Hockey Concussion Education Project, Part 3. White matter microstructure in ice hockey players with a history of concussion: a diffusion tensor imaging study

Clinical article

View More View Less
  • 1 Psychiatry Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital/Harvard Medical School, Boston, Massachusetts;
  • 2 Department of Psychiatry and Behavioral Sciences, Tokyo Medical and Dental University Graduate School, Tokyo, Japan;
  • 3 Institute for Clinical Radiology, Ludwig-Maximilians-University, Munich, Germany;
  • 4 Department of Radiology, Brigham and Women's Hospital/Harvard Medical School, Boston;
  • 5 Massachusetts General Hospital/Massachusetts Institute of Technology/Harvard Medical School/Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, Massachusetts;
  • 6 School of Health Studies;
  • 7 School of Occupational Therapy;
  • 8 Fowler Kennedy Sport Medicine Clinic; and
  • 9 School of Physical Therapy, The University of Western Ontario, London, Ontario;
  • 10 Ruth Lilly Medical Library, Indiana University, Indianapolis, Indiana;
  • 11 VA Boston Healthcare System, Brockton, Massachusetts; and
  • 12 The Elliott Sports Medicine Clinic, Burlington, Ontario, Canada
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

Object

The aim of this study was to examine the brain's white matter microstructure by using MR diffusion tensor imaging (DTI) in ice hockey players with a history of clinically symptomatic concussion compared with players without a history of concussion.

Methods

Sixteen players with a history of concussion (concussed group; mean age 21.7 ± 1.5 years; 6 female) and 18 players without a history of concussion (nonconcussed group; mean age 21.3 ± 1.8 years, 10 female) underwent 3-T DTI at the end of the 2011–2012 Canadian Interuniversity Sports ice hockey season. Tract-based spatial statistics (TBSS) was used to test for group differences in fractional anisotropy (FA), axial diffusivity (AD), radial diffusivity (RD), and the measure “trace,” or mean diffusivity. Cognitive evaluation was performed using the Immediate Postconcussion Assessment and Cognitive Test (ImPACT) and the Sport Concussion Assessment Tool–2 (SCAT2).

Results

TBSS revealed a significant increase in FA and AD, and a significant decrease in RD and trace in several brain regions in the concussed group, compared with the nonconcussed group (p < 0.05). The regions with increased FA and decreased RD and trace included the right posterior limb of the internal capsule, the right corona radiata, and the right temporal lobe. Increased AD was observed in a small area in the left corona radiata. The DTI measures correlated with neither the ImPACT nor the SCAT2 scores.

Conclusions

The results of the current study indicate that a history of concussion may result in alterations of the brain's white matter microstructure in ice hockey players. Increased FA based on decreased RD may reflect neuroinflammatory or neuroplastic processes of the brain responding to brain trauma. Future studies are needed that include a longitudinal analysis of the brain's structure and function following a concussion to elucidate further the complex time course of DTI changes and their clinical meaning.

Abbreviations used in this paper:AD = axial diffusivity; CIS = Canadian Interuniversity Sports; DTI = diffusion tensor imaging; FA = fractional anisotropy; HCEP = Hockey Concussion Education Project; ImPACT = Immediate Postconcussion Assessment and Cognitive Test; mTBI = mild traumatic brain injury; RD = radial diffusivity; SCAT2 = Sport Concussion Assessment Tool–2; SHB = subconcussive head blow; TBSS = tract-based spatial statistics.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Drs. Echlin and Koerte share senior authorship of this work.

Address correspondence to: Paul S. Echlin, M.D., Elliott Sports Medicine Clinic, 1100 Walkers Line, Ste. 2, Burlington, ON, Canada L7N 2G3. email: psechlin@gmail.com.

Please include this information when citing this paper: published online February 4, 2014; DOI: 10.3171/2013.12.JNS132092.

  • 1

    Agel J, & Harvey EJ: A 7-year review of men's and women's ice hockey injuries in the NCAA. Can J Surg 53:319323, 2010

  • 2

    Arfanakis K, , Haughton VM, , Carew JD, , Rogers BP, , Dempsey RJ, & Meyerand ME: Diffusion tensor MR imaging in diffuse axonal injury. AJNR Am J Neuroradiol 23:794802, 2002

    • Search Google Scholar
    • Export Citation
  • 3

    Bazarian JJ, , Zhu T, , Blyth B, , Borrino A, & Zhong J: Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion. Magn Reson Imaging 30:171180, 2012

