Soccer Heading Exposure-Dependent Microstructural Injury at Depths of Sulci in Adult Amateur Players

Repetitive head impacts (RHIs) in sports are associated with adverse clinical and neuropathologic outcomes, but there is limited evidence from in vivo human imaging studies to inform risk assessment, exposure standards, and interventions. We tested the association of RHI with in vivo microstructural disruption at the depths of cerebral sulci, a region vulnerable to trauma.

We examined the relationship between soccer-related RHI exposure over 12 months and imaging measures. Participants included amateur soccer players and noncollision sport athletes aged 18-55 years from the Greater New York City area. We analyzed diffusion MRI measures specifically within the juxtacortical white matter at the depths of cortical sulci and crests of gyri, as well as within deep white matter. Cognitive function was assessed using components of the CogState computerized battery, focusing on verbal learning and memory performance.

A total of 352 soccer players (mean [SD] age, 25.6 [7.5] years; 245 men [70%]) and 77 controls (22.8 [5.1] years; 30 men [39%]) were included. In multivariable regression, greater RHI was associated with lower fractional anisotropy (FA) (standardized β = -0.234; p < 0.001) and higher orientation dispersion index (ODI) (β = 0.156; p = 0.008), averaged over depths of cerebral sulci, in an RHI exposure-dependent manner. Worse cognitive performance on verbal learning and memory tests was associated with lower FA (Pearson r = 0.16 to 0.24, p < 0.001) and higher ODI (r = -0.25 to -0.17, p < 0.001) at depths of sulci in the orbitofrontal region. Diffusion measures from deep white matter were not associated with RHI or cognitive measures. Mediation analyses revealed that orbitofrontal depths of sulci microstructural disruption (lower FA and higher ODI) partially mediated the relationship between RHI exposure and poorer performance on verbal learning (indirect effects = -0.26 to -0.25, p < 0.001), weighted verbal learning (-0.51 to -0.48, p < 0.001), and verbal memory (-0.05 to -0.04, p = 0.04).

Higher RHI exposure was associated with MRI measures of microstructural disruption at the depths of sulci in an exposure-dependent manner. By contrast, deep white matter regions were relatively insensitive to RHI effects. Diffusion MRI at the depths of sulci may serve as a more specific marker of RHI-related brain injury.