Microstructural Alterations in Tract Development in College Football and Volleyball Players: A Longitudinal Diffusion MRI Study.


Journal

Neurology
ISSN: 1526-632X
Titre abrégé: Neurology
Pays: United States
ID NLM: 0401060

Informations de publication

Date de publication:
29 08 2023
Historique:
received: 10 08 2022
accepted: 05 05 2023
pmc-release: 29 08 2024
medline: 31 8 2023
pubmed: 22 7 2023
entrez: 21 7 2023
Statut: ppublish

Résumé

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. 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. 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, 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.

Sections du résumé

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,
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.

Identifiants

pubmed: 37479529
pii: WNL.0000000000207543
doi: 10.1212/WNL.0000000000207543
pmc: PMC10501097
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e953-e965

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2023 American Academy of Neurology.

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Auteurs

Maged Goubran (M)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Brian David Mills (BD)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Marios Georgiadis (M)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Mahta Karimpoor (M)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Nicole Mouchawar (N)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Sohrab Sami (S)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Emily Larson Dennis (EL)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Carolyn Akers (C)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Lex Mitchell (L)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Brian Boldt (B)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

David Douglas (D)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Phillip Scott DiGiacomo (PS)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Jarrett Rosenberg (J)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Gerald Grant (G)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Max Wintermark (M)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

David Benjamin Camarillo (DB)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA.

Michael Zeineh (M)

From the Departments of Radiology (Maged Goubran, B.D.M., Marios Georgiadis, M.K., N.M., C.A., L.M., D.D., P.S.D., J.R., M.W., M.Z.), Neurosurgery (G.G.), and Bioengineering (D.B.C.), Stanford University, CA; Department of Medical Biophysics (Maged Goubran) and Physical Sciences Platform & Hurvitz Brain Sciences Research Program (Maged Goubran), Sunnybrook Research Institute, University of Toronto, ON, Canada; Stanford Center for Clinical Research (S.S.), CA; Department of Neurology (E.L.D.), University of Utah School of Medicine, Salt Lake City; Department of Radiology (B.B.), Uniformed Services University of the Health Sciences, Bethesda, MD; and Department of Radiology (B.B.), Madigan Army Medical Center, Tacoma, WA. mzeineh@stanford.edu.

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