Repetitive Subconcussive Head Impacts in Sports and Their Impact on Brain Anatomy and Function: A Systematic Review

Abstract

Repetitive subconcussive head impacts occur regularly in sports. However, the exact relationship between their biomechanical properties and their consequences on brain structure and function has not been clarified yet. We therefore reviewed prospective cohort studies that objectively reported the biomechanical characteristics of repetitive subconcussive head impacts and their impact on brain anatomy and function. Only studies with a pre- to post-measurement design were included. Twenty-four studies met the inclusion criteria. Structural white matter alterations, such as reduced fractional anisotropy and an increase in mean diffusivity values, seem to be evident in athletes exposed to repetitive subconcussive head impacts exceeding 10 g. Such changes are observable after only one season of play. Furthermore, a dose-response relationship exists between white matter abnormalities and the total number of subconcussive head impacts. However, functional changes after repetitive subconcussive head impacts remain inconclusive. We therefore conclude that repetitive subconcussive head impacts induce structural changes, but thus far without overt functional changes.

Keywords

neurodegeneration - repetitive head impacts - brain injury - concussion - contact sports

Publikationsverlauf

Eingereicht: 24. Januar 2024

Angenommen: 06. Juni 2024

Accepted Manuscript online:
10. Juni 2024

Artikel online veröffentlicht:
19. Juli 2024

• References

• 1 Hillman CH, Erickson KI, Kramer AF. Be smart, exercise your heart: Exercise effects on brain and cognition. Nat Rev Neurosci 2008; 9: 58-65
• 2 Ye K, Fleysher R, Lipton RB. et al. Repetitive soccer heading adversely impacts short-term learning among adult women. J Sci Med Sport 2022; 25: 935-941
• 3 Huber BR, Alosco ML, Stein TD. et al. Potential Long-Term Consequences of Concussive and Subconcussive Injury. Phys Med Rehabil Clin N Am 2016; 27: 503-511
• 4 Bailes JE, Petraglia AL, Omalu BI. et al. Role of subconcussion in repetitive mild traumatic brain injury. J Neurosurg 2013; 119: 1235-1245
• 5 Patricios JS, Schneider KJ, Dvorak J. et al. Consensus statement on concussion in sport: The 6th International Conference on Concussion in Sport-Amsterdam, October 2022. Br J Sports Med 2023; 57: 695-711
• 6 Wilcox BJ, Beckwith JG, Greenwald RM. et al. Head impact exposure in male and female collegiate ice hockey players. J Biomech 2014; 47: 109-114
• 7 Davenport EM, Urban JE, Mokhtari F. et al. Subconcussive impacts and imaging findings over a season of contact sports. Concussion 2016; 1: CNC19
• 8 McCunn R, Beaudouin F, Stewart K. et al. Heading in Football: Incidence, Biomechanical Characteristics and the Association with Acute Cognitive Function-A Three-Part Systematic Review. Sports Med 2021; 51: 2147-2163
• 9 King D, Hume P, Gissane C. et al. The Influence of Head Impact Threshold for Reporting Data in Contact and Collision Sports: Systematic Review and Original Data Analysis. Sports Med 2016; 46: 151-169
• 10 Tierney G. Concussion biomechanics, head acceleration exposure and brain injury criteria in sport: A review. Sports Biomech 2021; 23: 1-29
• 11 Nguyen JVK, Brennan JH, Mitra B. et al. Frequency and Magnitude of Game-Related Head Impacts in Male Contact Sports Athletes: A Systematic Review and Meta-Analysis. Sports Med 2019; 49: 1575-1583
