White matter alterations in college football players: a longitudinal diffusion tensor imaging study
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The aim of this study was to evaluate longitudinal changes in the diffusion characteristics of brain white matter (WM) in collegiate athletes at three time points: prior to the start of the football season (T1), after one season of football (T2), followed by six months of no-contact rest (T3). Fifteen male collegiate football players and 5 male non-athlete student controls underwent diffusion MR imaging and computerized cognitive testing at all three timepoints. Whole-brain tract-based spatial statistics (TBSS) were used to compare fractional anisotropy (FA), radial diffusivity (RD), axial diffusivity (AD), and trace between all timepoints. Average diffusion values were obtained from statistically significant clusters for each individual. No athlete suffered a concussion during the study period. After one season of play (T1 to T2), we observed a significant increase in trace in a cluster located in the brainstem and left temporal lobe, and a significant increase in FA in the left parietal lobe. After six months of no-contact rest (T2 to T3), there was a significant decrease in trace and FA in clusters that were partially overlapping or in close proximity with the initial clusters (T1 to T2), with no significant changes from T1 to T3. Repetitive head impacts (RHI) sustained during a single football season may result in alterations of the brain’s WM in collegiate football players. These changes appear to return to baseline after 6 months of no-contact rest, suggesting remission of WM alterations. Our preliminary results suggest that collegiate football players might benefit from periods without exposure to RHI.
Key wordsTBSS Diffusion tensor imaging White matter Longitudinal High magnitude impact Sports Athletics Subconcussive head trauma Human studies Football Repetitive head impacts Fractional anisotropy
Inga Koerte was supported by the Else Kröner-Fresenius Stiftung, Germany. Michael Mayinger was supported by the Petraeic Legate Foundation. This work was part of the doctoral thesis of Michael Mayinger. This study was supported by funds from the National Football League Charities.
Compliance with ethical standards
This study was funded in part by the National Football League Charities.
Conflict of interest
Author Mayinger declares that he has no conflict of interest. Author Merchant-Borna declares that he has no conflict of interest. Author Hufschmidt declares that he has no conflict of interest. Author Muehlmann declares that he has no conflict of interest. Author Weir declares that she has no conflict of interest. Author Rauchmann declares that he has no conflict of interest. Author Shenton declares that she has no conflict of interest. Author Koerte declares that she has no conflict of interest. Author Bazarian declares that he has no conflict of interest.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent was obtained from all individual participants included in the study.
- Bouix, S., Pasternak, O., Rathi, Y., Pelavin, P. E., Zafonte, R., & Shenton, M. E. (2013). Increased gray matter diffusion anisotropy in patients with persistent post-concussive symptoms following mild traumatic brain injury. PloS One, 8(6), e66205. doi: 10.1371/journal.pone.0066205.CrossRefPubMedPubMedCentralGoogle Scholar
- Budde, M. D., Xie, M., Cross, A. H., & Song, S. K. (2009). Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: a quantitative pixelwise analysis. The Journal of Neuroscience, 29(9), 2805–2813. doi: 10.1523/JNEUROSCI.4605-08.2009.CrossRefPubMedPubMedCentralGoogle Scholar
