Subconcussive Head Impact Exposure and White Matter Tract Changes over a Single Season of Youth Football
Abstract
Our study adds to the growing body of evidence that a season of play in a contact sport can result in brain MR imaging changes, even in the absence of concussion.
Purpose
To examine the effects of subconcussive impacts resulting from a single season of youth (age range, 8–13 years) football on changes in specific white matter (WM) tracts as detected with diffusion-tensor imaging in the absence of clinically diagnosed concussions.
Materials and Methods
Head impact data were recorded by using the Head Impact Telemetry system and quantified as the combined-probability risk-weighted cumulative exposure (RWECP). Twenty-five male participants were evaluated for seasonal fractional anisotropy (FA) changes in specific WM tracts: the inferior fronto-occipital fasciculus (IFOF), inferior longitudinal fasciculus, and superior longitudinal fasciculus (SLF). Fiber tracts were segmented into a central core and two fiber terminals. The relationship between seasonal FA change in the whole fiber, central core, and the fiber terminals with RWECP was also investigated. Linear regression analysis was conducted to determine the association between RWECP and change in fiber tract FA during the season.
Results
There were statistically significant linear relationships between RWEcp and decreased FA in the whole (R2 = 0.433; P = .003), core (R2 = 0.3649; P = .007), and terminals (R2 = 0.5666; P < .001) of left IFOF. A trend toward statistical significance (P = .08) in right SLF was observed. A statistically significant correlation between decrease in FA of the right SLF terminal and RWECP was also observed (R2 = 0.2893; P = .028).
Conclusion
This study found a statistically significant relationship between head impact exposure and change of FA value of whole, core, and terminals of left IFOF and right SLF’s terminals where WM and gray matter intersect, in the absence of a clinically diagnosed concussion.
© RSNA, 2016
References
- 1. . The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil 2006;21(5):375–378. Crossref, Medline, Google Scholar
- 2. . Youth sports & public health: framing risks of mild traumatic brain injury in american football and ice hockey. J Law Med Ethics 2014;42(3):323–333. Crossref, Medline, Google Scholar
- 3. Nonfatal Traumatic Brain Injuries Related to Sports and Recreation Activities Among Persons Aged ≤19 Years—United States, 2001–2009. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6039a1.htm. Accessed February 3, 2015. Google Scholar
- 4. . Incidence of sports-related concussion among youth football players aged 8-12 years. J Pediatr 2013;163(3):717–720. Crossref, Medline, Google Scholar
- 5. . Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004;23(Suppl 1):S208–S219. Crossref, Medline, Google Scholar
- 6. . Post-concussion cognitive declines and symptomatology are not related to concussion biomechanics in high school football players. J Neurotrauma 2011;28(10):2061–2068. Crossref, Medline, Google Scholar
- 7. . Timing of concussion diagnosis is related to head impact exposure prior to injury. Med Sci Sports Exerc 2013;45(4):747–754. Crossref, Medline, Google Scholar
- 8. . Diffusion tensor imaging and magnetic resonance spectroscopy in traumatic brain injury: a review of recent literature. Brain Imaging Behav 2014;8(4):487–496. Crossref, Medline, Google Scholar
- 9. . Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes. Neurology 2014;82(1):63–69. Crossref, Medline, Google Scholar
- 10. . A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 2010;74(8):643–650. Crossref, Medline, Google Scholar
- 11. . Diffusion tensor imaging of traumatic brain injury review: implications for neurorehabilitation. NeuroRehabilitation 2012;31(3):281–293. Crossref, Medline, Google Scholar
- 12. . Combining whole-brain voxel-wise analysis with in vivo tractography of diffusion behavior after sports-related concussion in adolescents: a preliminary report. J Neurotrauma 2013;30(14):1243–1249. Crossref, Medline, Google Scholar
- 13. . Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: a pilot study. J Neurotrauma 2007;24(9):1447–1459. Crossref, Medline, Google Scholar
- 14. . Subconcussive head impact biomechanics: comparing differing offensive schemes. Med Sci Sports Exerc 2013;45(4):755–761. Crossref, Medline, Google Scholar
- 15. . Head impact exposure in youth football: elementary school ages 9-12 years and the effect of practice structure. Ann Biomed Eng 2013;41(12):2463–2473. Crossref, Medline, Google Scholar
- 16. . Validation of concussion risk curves for collegiate football players derived from HITS data. Ann Biomed Eng 2012;40(1):79–89. Crossref, Medline, Google Scholar
- 17. . Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: a 3T diffusion tensor imaging study of mild traumatic brain injury. AJNR Am J Neuroradiol 2008;29(5):967–973. Crossref, Medline, Google Scholar
- 18. . Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage 2008;42(2):503–514. Crossref, Medline, Google Scholar
- 19. . Neurometabolic and microstructural alterations following a sports-related concussion in female athletes. Brain Inj 2013;27(9):1038–1046. Crossref, Medline, Google Scholar
- 20. . Neuroimaging changes in the brain in contact versus noncontact sport athletes using diffusion tensor imaging. World Neurosurg 2013;80(6):824–828. Crossref, Medline, Google Scholar
- 21. . White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain 2007;130(Pt 10):2508–2519. Crossref, Medline, Google Scholar
- 22. . The neurobiology of childhood structural brain development: conception through adulthood. Curr Top Behav Neurosci 2014;16:3–17. Crossref, Medline, Google Scholar
