Soccer Heading Is Associated with White Matter Microstructural and Cognitive Abnormalities
Abstract
Our current study results suggest that a nonlinear relationship exists between exposure to heading during the previous year, as measured by the Einstein Heading Questionnaire, and both abnormal white matter microstructure and poorer neurocognitive performance on a memory test.
Purpose
To investigate the association of soccer heading with subclinical evidence of traumatic brain injury.
Materials and Methods
With institutional review board approval and compliance with HIPAA guidelines, 37 amateur soccer players (mean age, 30.9 years; 78% [29] men, 22% [eight] women) gave written informed consent and completed a questionnaire to quantify heading in the prior 12 months and lifetime concussions. Diffusion-tensor magnetic resonance (MR) imaging at 3.0 T was performed (32 directions; b value, 800 sec/mm2; 2 × 2 × 2-mm voxels). Cognitive function was measured by using a computerized battery of tests. Voxelwise linear regression (heading vs fractional anisotropy [FA]) was applied to identify significant regional associations. FA at each location and cognition were tested for a nonlinear relationship to heading by using an inverse logit model that incorporated demographic covariates and history of concussion.
Results
Participants had headed 32–5400 times (median, 432 times) over the previous year. Heading was associated with lower FA at three locations in temporo-occipital white matter with a threshold that varied according to location (885–1550 headings per year) (P < .00001). Lower levels of FA were also associated with poorer memory scores (P < .00001), with a threshold of 1800 headings per year. Lifetime concussion history and demographic features were not significantly associated with either FA or cognitive performance.
Conclusion
Heading is associated with abnormal white matter microstructure and with poorer neurocognitive performance. This relationship is not explained by a history of concussion.
© RSNA, 2013
References
- 1 . Punch drunk. JAMA 1928;91(15):1103–1107. Crossref, Google Scholar
- 2 . Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 2009;68(7):709–735. Crossref, Medline, Google Scholar
- 3 . The neuropsychology of heading and head trauma in Association Football (soccer): a review. Neuropsychol Rev 2003;13(3):153–179. Crossref, Medline, Google Scholar
- 4 . Subconcussive impact in sports: a new era of awareness. World Neurosurg 2011;75(2):175–178. Crossref, Medline, Google Scholar
- 5 . The relationship between subconcussive impacts and concussion history on clinical measures of neurologic function in collegiate football players. Ann Biomed Eng 2012;40(1):14–22. Crossref, Medline, Google Scholar
- 6 . Heading in soccer: dangerous play? Neurosurgery 2012;70(1):1–11; discussion 11. Crossref, Medline, Google Scholar
- 7 , Board on Neuroscience and Behavioral Health. Is soccer bad for children’s heads? summary of the IOM Workshop on Neuropsychological Consequences of Head Impact in Youth Soccer. Washington, DC: National Academies Press, 2002. Google Scholar
- 8 ; American Academy of Pediatrics. Council on Sports Medicine and Fitness. Injuries in youth soccer. Pediatrics 2010;125(2):410–414. Crossref, Medline, Google Scholar
- 9 . Neuropsychological impairment in amateur soccer players. JAMA 1999;282(10):971–973. Crossref, Medline, Google Scholar
- 10 . Chronic traumatic brain injury in professional soccer players. Neurology 1998;51(3):791–796. Crossref, Medline, Google Scholar
- 11 . Neuropsychological impairment as a consequence of football (soccer) play and football heading: a preliminary analysis and report on school students (13-16 years). Child Neuropsychol 2005;11(6):513–526. Crossref, Medline, Google Scholar
- 12 . Traumatic brain injury in high school athletes. JAMA 1999;282(10):958–963. Crossref, Medline, Google Scholar
- 13 . White matter integrity in the brains of professional soccer players without a symptomatic concussion. JAMA 2012;308(18):1859–1861. Crossref, Medline, Google Scholar
- 14 . Diffusion tensor imaging of mild traumatic brain injury. J Head Trauma Rehabil 2010;25(4):241–255. Crossref, Medline, Google Scholar
- 15 . The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 1998;59(suppl 20):22–33; quiz 34–57. Medline, Google Scholar
- 16 . The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971;9(1):97–113. Crossref, Medline, Google Scholar
- 17 . The effects of practice on the cognitive test performance of neurologically normal individuals assessed at brief test-retest intervals. J Int Neuropsychol Soc 2003;9(3):419–428. Crossref, Medline, Google Scholar
- 18 . Validity of the CogState brief battery: relationship to standardized tests and sensitivity to cognitive impairment in mild traumatic brain injury, schizophrenia, and AIDS dementia complex. Arch Clin Neuropsychol 2009;24(2):165–178. Crossref, Medline, Google Scholar
- 19 . Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nat Protoc 2007;2(3):499–503. Crossref, Medline, Google Scholar
- 20 . Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury. Radiology 2009;252(3):816–824. Link, Google Scholar
- 21 . Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 1994;2(4):189–210. Crossref, Google Scholar
- 22 . An R companion to applied regression. 2nd ed. Los Angeles, Calif: Sage, 2011. Google Scholar
- 23 . Mixed-effects models in S and S-PLUS. New York, NY: Springer, 2000. Crossref, Google Scholar
- 24 . Nonlinear mixed effects models for repeated measures data. Biometrics 1990;46(3):673–687. Crossref, Medline, Google Scholar
- 25 . Robust regression using interactively reweighted least-squares. Commun Stat Theory Methods 1977;6(9):813–827. Crossref, Google Scholar
- 26 . Long-term declarative memory deficits in diffuse TBI: correlations with cortical thickness, white matter integrity and hippocampal volume. Cortex 2013;49(3):646–657. Crossref, Medline, Google Scholar
- 27 . Update of neuropathology and neurological recovery after traumatic brain injury. J Head Trauma Rehab 2005;20(1):76–94. Crossref, Medline, Google Scholar
- 28 . Prevention of arm injury in youth baseball pitchers. J La State Med Soc 2008;160(2):95–98. Medline, Google Scholar
Article History
Received March 2, 2013; revision requested April 22; final revision received May 7; accepted May 10; final version accepted May 14.Published online: Sept 2013
Published in print: Sept 2013