Effects of Career Duration, Concussion History, and Playing Position on White Matter Microstructure and Functional Neural Recruitment in Former College and Professional Football Athletes

Abstract

Purpose To better understand the relationship between exposure to concussive and subconcussive head impacts, white matter integrity, and functional task-related neural activity in former U.S. football athletes. Materials and Methods Between 2011 and 2013, 61 cognitively unimpaired former collegiate and professional football players (age range, 52-65 years) provided informed consent to participate in this cross-sectional study. Participants were stratified across three crossed factors: career duration, concussion history, and primary playing position. Fractional anisotropy (FA) and blood oxygen level-dependent (BOLD) percent signal change (PSC) were measured with diffusion-weighted and task-related functional magnetic resonance imaging, respectively. Analyses of variance of FA and BOLD PSC were used to determine main or interaction effects of the three factors. Results A significant interaction between career duration and concussion history was observed; former college players with more than three concussions had lower FA in a broadly distributed area of white matter compared with those with zero to one concussion (t29 = 2.774; adjusted P = .037), and the opposite was observed for former professional players (t29 = 3.883; adjusted P = .001). A separate interaction between concussion history and position was observed: Nonspeed players with more than three concussions had lower FA in frontal white matter compared with those with zero to one concussion (t25 = 3.861; adjusted P = .002). Analysis of working memory-task BOLD PSC revealed a similar interaction between concussion history and position (all adjusted P < .004). Overall, former players with lower FA tended to have lower BOLD PSC across three levels of a working memory task. Conclusion Career duration and primary playing position seem to modify the effects of concussion history on white matter structure and neural recruitment. The differences in brain structure and function were observed in the absence of clinical impairment, which suggested that multimodal imaging may provide early markers of onset of traumatic neurodegenerative disease. © RSNA, 2017 Online supplemental material is available for this article.

Figures

Figure 1:

Axial MR images show results of tract-based spatial statistics analysis of white matter FA clusters of voxels with a significant crossover interaction (P < .05, corrected) between concussion history and career duration (red and orange) and between concussion history and playing position (blue). Clusters are overlaid on the mean white matter skeleton (white) in Montreal Neuroimaging Institute space (y coordinates are shown in millimeters). Voxels were filled out for viewing by using tbss_fill tool in FSL.

Figure 2:

Box-and-whisker plots show mean FA values from the significant clusters for the interaction of concussion history and career duration.

Figure 3:

Box-and-whisker plots show mean FA values from the significant clusters for the interaction of concussion history and playing position.

Figure 4:

Axial functional MR images show analysis of the interaction between concussion history and playing position for the task-related functional MR imaging BOLD response during a working memory N-back task. Each task-level contrast was modeled separately: 1-back greater than 0-back (orange), 2-back greater than 1-back (red), 2-back greater than 0-back (blue). Clusters with a significant interaction (P < .001) between concussion history and playing position are overlaid on the Montreal Neuroimaging Institute template brain. Numbers are the y coordinate of the Montreal Neuroimaging Institute space (in millimeters).

Figure 5:

Box-and-whisker plots show mean PSC from the significant clusters for the interaction of concussion history and playing position for each comparison of the functional MR imaging task.