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Management of concussion in soccer

  • Review Article - Brain trauma
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

When participating in contact sports, (mild) head trauma is a common incident—observed in both professional and amateur sports. When head trauma results in transient neurological impairment, a sports-related concussion has occurred. Acute concussion, repetitive concussions, as well as cumulative “sub-concussive” head impacts may increase the risk of developing cognitive and behavioral deficits for athletes, as well as accelerated cerebral degeneration. While this concept has been well established for classic contact sports like American Football, Rugby, or Boxing, there is still an awareness gap for the role of sports-related concussion in the context of the world’s most popular sport—Soccer.

Methods

Here, we review the relevance of sport-related concussion for Soccer as well as its diagnosis and management. Finally, we provide insight into future directions for research in this field.

Results

Soccer fulfills the criteria of a contact sport and is characterized by a high incidence of concussion. There is ample evidence that these events cause functional and structural cerebral disorders. Furthermore, heading, as a repeat sub-concussive impact, has been linked to structural brain changes and neurocognitive impairment. As a consequence, recommendations for the diagnosis and management of concussion in soccer have been formulated by consensus groups. In order to minimize the risk of repetitive concussion in soccer the rapid and reliable side-line diagnosis of concussion with adoption of a strict remove-from-play protocol is essential, followed by a supervised, graduated return-to-play protocol. Recent studies, however, demonstrate that adherence to these recommendations by players, coaches, clubs, and officials is insufficient, calling for stricter enforcement. In addition, future research to solidify the pathophysiological relevance of concussion for soccer athletes seems to be needed. Advanced neuroimaging and neurochemical biomarker analyses (e.g. S100β, tau and neurofilament light (NfL)) may assist in detecting concussion-related structural brain changes and selecting athletes at risk for irreversible damage.

Conclusion

Sports-related concussion represents a genuine neurosurgical field of interest. Given the high socioeconomic relevance, neurosurgeons should get involved in prevention and management of concussion in soccer.

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Abbreviations

CISG:

Concussion in Sports Group

CSF:

Cerebrospinal fluid

CT:

Computed tomography

CTE:

Chronic traumatic encephalopathy

DMN:

Default mode network

DTI:

Diffusion tensor imaging

FIFA:

Fédération Internationale de Football Association

fMRI:

Functional magnetic resonance imaging

GFAP:

Glial fibrillary acidic protein

MRI:

Magnetic resonance imaging

MRP:

Magnetic resonance perfusion

MRS:

Magnetic resonance spectroscopy

NAA:

N-acetylaspartate

NFL:

National Football League

NfL:

Neurofilament light

NSE:

Neuron specific enolase

PCS:

Post-concussion syndrome

PET:

Positron emission tomography

RTS:

Return to sport

SCAT:

Sport Concussion Assessment Tool

SIS:

Second impact syndrome

SRC:

Sports-related concussion

TBI:

Traumatic brain injury

TMS:

Transcranial magnetic stimulation

References

  1. Alosco M, Kasimis A, Stamm J et al (2017) Age of first exposure to American football and long-term neuropsychiatric and cognitive outcomes. Transl Psychiatry. https://doi.org/10.1038/tp.2017.197

  2. Bahrami N, Sharma D, Rosenthal S et al (2016) Subconcussive head impact exposure and white matter tract changes over a single season of youth football. Radiology 281(3):919–926

    Article  PubMed  Google Scholar 

  3. Barger SW, Van Eldik LJ (1992) S100 beta stimulates calcium fluxes in glial and neuronal cells. J Biol Chem 267(14):9689–9694

    CAS  PubMed  Google Scholar 

  4. Bleiberg J, Cernich AN, Cameron K, Sun W, Peck K, Ecklund PJ, Reeves D, Uhorchak J, Sparling MB, Warden DL (2004) Duration of cognitive impairment after sports concussion. Neurosurgery 54(5):1073–1078 discussion 1078-80