- Budde, M. D., Janes, L., Gold, E., Turtzo, L. C., & Frank, J. A. (2011). 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(Pt 8), 2248–2260. doi: 10.1093/brain/awr161.CrossRefPubMedPubMedCentralGoogle Scholar
- Chappell, M. H., Ulug, A. M., Zhang, L., Heitger, M. H., Jordan, B. D., Zimmerman, R. D., & Watts, R. (2006). Distribution of microstructural damage in the brains of professional boxers: a diffusion MRI study. Journal of Magnetic Resonance Imaging, 24(3), 537–542. doi: 10.1002/jmri.20656.CrossRefPubMedGoogle Scholar
- Darquie, A., Poline, J. B., Poupon, C., Saint-Jalmes, H., & Le Bihan, D. (2001). Transient decrease in water diffusion observed in human occipital cortex during visual stimulation. Proceedings of the National Academy of Sciences of the United States of America, 98(16), 9391–9395. doi: 10.1073/pnas.151125698.CrossRefPubMedPubMedCentralGoogle Scholar
- Fedorov, A., Beichel, R., Kalpathy-Cramer, J., Finet, J., Fillion-Robin, J. C., Pujol, S., et al. (2012). 3D slicer as an image computing platform for the quantitative imaging network. Magnetic Resonance Imaging, 30(9), 1323–1341. doi: 10.1016/j.mri.2012.05.001.CrossRefPubMedPubMedCentralGoogle Scholar
- Gale, S. D., Baxter, L., Roundy, N., & Johnson, S. C. (2005). Traumatic brain injury and grey matter concentration: a preliminary voxel based morphometry study. Journal of Neurology, Neurosurgery, and Psychiatry, 76(7), 984–988. doi: 10.1136/jnnp.2004.036210.CrossRefPubMedPubMedCentralGoogle Scholar
- Gurdjian, E. S., Lissner, H. R., Evans, F. G., Patrick, L. M., & Hardy, W. G. (1961). Intracranial pressure and acceleration accompanying head impacts in human cadavers. Surgery, Gynecology & Obstetrics, 113, 185–190.Google Scholar
- Hart Jr., J., Kraut, M. A., Womack, K. B., Strain, J., Didehbani, N., Bartz, E., et al. (2013). Neuroimaging of cognitive dysfunction and depression in aging retired National Football League players: a cross-sectional study. JAMA Neurology, 70(3), 326–335. doi: 10.1001/2013.jamaneurol.340.CrossRefPubMedPubMedCentralGoogle Scholar
- Iverson, G. L., Hakulinen, U., Waljas, M., Dastidar, P., Lange, R. T., Soimakallio, S., & Ohman, J. (2011). To exclude or not to exclude: white matter hyperintensities in diffusion tensor imaging research. Brain Injury, 25(13–14), 1325–1332. doi: 10.3109/02699052.2011.608409.CrossRefPubMedGoogle Scholar
- Koerte, I. K., Kaufmann, D., Hartl, E., Bouix, S., Pasternak, O., Kubicki, M., et al. (2012b). A prospective study of physician-observed concussion during a varsity university hockey season: white matter integrity in ice hockey players. Part 3 of 4. Neurosurgical Focus, 33(6) E3, 1–7. doi: 10.3171/2012.10.FOCUS12303.CrossRefGoogle Scholar
- Koerte, I. K., Lin, A. P., Muehlmann, M., Merugumala, S., Liao, H., Starr, T., et al. (2015a). Altered neurochemistry in former professional soccer players without a history of concussion. Journal of Neurotrauma, 32(17), 1287–1293. doi: 10.1089/neu.2014.3715.CrossRefPubMedPubMedCentralGoogle Scholar
- Li, X., Chen, J., Hong, G., Sun, C., Wu, X., Peng, M. J., & Zeng, G. (2013). In vivo DTI longitudinal measurements of acute sciatic nerve traction injury and the association with pathological and functional changes. European Journal of Radiology, 82(11), e707–e714. doi: 10.1016/j.ejrad.2013.07.018.CrossRefPubMedGoogle Scholar
- Luker, R. (2011). Fan base complexity sets up intense competition for attention. sportsbuisnessdaily, 14(11).Google Scholar
- Mac Donald, C. L., Dikranian, K., Bayly, P., Holtzman, D., & Brody, D. (2007). Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. The Journal of Neuroscience, 27(44), 11869–11876. doi: 10.1523/JNEUROSCI.3647-07.2007.CrossRefPubMedPubMedCentralGoogle Scholar