    • Search Google Scholar
    • Export Citation
  • 4

    Budde MD, , Janes L, , Gold E, , Turtzo LC, & Frank JA: The contribution of gliosis to diffusion tensor anisotropy and tractography following traumatic brain injury: validation in the rat using Fourier analysis of stained tissue sections. Brain 134:22482260, 2011

    • Search Google Scholar
    • Export Citation
  • 5

    Chappell MH, , Brown JA, , Dalrymple-Alford JC, , Uluğ AM, & Watts R: Multivariate analysis of diffusion tensor imaging data improves the detection of microstructural damage in young professional boxers. Magn Reson Imaging 26:13981405, 2008

    • Search Google Scholar
    • Export Citation
  • 6

    Chappell MH, , Uluğ AM, , Zhang L, , Heitger MH, , Jordan BD, & Zimmerman RD, : Distribution of microstructural damage in the brains of professional boxers: a diffusion MRI study. J Magn Reson Imaging 24:537542, 2006

    • Search Google Scholar
    • Export Citation
  • 7

    Cubon VA, , Putukian M, , Boyer C, & Dettwiler A: A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. J Neurotrauma 28:189201, 2011

    • Search Google Scholar
    • Export Citation
  • 8

    Donaldson L, , Asbridge M, & Cusimano MD: Bodychecking rules and concussion in elite hockey. PLoS ONE 8:e69122, 2013

  • 9

    Echlin PS: A prospective study of physician-observed concussion during a varsity university ice hockey season. Part 1 of 4. Neurosurg Focus 33:6 E1, 2012

    • Search Google Scholar
    • Export Citation
  • 10

    Echlin PS, , Skopelja EN, , Worsley R, , Dadachanji SB, , Lloyd-Smith DR, & Taunton JA, : A prospective study of physician-observed concussion during a varsity university ice hockey season: incidence and neuropsychological changes. Part 2 of 4. Neurosurg Focus 33:6 E2, 2012

    • Search Google Scholar
    • Export Citation
  • 11

    Echlin PS, , Tator CH, , Cusimano MD, , Cantu RC, , Taunton JE, & Upshur RE, : A prospective study of physician-observed concussions during junior ice hockey: implications for incidence rates. Neurosurg Focus 29:5 E4, 2010

    • Search Google Scholar
    • Export Citation
  • 12

    Faul M, , Xu L, , Wald MM, & Coronado VG: Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations, and Deaths, 2002–2006 Atlanta, Centers for Disease Control and Prevention, 2010

    • Search Google Scholar
    • Export Citation
  • 13

    Gentleman SM, , Leclercq PD, , Moyes L, , Graham DI, , Smith C, & Griffin WS, : Long-term intracerebral inflammatory response after traumatic brain injury. Forensic Sci Int 146:97104, 2004

    • Search Google Scholar
    • Export Citation
  • 14

    Guskiewicz KM, , Register-Mihalik J, , McCrory P, , McCrea M, , Johnston K, & Makdissi M, : Evidence-based approach to revising the SCAT2: introducing the SCAT3. Br J Sports Med 47:289293, 2013

    • Search Google Scholar
    • Export Citation
  • 15

    Harmon KG, , Drezner JA, , Gammons M, , Guskiewicz KM, , Halstead M, & Herring SA, : American Medical Society for Sports Medicine position statement: concussion in sport. Br J Sports Med 47:1526, 2013

    • Search Google Scholar
    • Export Citation
  • 16

    Hart J Jr, , Kraut MA, , Womack KB, , Strain J, , Didehbani N, & Bartz E, : Neuroimaging of cognitive dysfunction and depression in aging retired National Football League players: a cross-sectional study. JAMA Neurol 70:326335, 2013

    • Search Google Scholar
    • Export Citation
  • 17

    Hartikainen KM, , Waljas M, , Isoviita T, , Dastidar P, , Liimatainen S, & Solbakk AK, : Persistent symptoms in mild to moderate traumatic brain injury associated with executive dysfunction. J Clin Exp Neuropsychol 32:767774, 2010

    • Search Google Scholar
    • Export Citation
  • 18

    Henry LC, , Tremblay J, , Tremblay S, , Lee A, , Brun C, & Lepore N, : Acute and chronic changes in diffusivity measures after sports concussion. J Neurotrauma 28:20492059, 2011

    • Search Google Scholar
    • Export Citation
  • 19

    Inglese M, , Makani S, , Johnson G, , Cohen BA, , Silver JA, & Gonen O, : Diffuse axonal injury in mild traumatic brain injury: a diffusion tensor imaging study. J Neurosurg 103:298303, 2005

