some recovery after the season, indicating a complex pathology that can be quantified with MRE.
Overview of the study methods and design is shown in Figure 1.
Subjects: We examined 13 club-level college hockey players (8/5 M/F). Players were scanned four times over a year: (1) preseason, within one week prior to the first game in September 2017; (2) midseason, in December 2017 before winter break; (3) postseason, within 10 days of the last game played, in February/March 2018; and (4) recovery, before the season began in September 2018 (Figure 1C). Six players graduated and were not scanned at the recovery time point.
Imaging: All scans were performed on a Siemens 3T Prisma scanner. The scan protocol included MRE with a 3D multiband, multishot spiral sequence [6]. MRE imaging parameters included: TR/TE = 2133/70 ms; 240x240 mm2 FOV; 120x120 matrix; 64 slices; 2.0 mm isotropic resolution. Vibrations at 60 Hz were generated by the Resoundant pneumatic actuator system. Additional scans for creating anatomical regions-of-interest include diffusion tensor imaging (2.0 mm resolution, co-registered with MRE data) and 1.0 mm resolution T1-weighted MPRAGE.
Analysis: We used a nonlinear inversion algorithm (NLI) [7] to estimate the viscoelastic shear stiffness and damping ratio from measured displacement fields. The MPRAGE and DTI scans were used to create a region-of-interest incorporating all cerebral white matter (WM). We used a repeated measures ANOVA with a post-hoc Tukey test to determine whether stiffness and damping ratio changed between time points, excluding missing data and MRE scans with poor SNR [8].
[1] Langlois, J. A., Rutland-Brown, W., and Wald, M. M., 2006, The Epidemiology and Impact of Traumatic Brain Injury A Brief Overview. [
2] Baugh, C. M., Stamm, J. M., Riley, D. O., Gavett, B. E., Shenton, M. E., Lin, A., Nowinski, C. J., Cantu, R. C., McKee, A. C., and Stern, R. A., 2012, “Chronic Traumatic Encephalopathy: Neurodegeneration Following Repetitive Concussive and Subconcussive Brain Trauma,” Brain Imaging Behav., 6(2), pp. 244–254.
[3] Manning, K. Y., Schranz, A., Bartha, R., Dekaban, G. A., Barreira, C., Brown, A., Fischer, L., Asem, K., Doherty, T. J., Fraser, D. D., Holmes, J., and Menon, R. S., 2017, “Multiparametric MRI Changes Persist beyond Recovery in Concussed Adolescent Hockey Players.,” Neurology, 89(21), pp. 2157–2166.
[4] Muthupillai, R., Lomas, D. J., Rossman, P. J., Greenleaf, J. F., Manduca, A., and Ehman, R. L., 1995, “Magnetic Resonance Elastography by Direct Visualization of Propagating Acoustic Strain Waves.,” Science, 269(5232), pp. 1854–7.
[5] Hiscox, L. V, Johnson, C. L., Barnhill, E., McGarry, M. D. J., Huston, J., van Beek, E. J. R., Starr, J. M., and Roberts, N., 2016, “Magnetic Resonance Elastography (MRE) of the Human Brain: Technique, Findings and Clinical Applications,” Phys. Med. Biol., 61(24), pp. R401–R437.
[6] CL Johnson, JL Holtrop, AT Anderson, BP Sutton, “Brain MR Elastography with Multiband Excitation and Nonlinear Motion-Induced Phase Error Correction,” 24th Annual Meeting of the International Society for Magnetic Resonance in Medicine, Singapore, May 7-13, 2016, p. 1951.
[7] MDJ McGarry, EEW Van Houten, CL Johnson, JG Georgiadis, BP Sutton, JB Weaver, KD Paulsen, “Multiresolution MR Elastography Using Nonlinear Inversion,” Medical Physics, 2012; 39(10):6388-6396.
[8] McGarry, M. D. J., Van Houten, E. E. W., Perriñez, P. R., Pattison, A. J., Weaver, J. B., and Paulsen, K. D., 2011, “An Octahedral Shear Strain-Based Measure of SNR for 3D MR Elastography.,” Phys. Med. Biol., 56(13), pp. N153-64.
[9] Arani, A., Min, H.-K., Fattahi, N., Wetjen, N. M., Trzasko, J. D., Manduca, A., Jack, C. R., Lee, K. H., Ehman, R. L., and Huston, J., 2018, “Acute Pressure Changes in the Brain Are Correlated with MR Elastography Stiffness Measurements: Initial Feasibility in an in Vivo Large Animal Model,” Magn. Reson. Med., 79(2), pp. 1043–1051.
[10] Sack, I., Jöhrens, K., Würfel, J., and Braun, J., 2013, “Structure-Sensitive Elastography: On the Viscoelastic Powerlaw Behavior of in Vivo Human Tissue in Health and Disease,” Soft Matter, 9(24), p. 5672.