Concussions and heading in soccer: A review of the evidence of incidence, mechanisms, biomarkers and neurocognitive outcomes

References

• Halstead ME, Walter KD. American Academy of Pediatrics. Clinical report–sport-related concussion in children and adolescents. Pediatrics 2010;126:597–615
   PubMed Web of Science ®Google Scholar
• Bazarian JJ, Veazie P, Mookerjee S, Lerner EB. Accuracy of mild traumatic brain injury case ascertainment using ICD-9 codes. Academic Emergency Medicine: Official Journal of the Society for Academic Emergency Medicine 2006;13:31–38
   PubMed Web of Science ®Google Scholar
• CDC. Nonfatal Traumatic Brain Injuries from Sports and Recreation Activities -- United States, 2001--2005. MMWR [Internet]. 2007 [cited 2013 June 7]: 733--737. Available from: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6039a1.htm?s_cid=mm6039a1_w
   Google Scholar
• McCrory P, Meeuwisse W, Aubry M, Cantu R, Dvorak J, Echemendia R, Engebretsen L, Johnston K, Kutcher J, Raftery M, et al. Consensus statement on concussion in sport - The 4th International Conference on Concussion in Sport held in Zurich, November 2012. Physical Therapy in Sport 2013;14:e1–e13
   PubMedGoogle Scholar
• FIFA. FIFA Big Count. [Internet]. 2006 [cited 2012 May 13]. Available from: www.fifa.com/worldfootball/bigcount/index.html
   Google Scholar
• Fuller CW, Junge A, Dvorak J. A six year prospective study of the incidence and causes of head and neck injuries in international football. British Journal of Sports Medicine 2005;39(Suppl 1):i3–9
   PubMed Web of Science ®Google Scholar
• Comper P, Hutchison M, Magrys S, Mainwaring L, Richards D. Evaluating the methodological quality of sports neuropsychology concussion research: A systematic review. Brain injury 2010;24:1257–1271
   PubMed Web of Science ®Google Scholar
• Guskiewicz KM, McCrea M, Marshall SW, Cantu RC, Randolph C, Barr W, Onate JA, Kelly JP. Cumulative effects associated with recurrent concussion in collegiate football players: The NCAA concussion study. Journal of the American Medical Association 2003;290:2549–2555
   PubMed Web of Science ®Google Scholar
• Iverson GL, Gaetz M, Lovell MR, Collins MW. Cumulative effects of concussion in amateur athletes. Brain Injury 2004;18:433–443
   PubMed Web of Science ®Google Scholar
• Macciocchi SN, Barth JT, Littlefield L, Cantu RC. Multiple Concussions and neuropsychological functioning in Collegiate Football Players. Journal of Athletic Training 2001;36:303–306
   PubMed Web of Science ®Google Scholar
• Zemper ED. Two-year prospective study of relative risk of a second cerebral concussion. American Journal of Physical Medicine & Rehabilitation 2003;82:653–659
   PubMed Web of Science ®Google Scholar
• Stephens R, Rutherford A, Potter D, Fernie G. Neuropsychological consequence of soccer play in adolescent U.K. school team soccer players. Journal of Neuropsychiatry & Clinical Neuroscience 2010;22:295–303
   PubMed Web of Science ®Google Scholar
• Broglio SP, Eckner JT, Paulson HL, Kutcher JS. Cognitive decline and aging: The role of concussive and subconcussive impacts. Exercise and Sport Sciences Reviews 2012;40:138–144
   PubMed Web of Science ®Google Scholar
• Bramley H, Patrick K, Lehman E, Silvis M. High school soccer players with concussion education are more likely to notify their coach of a suspected concussion. Clinical Pediatrics 2012;51:332–336
   PubMed Web of Science ®Google Scholar
• Shenouda C, Hendrickson P, Davenport K, Barber J, Bell KR. The effects of concussion legislation one year later–what have we learned: A descriptive pilot survey of youth soccer player associates. PM&R: The Journal of Injury, Function, and Rehabilitation 2012;4:427–435
   PubMedGoogle Scholar
• Covassin T, Elbin RJ, Sarmiento K. Educating coaches about concussion in sports: Evaluation of the CDC’s “Heads Up: Concussion in youth sports” initiative. The Journal of School Health 2012;82:233–238
   PubMed Web of Science ®Google Scholar
• Iverson GL, Lovell MR, Collins MW. Interpreting change on ImPACT following sport concussion. Clinical Neuropsychology 2003;17:460–467
   PubMed Web of Science ®Google Scholar
