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The effects of repetitive head impact exposure on cerebrovascular reactivity in middle and high-school athletes1Radiology, Medical College of Wisconsin, Milwaukee, WI, United States, 2Neurosurgery, Medical College of Wisconsin, Milwaukee, WI, United States
Synopsis
Keywords: Traumatic brain injury, fMRI, Cerebrovascular reactivity, Breath hold
Cerebrovascular reactivity (CVR) can provide a marker of vascular injury. The effects of repetitive head impact exposure (RHIE) during contact sports remains to be fully elucidated. We investigated the effect of sport, time, and their interaction on CVR in contact sport (CS) and non-contact sport (NCS) middle school and high school athletes. There was a significant effect of time and a significant interaction effect between contact group and time on CVR with CVR decreasing pre to post season in the NCS group but remaining unchanged in the CS group.
Introduction
Cerebrovascular reactivity (CVR) measures the blood vessels’ response to a vasoactive stimulus and can provide a marker of vascular injury. A number of studies have investigated the effects of mild traumatic brain injury on cerebrovascular reactivity (CVR). For example, studies have shown CVR is increased in the acute phase following TBI1,2 followed by decreases continuing months after and potentially into the chronic state3. Repetitive head impact exposure (RHIE), without concussion, during contact sports can also have harmful neurocognitive effects4-6. The effects of RHIE on CVR have been underexplored. We evaluated the effect of sport, time, and their interaction in contact sport (CS) and non-contact sport (NCS) middle school and high school athletes imaged pre- and post-season using CVR measured with an advanced multiband, multi-echo (MBME) MRI sequence.Methods
Thirty-six male, non-concussed, United States middle school and high school contact sport (CS, N=15) and non-contact sport (NCS, N=21) athletes underwent MRI scans before and after their respective seasons. Overall, 11 CS and 14 NCS athletes completed both preseason and follow-up postseason scans.Imaging was performed on a 3T GE Premier scanner. A T1-weighted MPRAGE anatomical image was acquired, followed by a gradient echo multiband, multi-echo (MBME) breath hold (BH) task fMRI scan with the following parameters: TR/TE=1000/11,30,49ms, FOV=24cm, matrix size=80x80 with slice thickness = 3mm (3x3x3mm voxel size), 11 slices with multiband factor=4 (44 total slices), FA=60°, partial Fourier factor=0.85, and in-plane acceleration (R)=2. The BH task consisted of 66 s of paced breathing, followed by four cycles of 24 s of paced breathing, 16s of BH on expiration, and 16 s of self-paced recovery breathing. Scans ended with an additional 30s of paced breathing7. The paced breathing portions consisted of alternating 3s inspiration and expiration blocks. A short, reversed polarity MBME scan was also collected to allow for image distortion correction.
Data was analyzed using a combination of AFNI and FSL. First, the anatomical MPRAGE image was coregistered to Montreal Neurological Institute (MNI) space. Then, the first-echo functional data was volume registered to the first volume. Subsequent echoes were registered using the transformation matrices from the first echo. Image distortion was corrected using topup. The three echoes were then combined using the -weighted approach8 and denoised using multi-echo independent component analysis (ME-ICA)9-11 by regressing non-BOLD independent components out of the combined ME data. The denoised MBME dataset was then registered to the MPRAGE image and registered to MNI space using the anatomical transformations computed above.
The BH response was evaluated using a general linear model with 3dDeconvolve in AFNI. After 3dDeconvolve, a restricted maximum likelihood model (3dREMLfit) was used to model temporal autocorrelations in the data. BH regressors were generated by convolving a square wave with the respiration response function12 and shifting the regressor from −8s to 16s in steps of 2s. For each voxel, the regressor that resulted in the highest positive t-score was chosen. CVR was calculated as the percent signal change of the BH response.
Linear mixed-effects models were fit using 3dLMEr in AFNI to test the effects of time (pre- to post-season difference), contact group (CS vs. NCS), and group-by-time interactions in CVR. Age, BMI, and concussion history were included as covariates. Post-hoc general linear tests were performed to compare across time for each group individually and across groups at each time. Multiple comparisons were controlled for using a cluster size correction technique and 3dClustSim in AFNI (p < 0.05, α < 0.05).
Results
Results from the linear mixed effects model showed there was a significant effect of time and a significant interaction effect between contact group and time with clusters centered in the primary visual cortex (Figure 1). Post-hoc analyses (Figure 2) revealed the time effect was driven by a largely global significant decrease in CVR from post- to pre-season in the NCS group with clusters encompassing visual cortex, components of the default mode network (posterior cingulate cortex, precuneus, anterior cingulate cortex), motor cortex, and insula. A significant decrease in CVR was observed between CS and NCS groups at the preseason scan in the superior visual cortex, precuneus, and motor cortex.Discussion/Conclusions
Changes in CVR have been observed in female soccer players compared to a NCS control group with CVR decreasing post-season vs. preseason in athletes with more head acceleration events13. Another study demonstrated regionally decreased CVR in football players mid- and post-season compared to preseason14. Interestingly, in this study, we did not observe significant changes pre- to post-season in the CS group but did find significant decreases in CVR in the NCS group. It is possible there are competing effects with overall sport activity and collisions causing opposite effects on CVR. Thus, additional research is needed linking these findings to clinical measures and/or head impact telemetry or accelerometer measurements.Acknowledgements
No acknowledgement found.References
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Figures
Figure 1. Overall effect of time and the interaction of sport and time on CVR. CVR tended to decrease over the course of one season while the interaction was positive.
Figure 2. Post hoc general linear tests. NCS participants saw a decrease in CVR over the course of one season.