    Article  PubMed  Google Scholar 

  5. Blennow K, Brody DL, Kochanek PM, Levin H, McKee A, Ribbers GM, Yaffe K, Zetterberg H (2016) Traumatic brain injuries. Nat Rev Dis Prim 2:16084

    Article  PubMed  Google Scholar 

  6. Broglio SP, Macciocchi SN, Ferrara MS (2007) Neurocognitive performance of concussed athletes when symptom free. J Athl Train 42(4):504–508

    PubMed  PubMed Central  Google Scholar 

  7. Caccese JB, Kaminski TW (2016) Minimizing head acceleration in soccer: a review of the literature. Sports Med 46(11):1591–1604

    Article  PubMed  Google Scholar 

  8. Cantu RC (1998) Second-impact syndrome. Clin Sports Med 17(1):37–44

    Article  CAS  PubMed  Google Scholar 

  9. Cantu RC (2006) An overview of concussion consensus statements since 2000. Neurosurg Focus 21(4):1–6

    Article  Google Scholar 

  10. Castellani RJ, Perry G, Iverson GL (2015) Chronic effects of mild neurotrauma: putting the cart before the horse? J Neuropathol Exp Neurol 74(6):493–500

    Article  PubMed  Google Scholar 

  11. Collie A, Darby D, Maruv P (2001) Computerised cognitive assessment of athletes with sports related head injury. Br J Sports Med 35:297–302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Collie A, Maruff P (2003) Computerised neuropsychological testing. Br J Sports Med. https://doi.org/10.1136/bjsm.37.1.2

  13. Collins MW, Grindel SH, Lovell MR et al (1999) Relationship between concussion and neuropsychological performance in college football players. JAMA 282(10):964–970

    Article  CAS  PubMed  Google Scholar 

  14. Cusimano MD (2009) Canadian minor hockey participants’ knowledge about concussion. Can J Neurol Sci 36(3):315–320

    Article  PubMed  Google Scholar 

  15. Cusimano MD, Casey J, Jing R, Mishra A, Solarski M, Techar K, Zhang S (2017) Assessment of head collision events during the 2014 FIFA world cup tournament. JAMA 317(24):2548–2549

    Article  PubMed  PubMed Central  Google Scholar 

  16. Davis G (2017) Sport concussion assessment tool - 5th edition. Br J Sports Med. https://doi.org/10.1136/bjsports-2017-097506SCAT5

  17. Davis GA, Anderson V, Babl FE et al (2017) What is the difference in concussion management in children as compared with adults? A systematic review. Br J Sports Med 51(12):949–957

    Article  PubMed  Google Scholar 

  18. Dietrich MO, Tort AB, Schaf DV, Farina M, Gonçalves CA, Souza DO, Portela LV (2003) Increase in serum S100B protein level after a swimming race. Can J Appl Physiol 28(5):710–716

    Article  CAS  PubMed  Google Scholar 

  19. DiVirgilio TG, Hunter A, Wilson L, Stewart W, Goodall S, Howatson G, Donaldson DI, Ietswaart M (2016) Evidence for acute electrophysiological and cognitive changes following routine soccer heading. EBioMedicine 13:66–71

    Article  Google Scholar 

  20. Donato R (1999) Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta 1450(3):191–231

    Article  CAS  PubMed  Google Scholar 

  21. Echemendia RJ, Giza CC, Kutcher JS (2015) Developing guidelines for return to play: consensus and evidence-based approaches. Brain Inj 29(2):185–194

    Article  PubMed  Google Scholar 

  22. Gardner A, Iverson G, McCrory P (2014) Chronic traumatic encephalopathy in sport: a systematic review. Br J Sports Med 48:84–90

    Article  PubMed  Google Scholar 

  23. Gavett BE, Cantu RC, Shenton M, Lin AP, Nowinski CJ, McKee AC, Stern RA (2011) Clinical appraisal of chronic traumatic encephalopathy. Curr Opin Neurol 24(6):525–531

