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Novel Method of Weighting Cumulative Helmet Impacts Improves Correlation with Brain White Matter Changes After One Football Season of Sub-concussive Head Blows

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Abstract

One football season of sub-concussive head blows has been shown to be associated with subclinical white matter (WM) changes on diffusion tensor imaging (DTI). Prior research analyses of helmet-based impact metrics using mean and peak linear and rotational acceleration showed relatively weak correlations to these WM changes; however, these analyses failed to account for the emerging concept that neuronal vulnerability to successive hits is inversely related to the time between hits (TBH). To develop a novel method for quantifying the cumulative effects of sub-concussive head blows during a single season of collegiate football by weighting helmet-based impact measures for time between helmet impacts. We further aim to compare correlations to changes in DTI after one season of collegiate football using weighted cumulative helmet-based impact measures to correlations using non-weighted cumulative helmet-based impact measures and non-cumulative measures. We performed a secondary analysis of DTI and helmet impact data collected on ten Division III collegiate football players during the 2011 season. All subjects underwent diffusion MR imaging before the start of the football season and within 1 week of the end of the football season. Helmet impacts were recorded at each practice and game using helmet-mounted accelerometers, which computed five helmet-based impact measures for each hit: linear acceleration (LA), rotational acceleration (RA), Gadd Severity Index (GSI), Head Injury Criterion (HIC15), and Head Impact Technology severity profile (HITsp). All helmet-based impact measures were analyzed using five methods of summary: peak and mean (non-cumulative measures), season sum-totals (cumulative unweighted measures), and season sum-totals weighted for time between hits (TBH), the interval of time from hit to post-season DTI assessment (TUA), and both TBH and TUA combined. Summarized helmet-based impact measures were correlated to statistically significant changes in fractional anisotropy (FA) using bivariate and multivariable correlation analyses. The resulting R 2 values were averaged in each of the five summary method groups and compared using one-way ANOVA followed by Tukey post hoc tests for multiple comparisons. Total head hits for the season ranged from 431 to 1850. None of the athletes suffered a clinically evident concussion during the study period. The mean R 2 value for the correlations using cumulative helmet-based impact measures weighted for both TUA and TBH combined (0.51 ± 0.03) was significantly greater than the mean R 2 value for correlations using non-cumulative HIMs (vs. 0.19 ± 0.04, p < 0.0001), unweighted cumulative helmet-based impact measures (vs. 0.27 + 0.03, p < 0.0001), and cumulative helmet-based impact measures weighted for TBH alone (vs. 0.34 ± 0.02, p < 0.001). R 2 values for weighted cumulative helmet-based impact measures ranged from 0.32 to 0.77, with 60% of correlations being statistically significant. Cumulative GSI weighted for TBH and TUA explained 77% of the variance in the percent of white matter voxels with statistically significant (PWMVSS) increase in FA from pre-season to post-season, while both cumulative GSI and cumulative HIC15 weighted for TUA accounted for 75% of the variance in PWMVSS decrease in FA. A novel method for weighting cumulative helmet-based impact measures summed over the course of a football season resulted in a marked improvement in the correlation to brain WM changes observed after a single football season of sub-concussive head blows. Our results lend support to the emerging concept that sub-concussive head blows can result in sub-clinical brain injury, and this may be influenced by the time between hits. If confirmed in an independent data set, our novel method for quantifying the cumulative effects of sub-concussive head blows could be used to develop threshold-based countermeasures to prevent the accumulation of WM changes with multiple seasons of play.

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References

  1. Bailes, J. E., A. L. Petraglia, B. I. Omalu, E. Nauman, and T. Talavage. Role of subconcussion in repetitive mild traumatic brain injury. J. Neurosurg. 119(5):1235–1245, 2013.

    Article  PubMed  Google Scholar 

  2. Bain, A. C., and D. F. Meaney. Tissue-level thresholds for axonal damage in an experimental model of central nervous system white matter injury. J. Biomech. Eng. 122(6):615–622, 2001.

    Article  Google Scholar 

  3. Baugh, C. M., J. M. Stamm, D. O. Riley, et al. Chronic traumatic encephalopathy: neurodegeneration following repetitive concussive and subconcussive brain trauma. Brain Imaging Behav. 6(2):244–254, 2012.