    • Search Google Scholar
    • Export Citation
  • 20

    Johnson VE, , Stewart JE, , Begbie FD, , Trojanowski JQ, , Smith DH, & Stewart W: Inflammation and white matter degeneration persist for years after a single traumatic brain injury. Brain 136:2842, 2013

    • Search Google Scholar
    • Export Citation
  • 21

    Kerr ZY, , Marshall SW, & Guskiewicz KM: Reliability of concussion history in former professional football players. Med Sci Sports Exerc 44:377382, 2012

    • Search Google Scholar
    • Export Citation
  • 22

    Koerte IK, , Ertl-Wagner B, , Reiser M, , Zafonte R, & Shenton ME: White matter integrity in the brains of professional soccer players without a symptomatic concussion. JAMA 308:18591861, 2012

    • Search Google Scholar
    • Export Citation
  • 23

    Koerte IK, , Kaufmann D, , Hartl E, , Bouix S, , Pasternak O, & Kubicki M, : A prospective study of physician-observed concussion during a varsity university hockey season: white matter integrity in ice hockey players. Part 3 of 4. Neurosurg Focus 33:6 E3, 2012

    • Search Google Scholar
    • Export Citation
  • 24

    Kraus MF, , Susmaras T, , Caughlin BP, , Walker CJ, , Sweeney JA, & Little DM: White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain 130:25082519, 2007

    • Search Google Scholar
    • Export Citation
  • 25

    Ling JM, , Peña A, , Yeo RA, , Merideth FL, , Klimaj S, & Gasparovic C, : Biomarkers of increased diffusion anisotropy in semi-acute mild traumatic brain injury: a longitudinal perspective. Brain 135:12811292, 2012

    • Search Google Scholar
    • Export Citation
  • 26

    Lipton ML, , Gellella E, , Lo C, , Gold T, , Ardekani BA, & Shifteh K, : Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: a voxelwise analysis of diffusion tensor imaging. J Neurotrauma 25:13351342, 2008

    • Search Google Scholar
    • Export Citation
  • 27

    Lipton ML, , Gulko E, , Zimmerman ME, , Friedman BW, , Kim M, & Gellella E, : Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury. Radiology 252:816824, 2009

    • Search Google Scholar
    • Export Citation
  • 28

    Lipton ML, , Kim N, , Park YK, , Hulkower MB, , Gardin TM, & Shifteh K, : Robust detection of traumatic axonal injury in individual mild traumatic brain injury patients: intersubject variation, change over time and bidirectional changes in anisotropy. Brain Imaging Behav 6:329342, 2012

    • Search Google Scholar
    • Export Citation
  • 29

    Lipton ML, , Kim N, , Zimmerman ME, , Kim M, , Stewart WF, & Branch CA, : Soccer heading is associated with white matter microstructural and cognitive abnormalities. Radiology 268:850857, 2013

    • Search Google Scholar
    • Export Citation
  • 30

    Lo C, , Shifteh K, , Gold T, , Bello JA, & Lipton ML: Diffusion tensor imaging abnormalities in patients with mild traumatic brain injury and neurocognitive impairment. J Comput Assist Tomogr 33:293297, 2009

    • Search Google Scholar
    • Export Citation
  • 31

    Marchi N, , Bazarian JJ, , Puvenna V, , Janigro M, , Ghosh C, & Zhong J, : Consequences of repeated blood-brain barrier disruption in football players. PLoS ONE 8:e56805, 2013

    • Search Google Scholar
    • Export Citation
  • 32

    Matsushita M, , Hosoda K, , Naitoh Y, , Yamashita H, & Kohmura E: Utility of diffusion tensor imaging in the acute stage of mild to moderate traumatic brain injury for detecting white matter lesions and predicting long-term cognitive function in adults. Clinical article. J Neurosurg 115:130139, 2011

    • Search Google Scholar
    • Export Citation
  • 33

    Mayer AR, , Ling J, , Mannell MV, , Gasparovic C, , Phillips JP, & Doezema D, : A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 74:643650, 2010

    • Search Google Scholar
    • Export Citation
  • 34

    McAllister TW, , Flashman LA, , Maerlender A, , Greenwald RM, , Beckwith JG, & Tosteson TD, : Cognitive effects of one season of head impacts in a cohort of collegiate contact sport athletes. Neurology 78:17771784, 2012

    • Search Google Scholar
    • Export Citation
  • 35

    McAllister TW, , Ford JC, , Ji S, , Beckwith JG, , Flashman LA, & Paulsen K, : Maximum principal strain and strain rate associated with concussion diagnosis correlates with changes in corpus callosum white matter indices. Ann Biomed Eng 40:127140, 2012