    Article  PubMed  Google Scholar 

  24. Gavett BE, Stern RA, Mckee AC (2011) Chronic traumatic encephalopathy: a potential late effect of sport-related concussive and subconcussive head trauma 1. Clin Sports Med. https://doi.org/10.1016/j.csm.2010.09.007

  25. Gessel LM, Fields SK, Collins CL, Dick RW, Dawn Comstock R (2007) Concussions among United States high school and collegiate athletes. J Athl Train 42(4):495–503

    PubMed  PubMed Central  Google Scholar 

  26. Gill J, Merchant-Borna K, Jeromin MA, Livingston W, Bazarian J (2017) Acute plasma tau relates to prolonged return to play after concussion. Neurology 88:595–602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Haimoto H, Hosoda S, Kato K (1987) Differential distribution of immunoreactive S100-alpha and S100-beta proteins in normal nonnervous human tissues. Lab Investig 57(5):489–498

    CAS  PubMed  Google Scholar 

  28. Haller S (2017) Advance MR imaging in sports-related concussion and mild traumatic brain injury - ready for clinical use? Eur J Neurosci 46:1954–1955

    Article  PubMed  Google Scholar 

  29. Harmon KG, Drezner JA, Gammons M, Guskiewicz KM, Halstead M, Herring SA, Kutcher JS, Pana A, Putukian M, Roberts WO (2013) American Medical Society for Sports Medicine position statement: concussion in sport. Br J Sports Med 4747:15–2615

    Article  Google Scholar 

  30. Hasselblatt M, Mooren FC, von Ahsen N, Keyvani K, Fromme A, Schwarze-Eicker K, Senner V, Paulus W (2004) Serum S100beta increases in marathon runners reflect extracranial release rather than glial damage. Neurology 62(9):1634–1636

    Article  CAS  PubMed  Google Scholar 

  31. Helmich I (2018) Game-specific characteristics of sport-related concussions. J Sports Med Phys Fitness 58(1–2):172–179

    PubMed  Google Scholar 

  32. Henry LC, Tremblay S, Boulanger Y, Ellemberg D, Lassonde M (2010) Neurometabolic changes in the acute phase after sports concussions correlate with symptom severity. J Neurotrauma 27(1):65–76

    Article  PubMed  Google Scholar 

  33. Iverson GL (2014) Chronic traumatic encephalopathy and risk of suicide in former athletes. Br J Sports Med 48(2):162–165

    Article  PubMed  Google Scholar 

  34. Iverson GL (2016) Suicide and chronic traumatic encephalopathy. J Neuropsychiatr Clin Neurosci 28(1):9–16

    Article  Google Scholar 

  35. Iverson GL, Gardner A, McCrory P, Zafronte R, Castellano R (2015) A critical review of chronic traumatic encephalopathy. Neurosci Biobehav Rev 56:276–293

    Article  PubMed  Google Scholar 

  36. Iverson GL, Keene C, Perry G, Castellani R (2018) The need to separate chronic traumatic encephalopathy neuropathology from clinical features. J Alzheimers Dis 61:17–28

    Article  PubMed  Google Scholar 

  37. Johnston KM, Bloom GA, Ramsay J, Kissick J, Montgomery D, Foley D, Chen J-K, Ptito A (2004) Current concepts in concussion rehabilitation. Curr Sports Med Rep 3:316–323

    PubMed  Google Scholar 

  38. Kamins J, Bigler E, Covassin T et al (2017) What is the physiological time to recovery after concussion? A systematic review. Br J Sports Med 51(12):935–940

    Article  PubMed  Google Scholar 

  39. Kerr ZY, Zuckerman SL, Wasserman EB, Covassin T, Djoko A, Dompier TP (2016) Concussion symptoms and return to play time in youth, high school, and college American football athletes. JAMA Pediatr 170(7):647

