Cumulative Effects of Prior Concussion and Primary Sport Participation on Brain Morphometry in Collegiate Athletes: A Study From the NCAA–DoD CARE Consortium

Prior studies have reported long-term differences in brain structure (brain morphometry) as being associated with cumulative concussion and contact sport participation. There is emerging evidence to suggest that similar effects of prior concussion and contact sport participation on brain morphometry may be present in younger cohorts of active athletes. We investigated the relationship between prior concussion and primary sport participation with subcortical and cortical structures in active collegiate contact sport and non-contact sport athletes. Contact sport athletes (CS; N = 190) and matched non-contact sport athletes (NCS; N = 95) completed baseline clinical testing and participated in up to four serial neuroimaging sessions across a 6-months period. Subcortical and cortical structural metrics were derived using FreeSurfer. Linear mixed-effects (LME) models examined the effects of years of primary sport participation and prior concussion (0, 1+) on brain structure and baseline clinical variables. Athletes with prior concussion across both groups reported significantly more baseline concussion and psychological symptoms (all ps < 0.05). The relationship between years of primary sport participation and thalamic volume differed between CS and NCS (p = 0.015), driven by a significant inverse association between primary years of participation and thalamic volume in CS (p = 0.007). Additional analyses limited to CS alone showed that the relationship between years of primary sport participation and dorsal striatal volume was moderated by concussion history (p = 0.042). Finally, CS with prior concussion had larger hippocampal volumes than CS without prior concussion (p = 0.015). Years of contact sport exposure and prior concussion(s) are associated with differences in subcortical volumes in young-adult, active collegiate athletes, consistent with prior literature in retired, primarily symptomatic contact sport athletes. Longitudinal follow-up studies in these athletes are needed to determine clinical significance of current findings.

[1]  I. Janssen,et al.  Adolescents' engagement in multiple risk behaviours is associated with concussion. , 2020 .

[2]  M. Okano,et al.  Cohort Study , 2020, Definitions.

[3]  M. McCrea,et al.  Age of First Exposure to American Football and Behavioral, Cognitive, Psychological, and Physical Outcomes in High School and Collegiate Football Players , 2019, Sports health.

[4]  N. Makris,et al.  Limbic system structure volumes and associated neurocognitive functioning in former NFL players , 2019, Brain Imaging and Behavior.

[5]  T. Kaminski,et al.  Estimated Age of First Exposure to American Football and Neurocognitive Performance Amongst NCAA Male Student-Athletes: A Cohort Study , 2019, Sports Medicine.

[6]  Mark Hamer,et al.  Association of body mass index and waist-to-hip ratio with brain structure , 2019, Neurology.

[7]  Naomi J. Goodrich-Hunsaker,et al.  Cortical thickness in pediatric mild traumatic brain injury including sports-related concussion. , 2018, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[8]  D. Ramasamy,et al.  Multimodal Imaging of Retired Professional Contact Sport Athletes Does Not Provide Evidence of Structural and Functional Brain Damage , 2018, The Journal of head trauma rehabilitation.

[9]  D. Terry,et al.  Repeated mild traumatic brain injuries is not associated with volumetric differences in former high school football players , 2018, Brain Imaging and Behavior.

[10]  R. Wennberg,et al.  The relationship between brain atrophy and cognitive-behavioural symptoms in retired Canadian football players with multiple concussions , 2018, NeuroImage: Clinical.

[11]  B. Dickerson,et al.  Cortical thickness and subcortical brain volumes in professional rugby league players , 2018, NeuroImage: Clinical.

[12]  R. Bauer,et al.  Concussion-Like Symptom Reporting in Non-Concussed Collegiate Athletes , 2017, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[13]  M. Shenton,et al.  Age at First Exposure to Repetitive Head Impacts Is Associated with Smaller Thalamic Volumes in Former Professional American Football Players. , 2017, Journal of neurotrauma.

[14]  Ryan M. Lee,et al.  Serial Assessment of Gray Matter Abnormalities after Sport-Related Concussion. , 2017, Journal of neurotrauma.

[15]  R. Killiany,et al.  White matter signal abnormalities in former National Football League players , 2017, Alzheimer's & dementia.

[16]  S. DeKosky,et al.  Research Gaps and Controversies in Chronic Traumatic Encephalopathy: A Review , 2017, JAMA neurology.

[17]  R. Au,et al.  Age of first exposure to American football and long-term neuropsychiatric and cognitive outcomes , 2017, Translational Psychiatry.

[18]  Steven B Cohen,et al.  Early Single-Sport Specialization: A Survey of 3090 High School, Collegiate, and Professional Athletes , 2017, Orthopaedic journal of sports medicine.

[19]  Robin O Cleveland,et al.  Concussion, microvascular injury, and early tauopathy in young athletes after impact head injury and an impact concussion mouse model , 2017, Alzheimer's & Dementia.

[20]  Joanna M. Wardlaw,et al.  Risk and protective factors for structural brain ageing in the eighth decade of life , 2017, Brain Structure and Function.

[21]  J. Ortega,et al.  A National Study on the Effects of Concussion in Collegiate Athletes and US Military Service Academy Members: The NCAA–DoD Concussion Assessment, Research and Education (CARE) Consortium Structure and Methods , 2017, Sports Medicine.

[22]  N. Churchill,et al.  Brain Structure and Function Associated with a History of Sport Concussion: A Multi-Modal Magnetic Resonance Imaging Study , 2017 .

[23]  Simon J. Graham,et al.  Brain Structure and Function Associated with a History of Sport Concussion: A Multi-Modal Magnetic Resonance Imaging Study. , 2017, Journal of neurotrauma.