- Matsushita, M., Hosoda, K., Naitoh, Y., Yamashita, H., & Kohmura, E. (2011). 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. Journal of Neurosurgery, 115(1), 130–139. doi: 10.3171/2011.2.JNS101547.CrossRefPubMedGoogle Scholar
- McAllister, T. W., Flashman, L. A., Maerlender, A., Greenwald, R. M., Beckwith, J. G., Tosteson, T. D., et al. (2012). Cognitive effects of one season of head impacts in a cohort of collegiate contact sport athletes. Neurology, 78(22), 1777–1784. doi: 10.1212/WNL.0b013e3182582fe7.CrossRefPubMedPubMedCentralGoogle Scholar
- McAllister, T. W., Ford, J. C., Flashman, L. A., Maerlender, A., Greenwald, R. M., Beckwith, J. G., et al. (2014). Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes. Neurology, 82(1), 63–69. doi: 10.1212/01.wnl.0000438220.16190.42.CrossRefPubMedPubMedCentralGoogle Scholar
- McCrory, P., Meeuwisse, W., Johnston, K., Dvorak, J., Aubry, M., Molloy, M., & Cantu, R. (2009). Consensus statement on concussion in sport - the 3rd international conference on concussion in sport held in Zurich, November 2008. PM R, 1(5), 406–420. doi: 10.1016/j.pmrj.2009.03.010.CrossRefPubMedGoogle Scholar
- McKee, A. C., Cantu, R. C., Nowinski, C. J., Hedley-Whyte, E. T., Gavett, B. E., Budson, A. E., et al. (2009). Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. Journal of Neuropathology and Experimental Neurology, 68(7), 709–735. doi: 10.1097/NEN.0b013e3181a9d503.CrossRefPubMedPubMedCentralGoogle Scholar
- Messe, A., Caplain, S., Paradot, G., Garrigue, D., Mineo, J. F., Soto Ares, G., et al. (2011). Diffusion tensor imaging and white matter lesions at the subacute stage in mild traumatic brain injury with persistent neurobehavioral impairment. Human Brain Mapping, 32(6), 999–1011. doi: 10.1002/hbm.21092.CrossRefPubMedGoogle Scholar
- Nakayama, N., Okumura, A., Shinoda, J., Yasokawa, Y. T., Miwa, K., Yoshimura, S. I., & Iwama, T. (2006). Evidence for white matter disruption in traumatic brain injury without macroscopic lesions. Journal of Neurology, Neurosurgery, and Psychiatry, 77(7), 850–855. doi: 10.1136/jnnp.2005.077875.CrossRefPubMedPubMedCentralGoogle Scholar
- Reeves, A. G. (1981). Disorders of the nervous system : A primer. Chicago, Ill: Year Book Medical Publishers.Google Scholar
- Shenton, M. E., Hamoda, H. M., Schneiderman, J. S., Bouix, S., Pasternak, O., Rathi, Y., et al. (2012). A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging and Behavior, 6(2), 137–192. doi: 10.1007/s11682-012-9156-5.CrossRefPubMedPubMedCentralGoogle Scholar
- Shin, W., Mahmoud, S. Y., Sakaie, K., Banks, S. J., Lowe, M. J., Phillips, M., et al. (2014). Diffusion measures indicate fight exposure-related damage to cerebral white matter in boxers and mixed martial arts fighters. AJNR. American Journal of Neuroradiology, 35(2), 285–290. doi: 10.3174/ajnr.A3676.CrossRefPubMedGoogle Scholar
- U.S.-Census-Bureau. (2009). Participation in Selected Sports Activities:. census.gov.
- Wilde, E. A., Ramos, M. A., Yallampalli, R., Bigler, E. D., McCauley, S. R., Chu, Z., et al. (2010). Diffusion tensor imaging of the cingulum bundle in children after traumatic brain injury. Developmental Neuropsychology, 35(3), 333–351. doi: 10.1080/87565641003696940.CrossRefPubMedPubMedCentralGoogle Scholar
- Zhang, K., Johnson, B., Pennell, D., Ray, W., Sebastianelli, W., & Slobounov, S. (2010). Are functional deficits in concussed individuals consistent with white matter structural alterations: combined FMRI & DTI study. Experimental Brain Research, 204(1), 57–70. doi: 10.1007/s00221-010-2294-3.CrossRefPubMedPubMedCentralGoogle Scholar