    Article  PubMed  Google Scholar 

  40. Kinnunen KM, Greenwood R, Powell JH, Leech R, Hawkins PC, Bonnelle V, Patel MC, Counsell SJ, Sharp DJ, Sharp DJ (2011) White matter damage and cognitive impairment after traumatic brain injury. Brain 134:449–463

    Article  PubMed  Google Scholar 

  41. Kirkendall DT, Jordan SE, Garrett WE (2001) Heading and head injuries in soccer. Sports Med 31(5):369–386

    Article  CAS  PubMed  Google Scholar 

  42. Koerte IK, Ertl-Wagner B, Reiser M, Zafonte R, Shenton ME (2012) White matter integrity in the brains of professional soccer players without a symptomatic concussion. JAMA 308(18):1859–1861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Kunz M (2007) 265 million playing football. Fifa Mag:10–15

  44. Lee YM, Odom MJ, Zuckerman SL, Solomon GS, Sills AK (2013) Does age affect symptom recovery after sports-related concussion? A study of high school and college athletes. J Neurosurg Pediatr J Neurosurg Pediatr 12(12):537–544

    Article  PubMed  Google Scholar 

  45. Leininger BE, Gramling SE, Farrell AD, Kreutzer JS, Peck Iii EA (1991) Neuropsychological deficits in symptomatic minor head injury patients after concussion and mild concussion. J Neurol Neurosurg Psychiatry 54:846–847

    Google Scholar 

  46. Levy ML, Kasasbeh AS, Baird LC, Amene C, Skeen J, Marshall L (2012) Concussions in soccer: a current understanding. World Neurosurg 78:535–544

    Article  PubMed  Google Scholar 

  47. Ling H, Morris HR, Neal JW, Lees AJ, Hardy J, Holton JL, Revesz T, Williams DDR (2017) Mixed pathologies including chronic traumatic encephalopathy account for dementia in retired association football (soccer) players. Acta Neuropathol 133:337–352

    Article  PubMed  PubMed Central  Google Scholar 

  48. Lipton ML, Kim N, Zimmerman ME, Kim M, Stewart WF, Branch CA, Lipton RB (2013) Soccer heading is associated with white matter microstructural and cognitive abnormalities. Radiology 268(3):850–857

    Article  PubMed  PubMed Central  Google Scholar 

  49. Llewellyn T, Burdette GT, Joyner AB, Buckley TA (2014) Concussion reporting rates at the conclusion of an intercollegiate athletic career. Clin J Sport Med 24(1):76–79

    Article  PubMed  Google Scholar 

  50. Lovell MR (2002) The relevance of neuropsychologic testing for sports-related head injuries. Curr Sports Med Rep 1(1):7–11

    Article  PubMed  Google Scholar 

  51. Lovell MR, Iverson GL, Collins MW, McKeag D, Maroon JC (1999) Does loss of consciousness predict neuropsychological decrements after concussion? Clin J Sport Med 9(4):193–198

    Article  CAS  PubMed  Google Scholar 

  52. Lovell MR, Iverson GL, Collins MW, Podell K, Johnston KM, Pardini D, Pardini J, Norwig J, Maroon JC (2006) Measurement of symptoms following sports-related concussion: reliability and normative data for the post-concussion scale. Appl Neuropsychol 13(3):166–174

    Article  PubMed  Google Scholar 

  53. Maher ME, Hutchison M, Cusimano M, Comper P, Schweizer TA (2014) Concussions and heading in soccer: a review of the evidence of incidence, mechanisms, biomarkers and neurocognitive outcomes. Brain Inj 28(3):271–285

    Article  PubMed  Google Scholar 

  54. Makdissi M, Cantu RC, Johnston KM, McCrory P, Meeuwisse WH (2013) The difficult concussion patient: what is the best approach to investigation and management of persistent (> 10 days) postconcussive symptoms? Br J Sports Med 47(5):308–313

  55. Manley G, Gardner AJ, Schneider KJ et al (2017) A systematic review of potential long-term effects of sport-related concussion. Br J Sports Med 51:969–977

