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

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 R2 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 R2 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 R2 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). R2 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.

[1]  Namhee Kim,et al.  Soccer heading is associated with white matter microstructural and cognitive abnormalities. , 2013, Radiology.

[2]  Stefan M Duma,et al.  Re: On the accuracy of the Head Impact Telemetry (HIT) system used in football helmets. , 2014, Journal of biomechanics.

[3]  G Allan Johnson,et al.  Diffusion tensor imaging reveals white matter injury in a rat model of repetitive blast-induced traumatic brain injury. , 2014, Journal of neurotrauma.

[4]  J. Corrigan,et al.  Initial Reliability and Validity of the Ohio State University TBI Identification Method , 2007, The Journal of head trauma rehabilitation.

[5]  K. Blennow,et al.  Neurochemical aftermath of amateur boxing , 2006, Archives of neurology.

[6]  J. Povlishock,et al.  Intensity- and interval-specific repetitive traumatic brain injury can evoke both axonal and microvascular damage. , 2012, Journal of neurotrauma.

[7]  J. Maldjian,et al.  Head Impact Exposure in Youth Football: High School Ages 14 to 18 Years and Cumulative Impact Analysis , 2013, Annals of Biomedical Engineering.

[8]  D. Hovda,et al.  Repeated mild traumatic brain injury: mechanisms of cerebral vulnerability. , 2013, Journal of neurotrauma.

[9]  Katherine Epstein,et al.  Diffusion tensor imaging findings in semi-acute mild traumatic brain injury. , 2014, Journal of neurotrauma.

[10]  Johnson G. Allan,et al.  Diffusion tensor imaging reveals white matter injury in a rat model of repetitive blast-induced traumatic brain injury. , 2014 .

[11]  A. Santucci,et al.  Assessing the enduring residual neuropsychological effects of head trauma in college athletes who participate in contact sports. , 2005, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[12]  Stefan M. Duma,et al.  Brain Injury Prediction: Assessing the Combined Probability of Concussion Using Linear and Rotational Head Acceleration , 2013, Annals of Biomedical Engineering.

[13]  Robert A. Gross,et al.  Spotlight on the January 6 Issue , 2015, Neurology.

[14]  J. Gilger,et al.  Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football. , 2012, Journal of biomechanics.

[15]  M. Lowe,et al.  Diffusion Measures Indicate Fight Exposure–Related Damage to Cerebral White Matter in Boxers and Mixed Martial Arts Fighters , 2014, American Journal of Neuroradiology.

[16]  P. Franzone,et al.  An in vivo evaluation , 1989 .

[17]  Ann C. McKee,et al.  Chronic traumatic encephalopathy: neurodegeneration following repetitive concussive and subconcussive brain trauma , 2012, Brain Imaging and Behavior.

[18]  P. Cole,et al.  Concussion in Professional Football: Biomechanics of the Struck Player-Part 14 , 2008 .

[19]  Maximilian Reiser,et al.  White matter integrity in the brains of professional soccer players without a symptomatic concussion. , 2012, JAMA.

[20]  B. DoddAndrew,et al.  Diffusion tensor imaging findings in semi-acute mild traumatic brain injury. , 2014 .

[21]  Å. Edman,et al.  Neurochemical aftermath of amateur boxing , 2006, Archives of Neurology.

[22]  Tong Zhu,et al.  Persistent, Long-term Cerebral White Matter Changes after Sports-Related Repetitive Head Impacts , 2014, PloS one.

[23]  James C. Ford,et al.  Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes , 2014, Neurology.

[24]  D. Meaney,et al.  Tissue-level thresholds for axonal damage in an experimental model of central nervous system white matter injury. , 2000, Journal of biomechanical engineering.

[25]  Joseph T. Gwin,et al.  HEAD IMPACT SEVERITY MEASURES FOR EVALUATING MILD TRAUMATIC BRAIN INJURY RISK EXPOSURE , 2008, Neurosurgery.

[26]  A. Uluğ,et al.  Diffusion anisotropy changes in the brains of professional boxers. , 2006, AJNR. American journal of neuroradiology.

[27]  D. Norris,et al.  Physical activity is related to the structural integrity of cerebral white matter , 2013, Neurology.

[28]  J. Povlishock.  The window of risk in repeated head injury. , 2013, Journal of neurotrauma.

[29]  David C Viano,et al.  On the accuracy of the Head Impact Telemetry (HIT) System used in football helmets. , 2013, Journal of biomechanics.

