Analysis of head impact exposure and brain microstructure response in a season-long application of a jugular vein compression collar: a prospective, neuroimaging investigation in American football

Background Historical approaches to protect the brain from outside the skull (eg, helmets and mouthpieces) have been ineffective in reducing internal injury to the brain that arises from energy absorption during sports-related collisions. We aimed to evaluate the effects of a neck collar, which applies gentle bilateral jugular vein compression, resulting in cerebral venous engorgement to reduce head impact energy absorption during collision. Specifically, we investigated the effect of collar wearing during head impact exposure on brain microstructure integrity following a competitive high school American football season. Methods A prospective longitudinal controlled trial was employed to evaluate the effects of collar wearing (n=32) relative to controls (CTRL; n=30) during one competitive football season (age: 17.04±0.67 years). Impact exposure was collected using helmet sensors and white matter (WM) integrity was quantified based on diffusion tensor imaging (DTI) serving as the primary outcome. Results With similar overall g-forces and total head impact exposure experienced in the two study groups during the season (p>0.05), significant preseason to postseason changes in mean diffusivity, axial diffusivity and radial diffusivity in the WM integrity were noted in the CTRL group (corrected p<0.05) but not in the collar group (p>0.05). The CTRL group demonstrated significantly larger preseason to postseason DTI change in multiple WM regions compared with the collar group (corrected p<0.05). Discussion Reduced WM diffusivity alteration was noted in participants wearing a neck collar after a season of competitive football. Collar wearing may have provided a protective effect against brain microstructural changes after repetitive head impacts. Trial registration number NCT02696200.

[1]  A. McKee,et al.  The epidemiology of sport-related concussion. , 2011, Clinics in sports medicine.

[2]  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.

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

[4]  W. Yuan,et al.  White matter alterations in youth with acute mild traumatic brain injury. , 2015, Journal of pediatric rehabilitation medicine.

[5]  Joseph F. Clark,et al.  Altitude Modulates Concussion Incidence , 2013, Orthopaedic journal of sports medicine.

[6]  Sylvain Bouix,et al.  Scholarship@Western Scholarship@Western , 2022 .

[7]  C. Rosen,et al.  Effect of slosh mitigation on histologic markers of traumatic brain injury: laboratory investigation. , 2012, Journal of neurosurgery.

[8]  Steven Rowson,et al.  Linear and angular head acceleration measurements in collegiate football. , 2009, Journal of biomechanical engineering.

[9]  P. Szeszko,et al.  MRI atlas of human white matter , 2006 .

[10]  A. Marmarou,et al.  Contribution of vasogenic and cellular edema to traumatic brain swelling measured by diffusion-weighted imaging. , 1997, Journal of neurosurgery.

[11]  Joseph T. Gwin,et al.  IN VIVO STUDY OF HEAD IMPACTS IN FOOTBALL: A COMPARISON OF NATIONAL COLLEGIATE ATHLETIC ASSOCIATION DIVISION I VERSUS HIGH SCHOOL IMPACTS , 2007, Neurosurgery.

[12]  Jason P Mihalik,et al.  MEASUREMENT OF HEAD IMPACTS IN COLLEGIATE FOOTBALL PLAYERS: AN INVESTIGATION OF POSITIONAL AND EVENT‐TYPE DIFFERENCES , 2007, Neurosurgery.

[13]  Arthur W. Toga,et al.  Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template , 2008, NeuroImage.

[14]  P. Basser,et al.  A simplified method to measure the diffusion tensor from seven MR images , 1998, Magnetic resonance in medicine.

[15]  J. Löfgren,et al.  CRANIAL AND SPINAL COMPONENTS OF THE CEREBROSPINAL FLUID PRESSURE‐VOLUME CURVE , 1973, Acta neurologica Scandinavica.

[16]  H. Levin,et al.  Diffusion tensor imaging of acute mild traumatic brain injury in adolescents , 2008, Neurology.

[17]  Murali Murugavel,et al.  A longitudinal diffusion tensor imaging study assessing white matter fiber tracts after sports-related concussion. , 2014, Journal of neurotrauma.

[18]  Steven P Broglio,et al.  Head impacts during high school football: a biomechanical assessment. , 2009, Journal of athletic training.

[19]  Michael Collins,et al.  Sex differences in white matter abnormalities after mild traumatic brain injury: localization and correlation with outcome. , 2014, Radiology.

[20]  Keith Paulsen,et al.  Maximum Principal Strain and Strain Rate Associated with Concussion Diagnosis Correlates with Changes in Corpus Callosum White Matter Indices , 2011, Annals of Biomedical Engineering.

[21]  J. Lloyd,et al.  Brain injury in sports. , 2016, Journal of neurosurgery.

[22]  A. Mayer,et al.  A prospective diffusion tensor imaging study in mild traumatic brain injury , 2010, Neurology.

[23]  S. Ashwal,et al.  Impaired neurovascular unit function contributes to persistent symptoms after concussion: a pilot study. , 2014, Journal of neurotrauma.

[24]  D. Cox,et al.  An Analysis of Transformations , 1964 .