    Article  PubMed  Google Scholar 

  56. Manville J, Laurer HL, Steudel W-I, Mautes AEM (2007) Changes in cortical and subcortical energy metabolism after repetitive and single controlled cortical impact injury in the mouse. J Mol Neurosci 31(2):95–100

    CAS  PubMed  Google Scholar 

  57. Marshak DR (1990) S100 beta as a neurotrophic factor. Prog Brain Res 86:169–181

    Article  CAS  PubMed  Google Scholar 

  58. Martland H (1928) Punch Drunk J Am Med Assoc 91(15):1103

    Article  Google Scholar 

  59. McCrea M, Meier T, Huber D et al (2017) Role of advanced neuroimaging, fluid biomarkers and genetic testing in the assessment of sport-related concussion: a systematic review. Br J Sports Med 51:919–929

    Article  PubMed  Google Scholar 

  60. McCrory PR, Berkovic SF (1998) Second impact syndrome. Neurology 50(3):677–683

    Article  CAS  PubMed  Google Scholar 

  61. McCrory P, Feddermann-Demont N (2017) What is the definition of sports-relted concussion: a systematic review. Zurich Open Repos Arch Univ Zurich. https://doi.org/10.1136/bjsports-2016-097393

  62. McCrory P, Johnston K, Meeuwisse W, Aubry M, Cantu R, Dvorak J, Graf-Baumann T, Kelly J, Lovell M, Schamasch P (2005) Summary and agreement statement of the 2nd International Conference on Concussion in port, Prague 2004. Br J Sports Med 39:196–204

    CAS  PubMed  PubMed Central  Google Scholar 

  63. McCrory P, Makdissi M, Davis G, Collie A (2005) Value of neuropsychological testing after head injuries in football. Br J Sports Med 39:58–63

    Article  Google Scholar 

  64. McCrory P, Meeuwisse WH, Aubry M et al (2013) Consensus statement on concussion in sport: the 4th International Conference on Concussion in sport, Zurich, November 2012. J Athl Train 48(4):554–575

    Article  PubMed  PubMed Central  Google Scholar 

  65. McCrory P, Meeuwisse W, Dvorak J et al (2017) Consensus statement on concussion in sport—the 5th international conference on concussion in sport held in Berlin, October 2016. Br J Sports Med. https://doi.org/10.1136/bjsports-2017-097699

  66. McKee AC, Cantu RC, Nowinski CJ, Tessa Hedley-Whyte E, Gavett BE, Budson AE, Santini VE, Lee H-S, Kubilus CA, Stern RA (2009) Chronic traumatic encephalopathy in athletes: progressive tauopathy following repetitive head injury. J Neuropathol Exp Neurol 68(7):709–735

    Article  PubMed  Google Scholar 

  67. McKee AC, Stein TD, Nowinski CJ et al (2013) The Spectrum of disease in chronic traumatic encephalopathy. Brain 136:43–64

    Article  PubMed  Google Scholar 

  68. McNamee MJ, Partridge B, Anderson L (2016) Concussion ethics and sports medicine. Clin Sports Med 35(2):257–267

    Article  PubMed  Google Scholar 

  69. Meaney DF, Smith DH (2011) Biomechanics of concussion. Clin Sports Med. https://doi.org/10.1016/j.csm.2010.08.009

  70. Mez J, Daneshvar DH, Kiernan PT et al (2017) Clinicopathological evaluation of chronic traumatic encephalopathy in players of American football. JAMA 318(4):360–370

    Article  PubMed  PubMed Central  Google Scholar 

  71. Millspaugh JA (1937) Dementia pugilistica. US Nav Med Bull 35:297–303

    Google Scholar 

  72. Morgan CD, Zuckerman SL, King LE, Beaird SE, Sills AK, Solomon GS (2015) Post-concussion syndrome (PCS) in a youth population: defining the diagnostic value and cost-utility of brain imaging. Childs Nerv Syst 31(12):2305–2309