• Jinguji TM, Bompadre V, Harmon KG, Satchell EK, Gilbert K, Wild J, Eary JF. Sport Concussion Assessment Tool-2: Baseline values for high school athletes. British Journal of Sports Medicine 2012;46:365–370
   PubMed Web of Science ®Google Scholar
• Harmon KG, Drezner JA, Gammons M, Guskiewicz KM, Halstead M, Herring SS, Kutcher JS, Pana A, Putukian M, Roberts WO. American Medical Society for Sports Medicine position statement: Concussion in sport. British Journal of Sports Medicine 2013;47:15–26
   PubMed Web of Science ®Google Scholar
• HockeyCanada. Hockey Canada’s New Head Contact Rule. 2011. [Internet]. 2011 [cited 2013 May 29]. Available from: http://www.hockeycanada.ca/en-ca/news/2011-GN-018-en
   Google Scholar
• NHL. Official Rules: Rule 48 -- Illegal Check to the Head. [Internet]. 2012 [cited 2013 May 29]. Available from: http://www.nhl.com/ice/page.htm?id=64063
   Google Scholar
• NFL. New NFL rules designed to limit head injuries. [Internet]. 2010 [cited 2013 June 7]. Available from: http://www.nfl.com/news/story/09000d5d81990bdf/article/new-nfl-rules-designed-to-limit-head-injuries
   Google Scholar
• HockeyCanada. Hockey Canada's 49th Annual General Meeting concludes in Charlottetown, P.E.I.; body-checking rule change approved; Jim Hornell elected chair of Hockey Canada Board of Directors. [Internet]. 2013 [cited 2013 June 7]. Available from: http://www.hockeycanada.ca/en-ca/news/agm-concludes-in-charlottetown
   Google Scholar
• NBCSports. Youth soccer league bans heading: is the the beginning of the end for the noggin tactic? Off the Bench [Internet]. 2012 [cited 2013 June 7]. Available from: http://offthebench.nbcsports.com/2012/09/14/youth-soccer-league-bans-heading-is-this-the-beginning-of-the-end-for-the-storied-tactic/
   Google Scholar
• Agel J, Evans TA, Dick R, Putukian M, Marshall SW. Descriptive epidemiology of collegiate men’s soccer injuries: National Collegiate Athletic Association Injury Surveillance System, 1988–1989 through 2002–2003. Journal of Athletic Training 2007;42:270–277
   PubMed Web of Science ®Google Scholar
• Dick R, Putukian M, Agel J, Evans TA, Marshall SW. Descriptive Epidemiology of Collegiate Women’s Soccer Injuries: National Collegiate Athletic Association Injury Surveillance System, 1988–1989 through 2002–2003. Journal of Athletic Training 2007;42:278–285
   PubMed Web of Science ®Google Scholar
• Marar M, McIlvain NM, Fields SK, Comstock RD. Epidemiology of concussions among United States high school athletes in 20 sports. The American Journal of Sports Medicine 2012;40:747–755
   PubMed Web of Science ®Google Scholar
• Lincoln AE, Caswell SV, Almquist JL, Dunn RE, Norris JB, Hinton RY. Trends in concussion incidence in high school sports: A prospective 11-year study. The American Journal of Sports Medicine 2011;39:958–963
   PubMed Web of Science ®Google Scholar
• Gessel LM, Fields SK, Collins CL, Dick RW, Comstock RD. Concussions among United States high school and collegiate athletes. Journal of Athletic Training 2007;42:495–503
   PubMed Web of Science ®Google Scholar
• Boden BP, Kirkendall DT, Garrett WE. Concussion incidence in elite college soccer players. The American Journal of Sports Medicine 1998;26:238–241
   PubMed Web of Science ®Google Scholar
• Delaney JS, Lacroix VJ, Leclerc S, Johnston KM. Concussions among university football and soccer players. Clinical Journal of Sport Medicine: Official Journal of The Canadian Academy of Sport Medicine 2002;12:331–338
   PubMed Web of Science ®Google Scholar
• Yard EE, Schroeder MJ, Fields SK, Collins CL, Comstock RD. The epidemiology of United States high school soccer injuries, 2005–2007. The American Journal of Sports Medicine 2008;36:1930–1937
   PubMed Web of Science ®Google Scholar
• Rechel JA, Yard EE, Comstock RD. An epidemiologic comparison of high school sports injuries sustained in practice and competition. Journal of Athletic Training 2008;43:197–204
   PubMed Web of Science ®Google Scholar
• Powell JW, Barber-Foss KD. Sex-related injury patterns among selected high school sports. The American Journal of Sports Medicine 2000;28:385–391
   PubMed Web of Science ®Google Scholar