[30]  H. Lei,et al.  Temporal profiles of axonal injury following impact acceleration traumatic brain injury in rats—a comparative study with diffusion tensor imaging and morphological analysis , 2012, International Journal of Legal Medicine.

[31]  Christine M Baugh,et al.  Age of first exposure to football and later-life cognitive impairment in former NFL players , 2015, Neurology.

[32]  Tong Zhu,et al.  Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion. , 2012, Magnetic resonance imaging.

[33]  D. Rosenbaum,et al.  Abnormal white matter integrity related to head impact exposure in a season of high school varsity football. , 2014, Journal of neurotrauma.

[34]  T. Talavage,et al.  Role of subconcussion in repetitive mild traumatic brain injury A review , 2013 .

[35]  N. Obuchowski,et al.  Repeated head trauma is associated with smaller thalamic volumes and slower processing speed: the Professional Fighters’ Brain Health Study , 2015, British Journal of Sports Medicine.

[36]  D. Holtzman,et al.  Diffusion Tensor Imaging Reliably Detects Experimental Traumatic Axonal Injury and Indicates Approximate Time of Injury , 2007, The Journal of Neuroscience.

[37]  Douglas H. Smith,et al.  Sodium channelopathy induced by mild axonal trauma worsens outcome after a repeat injury , 2009, Journal of neuroscience research.

[38]  Corey T Walker,et al.  The spectrum of neurobehavioral sequelae after repetitive mild traumatic brain injury: a novel mouse model of chronic traumatic encephalopathy. , 2014, Journal of neurotrauma.

[39]  Tong Zhu,et al.  An optimized wild bootstrap method for evaluation of measurement uncertainties of DTI-derived parameters in human brain , 2008, NeuroImage.

[40]  R. Kikinis,et al.  A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury , 2012, Brain Imaging and Behavior.

[41]  J J Crisco,et al.  Solitary sclerosis: Progressive myelopathy from solitary demyelinating lesion , 2012, Neurology.

[42]  J. Bailes,et al.  An overview of the basic science of concussion and subconcussion: where we are and where we are going. , 2012, Neurosurgical focus.

[43]  Antonio Belli,et al.  TEMPORAL WINDOW OF METABOLIC BRAIN VULNERABILITY TO CONCUSSIONS: MITOCHONDRIAL‐RELATED IMPAIRMENT—PART I , 2007, Neurosurgery.

[44]  Sharon Peled,et al.  New Perspectives on the Sources of White Matter DTI Signal , 2007, IEEE Transactions on Medical Imaging.

[45]  A. McKee,et al.  Long‐term Consequences of Repetitive Brain Trauma: Chronic Traumatic Encephalopathy , 2011, PM & R : the journal of injury, function, and rehabilitation.

[46]  S. Duma,et al.  Validation of Concussion Risk Curves for Collegiate Football Players Derived from HITS Data , 2011, Annals of Biomedical Engineering.

[47]  Helena Brisby,et al.  CSF-Biomarkers in Olympic Boxing: Diagnosis and Effects of Repetitive Head Trauma , 2012, PloS one.

[48]  Barclay Morrison,et al.  A Model of Repetitive, Mild Traumatic Brain Injury and a Novel Pharmacological Intervention to Block Repetitive Injury Synergy , 2012 .

[49]  T. Talavage,et al.  Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. , 2014, Journal of neurotrauma.

[50]  M. Prange,et al.  Regional, directional, and age-dependent properties of the brain undergoing large deformation. , 2002, Journal of biomechanical engineering.

[51]  Guy M Genin,et al.  Deformation of the human brain induced by mild angular head acceleration. , 2008, Journal of biomechanics.

[52]  Helena Brisby,et al.  Olympic boxing is associated with elevated levels of the neuronal protein tau in plasma , 2013, Brain injury.

[53]  Steven P Broglio,et al.  No evidence for a cumulative impact effect on concussion injury threshold. , 2011, Journal of neurotrauma.

[54]  David B. Camarillo,et al.  In Vivo Evaluation of Wearable Head Impact Sensors , 2015, Annals of Biomedical Engineering.

[55]  John T. Weber,et al.  The extent of damage following repeated injury to cultured hippocampal cells is dependent on the severity of insult and inter-injury interval , 2005, Neurobiology of Disease.

[56]  Helena Brisby,et al.  Increased CSF Levels of Phosphorylated Neurofilament Heavy Protein following Bout in Amateur Boxers , 2013, PloS one.