- 23. . Morphometric study of human cerebral cortex development. Neuropsychologia 1990;28(6):517–527. Crossref, Medline, Google Scholar
- 24. . Correlation of white matter diffusivity and anisotropy with age during childhood and adolescence: a cross-sectional diffusion-tensor MR imaging study. Radiology 2002;222(1):212–218. Link, Google Scholar
- 25. . White matter structure in autism: preliminary evidence from diffusion tensor imaging. Biol Psychiatry 2004;55(3):323–326. Crossref, Medline, Google Scholar
- 26. . White matter development during late adolescence in healthy males: a cross-sectional diffusion tensor imaging study. Neuroimage 2007;35(2):501–510. Crossref, Medline, Google Scholar
- 27. . White matter development in adolescence: a DTI study. Cereb Cortex 2010;20(9):2122–2131. Crossref, Medline, Google Scholar
- 28. . Longitudinal changes in grey and white matter during adolescence. Neuroimage 2010;49(1):94–103. Crossref, Medline, Google Scholar
- 29. . Quantitative diffusion tensor tractography of association and projection fibers in normally developing children and adolescents. Cereb Cortex 2007;17(12):2760–2768. Crossref, Medline, Google Scholar
- 30. . The anatomy of the callosal and visual-association pathways in high-functioning autism: a DTI tractography study. Cortex 2011;47(7):863–873. Crossref, Medline, Google Scholar
- 31. . White matter development in adolescence: diffusion tensor imaging and meta-analytic results. Schizophr Bull 2012;38(6):1308–1317. Crossref, Medline, Google Scholar
- 32. . Prospective clinical assessment using Sideline Concussion Assessment Tool-2 testing in the evaluation of sport-related concussion in college athletes. Clin J Sport Med 2015;25(1):36–42. Crossref, Medline, Google Scholar
- 33. . Head impact exposure in youth football: high school ages 14 to 18 years and cumulative impact analysis. Ann Biomed Eng 2013;41(12):2474–2487. Crossref, Medline, Google Scholar
- 34. . Abnormal white matter integrity related to head impact exposure in a season of high school varsity football. J Neurotrauma 2014;31(19):1617–1624 . Crossref, Medline, Google Scholar
- 35. . An algorithm for estimating acceleration magnitude and impact location using multiple nonorthogonal single-axis accelerometers. J Biomech Eng 2004;126(6):849–854. Crossref, Medline, Google Scholar
- 36. . Development of the STAR evaluation system for football helmets: integrating player head impact exposure and risk of concussion. Ann Biomed Eng 2011;39(8):2130–2140. Crossref, Medline, Google Scholar
- 37. . Brain injury prediction: assessing the combined probability of concussion using linear and rotational head acceleration. Ann Biomed Eng 2013;41(5):873–882. Crossref, Medline, Google Scholar
- 38. . Tract profiles of white matter properties: automating fiber-tract quantification. PLoS One 2012;7(11):e49790. Crossref, Medline, Google Scholar
- 39. . Diffusion tensor imaging and white matter lesions at the subacute stage in mild traumatic brain injury with persistent neurobehavioral impairment. Hum Brain Mapp 2011;32(6):999–1011. Crossref, Medline, Google Scholar
- 40. . Diffusion tractography based group mapping of major white-matter pathways in the human brain. Neuroimage 2003;19(4):1545–1555. Crossref, Medline, Google Scholar
- 41. . Linking white matter tracts to associated cortical grey matter: a tract extension methodology. Neuroimage 2012;59(4):3094–3102. Crossref, Medline, Google Scholar
- 42. . Temporal lobe association fiber tractography as compared to histology and dissection. Surg Radiol Anat 2011;33(8):713–722. Crossref, Medline, Google Scholar
- 43. . The Mahalanobis distance. Chemometr Intell Lab Syst 2000;50(1):1–18. Crossref, Google Scholar
- 44. . Diffusion tensor MR imaging reveals persistent white matter alteration after traumatic brain injury experienced during early childhood. AJNR Am J Neuroradiol 2007;28(10):1919–1925. Crossref, Medline, Google Scholar
- 45. . A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. J Neurotrauma 2011;28(2):189–201. Crossref, Medline, Google Scholar
- 46. . White matter integrity in the brains of professional soccer players without a symptomatic concussion. JAMA 2012;308(18):1859–1861. Crossref, Medline, Google Scholar
- 47. . A longitudinal diffusion tensor imaging study assessing white matter fiber tracts after sports-related concussion. J Neurotrauma 2014;31(22):1860–1871. Crossref, Medline, Google Scholar
- 48. . Mechanical properties of gray and white matter brain tissue by indentation. J Mech Behav Biomed Mater 2015;46:318–330. Crossref, Medline, Google Scholar
- 49. . Developmental features of the neonatal brain: MR imaging. Part I. Gray-white matter differentiation and myelination. Radiology 1987;162(1 Pt 1):223–229. Link, Google Scholar
- 50. . Mechanical difference between white and gray matter in the rat cerebellum measured by scanning force microscopy. J Biomech 2010;43(15):2986–2992. Crossref, Medline, Google Scholar
- 51. . Diffuse axonal injury after traumatic cerebral microbleeds: an evaluation of imaging techniques. Neural Regen Res 2014;9(12):1222–1230. Crossref, Medline, Google Scholar
- 52. . Blast-associated shock waves result in increased brain vascular leakage and elevated ROS levels in a rat model of traumatic brain injury. PLoS One 2015;10(5):e0127971. Crossref, Medline, Google Scholar
- 53. . Markov random field segmentation of brain MR images. IEEE Trans Med Imaging 1997;16(6):878–886. Crossref, Medline, Google Scholar
Article History
Received March 17, 2016; revision requested April 26; revision received July 8; accepted July 25; final version accepted August 25.Published online: Oct 24 2016
Published in print: Dec 2016