Every hit matters: White matter diffusivity changes in high school football athletes are correlated with repetitive head acceleration event exposure.

Ikbeom Jang,Ulrike Dydak,Yukai Zou,Larry J Leverenz,Thomas M Talavage,Taylor A Lee,Gregory G Tamer,Il Yong Chun,Sumra Bari,Diana O Svaldi,Roy J Lycke,Victoria N Poole,Eric A Nauman,Trey E Shenk,Brian R Cummiskey,Jared R Brosch

doi:10.1016/j.nicl.2019.101930

Abstract

Recent evidence of short-term alterations in brain physiology associated with repeated exposure to moderate intensity subconcussive head acceleration events (HAEs), prompts the question whether these alterations represent an underlying neural injury. A retrospective analysis combining counts of experienced HAEs and longitudinal diffusion-weighted imaging explored whether greater exposure to incident mechanical forces was associated with traditional diffusion-based measures of neural injury—reduced fractional anisotropy (FA) and increased mean diffusivity (MD). Brains of high school athletes (N = 61) participating in American football exhibited greater spatial extents (or volumes) experiencing substantial changes (increases and decreases) in both FA and MD than brains of peers who do not participate in collision-based sports (N = 15). Further, the spatial extents of the football athlete brain exhibiting traditional diffusion-based markers of neural injury were found to be significantly correlated with the cumulative exposure to HAEs having peak translational acceleration exceeding 20 g. This finding demonstrates that subconcussive HAEs induce low-level neurotrauma, with prolonged exposure producing greater accumulation of neural damage. The duration and extent of recovery associated with periods in which athletes do not experience subconcussive HAEs now represents a priority for future study, such that appropriate participation and training schedules may be developed to minimize the risk of long-term neurological dysfunction.

Highlights

Researchers have observed that retired American football athletes may have a higher risk of developing neurodegenerative disorders such as chronic traumatic encephalopathy, Alzheimer's disease, and Parkinson's disease (Omalu et al, 2006; Broglio et al, 2009; McKee et al, 2009; Stern et al, 2011; Lehman et al, 2012)
A repeated measures analysis of variance (ANOVA) revealed no effect of race—the only demographic factor that differed across the Noncollision-sport athletes (NCA) and Football athletes (FBA) groups—on to-date head acceleration events (HAEs) at each follow-up session
There was no significant difference in either mean fractional anisotropy (FA) or mean mean diffusivity (MD) between FBA and NCA

Summary

Introduction

Researchers have observed that retired American football athletes (who have extended histories of exposure to subconcussive impacts) may have a higher risk of developing neurodegenerative disorders such as chronic traumatic encephalopathy, Alzheimer's disease, and Parkinson's disease (Omalu et al, 2006; Broglio et al, 2009; McKee et al, 2009; Stern et al, 2011; Lehman et al, 2012). Previous neuroimaging work has demonstrated changes in brain function and chemistry are associated with the accumulation of exposure to head acceleration events (HAEs), even in the absence of a diagnosis of concussion Exposure to these “subconcussive” HAEs has been observed to be associated with alterations in the brain's response to task demands (Talavage et al, 2014; Robinson et al, 2015; Shenk et al, 2015), functional connectivity (Johnson et al, 2014; Abbas et al, 2015a,b), cerebrovascular reactivity (Svaldi et al, 2015, 2017, 2018), biochemical concentrations (Poole et al, 2014, 2015; Bari et al, 2018), and resting perfusion (Slobounov et al, 2017). Changes in the DTI-based measures of fractional anisotropy (FA) and the associated mean diffusivity (MD) are interpreted as markers or confirmation of changes to white matter health (e.g., Beaulieu, 2002; Arfanakis et al, 2002; Inglese et al, 2005; Bazarian et al, 2007)

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