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Abstract
Background and Objectives Repeated impacts in high-contact sports such as American football can affect the brain's microstructure, which can be studied using diffusion MRI. Most imaging studies are cross-sectional, do not include low-contact players as controls, or lack advanced tract-specific microstructural metrics. We aimed to investigate longitudinal changes in high-contact collegiate athletes compared with low-contact controls using advanced diffusion MRI and automated fiber quantification.
Methods We examined brain microstructure in high-contact (football) and low-contact (volleyball) collegiate athletes with up to 4 years of follow-up. Inclusion criteria included university and team enrollment. Exclusion criteria included history of neurosurgery, severe brain injury, and major neurologic or substance abuse disorder. We investigated diffusion metrics along the length of tracts using nested linear mixed-effects models to ascertain the acute and chronic effects of subconcussive and concussive impacts, and associations between diffusion changes with clinical, behavioral, and sports-related measures.
Results Forty-nine football and 24 volleyball players (271 total scans) were included. Football players had significantly divergent trajectories in multiple microstructural metrics and tracts. Longitudinal increases in fractional anisotropy and axonal water fraction, and decreases in radial/mean diffusivity and orientation dispersion index, were present in volleyball but absent in football players (all findings |T-statistic|> 3.5, p value <0.0001). This pattern was present in the callosum forceps minor, superior longitudinal fasciculus, thalamic radiation, and cingulum hippocampus. Longitudinal differences were more prominent and observed in more tracts in concussed football players (n = 24, |T|> 3.6, p < 0.0001). An analysis of immediate postconcussion scans (n = 12) demonstrated a transient localized increase in axial diffusivity and mean/radial kurtosis in the uncinate and cingulum hippocampus (|T| > 3.7, p < 0.0001). Finally, within football players, those with high position-based impact risk demonstrated increased intracellular volume fraction longitudinally (T = 3.6, p < 0.0001).
Discussion The observed longitudinal changes seen in football, and especially concussed athletes, could reveal diminished myelination, altered axonal calibers, or depressed pruning processes leading to a static, nondecreasing axonal dispersion. This prospective longitudinal study demonstrates divergent tract-specific trajectories of brain microstructure, possibly reflecting a concussive and repeated subconcussive impact-related alteration of white matter development in football athletes.
Glossary
- AD=
- axial diffusivity;
- AFQ=
- automated fiber quantification;
- AK=
- axial;
- AWF=
- axonal water fraction;
- BMI=
- body mass index;
- DKI=
- diffusion kurtosis imaging;
- dMRI=
- diffusion MRI;
- DTI=
- diffusion tensor imaging;
- FA=
- fractional anisotropy;
- FICVF=
- intracellular volume fraction;
- HITsp=
- high position-based impact risk;
- MD=
- mean diffusivity;
- MK=
- mean kurtosis;
- mTBI=
- mild traumatic brain injury;
- NODDI=
- neurite orientation dispersion and density imaging;
- ODI=
- orientation dispersion;
- RD=
- radial diffusivity;
- RK=
- radial kurtosis;
- SCAT=
- Standardized Concussion Assessment Tool;
- SLF=
- superior longitudinal fasciculus;
- WM=
- white matter;
- WM=
- white matter;
- WMTI=
- white matter tract integrity
Footnotes
Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.
Previously published at bioRxiv: doi.org/10.1101/2022.04.01.486632.
Submitted and externally peer reviewed. The handling editor was Associate Editor Rebecca Burch, MD.
Editorial, page 380
- Received August 10, 2022.
- Accepted in final form May 5, 2023.
- © 2023 American Academy of Neurology
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