    Article  PubMed  Google Scholar 

  4. Bazarian, J. J. Z. T., J. Zhong, D. Janigro, E. Rozen, A. Roberts, H. Jaiven, K. Merchant-Borna, B. Abar, and E. G. Blackman. Persistent, long-term cerebral white matter changes after sports-related repetitive head impacts. PLoS One 9(4):e94734, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bazarian, J. J., T. Zhu, B. Blyth, A. Borrino, and J. Zhong. Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion. Magn. Reson. Imaging. 30(2):171–180, 2012.

    Article  PubMed  Google Scholar 

  6. Bernick, C., S. J. Banks, W. Shin, et al. Repeated head trauma is associated with smaller thalamic volumes and slower processing speed: the Professional Fighters’ Brain Health Study. Br. J. Sports Med. 49(15):1007–1011, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Breedlove, E. L., M. Robinson, T. M. Talavage, et al. Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football. J. Biomech. 45(7):1265–1272, 2012.

    Article  PubMed  Google Scholar 

  8. Calabrese, E., F. Du, R. H. Garman, et al. Diffusion tensor imaging reveals white matter injury in a rat model of repetitive blast-induced traumatic brain injury. J. Neurotrauma. 31(10):938–950, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Corrigan, J. D., and J. Bogner. Initial reliability and validity of the Ohio State University TBI Identification Method. J. Head Trauma Rehabil. 22(6):318–329, 2007.

    Article  PubMed  Google Scholar 

  10. Dashnaw, M. L., A. L. Petraglia, and J. E. Bailes. An overview of the basic science of concussion and subconcussion: where we are and where we are going. Neurosurg. Focus 33(6):E5, 2012; (1-9).

    Article  PubMed  Google Scholar 

  11. Davenport, E. M. W. C., J. E. Urban, M. A. Espeland, Y. Jung, D. A. Rosenbaum, G. A. Gioia, A. K. Powers, J. D. Stitzel, and J. A. Maldjian. Abnormal white matter integrity related to head impact exposure in a season of high school varsity football. J. Neurotrauma. 31(19):1617–1624, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Dodd, A. B., K. Epstein, J. M. Ling, and A. R. Mayer. Diffusion tensor imaging findings in semi-acute mild traumatic brain injury. J. Neurotrauma. 31(14):1235–1248, 2014.

    Article  PubMed  Google Scholar 

  13. Duma, S. M., and S. Rowson. Re: On the accuracy of the Head Impact Telemetry (HIT) system used in football helmets. J. Biomech. 47(6):1557–1558, 2014.

    Article  PubMed  Google Scholar 

  14. Eckner, J. T., M. Sabin, J. S. Kutcher, and S. P. Broglio. No evidence for a cumulative impact effect on concussion injury threshold. J. Neurotrauma. 28(10):2079–2090, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Effgen, G. W., Gill, E., Morrison, B. A model of repetitive, mild traumatic brain injury and a novel pharmacological intervention to block repetitive injury synergy. In: Proceedings of the 2012 International IRCOBI Conference on the Biomechanics of Injury, 2012, pp. 455–466.

  16. Fujita, M., E. P. Wei, and J. T. Povlishock. Intensity- and interval-specific repetitive traumatic brain injury can evoke both axonal and microvascular damage. J. Neurotrauma. 29(12):2172–2180, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Fujita, M., E. P. Wei, and J. T. Povlishock. Intensity- and interval-specific repetitive traumatic brain injury can evoke both axonal and microvascular damage. J. Neurotrauma. 29(12):2172–2180, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Funk, J. R., S. Rowson, R. W. Daniel, and S. M. Duma. Validation of concussion risk curves for collegiate football players derived from HITS data. Ann. Biomed. Eng. 40(1):79–89, 2012.

    Article  PubMed  Google Scholar 

  19. Gons, R. A. R., A. M. Tuladhar, K. F. de Laat, et al. Physical activity is related to the structural integrity of cerebral white matter. Neurology. 81(11):971–976, 2013.

    Article  PubMed  Google Scholar 

  20. Greenwald, R. M., J. T. Gwin, J. J. Chu, and J. J. Crisco. Head impact severity measures for evaluating mild traumatic brain injury risk exposure. Neurosurgery 62(4):789–798, 2008; (discussion 798).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Jadischke, R., D. C. Viano, N. Dau, A. I. King, and J. McCarthy. On the accuracy of the Head Impact Telemetry (HIT) system used in football helmets. J. Biomech. 46(13):2310–2315, 2013.

    Article  PubMed  Google Scholar 

  22. Killam, C., R. L. Cautin, and A. C. Santucci. Assessing the enduring residual neuropsychological effects of head trauma in college athletes who participate in contact sports. Arch. Clin. Neuropsychol. 20(5):599–611, 2005.