• Covassin T, Swanik CB, Sachs ML. Sex differences and the incidence of concussions among collegiate athletes. Journal of Athletic Training 2003;38:238–244
   PubMed Web of Science ®Google Scholar
• Castile L, Collins CL, McIlvain NM, Comstock RD. The epidemiology of new versus recurrent sports concussions among high school athletes, 2005–2010. British Journal of Sports Medicine 2012;46:603–610
   PubMed Web of Science ®Google Scholar
• Andersen TE, Arnason A, Engebretsen L, Bahr R. Mechanisms of head injuries in elite football. British Journal of Sports Medicine 2004;38:690–696
   PubMed Web of Science ®Google Scholar
• Barnes BC, Cooper L, Kirkendall DT, McDermott TP, Jordan BD, Garrett WE. Concussion history in elite male and female soccer players. The American Journal of Sports Medicine 1998;26:433–438
   PubMed Web of Science ®Google Scholar
• Delaney JS, Frankovich R. Head injuries and concussions in soccer. Clinical Journal of Sport Medicine: Official Journal of The Canadian Academy of Sport Medicine 2005;15:216–219; discussion 212–213
   PubMedGoogle Scholar
• Giannotti M, Al-Sahab B, McFaull S, Tamim H. Epidemiology of acute head injuries in Canadian children and youth soccer players. Injury 2010;41:907–912
   PubMed Web of Science ®Google Scholar
• Cusimano MD, Cho N, Amin K, Shirazi M, McFaull SR, Do MT, Wong MC, Russell K. Mechanisms of team-sport-related brain injuries in children 5 to 19 years old: Opportunities for prevention. PloS One 2013;8:e58868
   PubMed Web of Science ®Google Scholar
• Hanlon EM, Bir CA. Real-time head acceleration measurement in girls’ youth soccer. Medicine & Science in Sports & Exercise 2012;44:1102–1108
   PubMed Web of Science ®Google Scholar
• Delaney J, Puni V, Rouah F. Mechanisms of injury for concussions in university football, ice hockey, and soccer: A pilot study. Clinical Journal of Sport Medicine: Official Journal of The Canadian Academy of Sport Medicine 2006;16:162–165
   PubMed Web of Science ®Google Scholar
• Ellemberg D, Leclerc S, Couture S, Daigle C. Prolonged neuropsychological impairments following a first concussion in female university soccer athletes. Clinical Journal of Sport Medicine: Official Journal of the Canadian Academy of Sport Medicine 2007;17:369–374
   PubMed Web of Science ®Google Scholar
• Colvin AC, Mullen J, Lovell MR, West RV, Collins MW, Groh M. The role of concussion history and gender in recovery from soccer-related concussion. The American Journal of Sports Medicine 2009;37:1699–1704
   PubMed Web of Science ®Google Scholar
• Zuckerman SL, Solomon GS, Forbes JA, Haase RF, Sills AK, Lovell MR. Response to acute concussive injury in soccer players: Is gender a modifying factor? Journal of Neurosurgery: Pediatrics 2012;2:1–7
   Google Scholar
• Guskiewicz KM, Marshall SW, Broglio SP, Cantu RC, Kirkendall DT. No evidence of impaired neurocognitive performance in collegiate soccer players. The American Journal of Sports Medicine 2002;30:157–162
   PubMed Web of Science ®Google Scholar
• Kontos AP, Dolese A, Elbin RJ, Covassin T, Warren BL. Relationship of soccer heading to computerized neurocognitive performance and symptoms among female and male youth soccer players. Brain Injury 2011;25:1234–1241
   PubMed Web of Science ®Google Scholar
• Janda DH, Bir CA, Cheney AL. An evaluation of the cumulative concussive effect of soccer heading in the youth population. Injury Control and Safety Promotion 2002;9:25–31
   PubMedGoogle Scholar
• Putukian M, Echemendia RJ, Mackin S. The acute neuropsychological effects of heading in soccer: A pilot study. Clinical Journal of Sport Medicine 2000;10:104–109
   PubMed Web of Science ®Google Scholar
• Webbe FM, Ochs SR. Recency and frequency of soccer heading interact to decrease neurocognitive performance. Applied Neuropsychology 2003;10:31–41
   PubMed Web of Science ®Google Scholar
• Stephens R, Rutherford A, Potter D, Fernie G. Neuropsychological impairment as a consequence of football (soccer) play and football heading: A preliminary analysis and report on school students (13–16 years). Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence 2005;11:513–526
   PubMed Web of Science ®Google Scholar