• 12 Wilcox BJ, Beckwith JG, Greenwald RM. et al. Biomechanics of head impacts associated with diagnosed concussion in female collegiate ice hockey players. J Biomech 2015; 48: 2201-2204
• 13 Gavett BE, Stern RA, McKee AC. Chronic traumatic encephalopathy: A potential late effect of sport-related concussive and subconcussive head trauma. Clin Sports Med 2011; 30: 179-188 xi
• 14 Mackay DF, Russell ER, Stewart K. et al. Neurodegenerative Disease Mortality among Former Professional Soccer Players. N Engl J Med 2019; 381: 1801-1808
• 15 Tarnutzer AA, Straumann D, Brugger P. et al. Persistent effects of playing football and associated (subconcussive) head trauma on brain structure and function: A systematic review of the literature. Br J Sports Med 2017; 51: 1592-1604
• 16 Walter AE, Wilkes JR, Arnett PA. et al. The accumulation of subconcussive impacts on cognitive, imaging, and biomarker outcomes in child and college-aged athletes: A systematic review. Brain Imaging Behav 2022; 16: 503-517
• 17 Helmich I, Chang YY, Gemmerich R. et al. Neurobehavioral consequences of repetitive head impacts in Para swimming: A case report. J Sci Med Sport 2024; 27: 16-19
• 18 Nauman EA, Talavage TM, Auerbach PS. Mitigating the Consequences of Subconcussive Head Injuries. Annu Rev Biomed Eng 2020; 22: 387-407
• 19 Schneider DK, Galloway R, Bazarian JJ. et al. Diffusion Tensor Imaging in Athletes Sustaining Repetitive Head Impacts: A Systematic Review of Prospective Studies. J Neurotrauma 2019; 36: 2831-2849
• 20 Koerte IK, Wiegand TLT, Bonke EM. et al. Diffusion Imaging of Sport-related Repetitive Head Impacts-A Systematic Review. Neuropsychol Rev 2023; 33: 122-143
• 21 Ntikas M, Binkofski F, Shah NJ. et al. Repeated Sub-Concussive Impacts and the Negative Effects of Contact Sports on Cognition and Brain Integrity. Int J Environ Res Public Health 2022; 19: 7098
• 22 Mainwaring L, Ferdinand Pennock KM, Mylabathula S. et al. Subconcussive head impacts in sport: A systematic review of the evidence. Int J Psychophysiol 2018; 132: 39-54
• 23 Koerte IK, Nichols E, Tripodis Y. et al. Impaired Cognitive Performance in Youth Athletes Exposed to Repetitive Head Impacts. J Neurotrauma 2017; 34: 2389-2395
• 24 Levitch CF, McConathey E, Aghvinian M. et al. The Impact of Sleep on the Relationship between Soccer Heading Exposure and Neuropsychological Function in College-Age Soccer Players. Journal of the International Neuropsychological Society 2020; 26: 633-644
• 25 Guskiewicz KM, Mihalik JP. Biomechanics of sport concussion: Quest for the elusive injury threshold. Exerc Sport Sci Rev 2011; 39: 4-11
• 26 Broglio SP, Sosnoff JJ, Shin S. et al. Head Impacts During High School Football: A Biomechanical Assessment. J Athl Train 2009; 44: 342-349
• 27 Brett BL, Wu Y-C, Mustafi SM. et al. The Association Between Persistent White-Matter Abnormalities and Repeat Injury After Sport-Related Concussion. Front Neurol 2020; 10: 1345
• 28 Tremblay S, Henry LC, Bedetti C. et al. Diffuse white matter tract abnormalities in clinically normal ageing retired athletes with a history of sports-related concussions. Brain 2014; 137: 2997-3011
• 29 Romeu-Mejia R, Giza CC, Goldman JT. Concussion Pathophysiology and Injury Biomechanics. Curr Rev Musculoskelet Med 2019; 12: 105-116
• 30 Brennan JH, Mitra B, Synnot A. et al. Accelerometers for the Assessment of Concussion in Male Athletes: A Systematic Review and Meta-Analysis. Sports Medicine 2017; 47: 469-478
• 31 Wilcox BJ, Machan JT, Beckwith JG. et al. Head-Impact Mechanisms in Men’s and Women’s Collegiate Ice Hockey. J Athl Train 2014; 49: 514-520
