The Effects of External Jugular Compression Applied during Head Impact Exposure on Longitudinal Changes in Brain Neuroanatomical and Neurophysiological Biomarkers: A Preliminary Investigation

Gregory D Myer, Weihong Yuan, Kim D Barber Foss, David Smith, Mekibib Altaye, Amit Reches, James Leach, Adam W Kiefer, Jane C Khoury, Michal Weiss, Staci Thomas, Chris Dicesare, Janet Adams, Paul J Gubanich, Amir Geva, Joseph F Clark, William P Meehan 3rd, Jason P Mihalik, Darcy Krueger, Gregory D Myer, Weihong Yuan, Kim D Barber Foss, David Smith, Mekibib Altaye, Amit Reches, James Leach, Adam W Kiefer, Jane C Khoury, Michal Weiss, Staci Thomas, Chris Dicesare, Janet Adams, Paul J Gubanich, Amir Geva, Joseph F Clark, William P Meehan 3rd, Jason P Mihalik, Darcy Krueger

Abstract

Objectives: Utilize a prospective in vivo clinical trial to evaluate the potential for mild neck compression applied during head impact exposure to reduce anatomical and physiological biomarkers of brain injury.

Methods: This project utilized a prospective randomized controlled trial to evaluate effects of mild jugular vein (neck) compression (collar) relative to controls (no collar) during a competitive hockey season (males; 16.3 ± 1.2 years). The collar was designed to mildly compress the jugular vein bilaterally with the goal to increase intracranial blood volume to reduce risk of brain slosh injury during head impact exposure. Helmet sensors were used to collect daily impact data in excess of 20 g (games and practices) and the primary outcome measures, which included changes in white matter (WM) microstructure, were assessed by diffusion tensor imaging (DTI). Specifically, four DTI measures: fractional anisotropy, mean diffusivity (MD), axial diffusivity, and radial diffusivity (RD) were used in the study. These metrics were analyzed using the tract-based Spatial Statistics (TBSS) approach - a voxel-based analysis. In addition, electroencephalography-derived event-related potentials were used to assess changes in brain network activation (BNA) between study groups.

Results: For athletes not wearing the collar, DTI measures corresponding to a disruption of WM microstructure, including MD and RD, increased significantly from pre-season to mid-season (p < 0.05). Athletes wearing the collar did not show a significant change in either MD or RD despite similar accumulated linear accelerations from head impacts (p > 0.05). In addition to these anatomical findings, electrophysiological network analysis of the degree of congruence in the network electrophysiological activation pattern demonstrated concomitant changes in brain network dynamics in the non-collar group only (p < 0.05). Similar to the DTI findings, the increased change in BNA score in the non-collar relative to the collar group was statistically significant (p < 0.01). Changes in DTI outcomes were also directly correlated with altered brain network dynamics (r = 0.76; p < 0.05) as measured by BNA.

Conclusion: Group differences in the longitudinal changes in both neuroanatomical and electrophysiological measures, as well as the correlation between the measures, provide initial evidence indicating that mild jugular vein compression may have reduced alterations in the WM response to head impacts during a competitive hockey season. The data indicate sport-related alterations in WM microstructure were ameliorated by application of jugular compression during head impact exposure. These results may lead to a novel line of research inquiry to evaluate the effects of protecting the brain from sports-related head impacts via optimized intracranial fluid dynamics.

Keywords: EEG; head injury; pediatric traumatic brain injury; traumatic brain injury.

Figures

Figure 1
Figure 1
The Q-Collar designed to facilitate the actions of the compressive effect of the omohyoids to reduce blood outflow of the brain (A) and produce a tighter fit of the brain within the cranium (B).
Figure 2
Figure 2
Study subject allocation following randomization. Subjects randomly assigned to the collar (n = 7) or no-collar group (n = 8) for the first half of the season were crossed-over at the mid-season time point. The number of subjects who completed each test (EEG and MRI) at each time point is indicated in the blue and yellow boxes. In the second half of the season, five subjects did not comply with wearing the collar, which created a second “No-Collar” group in the latter part of the season, as indicated in the red box.
Figure 3
Figure 3
Pictorial representation of internal jugular vein (IJV) response via dilation to the application of the collar device.
Figure 4
Figure 4
Colored dots represent location of accelerometer measured the linear accelerations above 20 g (green), 50 g (yellow), and 100 g (red) sustained by either the collar or no-collar groups during the pre- to mid-season time period.
Figure 5
Figure 5
Increase in MD from pre- to mid-season in non-collar group. The red regions represent areas with statistically significant longitudinal changes at p < 0.05 level (FWE corrected). The red regions are thickened to improve visual display.
Figure 6
Figure 6
Increase in RD from pre- to mid-season in non-collar group. The red regions represent areas with statistically significant longitudinal changes at p < 0.05 level (FWE corrected). The red regions are thickened to improve visual display.
Figure 7
Figure 7
Increase in MD (A) and RD (B) from pre- to mid-season in non-collar group after accounting for longitudinal changes in collar group. The red regions represent areas where the increase of DTI measure in the non-collar group was significantly larger than that in the collar group, p < 0.05 level (FWE corrected). The red regions are thickened to improve visual display.
Figure 8
Figure 8
Representation of the group mean for absolute value of the change in the BNA synchronization score between baseline and mid-season visits in the non-collar group vs. the collar group (BNA change score). Heat map imaging highlight increased change as the color moves away from green (0 = no change) to red (1 = high change).

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