    • Search Google Scholar
    • Export Citation
  • 36

    McCrea M, , Hammeke T, , Olsen G, , Leo P, & Guskiewicz K: Unreported concussion in high school football players: implications for prevention. Clin J Sport Med 14:1317, 2004

    • Search Google Scholar
    • Export Citation
  • 37

    McCrory P, , Meeuwisse W, , Johnston K, , Dvorak J, , Aubry M, & Molloy M, : Consensus Statement on Concussion in Sport: the 3rd International Conference on Concussion in Sport held in Zurich, November 2008. Br J Sports Med 43:Suppl 1 i76i90, 2009

    • Search Google Scholar
    • Export Citation
  • 38

    McCrory P, , Meeuwisse WH, , Aubry M, , Cantu B, , Dvorák J, & Echemendia RJ, : Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Br J Sports Med 47:250258, 2013

    • Search Google Scholar
    • Export Citation
  • 39

    McCrory P, , Meeuwisse WH, , Kutcher JS, , Jordan BD, & Gardner A: What is the evidence for chronic concussion-related changes in retired athletes: behavioural, pathological and clinical outcomes?. Br J Sports Med 47:327330, 2013

    • Search Google Scholar
    • Export Citation
  • 40

    McKee AC, , Stern RA, , Nowinski CJ, , Stein TD, , Alvarez VE, & Daneshvar DH, : The spectrum of disease in chronic traumatic encephalopathy. Brain 136:4364, 2013

    • Search Google Scholar
    • Export Citation
  • 41

    Miles L, , Grossman RI, , Johnson G, , Babb JS, , Diller L, & Inglese M: Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Inj 22:115122, 2008

    • Search Google Scholar
    • Export Citation
  • 42

    Niogi SN, , Mukherjee P, , Ghajar J, , Johnson CE, , Kolster R, & Lee H, : Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. Brain 131:32093221, 2008

    • Search Google Scholar
    • Export Citation
  • 43

    Pasternak O, , Koerte IK, , Bouix S, , Fredman E, , Sasaki T, & Mayinger M, : Hockey Concussion Education Project, Part 2. Microstructural white matter alterations in acutely concussed ice hockey players: a longitudinal free-water MRI study. Clinical article. J Neurosurg [epub ahead of print February 4, 2014. DOI: 10.3171/2013.12.JNS132090]

    • Search Google Scholar
    • Export Citation
  • 44

    Rishiraj N, , Lloyd-Smith R, , Lorenz T, , Niven B, & Michel M: University men's ice hockey: rates and risk of injuries over 6-years. J Sports Med Phys Fitness 49:159166, 2009

    • Search Google Scholar
    • Export Citation
  • 45

    Seifert TD: Sports concussion and associated post-traumatic headache. Headache 53:726736, 2013

  • 46

    Shenton ME, , Hamoda HM, , Schneiderman JS, , Bouix S, , Pasternak O, & Rathi Y, : A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging Behav 6:137192, 2012

    • Search Google Scholar
    • Export Citation
  • 47

    Smith SM, , Jenkinson M, , Johansen-Berg H, , Rueckert D, , Nichols TE, & Mackay CE, : Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:14871505, 2006

    • Search Google Scholar
    • Export Citation
  • 48

    Song SK, , Sun SW, , Ju WK, , Lin SJ, , Cross AH, & Neufeld AH: Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 20:17141722, 2003

    • Search Google Scholar
    • Export Citation
  • 49

    Thurman DJ, , Branche CM, & Sniezek JE: The epidemiology of sports-related traumatic brain injuries in the United States: recent developments. J Head Trauma Rehabil 13:18, 1998

    • Search Google Scholar
    • Export Citation
  • 50

    Wilde EA, , McCauley SR, , Hunter JV, , Bigler ED, , Chu Z, & Wang ZJ, : Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology 70:948955, 2008

    • Search Google Scholar
    • Export Citation
  • 51

    Zhang L, , Heier LA, , Zimmerman RD, , Jordan B, & Ulug AM: Diffusion anisotropy changes in the brains of professional boxers. AJNR Am J Neuroradiol 27:20002004, 2006

    • Search Google Scholar
    • Export Citation
  • 52

    Zhang L, , Ravdin LD, , Relkin N, , Zimmerman RD, , Jordan B, & Lathan WE, : Increased diffusion in the brain of professional boxers: a preclinical sign of traumatic brain injury?. AJNR Am J Neuroradiol 24:5257, 2003

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 340 340 23
Full Text Views 735 24 0
PDF Downloads 245 13 0
EPUB Downloads 0 0 0