    Article  PubMed  Google Scholar 

  23. Koerte, I. K., B. Ertl-Wagner, M. Reiser, R. Zafonte, and M. E. Shenton. White matter integrity in the brains of professional soccer players without a symptomatic concussion. JAMA. 308(18):1859–1861, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Li, S. S. Y., D. Shan, B. Feng, J. Xing, Y. Duan, J. Dai, H. Lei, and Y. Zhou. Temporal profiles of axonal injury following impact acceleration traumatic brain injury in rats–a comparative study with diffusion tensor imaging and morphological analysis. Int. J. Legal Med. 127(1):159–167, 2013.

    Article  PubMed  Google Scholar 

  25. Lipton, M. L., N. Kim, M. E. Zimmerman, et al. Soccer heading is associated with white matter microstructural and cognitive abnormalities. Radiology 268(3):850–857, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Mac Donald, C. L., K. Dikranian, P. Bayly, D. Holtzman, and D. Brody. Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J. Neurosci. 27(44):11869–11876, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Mac Donald, C. L., K. Dikranian, P. Bayly, D. Holtzman, and D. Brody. Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J. Neurosci. 27(44):11869–11876, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. McAllister, T. W. F. J., L. A. Flashman, A. Maerlender, R. M. Greenwald, J. G. Beckwith, R. P. Bolander, T. D. Tosteson, J. H. Turcl, R. Raman, and S. Jain. Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes. Neurology 2013. doi:10.1212/01.wnl.0000438220.16190.42.

    PubMed  Google Scholar 

  29. McAllister, T. W., L. A. Flashman, A. Maerlender, et al. Cognitive effects of one season of head impacts in a cohort of collegiate contact sport athletes. Neurology 78(22):1777–1784, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Neselius, S., H. Brisby, A. Theodorsson, K. Blennow, H. Zetterberg, and J. Marcusson. CSF-biomarkers in Olympic boxing: diagnosis and effects of repetitive head trauma. PLoS One 7(4):e33606, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Neselius, S., H. Zetterberg, K. Blennow, J. Marcusson, and H. Brisby. Increased CSF levels of phosphorylated neurofilament heavy protein following bout in amateur boxers. PLoS One 8(11):e81249, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Neselius, S., H. Zetterberg, K. Blennow, et al. Olympic boxing is associated with elevated levels of the neuronal protein tau in plasma. Brain Inj. 27(4):425–433, 2013.

    Article  PubMed  Google Scholar 

  33. Peled, S. New perspectives on the sources of white matter DTI signal. IEEE Trans. Med. Imaging. 26(11):1448–1455, 2007.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Petraglia, A. L., B. A. Plog, S. Dayawansa, et al. The spectrum of neurobehavioral sequelae after repetitive mild traumatic brain injury: a novel mouse model of chronic traumatic encephalopathy. J. Neurotrauma. 31(13):1211–1224, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Povlishock, J. T. The window of risk in repeated head injury. J. Neurotrauma. 30(1):1, 2013.

    Article  PubMed  Google Scholar 

  36. Prange, M. T., and S. S. Margulies. Regional, directional, and age-dependent properties of the brain undergoing large deformation. J. Biomech. Eng. 124(2):244–252, 2002.

    Article  PubMed  Google Scholar 

  37. Prins, M. L., D. Alexander, C. C. Giza, and D. A. Hovda. Repeated mild traumatic brain injury: mechanisms of cerebral vulnerability. J. Neurotrauma. 30(1):30–38, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Rowson, S., and S. M. Duma. Brain injury prediction: assessing the combined probability of concussion using linear and rotational head acceleration. Ann. Biomed. Eng. 41(5):873–882, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Sabet, A. A., E. Christoforou, B. Zatlin, G. M. Genin, and P. V. Bayly. Deformation of the human brain induced by mild angular head acceleration. J. Biomech. 41(2):307–315, 2008.

    Article  PubMed  Google Scholar 

  40. Shenton, M. E., H. M. Hamoda, J. S. Schneiderman, et al. A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging Behav. 6(2):137–192, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Shin, W., S. Y. Mahmoud, K. Sakaie, et al. Diffusion measures indicate fight exposure-related damage to cerebral white matter in boxers and mixed martial arts fighters. AJNR Am. J. Neuroradiol. 35(2):285–290, 2014.

