MRI-defined White Matter Microstructural Alteration Associated with Soccer Heading Is More Extensive in Women than Men

Abstract

Purpose To examine the role of sex in abnormal white matter microstructure after soccer heading as identified by using the diffusion-tensor imaging (DTI) metric fractional anisotropy (FA). Materials and Methods In this prospective cross-sectional study, 98 individuals who were enrolled in a larger prospective study of amateur soccer players (from 2013 to 2016) were matched 1:1 for age and history of soccer heading in the prior 12 months. Among the subjects, 49 men (mean age, 25.7 years; range, 18-50 years) and 49 women (mean age, 25.8 years; range, 18-50 years) with median total soccer headings per year of 487 and 469, respectively, underwent 3.0-T DTI. Images were registered to the Johns Hopkins University template. A voxelwise linear regression was fitted for FA with terms for the number of headings during the previous 12 months and its interaction with sex after controlling for the following potential confounders: age, years of education, number of lifetime concussions, and handedness. In the resulting statistical maps, P < .01 indicated a statistically significant difference, with a threshold cluster size larger than 100 mm³. Results Among men, three regions were identified in which greater heading exposure was associated with lower FA; eight such regions were identified among women (>100 contiguous voxels, P < .01). In seven of the eight regions identified in women, the association between heading and FA was stronger in women than in men. There was no significant difference of heading with FA between the sexes for any region in which heading was associated with FA among men (P > .01, <100 contiguous voxels). Conclusion With similar exposure to heading, women exhibit more widespread evidence of microstructural white matter alteration than do men, suggesting preliminary support for a biologic divergence of brain response to repetitive trauma. © RSNA, 2018 Online supplemental material is available for this article.

Figure 1:

Flowchart shows selection of amateur soccer players included in analysis. With exclusion of participants who did not meet image quality standards, the paired participant was also removed, resulting in removal of six pairs (n = 12) from the analysis.

Figure 2:

A, B, Three-dimensional semitransparent images of the Johns Hopkins University template brain oriented facing the right hemisphere in, A, male, and, B, female soccer players demonstrate that lower fractional anisotropy (FA) is associated with heading more extensively in women than in men. Fewer regions of significant association of FA with heading are detected in men than in women. C, Image shows that significant differences in association of heading and FA between men and women are predominantly co-located with areas where women, but not men, show significant association of heading and FA.

Figure 3:

Volume of regions where heading was associated with changes at diffusion-tensor imaging. AD = axial diffusivity, FA = fractional anisotropy, MD = mean diffusivity, RD = radial diffusivity, ΔMen-Women = difference between men and women. A, Graph shows total volume of all regions where imaging parameter (fractional anisotropy, radial diffusivity, axial diffusivity, mean diffusivity) demonstrates significant association with heading. Positive volumes correspond to positive association of parameter with heading, and negative volumes correspond to negative association of parameter with heading. B–E, Graphs show volume of individual regions where each parameter is associated with heading. Each point in plots represents volume of individual region (see Fig 1) found in group analysis, not individual participant. Values depicted in B–E were summed to generate graph in A.