• Kaminski TW, Cousino ES, Glutting JJ. Examining the relationship between purposeful heading in soccer and computerized Neuropsychological Test Performance. Research Quarterly for Exercise and Sport 2008;79:235–244
   PubMed Web of Science ®Google Scholar
• Matser JT, Kessels AG, Jordan BD, Lezak MD, Troost J. Chronic traumatic brain injury in professional soccer players. Neurology 1998;51:791–796
   PubMed Web of Science ®Google Scholar
• Matser EJT, Kessels AG, Lezak MD, Jordan BD, Troost J. Neuropsychological impairment in amateur soccer players. Journal of the American Medical Association 1999;282:971–973
   PubMed Web of Science ®Google Scholar
• Matser JT, Kessels AGH, Lezak MD, Troost J. A dose-response relation of headers and concussions with cognitive impairment in professional soccer players. Journal of Clinical and Experimental Neuropsychology 2001;23:770–774
   PubMed Web of Science ®Google Scholar
• Downs DS, Abwender D. Neuropsychological impairment in soccer athletes. The Journal of Sports Medicine and Physical Fitness 2002;42:103–107
   PubMed Web of Science ®Google Scholar
• Tysvaer A, Lochen E. Soccer injuries to the brain: A neuropsychologic study of former soccer players. The American Journal of Sports Medicine 1991;19:56–60
   PubMed Web of Science ®Google Scholar
• Rutherford A, Stephens R, Potter D, Fernie G. Neuropsychological impairment as a consequence of football (soccer) play and football heading: Preliminary analyses and report on university footballers. Journal of Clinical and Experimental Neuropsychology 2005;27:299–319
   PubMed Web of Science ®Google Scholar
• Rutherford A, Stephens R, Fernie G, Potter D. Do UK university football club players suffer neuropsychological impairment as a consequence of their football (soccer) play? Journal of Clinical and Experimental Neuropsychology 2009;31:664–681
   PubMed Web of Science ®Google Scholar
• Straume-Naesheim TM, Andersen TE, Dvorak J, Bahr R. Effects of heading exposure and previous concussions on neuropsychological performance among Norwegian elite footballers. British Journal of Sports Medicine 2005;39(Suppl 1):i70–77
   PubMed Web of Science ®Google Scholar
• Kaminski TW, Wikstrom AM, Gutierrez GM, Glutting JJ. Purposeful heading during a season does not influence cognitive function or balance in female soccer players. Journal of Clinical and Experimental Neuropsychology 2007;29:742–751
   PubMed Web of Science ®Google Scholar
• Mussack T, Dvorak J, Graf-Baumann T, Jochum M. Serum S-100B protein levels in young amateur soccer players after controlled heading and normal exercise. European Journal of Medical Research 2003;8:457–464
   PubMed Web of Science ®Google Scholar
• Stålnacke B-M, Tegner Y, Sojka P. Playing soccer increases serum concentrations of the biochemical markers of brain damage S-100B and neuron-specific enolase in elite players: A pilot study. Brain Injury 2004;18:899–909
   PubMed Web of Science ®Google Scholar
• Stålnacke B-M, Ohlsson A, Tegner Y, Sojka P. Serum concentrations of two biochemical markers of brain tissue damage S-100B and neurone specific enolase are increased in elite female soccer players after a competitive game. British Journal of Sports Medicine 2006;40:313–316
   PubMed Web of Science ®Google Scholar
• Stålnacke B-M, Sojka P. repeatedly heading a soccer ball does not increase serum levels of S-100B, a biochemical marker of brain tissue damage: An Experimental Study. Biomarker Insights 2008;3:87–91
   PubMedGoogle Scholar
• Zetterberg H, Jonsson M, Rasulzada A, Popa C, Styrud E, Hietala MA, Rosengren L, Wallin A, Blennow K. No neurochemical evidence for brain injury caused by heading in soccer. British Journal of Sports Medicine 2007;41:574–577
   PubMedGoogle Scholar
• Adams J, Adler CM, Jarvis K, DelBello MP, Strakowski SM. Evidence of anterior temporal atrophy in college-level soccer players. Clinical Journal of Sport Medicine 2007;17:304–306
   PubMedGoogle Scholar
• Jordan BD, Green GA, Galanty HL, Mandelbaum BR, Jabour BA. Acute and chronic brain injury in United States National Team Soccer Players. The American Journal of Sports Medicine 1996;24:690–696
   Google Scholar
• Sortland O, Tysvaer A. Brain damage in former association football players. Neuroradiology 1989;31:44–48
