Sex differences in white matter alterations following repetitive subconcussive head impacts in collegiate ice hockey players

Nico Sollmann¹, Paul S Echlin², Vivian Schultz³, Petra V Viher⁴, Amanda E Lyall⁵, Yorghos Tripodis⁶, David Kaufmann⁷, Elisabeth Hartl⁸, Philipp Kinzel⁹, Lorie A Forwell¹⁰, Andrew M Johnson¹¹, Elaine N Skopelja¹², Christian Lepage¹³, Sylvain Bouix¹⁴, Ofer Pasternak¹⁵, Alexander P Lin¹⁶, Martha E Shenton¹⁷, Inga K Koerte¹⁸

Affiliations

¹ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Neuroradiology, Klinikum rechts der Isar, Technische Universität München, Munich, Germany; TUM-Neuroimaging Center, Klinikum rechts der Isar, Technische Universität München, Munich, Germany; Department of Neurosurgery, Klinikum rechts der Isar, Technische Universität München, Munich, Germany. Electronic address: Nico.Sollmann@tum.de.
² Elliott Sports Medicine Clinic, Burlington, ON, Canada. Electronic address: Psechlin@gmail.com.
³ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Child and Adolescent Psychiatry, Psychosomatic and Psychotherapy, Ludwig-Maximilians-Universität, Munich, Germany. Electronic address: VivianSchultz@gmx.de.
⁴ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Translational Research Center, University Hospital of Psychiatry, Bern, Switzerland. Electronic address: Petra.Viher@puk.unibe.ch.
⁵ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA. Electronic address: Alyall@bwh.harvard.edu.
⁶ Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA; Boston University Alzheimer's Disease and CTE Center, Boston University School of Medicine, Boston, MA, USA. Electronic address: Yorghos@bu.edu.
⁷ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Child and Adolescent Psychiatry, Psychosomatic and Psychotherapy, Ludwig-Maximilians-Universität, Munich, Germany; Department of Radiology, Charité Universitätsmedizin, Berlin, Germany. Electronic address: David.Kaufmann@charite.de.
⁸ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Neurology, Epilepsy Center, Ludwig-Maximilians-Universität, Munich, Germany. Electronic address: Elisabeth.Hartl@med.uni-muenchen.de.
⁹ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Child and Adolescent Psychiatry, Psychosomatic and Psychotherapy, Ludwig-Maximilians-Universität, Munich, Germany. Electronic address: Pkinzel@bwh.harvard.edu.
¹⁰ 3M Centre, The University of Western Ontario, London, ON, Canada. Electronic address: Lforwell@uwo.ca.
¹¹ School of Health Studies, The University of Western Ontario, London, ON, Canada. Electronic address: Ajohnson@uwo.ca.
¹² Ruth Lilly Medical Library, Indiana University, Indianapolis, IN, USA. Electronic address: Eskopelj@iu.edu.
¹³ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; School of Psychology, University of Ottawa, Ottawa, ON, Canada. Electronic address: Clepage@uottawa.ca.
¹⁴ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. Electronic address: Sylvain@bwh.harvard.edu.
¹⁵ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. Electronic address: Ofer@bwh.harvard.edu.
¹⁶ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Center for Clinical Spectroscopy, Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. Electronic address: Aplin@bwh.harvard.edu.
¹⁷ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Center for Clinical Spectroscopy, Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; VA Boston Healthcare System, Brockton Division, Brockton, MA, USA. Electronic address: Shenton@bwh.harvard.edu.
¹⁸ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Child and Adolescent Psychiatry, Psychosomatic and Psychotherapy, Ludwig-Maximilians-Universität, Munich, Germany; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA. Electronic address: Ikoerte@bwh.harvard.edu.

PMID: 29204342
PMCID: PMC5709295
DOI: 10.1016/j.nicl.2017.11.020

Sex differences in white matter alterations following repetitive subconcussive head impacts in collegiate ice hockey players

Nico Sollmann et al. Neuroimage Clin. 2017.