    Article  PubMed  Google Scholar 

  73. Mussack T, Dvorak J, Graf-Baumann T, Jochum M (2003) Serum S-100B protein levels in young amateur soccer players after controlled heading and normal exercise. Eur J Med Res 8(10):457–464

    CAS  PubMed  Google Scholar 

  74. Neselius S, Zetterberg H, Blennow K, Randall J, Wilson D, Marcusson J, Brisby H (2013) Olympic boxing is associated with elevated levels of the neuronal protein tau in plasma. Brain Inj 27(4):425–433

    Article  PubMed  Google Scholar 

  75. O’Connor KL, Baker MM, Dalton SL, Dompier TP, Broglio SP, Kerr ZY (2017) Epidemiology of sport-related concussions in high school athletes: National Athletic Treatment, Injury and Outcomes Network (NATION), 2011–2012 through 2013–2014. J Athl Train 52(3):175–185

    Article  PubMed  PubMed Central  Google Scholar 

  76. Otto M, Holthusen S, Bahn E, Söhnchen N, Wiltfang J, Geese R, Fischer A, Reimers CD (2000) Boxing and running lead to a rise in serum levels of S-100B protein. Int J Sports Med 21(8):551–555

    Article  CAS  PubMed  Google Scholar 

  77. Papa L, Ramia MM, Edwards D, Johnson BD, Slobounov SM (2015) Systematic review of clinical studies examining biomarkers of brain injury in athletes after sports-related concussion. J Neurotrauma 32:661–673

    Article  PubMed  PubMed Central  Google Scholar 

  78. Partridge B (2014) Dazed and confused: sports medicine, conflicts of interest, and concussion management. J Bioeth Inq 11(1):65–74

    Article  PubMed  Google Scholar 

  79. Pauelsen M, Nyberg G, Tegner C, Tegner Y (2017) Concussion in ice hockey—a cohort study across 29 seasons. Clin J Sport Med 27(3):283–287

    Article  PubMed  Google Scholar 

  80. Pfister T, Pfister K, Hagel B, Ghali WA, Ronksley PE (2016) The incidence of concussion in youth sports: a systematic review and meta-analysis. Br J Sports Med 50:292–297

    Article  PubMed  Google Scholar 

  81. Reid MW, Cooper DB, Lu LH, Iverson GL, Kennedy JE (2018) Adversity and resilience are associated with outcome after mild traumatic brain injury in military service members. J Neurotrauma 35:1146–1155

    Article  PubMed  Google Scholar 

  82. Reynolds BB, Patrie J, Henry EJ, Goodkin HP, Broshek DK, Wintermark M, Druzgal TJ (2017) Comparative analysis of head impact in contact and collision sports. J Neurotrauma 34:38–49

    Article  PubMed  PubMed Central  Google Scholar 

  83. Routsi C, Stamataki E, Nanas S, Psachoulia C, Stathopoulos A, Koroneos A, Zervou M, Jullien G, Roussos C (2006) Increased levels of serum S100B protein in critically ill patients without brain injury. Shock 26(1):20–24

    Article  PubMed  Google Scholar 

  84. Rutherford A, Stephens R, Potter D (2003) The neuropsychology of heading and head trauma in association football (soccer): a review. Neuropsychol Rev 13(3):153–179

    Article  PubMed  Google Scholar 

  85. Shahim P, Gren M, Liman V et al (2016) Serum neurofilament light protein predicts clinical outcome in traumatic brain injury. Nat Publ Gr. https://doi.org/10.1038/srep36791

  86. Shahim P, Linemann T, Inekci D, Karsdal MA, Blennow K, Tegner Y, Zetterberg H, Henriksen K (2016) Serum tau fragments predict return to play in concussed professional ice hockey players. J Neurotrauma 33(22):1995–1999