   PubMed Web of Science ®Google Scholar
• Koerte IK, Ertl-Wagner B, Reiser M, Zafonte R, Shenton ME. White matter integrity in the brains of professional soccer players without a symptomatic concussion. Journal of the American Medical Association 2012;308:1859–1861
   PubMed Web of Science ®Google Scholar
• Tysvaer A, Storli O, Bachen N. Soccer injuries to the brain. A neurologic and electroencephalographic study of former players. Acta Neurologica Scandinavica 1989;80:151–156
   PubMed Web of Science ®Google Scholar
• Tysvaer A, Storli O. Soccer injuries to the brain. A neurologic and electroencephalographic study of active football players. American Journal of Sports Medicine 1989;17:573–578
   PubMed Web of Science ®Google Scholar
• Kucera KL, Marshall SW, Bell DR, Distefano MJ, Goerger CP, Oyama S. Validity of soccer injury data from the National Collegiate Athletic Association’s Injury Surveillance System. Journal of Athletic Training 2011;46:489–499
   PubMed Web of Science ®Google Scholar
• Manzo G, Wadsworth LT. Comparison of injury-tracking programs. Current Sports Medicine Reports 2008;7:338–342
   PubMedGoogle Scholar
• Witol AD, Webbe FM. Soccer heading frequency predicts neuropsychological deficits. Archives of Clinical Neuropsychology 2003;18:397–417
   PubMed Web of Science ®Google Scholar
• Straume-Naesheim TM, Andersen TE, Holme IMK, McIntosh AS, Dvorak J, Bahr R. Do minor head impacts in soccer cause concussive injury? A prospective case-control study. Neurosurgery 2009;64:719–725
   PubMed Web of Science ®Google Scholar
• Mckee AC, Cantu RC, Nowinski CJ, Hedley-Whyte T, Gavett BE, Budson AE, Santini VE, Lee H-S, Kubilus CA, Stern RA. Chronic traumatic encephalopathy in athletes: Progressive tauopathy following repetitive head injnury. Journal of Neuropathology & Experimental Neurology 2009;68:709–735
   PubMed Web of Science ®Google Scholar
• Punnoose AR. Study raises concerns about “heading” in soccer, but jury is still out on risks. The Journal of the American Medical Association 2012;307:1012–1014
   Google Scholar
• Broglio SP, Ju Y-Y, Broglio MD, Sell TC. The efficacy of soccer headgear. Journal of Athletic Training 2003;38:220–224
   PubMed Web of Science ®Google Scholar
• Delaney JS, Al-Kashmiri A, Drummond R, Correa JA. The effect of protective headgear on head injuries and concussions in adolescent football (soccer) players. British Journal of Sports Medicine 2008;42:110–115; discussion 115
   PubMed Web of Science ®Google Scholar
• Levy ML, Kasasbeh AS, Baird LC, Amene C, Skeen J, Marshall L. Concussions in soccer: A current understanding. World Neurosurgery 2011;1:1–10
   Google Scholar
• Frommer LJ, Gurka KK, Cross KM, Ingersoll CD, Comstock RD, Saliba SA. Sex differences in concussion symptoms of high school athletes. Journal of Athletic Training 2011;46:76–84
   PubMed Web of Science ®Google Scholar
• Dick RW. Is there a gender difference in concussion incidence and outcomes? British Journal of Sports Medicine 2009;43(Suppl 1):i46–50
   PubMed Web of Science ®Google Scholar
• Bazarian JJ, Blyth B, Mookerjee S, He H, McDermott MP. Sex differences in outcome after mild traumatic brain injury. Journal of Neurotrauma 2010;27:527–539
   PubMed Web of Science ®Google Scholar
• Preiss-Farzanegan SJ, Chapman B, Wong TM, Wu J, Bazarian JJ. The relationship between gender and postconcussion symptoms after sport-related mild traumatic brain injury. PM&R: The Journal of Injury, Function, and Rehabilitation 2009;1:245–253
   PubMedGoogle Scholar
• Rauh MJ, Macera CA, Ji M, Wiksten DL. Subsequent injury patterns in girls’ high school sports. Journal of Athletic Training 2007;42:486–494
   PubMed Web of Science ®Google Scholar
• Dashnaw ML, Petraglia AL, Bailes JE. An overview of the basic science of concussion and subconcussion: Where we are and where we are going. Neurosurgical Focus 2012;33:E5
   PubMed Web of Science ®Google Scholar
• Cubon VA, Putukian M, Boyer C, Dettwiler A. A diffusion tensor imaging study on the white matter skeleton in individuals with sports-related concussion. Journal of Neurotrauma 2011;28:189–201
   PubMed Web of Science ®Google Scholar