. 2017 Nov 21:17:642-649.

doi: 10.1016/j.nicl.2017.11.020. eCollection 2018.

Authors

Affiliations

¹ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Neuroradiology, Klinikum rechts der Isar, Technische Universität München, Munich, Germany; TUM-Neuroimaging Center, Klinikum rechts der Isar, Technische Universität München, Munich, Germany; Department of Neurosurgery, Klinikum rechts der Isar, Technische Universität München, Munich, Germany. Electronic address: Nico.Sollmann@tum.de.
² Elliott Sports Medicine Clinic, Burlington, ON, Canada. Electronic address: Psechlin@gmail.com.
³ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Child and Adolescent Psychiatry, Psychosomatic and Psychotherapy, Ludwig-Maximilians-Universität, Munich, Germany. Electronic address: VivianSchultz@gmx.de.
⁴ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Translational Research Center, University Hospital of Psychiatry, Bern, Switzerland. Electronic address: Petra.Viher@puk.unibe.ch.
⁵ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA. Electronic address: Alyall@bwh.harvard.edu.
⁶ Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA; Boston University Alzheimer's Disease and CTE Center, Boston University School of Medicine, Boston, MA, USA. Electronic address: Yorghos@bu.edu.
⁷ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Child and Adolescent Psychiatry, Psychosomatic and Psychotherapy, Ludwig-Maximilians-Universität, Munich, Germany; Department of Radiology, Charité Universitätsmedizin, Berlin, Germany. Electronic address: David.Kaufmann@charite.de.
⁸ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Neurology, Epilepsy Center, Ludwig-Maximilians-Universität, Munich, Germany. Electronic address: Elisabeth.Hartl@med.uni-muenchen.de.
⁹ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Child and Adolescent Psychiatry, Psychosomatic and Psychotherapy, Ludwig-Maximilians-Universität, Munich, Germany. Electronic address: Pkinzel@bwh.harvard.edu.
¹⁰ 3M Centre, The University of Western Ontario, London, ON, Canada. Electronic address: Lforwell@uwo.ca.
¹¹ School of Health Studies, The University of Western Ontario, London, ON, Canada. Electronic address: Ajohnson@uwo.ca.
¹² Ruth Lilly Medical Library, Indiana University, Indianapolis, IN, USA. Electronic address: Eskopelj@iu.edu.
¹³ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; School of Psychology, University of Ottawa, Ottawa, ON, Canada. Electronic address: Clepage@uottawa.ca.
¹⁴ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. Electronic address: Sylvain@bwh.harvard.edu.
¹⁵ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. Electronic address: Ofer@bwh.harvard.edu.
¹⁶ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Center for Clinical Spectroscopy, Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. Electronic address: Aplin@bwh.harvard.edu.
¹⁷ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Center for Clinical Spectroscopy, Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; VA Boston Healthcare System, Brockton Division, Brockton, MA, USA. Electronic address: Shenton@bwh.harvard.edu.
¹⁸ Psychiatry Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Child and Adolescent Psychiatry, Psychosomatic and Psychotherapy, Ludwig-Maximilians-Universität, Munich, Germany; Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA. Electronic address: Ikoerte@bwh.harvard.edu.

PMID: 29204342
PMCID: PMC5709295
DOI: 10.1016/j.nicl.2017.11.020

Abstract

Objective: Repetitive subconcussive head impacts (RSHI) may lead to structural, functional, and metabolic alterations of the brain. While differences between males and females have already been suggested following a concussion, whether there are sex differences following exposure to RSHI remains unknown. The aim of this study was to identify and to characterize sex differences following exposure to RSHI.