• 32 Rowson S, Bland ML, Campolettano ET. et al. Biomechanical Perspectives on Concussion in Sport. Sports Med Arthrosc Rev 2016; 24: 100-107
• 33 Di Virgilio TG, Ietswaart M, Wilson L. et al. Understanding the Consequences of Repetitive Subconcussive Head Impacts in Sport: Brain Changes and Dampened Motor Control Are Seen After Boxing Practice. Front Hum Neurosci 2019; 13: 294
• 34 Broglio SP, Williams R, Rettmann A. et al. No Seasonal Changes in Cognitive Functioning Among High School Football Athletes: Implementation of a Novel Electrophysiological Measure and Standard Clinical Measures. Clin J Sport Med 2018; 28: 130-138
• 35 Caccese JB, Best C, Lamond LC. et al. Effects of Repetitive Head Impacts on a Concussion Assessment Battery. Med Sci Sports Exerc 2019; 51: 1355-1361
• 36 Lynall RC, Clark MD, Grand EE. et al. Head Impact Biomechanics in Women’s College Soccer. Med Sci Sports Exerc 2016; 48: 1772-1778
• 37 Gysland SM, Mihalik JP, Register-Mihalik JK. et al. The Relationship Between Subconcussive Impacts and Concussion History on Clinical Measures of Neurologic Function in Collegiate Football Players. Ann Biomed Eng 2012; 40: 14-22
• 38 Breedlove KM, Breedlove EL, Robinson M. et al. Detecting Neurocognitive and Neurophysiological Changes as a Result of Subconcussive Blows Among High School Football Athletes. Athl Train Sports Health Care 2014; 6: 119-127
• 39 Broglio SP, Eckner JT, Martini D. et al. Cumulative Head Impact Burden in High School Football. J Neurotrauma 2011; 28: 2069-2078
• 40 Nevins D, Hildenbrand K, Vasavada A. et al. In-Game Head Impact Exposure of Male and Female High School Soccer Players. Athl Train Sports Health Care 2019; 11: 174-182
• 41 Page MJ, McKenzie JE, Bossuyt PM. et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. Int J Surg 2021; 88: 105906
• 42 Methley AM, Campbell S, Chew-Graham C. et al. PICO, PICOS and SPIDER: a comparison study of specificity and sensitivity in three search tools for qualitative systematic reviews. BMC Health Serv Res 2014; 14: 579
• 43 Eriksen MB, Frandsen TF. The impact of patient, intervention, comparison, outcome (PICO) as a search strategy tool on literature search quality: A systematic review. J Med Libr Assoc 2018; 106: 420-431
• 44 Ouzzani M, Hammady H, Fedorowicz Z. et al. Rayyan-a web and mobile app for systematic reviews. Syst Rev 2016; 5: 210
• 45 Wells G, Shea B, O’Connell D. et al. Newcastle-Ottawa quality assessment scale cohort studies. 2014 retrieved from https://www.ncbi.nlm.nih.gov/books/NBK99082/bin/appb-fm4.pdf
• 46 Asselin PD, Gu Y, Merchant-Borna K. et al. Spatial regression analysis of MR diffusion reveals subject-specific white matter changes associated with repetitive head impacts in contact sports. Sci Rep 2020; 10: 13606
• 47 Bazarian JJ, Zhu T, Zhong J. et al. Persistent, long-term cerebral white matter changes after sports-related repetitive head impacts. PLoS One 2014; 9: e94734
• 48 Chrisman SPD, Ebel BE, Stein E. et al. Head Impact Exposure in Youth Soccer and Variation by Age and Sex. Clin J Sport Med 2019; 29: 3-10
• 49 Chrisman SPD, Mac Donald CL, Friedman S. et al. Head Impact Exposure During a Weekend Youth Soccer Tournament. J Child Neurol 2016; 31: 971-978
• 50 Marchesseault ER, Nguyen D, Spahr L. et al. Head impacts and cognitive performance in men’s lacrosse. Phys Sportsmed 2018; 46: 324-330
• 51 McAllister TW, Ford JC, Flashman LA. et al. Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes. Neurology 2014; 82: 63-69