    Article  CAS  PubMed  Google Scholar 

  42. Slemmer, J. E., and J. T. Weber. The extent of damage following repeated injury to cultured hippocampal cells is dependent on the severity of insult and inter-injury interval. Neurobiol. Dis. 18(3):421–431, 2005.

    Article  PubMed  Google Scholar 

  43. Stamm, J. M. B. A., C. M. Baugh, N. G. Fritts, D. H. Daneshvar, B. M. Martin, M. D. McClean, Y. Tripodis, and R. A. Stern. Age of first exposure to football and later-life cognitive impairment in former NFL players. Neurology 84:1–7, 2015.

    Article  Google Scholar 

  44. Stern, R. A., D. O. Riley, D. H. Daneshvar, C. J. Nowinski, R. C. Cantu, and A. C. McKee. Long-term consequences of repetitive brain trauma: chronic traumatic encephalopathy. PM&R. 3(10 Suppl 2):S460–467, 2011.

    Article  Google Scholar 

  45. Talavage, T. M. N. E., E. L. Breedlove, U. Yoruk, A. E. Dye, K. Morigaki, H. Feuer, and L. J. Leverenz. Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. J. Neurotrauma. 31:327–338, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Urban, J. E., E. M. Davenport, A. J. Golman, et al. Head impact exposure in youth football: high school ages 14 to 18 years and cumulative impact analysis. Ann. Biomed. Eng. 41(12):2474–2487, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Vagnozzi, R., B. Tavazzi, S. Signoretti, et al. Temporal window of metabolic brain vulnerability to concussions: mitochondrial-related impairment—part I. Neurosurgery 61(2):379–388, 2007; (discussion 388–379).

    Article  PubMed  Google Scholar 

  48. Viano, D. C., I. R. Casson, and E. J. Pellman. Concussion in professional football: biomechanics of the struck player-part 14. Neurosurgery 61(2):313–327, 2007; (discussion 327–318).

    Article  PubMed  Google Scholar 

  49. Wu, L. C., V. Nangia, K. Bui, et al. In vivo evaluation of wearable head impact sensors. Eng: Ann. Biomed., 2015.

    Google Scholar 

  50. Yuen, T. J., K. D. Browne, A. Iwata, and D. H. Smith. Sodium channelopathy induced by mild axonal trauma worsens outcome after a repeat injury. J. Neurosci. Res. 87(16):3620–3625, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Zetterberg, H., M. A. Hietala, M. Jonsson, et al. Neurochemical aftermath of amateur boxing. Arch. Neurol. 63(9):1277–1280, 2006.

    Article  PubMed  Google Scholar 

  52. Zhang, L., L. A. Heier, R. D. Zimmerman, B. Jordan, and A. M. Ulug. Diffusion anisotropy changes in the brains of professional boxers. AJNR Am. J. Neuroradiol. 27(9):2000–2004, 2006.

    CAS  PubMed  Google Scholar 

  53. Zhu, T., X. Liu, P. R. Connelly, et al. An optimized wild bootstrap method for evaluation of measurement uncertainties of DTI-derived parameters in human brain. Neuroimage. 40(3):1144–1156, 2008.

    Article  PubMed  Google Scholar 

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Funding

This study was supported by funds from the National Football League Charities https://www.nflcharities.org/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflict of interest

Dr. Bazarian reports grants from National Football League Charities during the conduct of the study. In addition, Mr. Merchant-Borna and Dr. Bazarian have a patent “system and method to assess risk of changes to brain white matter based on head impact dose equivalent number” pending.

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Authors and Affiliations

  1. Department of Emergency Medicine, University of Rochester School of Medicine and Dentistry, 265 Crittenden Blvd, Box 655C, Rochester, NY, 14642, USA

    Kian Merchant-Borna, Patrick Asselin, Beau Abar, Courtney M. C. Jones & Jeffrey J. Bazarian

  2. School of Mathematical Sciences, Rochester Institute of Technology, Rochester, NY, USA

    Darren Narayan

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  1. Kian Merchant-Borna
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  2. Patrick Asselin
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  3. Darren Narayan
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Correspondence to Kian Merchant-Borna.

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Associate Editor Stefan M Duma oversaw the review of this article.

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Merchant-Borna, K., Asselin, P., Narayan, D. et al. Novel Method of Weighting Cumulative Helmet Impacts Improves Correlation with Brain White Matter Changes After One Football Season of Sub-concussive Head Blows. Ann Biomed Eng 44, 3679–3692 (2016). https://doi.org/10.1007/s10439-016-1680-9

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