Methods: Twenty-five collegiate ice hockey players (14 males and 11 females, 20.6 ± 2.0 years), all part of the Hockey Concussion Education Project (HCEP), underwent diffusion-weighted magnetic resonance imaging (dMRI) before and after the Canadian Interuniversity Sports (CIS) ice hockey season 2011-2012 and did not experience a concussion during the season. Whole-brain tract-based spatial statistics (TBSS) were used to compare pre- and postseason imaging in both sexes for fractional anisotropy (FA), mean diffusivity (MD), axial diffusivity (AD), and radial diffusivity (RD). Pre- and postseason neurocognitive performance were assessed by the Immediate Post-Concussion Assessment and Cognitive Test (ImPACT).

Results: Significant differences between the sexes were primarily located within the superior longitudinal fasciculus (SLF), the internal capsule (IC), and the corona radiata (CR) of the right hemisphere (RH). In significant voxel clusters (p < 0.05), decreases in FA (absolute difference pre- vs. postseason: 0.0268) and increases in MD (0.0002), AD (0.00008), and RD (0.00005) were observed in females whereas males showed no significant changes. There was no significant correlation between the change in diffusion scalar measures over the course of the season and neurocognitive performance as evidenced from postseason ImPACT scores.

Conclusions: The results of this study suggest sex differences in structural alterations following exposure to RSHI. Future studies need to investigate further the underlying mechanisms and association with exposure and clinical outcomes.

Keywords: AD, axial diffusivity; CIS, Canadian Interuniversity Sports; CR, corona radiata; Diffusion tensor imaging; EC, external capsule; FA, fractional anisotropy; HCEP, Hockey Concussion Education Project; IC, internal capsule; Ice hockey; ImPACT, Immediate Post-Concussion Assessment and Cognitive Test; LH, left hemisphere; MD, mean diffusivity; MRI, magnetic resonance imaging; NCAA, National Collegiate Athletic Association; RD, radial diffusivity; RH, right hemisphere; RSHI, repetitive subconcussive head impacts; Repetitive subconcussive head impacts; SD, standard deviation; SLF, superior longitudinal fasciculus; Sex difference; TBI, traumatic brain injury; TBSS, tract-based spatial statistics; Traumatic brain injury; WM, white matter; White matter; dMRI, diffusion magnetic resonance imaging; rs, Spearman's rank correlation coefficient.

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Figures

**Fig. 1**
Results of the tract-based spatial statistics (TBSS) analysis I. This figure illustrates the results of the TBSS analysis (axial view). Voxel clusters with statistically significant differences (p < 0.05) in change over time (postseason minus preseason data sets) between male and female participants are highlighted in red to yellow. The TBSS analysis was carried out for fractional anisotropy (FA), mean diffusivity (MD), axial diffusivity (AD), and radial diffusivity (RD). Voxels of the statistically significant clusters are thickened into local tracts on a standardized FA skeleton (FMRIB58_FA-skeleton; green) and a standardized diffusion-weighted image (FMRIB58_FA). The left side in each image corresponds to the right hemisphere (RH). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

**Fig. 2**
Results of the tract-based spatial statistics (TBSS) analysis II. This figure depicts scatter plots of average values in the voxel clusters with statistically significant group differences (p < 0.05; Fig. 1) for fractional anisotropy (FA), mean diffusivity (MD), axial diffusivity (AD), and radial diffusivity (RD). The values are shown for males vs. females and pre- vs. postseason data, respectively. Circles or triangles represent individual values, whereas horizontal bars represent the median and interquartile range. There was a statistically significant difference between pre- and postseason FA, MD, AD, and RD in female participants (p < 0.05). In contrast, no statistically significant changes were observed in males over the course of one season with respect to FA, MD, AD, and RD (p > 0.05).

See this image and copyright information in PMC

References

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Sex differences in white matter alterations following repetitive subconcussive head impacts in collegiate ice hockey players

Affiliations

Sex differences in white matter alterations following repetitive subconcussive head impacts in collegiate ice hockey players

Authors

Affiliations

Abstract

Figures

References

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources

Medical

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