Hockey Concussion Education Project, Part 2. Microstructural white matter alterations in acutely concussed ice hockey players: a longitudinal free-water MRI study

Clinical article

Ofer PasternakPsychiatry Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital/Harvard Medical School, Boston, Massachusetts;

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 Ph.D.
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Inga K. KoertePsychiatry Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital/Harvard Medical School, Boston, Massachusetts;
Institute for Clinical Radiology, Ludwig-Maximilians-University, Munich, Germany;

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Sylvain BouixPsychiatry Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital/Harvard Medical School, Boston, Massachusetts;

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Eli FredmanPsychiatry Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital/Harvard Medical School, Boston, Massachusetts;

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Takeshi SasakiPsychiatry Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital/Harvard Medical School, Boston, Massachusetts;
Department of Psychiatry and Behavioral Sciences, Tokyo Medical and Dental University Graduate School, Tokyo, Japan;

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Michael MayingerPsychiatry Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital/Harvard Medical School, Boston, Massachusetts;
Institute for Clinical Radiology, Ludwig-Maximilians-University, Munich, Germany;

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Karl G. HelmerMassachusetts General Hospital/Massachusetts Institute of Technology/Harvard Medical School/Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, Massachusetts;

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Andrew M. JohnsonSchool of Health Studies,

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Jeffrey D. HolmesSchool of Occupational Therapy,

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Lorie A. ForwellFowler Kennedy Sport Medicine Clinic and
School of Physical Therapy, The University of Western Ontario, London, Ontario, Canada;

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Elaine N. SkopeljaRuth Lilly Medical Library, Indiana University, Indianapolis, Indiana;

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Martha E. ShentonPsychiatry Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital/Harvard Medical School, Boston, Massachusetts;
VA Boston Healthcare System, Brockton;
Department of Radiology, Brigham and Women's Hospital/Harvard Medical School, Boston, Massachusetts; and

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Paul S. EchlinThe Elliott Sports Medicine Clinic, Burlington, Ontario, Canada

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Object

Concussion is a common injury in ice hockey and a health problem for the general population. Traumatic axonal injury has been associated with concussions (also referred to as mild traumatic brain injuries), yet the pathological course that leads from injury to recovery or to long-term sequelae is still not known. This study investigated the longitudinal course of concussion by comparing diffusion MRI (dMRI) scans of the brains of ice hockey players before and after a concussion.

Methods

The 2011–2012 Hockey Concussion Education Project followed 45 university-level ice hockey players (both male and female) during a single Canadian Interuniversity Sports season. Of these, 38 players had usable dMRI scans obtained in the preseason. During the season, 11 players suffered a concussion, and 7 of these 11 players had usable dMRI scans that were taken within 72 hours of injury. To analyze the data, the authors performed free-water imaging, which reflects an increase in specificity over other dMRI analysis methods by identifying alterations that occur in the extracellular space compared with those that occur in proximity to cellular tissue in the white matter. They used an individualized approach to identify alterations that are spatially heterogeneous, as is expected in concussions.

Results

Paired comparison of the concussed players before and after injury revealed a statistically significant (p < 0.05) common pattern of reduced free-water volume and reduced axial diffusivity and fractional anisotropy following elimination of freewater. These free-water–corrected measures are less affected by partial volumes containing extracellular water and are therefore more specific to processes that occur within the brain tissue. Fractional anisotropy was significantly increased, but this change was no longer significant following the free-water elimination.

Conclusions

Concussion during ice hockey games results in microstructural alterations that are detectable using dMRI. The alterations that the authors found suggest decreased extracellular space and decreased diffusivities in white matter tissue. This finding might be explained by axonal injury and/or by increased cellularity of glia cells. Even though these findings in and of themselves cannot determine whether the observed microstructural alterations are related to long-term pathology or persistent symptoms, they are important nonetheless because they establish a clearer picture of how the brain responds to concussion.

Abbreviations used in this paper:

AD = axial diffusivity; ADt = axial diffusivity corrected for free-water; dMRI = diffusion MRI; DTI = diffusion tensor imaging; FA = fractional anisotropy; FAt = FA corrected for free-water; HCEP = Hockey Concussion Education Project; JHU-ICBM = Johns Hopkins University–International Consortium for Brain Mapping; RD = radial diffusivity; RDt = RD corrected for free-water; ROI = region of interest; TBI = traumatic brain injury; TBSS = tract-based spatial statistics.
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