The effect of repetitive subconcussive collisions on brain integrity in collegiate football players over a single football season: A multi-modal neuroimaging study

Abstract

The cumulative effect of repetitive subconcussive collisions on the structural and functional integrity of the brain remains largely unknown. Athletes in collision sports, like football, experience a large number of impacts across a single season of play. The majority of these impacts, however, are generally overlooked, and their long-term consequences remain poorly understood. This study sought to examine the effects of repetitive collisions across a single competitive season in NCAA Football Bowl Subdivision athletes using advanced neuroimaging approaches. Players were evaluated before and after the season using multiple MRI sequences, including T₁-weighted imaging, diffusion tensor imaging (DTI), arterial spin labeling (ASL), resting-state functional MRI (rs-fMRI), and susceptibility weighted imaging (SWI). While no significant differences were found between pre- and post-season for DTI metrics or cortical volumes, seed-based analysis of rs-fMRI revealed significant (p < 0.05) changes in functional connections to right isthmus of the cingulate cortex (ICC), left ICC, and left hippocampus. ASL data revealed significant (p < 0.05) increases in global cerebral blood flow (CBF), with a specific regional increase in right postcentral gyrus. SWI data revealed that 44% of the players exhibited outlier rates (p < 0.05) of regional decreases in SWI signal. Of key interest, athletes in whom changes in rs-fMRI, CBF and SWI were observed were more likely to have experienced high G impacts on a daily basis. These findings are indicative of potential pathophysiological changes in brain integrity arising from only a single season of participation in the NCAA Football Bowl Subdivision, even in the absence of clinical symptoms or a diagnosis of concussion. Whether these changes reflect compensatory adaptation to cumulative head impacts or more lasting alteration of brain integrity remains to be further explored.

Keywords: Accelerometers; Football; MRI; Repetitive impacts; Subconcussive.

Fig. 1

The mean connectivity to the right isthmus of cingulate cortex (ICC) (only showing R ≥ 0.1) are shown at (a) Pre, and (b) Post. (c) Whole-brain ANOVA revealed a significant change (p ≤ 0.048 after whole-brain correction; n = 18) from weak positive correlation prior to participation (Pre) to a post-participation (Post) anti-correlation of the right ICC with the left fusiform gyrus/middle occipital gyrus (FG/MOG).

Fig. 2

The mean connectivity to the left isthmus of cingulate cortex (ICC) (only showing R ≥ 0.1) are shown at (a) Pre, and (b) Post. (c) Whole-brain ANOVA revealed a significant change (p ≤ 0.048 after whole-brain correction; n = 18) from weak positive correlation prior to participation (Pre) to a post-participation (Post) anti-correlation of the left ICC with the left fusiform gyrus/middle occipital gyrus (FG/MOG).

Fig. 3

The mean connectivity to the left hippocampus (only showing R ≥ 0.1) are shown at (a) Pre, and (b) Post. (c) Whole-brain ANOVA revealed a significant change (p ≤ 0.048 after whole-brain correction; n = 18) from weak positive correlation prior to participation (Pre) to a post-participation (Post) anti-correlation of the left hippocampus with the right parahippocampal gyrus/lingual gyrus (PHG/LG).

Fig. 4

A significant global increase in cerebral blood flow (CBF) was observed when comparing Post to Pre (p = 0.048; n = 18). CBF maps—thresholded for CBF ≥ 70 ml (blood)/100 g (tissue)/min—are shown for (a) Pre, and (b) Post.

Fig. 5

6 of the 18 athletes for whom SWI data were analyzed exhibited supra-chance numbers of regions (8 of 55 regions; p_Bonferroni < 0.05) in which the distribution of intensity changes (Post–Pre) for the subject was significantly lower than the distribution of intensity changes in the other 17 subjects (Wilcoxon Rank Sum; p_Uncorrected < 0.05/990 = 0.00005).

Fig. 6

Selected slices for Subject 6 (a defensive back) with an overlay highlighting those voxels in which SWI signal decreases were observed at Post, relative to Pre. Highlighted voxels belong to several of the 10 regions in this subject found to be statistically-significantly decreased (see Fig. 5; Wilcoxon Rank Sum test at the p_Uncorrected < 0.00005 level, corresponding to p_Bonferroni < 0.05), with the saturation of the color reflecting the change measure in the given voxel.