• 52 Doan BK, Heaton KJ, Self BP. et al. Quantifying head impacts and neurocognitive performance in collegiate boxers. J Sports Sci 2022; 40: 509-517
• 53 Rose SC, Yeates KO, Nguyen JT. et al. Exposure to Head Impacts and Cognitive and Behavioral Outcomes in Youth Tackle Football Players Across 4 Seasons. JAMA Netw Open 2021; 4: e2140359
• 54 Rose SC, Yeates KO, Nguyen JT. et al. Neurocognitive Function and Head Impact Burden over Two Seasons of Youth Tackle Football. J Neurotrauma 2019; 36: 2803-2809
• 55 Stojsih S, Boitano M, Wilhelm M. et al. A prospective study of punch biomechanics and cognitive function for amateur boxers. Br J Sports Med 2010; 44: 725-730
• 56 Talavage TM, Nauman EA, Breedlove EL. et al. Functionally-Detected Cognitive Impairment in High School Football Players without Clinically-Diagnosed Concussion. J Neurotrauma 2014; 31: 327-338
• 57 McAllister TW, Flashman LA, Maerlender A. et al. Cognitive effects of one season of head impacts in a cohort of collegiate contact sport athletes. Neurology 2012; 78: 1777-1784
• 58 Yuan W, Barber Foss KD, Thomas S. et al. White matter alterations over the course of two consecutive high-school football seasons and the effect of a jugular compression collar: A preliminary longitudinal diffusion tensor imaging study. Hum Brain Mapp 2018; 39: 491-508
• 59 Slobounov SM, Walter A, Breiter HC. et al. The effect of repetitive subconcussive collisions on brain integrity in collegiate football players over a single football season: A multi-modal neuroimaging study. Neuroimage Clin 2017; 14: 708-718
• 60 Kelley ME, Urban JE, Jones DA. et al. Analysis of longitudinal head impact exposure and white matter integrity in returning youth football players. J Neurosurg Pediatr 2021; 28: 196-205
• 61 Manning KY, Brooks JS, Dickey JP. et al. Longitudinal changes of brain microstructure and function in nonconcussed female rugby players. Neurology 2020; 95: e402-e412
• 62 Chun IY, Mao X, Breedlove EL. et al. DTI Detection of Longitudinal WM Abnormalities Due to Accumulated Head Impacts. Dev Neuropsychol 2015; 40: 92-97
• 63 Gong N-J, Kuzminski S, Clark M. et al. Microstructural alterations of cortical and deep gray matter over a season of high school football revealed by diffusion kurtosis imaging. Neurobiol Dis 2018; 119: 79-87
• 64 Myer GD, Yuan W, Barber Foss KD. 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. Front Neurol 2016; 7: 74
• 65 Myer GD, Yuan W, Barber Foss KD. et al. 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. Br J Sports Med 2016; 50: 1276-1285
• 66 Myer GD, Barber Foss K, Thomas S. et al. Altered brain microstructure in association with repetitive subconcussive head impacts and the potential protective effect of jugular vein compression: A longitudinal study of female soccer athletes. Br J Sports Med 2019; 53: 1539-1551
• 67 Meehan WP, Taylor AM, Berkner P. et al. Division III Collision Sports Are Not Associated with Neurobehavioral Quality of Life. J Neurotrauma 2016; 33: 254-259
• 68 Breedlove KM, Breedlove EL, Robinson M. et al. Detecting Neurocognitive and Neurophysiological Changes as a Result of Subconcussive Blows Among High School Football Athletes. Athl Train Sports Health Care 2014; 6: 119-127
• 69 Diakogeorgiou E, Miyashita TL. Effect of Head Impact Exposures on Changes in Cognitive Testing. Orthop J Sports Med 2018; 6: 232596711876103
• 70 Gysland SM, Mihalik JP, Register-Mihalik JK. et al. The Relationship Between Subconcussive Impacts and Concussion History on Clinical Measures of Neurologic Function in Collegiate Football Players. Ann Biomed Eng 2012; 40: 14-22