[24]  Rhoda Au,et al.  Cumulative Head Impact Exposure Predicts Later-Life Depression, Apathy, Executive Dysfunction, and Cognitive Impairment in Former High School and College Football Players. , 2017, Journal of neurotrauma.

[25]  R. Zafonte,et al.  Consistency of Self-Reported Concussion History in Adolescent Athletes. , 2017, Journal of neurotrauma.

[26]  M. Keightley,et al.  Concussion-Like Symptoms in Child and Youth Athletes at Baseline: What Is "Typical"? , 2016, Journal of athletic training.

[27]  S. Strakowski,et al.  MRI Evidence of Neuropathic Changes in Former College Football Players , 2016, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[28]  Ann C McKee,et al.  Repetitive Head Impacts and Chronic Traumatic Encephalopathy. , 2016, Neurosurgery clinics of North America.

[29]  P. Bellgowan,et al.  Smaller Dentate Gyrus and CA2 and CA3 Volumes Are Associated with Kynurenine Metabolites in Collegiate Football Athletes. , 2016, Journal of neurotrauma.

[30]  W. Barr,et al.  Reliability and Validity of the Sport Concussion Assessment Tool–3 (SCAT3) in High School and Collegiate Athletes , 2016, The American journal of sports medicine.

[31]  P. Bellgowan,et al.  Thinner Cortex in Collegiate Football Players With, but not Without, a Self-Reported History of Concussion. , 2016, Journal of neurotrauma.

[32]  Wayne A. Gordon,et al.  The first NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy , 2015, Acta Neuropathologica.

[33]  R. Zafonte,et al.  Factors Associated With Concussion-like Symptom Reporting in High School Athletes. , 2015, JAMA pediatrics.

[34]  B. DoddAndrew,et al.  A Longitudinal Assessment of Structural and Chemical Alterations in Mixed Martial Arts Fighters. , 2015 .

[35]  A. McKee,et al.  Concussion in Chronic Traumatic Encephalopathy , 2015, Current Pain and Headache Reports.

[36]  Jeffrey S. Spence,et al.  Imaging Correlates of Memory and Concussion History in Retired National Football League Athletes. , 2015, JAMA neurology.

[37]  S. Marshall,et al.  Estimating Contact Exposure in Football Using the Head Impact Exposure Estimate. , 2015, Journal of neurotrauma.

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

[39]  R. Wennberg,et al.  Frontotemporal correlates of impulsivity and machine learning in retired professional athletes with a history of multiple concussions , 2015, Brain Structure and Function.

[40]  Shaojie Chen,et al.  Neuroinflammation and brain atrophy in former NFL players: An in vivo multimodal imaging pilot study , 2015, Neurobiology of Disease.

[41]  Matthew D. Albaugh,et al.  Postconcussion symptoms are associated with cerebral cortical thickness in healthy collegiate and preparatory school ice hockey players. , 2015, The Journal of pediatrics.

[42]  J. Ghajar,et al.  Concussion guidelines step 1: systematic review of prevalent indicators. , 2014, Neurosurgery.

[43]  P. Bellgowan,et al.  Relationship of collegiate football experience and concussion with hippocampal volume and cognitive outcomes. , 2014, Journal of the American Medical Association (JAMA).

[44]  Mert R. Sabuncu,et al.  Spatiotemporal Linear Mixed Effects Modeling for the Mass-univariate Analysis of Longitudinal Neuroimage Data ⁎ for the Alzheimer's Disease Neuroimaging Initiative 1 , 2022 .

[45]  Mert R. Sabuncu,et al.  Statistical analysis of longitudinal neuroimage data with Linear Mixed Effects models , 2013, NeuroImage.

[46]  Bruce Fischl,et al.  Within-subject template estimation for unbiased longitudinal image analysis , 2012, NeuroImage.

[47]  Daniel K Sodickson,et al.  Thalamic resting-state functional networks: disruption in patients with mild traumatic brain injury. , 2011, Radiology.

[48]  K. Guskiewicz,et al.  Association between Previous Concussion History and Symptom Endorsement during Preseason Baseline Testing in High School and Collegiate Athletes , 2009, Sports health.

[49]  S. Marshall,et al.  Association between Recurrent Concussion and Late-Life Cognitive Impairment in Retired Professional Football Players , 2005, Neurosurgery.

[50]  King H. Yang,et al.  A proposed injury threshold for mild traumatic brain injury. , 2004, Journal of biomechanical engineering.

[51]  C. Armatas,et al.  Surfing: an avenue for socially acceptable risk-taking, satisfying needs for sensation seeking and experience seeking☆ , 2004 .

[52]  J. R. Potgieter,et al.  Sensation Seeking among Medium- and Low-Risk Sports Participants , 1990 .

[53]  R. C. Macridis A review , 1963 .

[54]  Max Wintermark,et al.  Comparative Analysis of Head Impact in Contact and Collision Sports. , 2017, Journal of neurotrauma.

[55]  L. Ruvo Confidential: For Review Only The effect of repeated head trauma on brain structure and cognition: The Professional Fighters Brain Health Study , 2014 .

[56]  A. McKee,et al.  The spectrum of disease in chronic traumatic encephalopathy. , 2013, Brain : a journal of neurology.

[57]  Alain Ptito,et al.  Neural substrates of symptoms of depression following concussion in male athletes with persisting postconcussion symptoms. , 2008, Archives of general psychiatry.

[58]  Stephen W Marshall,et al.  Recurrent concussion and risk of depression in retired professional football players. , 2007, Medicine and science in sports and exercise.