[25]  J. Bailes,et al.  Internal jugular vein compression mitigates traumatic axonal injury in a rat model by reducing the intracranial slosh effect. , 2012, Neurosurgery.

[26]  O. Gilland,et al.  A cinemyelographic study of cerebrospinal fluid dynamics. , 1969, The American journal of roentgenology, radium therapy, and nuclear medicine.

[27]  David J Chalmers,et al.  Evaluation of protective equipment for prevention of injuries in rugby union. , 2004, International journal of epidemiology.

[28]  Steven P Broglio,et al.  Estimation of Head Impact Exposure in High School Football , 2013, The American journal of sports medicine.

[29]  M. Hulkower,et al.  A Decade of DTI in Traumatic Brain Injury: 10 Years and 100 Articles Later , 2013, American Journal of Neuroradiology.

[30]  J. Dvořák,et al.  Is protective equipment useful in preventing concussion? A systematic review of the literature , 2009, British Journal of Sports Medicine.

[31]  M. Lassonde,et al.  Long-Term Abnormalities in the Corpus Callosum of Female Concussed Athletes. , 2016, Journal of neurotrauma.

[32]  L. Boyd,et al.  Comparative incidence of concussion and return to play time in two Canadian minor hockey groups over the 2011–2012 season , 2013, British Journal of Sports Medicine.

[33]  J. Pater,et al.  Comparison of Mouth Guard Designs and Concussion Prevention in Contact Sports: A Multicenter Randomized Controlled Trial , 2005, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

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

[35]  Agatha D. Lee,et al.  Acute and chronic changes in diffusivity measures after sports concussion. , 2011, Journal of neurotrauma.

[36]  Peter Savadjiev,et al.  Hockey Concussion Education Project, Part 3. White matter microstructure in ice hockey players with a history of concussion: a diffusion tensor imaging study. , 2014, Journal of neurosurgery.

[37]  A. Macpherson,et al.  Epidemiology of sports-related injuries in children and youth presenting to Canadian emergency departments from 2007–2010 , 2013, Sports Medicine, Arthroscopy, Rehabilitation, Therapy & Technology.

[38]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[39]  L E Bilston,et al.  MR Elastography Can Be Used to Measure Brain Stiffness Changes as a Result of Altered Cranial Venous Drainage During Jugular Compression , 2015, American Journal of Neuroradiology.

[40]  Stefan Duma,et al.  Analysis of linear head accelerations from collegiate football impacts , 2006, Current sports medicine reports.

[41]  D. Pennell,et al.  Are functional deficits in concussed individuals consistent with white matter structural alterations: combined FMRI & DTI study , 2010, Experimental Brain Research.

[42]  E. Frost A Practical Approach to Neuroanesthesia , 2014 .

[43]  J. Hunter,et al.  Serial measurement of memory and diffusion tensor imaging changes within the first week following uncomplicated mild traumatic brain injury , 2012, Brain Imaging and Behavior.

[44]  Janet Adams,et al.  The Effects of External Jugular Compression Applied during Head Impact Exposure on Longitudinal Changes in Brain Neuroanatomical and Neurophysiological Biomarkers: A Preliminary Investigation , 2016, Front. Neurol..

[45]  K. Webster,et al.  Current state of concussion prevention strategies: a systematic review and meta-analysis of prospective, controlled studies , 2016, British Journal of Sports Medicine.

[46]  Colin W Fuller,et al.  The Epidemiology of Head Injuries in English Professional Rugby Union , 2008, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[47]  H. Levin,et al.  Voxel-Based Analysis of Diffusion Tensor Imaging in Mild Traumatic Brain Injury in Adolescents , 2010, American Journal of Neuroradiology.

[48]  Staci M Thomas,et al.  Rates of concussion are lower in National Football League games played at higher altitudes. , 2014, The Journal of orthopaedic and sports physical therapy.

[49]  Pratik Mukherjee,et al.  Diffusion Tensor Imaging of Mild Traumatic Brain Injury , 2010, The Journal of head trauma rehabilitation.

[50]  R. Demont,et al.  Role of mouthguards in reducing mild traumatic brain injury/concussion incidence in high school football athletes. , 2014, General dentistry.

[51]  M. McCrea,et al.  The Association of the Type of Football Helmet and Mouth Guard With the Incidence of Sport Related Concussion in High School Football Players , 2013, Orthopaedic Journal of Sports Medicine.

[52]  M. Lassonde,et al.  Neurometabolic and microstructural alterations following a sports-related concussion in female athletes , 2013, Brain injury.

[53]  Joseph J Crisco,et al.  Analysis of Real-time Head Accelerations in Collegiate Football Players , 2005, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[54]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[55]  M. Putukian,et al.  A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. , 2011, Journal of neurotrauma.

[56]  Andrew C Laing,et al.  Laboratory Evaluation of the gForce Tracker™, a Head Impact Kinematic Measuring Device for Use in Football Helmets , 2015, Annals of Biomedical Engineering.

[57]  S. Wakana,et al.  MRI Atlas of Human White Matter , 2005 .