• 71 Levitch CF, Zimmerman ME, Lubin N. et al. Recent and Long-Term Soccer Heading Exposure Is Differentially Associated With Neuropsychological Function in Amateur Players. J Int Neuropsychol Soc 2018; 24: 147-155
• 72 Montenigro PH, Alosco ML, Martin BM. et al. Cumulative Head Impact Exposure Predicts Later-Life Depression, Apathy, Executive Dysfunction, and Cognitive Impairment in Former High School and College Football Players. J Neurotrauma 2017; 34: 328-340
• 73 Breedlove EL, Robinson M, Talavage TM. et al. Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football. J Biomech 2012; 45: 1265-1272
• 74 Mez J, Daneshvar DH, Abdolmohammadi B. et al. Duration of American Football Play and Chronic Traumatic Encephalopathy. Ann Neurol 2020; 87: 116-131
• 75 Iverson GL, Castellani RJ, Cassidy JD. et al. Examining later-in-life health risks associated with sport-related concussion and repetitive head impacts: A systematic review of case-control and cohort studies. Br J Sports Med 2023; 57: 810-824
• 76 Mann DTY, Williams AM, Ward P. et al. Perceptual-cognitive expertise in sport: a meta-analysis. J Sport Exerc Psychol 2007; 29: 457-478
• 77 Seichepine DR, Stamm JM, Daneshvar DH. et al. Profile of Self-Reported Problems with Executive Functioning in College and Professional Football Players. J Neurotrauma 2013; 30: 1299-1304
• 78 Montenigro PH, Alosco ML, Martin BM. et al. Cumulative Head Impact Exposure Predicts Later-Life Depression, Apathy, Executive Dysfunction, and Cognitive Impairment in Former High School and College Football Players. J Neurotrauma 2017; 34: 328-340
• 79 Kelley ME, Urban JE, Miller LE. et al. Head Impact Exposure in Youth Football: Comparing Age- and Weight-Based Levels of Play. J Neurotrauma 2017; 34: 1939-1947
• 80 Manley G, Gardner AJ, Schneider KJ. et al. A systematic review of potential long-term effects of sport-related concussion. Br J Sports Med 2017; 51: 969-977
• 81 Koerte IK, Lin AP, Willems A. et al. A review of neuroimaging findings in repetitive brain trauma. Brain Pathol 2015; 25: 318-349
• 82 Kuzminski SJ, Clark MD, Fraser MA. et al. White Matter Changes Related to Subconcussive Impact Frequency during a Single Season of High School Football. AJNR Am J Neuroradiol 2018; 39: 245-251
• 83 Niogi SN, Mukherjee P. Diffusion tensor imaging of mild traumatic brain injury. J Head Trauma Rehabil 2010; 25: 241-255
• 84 Kim E, Yoo R-E, Seong MY. et al. A systematic review and data synthesis of longitudinal changes in white matter integrity after mild traumatic brain injury assessed by diffusion tensor imaging in adults. Eur J Radiol 2022; 147: 110117
• 85 Ting WK-C, Schweizer TA, Topolovec-Vranic J. et al. Antisaccadic Eye Movements Are Correlated with Corpus Callosum White Matter Mean Diffusivity, Stroop Performance, and Symptom Burden in Mild Traumatic Brain Injury and Concussion. Front Neurol 2016; 6: 271
• 86 Barulli D, Stern Y. Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci 2013; 17: 502-509
• 87 Dall’Acqua P, Johannes S, Mica L. et al. Functional and Structural Network Recovery after Mild Traumatic Brain Injury: A 1-Year Longitudinal Study. Front Hum Neurosci 2017; 11: 280
• 88 Hylin MJ, Kerr AL, Holden R. Understanding the Mechanisms of Recovery and/or Compensation following Injury. Neural Plast 2017; 2017: 1-12
• 89 Czerniak LL, Liebel SW, Garcia G-GP. et al. Sensitivity and Specificity of Computer-Based Neurocognitive Tests in Sport-Related Concussion: Findings from the NCAA-DoD CARE Consortium. Sports Med 2021; 51: 351-365