    Article  PubMed  Google Scholar 

  87. Shahim P, Tegner Y, Gustafsson B et al (2016) Neurochemical aftermath of repetitive mild traumatic brain injury. JAMA Neurol 73(11):1308

    Article  PubMed  Google Scholar 

  88. Shahim P, Tegner Y, Marklund N, Blennow K, Zetterberg H, Shahim C (2018) Neurofilament light and tau as blood biomarkers for sports-related concussion. Neurology. https://doi.org/10.1212/WNL.0000000000005518

  89. Shahim P, Tegner Y, Wilson DH, Randall J, Skillbäck T, Pazooki D, Kallberg B, Blennow K, Zetterberg H (2014) Blood Biomarkers for brain injury in concussed professional ice hockey players. JAMA Neurol 71(6):684

    Article  PubMed  Google Scholar 

  90. Shitaka Y, Tran HT, Bennett RE, Sanchez L, Levy MA, Dikranian K, Brody DL (2011) Repetitive closed-skull traumatic brain injury in mice causes persistent multifocal axonal injury and microglial reactivity. J Neuropathol Exp Neurol 70(7):551–567

    Article  PubMed  Google Scholar 

  91. Spiotta AM, Bartsch AJ, Benzel EC (2012) Heading in soccer. Neurosurgery 70(1):1–11

    Article  PubMed  Google Scholar 

  92. Stalnacke B-M, Ohlsson A, Tegner Y, Sojka P (2006) 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. Br J Sports Med 40(4):313–316

    Article  PubMed  PubMed Central  Google Scholar 

  93. Tator C, Davis H (2014) The postconcussion syndrome in sports and recreation. Neurosurgery 75(suppl_4):S106–S112

    Article  PubMed  Google Scholar 

  94. Tator C, Davis H, Dufort P, Carmella Tartaglia M, Davis K, Ebraheem A, Hiploylee C (2016) Postconcussion syndrome: demographics and predictors in 221 patients. J Neurosurg 125:1206–1216

    Article  PubMed  Google Scholar 

  95. Terry DP, Huebschmann N, Maxwell B, Cook N, Mannix R, Zafonte RD, Seifert T, Berkner PD, Iverson GL (2018) Pre-injury migraine history as a risk factor for prolonged return to school and sports following concussion. J Neurotrauma. https://doi.org/10.1089/neu.2017.5443

  96. Terwilliger VK, Pratson L, Vaughan CG, Gioia GA (2016) Additional post-concussion impact exposure may affect recovery in adolescent athletes. J Neurotrauma 33:761–765

    Article  PubMed  PubMed Central  Google Scholar 

  97. Turner RC, Lucke-Wold BP, Robson MJ, Omalu BI, Petraglia AL, Bailes JE, Hayes RL, Mondello S, Biomarkers B (2013) Repetitive traumatic brain injury and development of chronic traumatic encephalopathy: a potential role for biomarkers in diagnosis, prognosis, and treatment? Front Neurol. https://doi.org/10.3389/fneur.2012.00186

  98. Vagnozzi R, Signoretti S, Cristofori L et al (2010) Assessment of metabolic brain damage and recovery following mild traumatic brain injury: a multicentre, proton magnetic resonance spectroscopic study in concussed patients. Brain 133(11):3232–3242

    Article  PubMed  Google Scholar 

  99. Yengo-Khan A, Hale A, Zalneraitis B, Zuckerman S, Sills A, Solomon G (2016) The sport concussion assessment tool: a systematic review. Neurosurg Focus. https://doi.org/10.3171/2016.1.FOCUS15611

  100. Zetterberg H, Hietala MA, Jonsson M et al (2006) Neurochemical aftermath of amateur boxing. Arch Neurol 63(9):1277

    Article  PubMed  Google Scholar 

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Hubertus, V., Marklund, N. & Vajkoczy, P. Management of concussion in soccer. Acta Neurochir 161, 425–433 (2019). https://doi.org/10.1007/s00701-019-03807-6

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