3,052
Views
39
CrossRef citations to date
0
Altmetric
Original Articles

Neurophysiological and cognitive impairment following repeated sports concussion injuries in retired professional rugby league players

ORCID Icon, , , &
Pages 498-505 | Received 12 Feb 2017, Accepted 17 Jan 2018, Published online: 01 Feb 2018

References

  • Guskiewicz KM, Marshall SW, Bailes J, McCrea M, Cantu RC, Randolph C, Jordan BD. Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery. 2005;57(4):719–26. doi:10.1093/neurosurgery/57.4.719.
  • De Beaumont L, Théoret H, Mongeon D, Messier J, Leclerc S, Tremblay S, Ellemberg D, Lassonde M. Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain. 2009;132(3):695–708. doi:10.1093/brain/awn347.
  • Daneshvar DH, Nowinski CJ, McKee A, Cantu RC. The epidemiology of sport-related concussion. Clin Sports Med. 2011;30(1):1–17. doi:10.1016/j.csm.2010.08.006.
  • Jordan BD, Bailes JE. Concussion history and current neurological symptoms among retired professional football players. Neurology. 2000;54(suppl 3):A410–411.
  • Stamm JM, Bourlas AP, Baugh CM, Fritts NG, Daneshvar DH, Martin BM, McClean MD, Tripodis Y, Stern RA. Age of first exposure to football and later-life cognitive impairment in former NFL players. Neurology. 2015;84(11):1114–20. doi:10.1212/WNL.0000000000001358.
  • Stamm JM, Koerte IK, Muehlmann M, Pasternak O, Bourlas AP, Baugh CM, Giwerc MY, Zhu A, Coleman MJ, Bouix S, et al. Age at first exposure to football is associated with altered corpus callosum white matter microstructure in former professional football players. J Neurotrauma. 2015;32:1768–76. doi:10.1089/neu.2014.3822.
  • Koerte IK, Mayinger M, Muehlmann M, Kaufmann D, Lin AP, Steffinger D, Fisch B, Rauchmann B-S, Immler S, Karch S. Cortical thinning in former professional soccer players. Brain Imaging Behav. 2016;10:792–98. doi:10.1007/s11682-015-9442-0.
  • Gardner A, Iverson GL, Levi CR, Schofield PW, Kay-Lambkin F, Kohler RM, Stanwell P. A systematic review of concussion in rugby league. Br J Sports Med. 2015;49(8):495–98. doi:10.1136/bjsports-2013-093102.
  • Williams S, Trewartha G, Kemp S, Stokes K. A meta-analysis of injuries in senior men’s professional rugby union. Sports Med. 2013;43(10):1043–55. doi:10.1007/s40279-013-0078-1.
  • Roberts S, Trewartha G, England M, Goodison W, Stokes K. Concussion and head injuries in English community rugby union match play: community rugby union head injuries. Am J Sports Med. 2017;45(2):480–87. doi:10.1177/0363546516668296.
  • Hinton-Bayre A, Geffen G, Friis P. Presentation and mechanisms of concussion in professional rugby league football. J Sci Med Sport. 2004;7(3):400–04. doi:10.1016/S1440-2440(04)80035-5.
  • Hoskins W, Pollard H, Hough K, Tully C. Injury in rugby league. J Sci Med Sport. 2006;9(1):46–56. doi:10.1016/j.jsams.2006.03.013.
  • King D, Gissane C, Hume P, Flaws M. The King–devick test was useful in management of concussion in amateur rugby union and rugby league in New Zealand. J Neurol Sci. 2015;351(1):58–64. doi:10.1016/j.jns.2015.02.035.
  • Hume PA, Theadom A, Lewis GN, Quarrie KL, Brown SR, Hill R, Marshall SW. A comparison of cognitive function in former rugby union players compared with former non-contact-sport players and the impact of concussion history. Sports Medicine. 2016;1–12. doi:10.1007/s40279-016-0608-8.
  • McMillan T, McSkimming P, Wainman-Lefley J, Maclean L, Hay J, McConnachie A, Stewart W. Long-term health outcomes after exposure to repeated concussion in elite level: rugby union players. J Neurol Neurosurg Psychiatry. 2017;88(6):505–11. doi:10.1136/jnnp-2016-314279.
  • Gardner AJ, Iverson GL, Quinn TN, Makdissi M, Levi CR, Shultz SR, Wright DK, Stanwell P. A preliminary video analysis of concussion in the National Rugby League. Brain Inj. 2015;29(10):1182–85. doi:10.3109/02699052.2015.1034179.
  • Pearce AJ, Hoy K, Rogers MA, Corp DT, Maller JJ, Drury HG, Fitzgerald PB. The long-term effects of sports concussion on retired Australian football players: a study using transcranial magnetic stimulation. J Neurotrauma. 2014;31(3):1139–45. doi:10.1089/neu.2013.3219.
  • Major BP, Rogers MA, Pearce AJ. Using transcranial magnetic stimulation to quantify electrophysiological changes following concussive brain injury: a systematic review. Clin Exp Pharmacol Physiol. 2015;42:394–405. doi:10.1111/1440-1681.12363.
  • Di Virgilio TG, Hunter A, Wilson L, Stewart W, Goodall S, Howatson G, Donaldson DI, Ietswaart M. Evidence for acute electrophysiological and cognitive changes following routine soccer heading. EBioMedicine. 2016;13:66–71. doi:10.1016/j.ebiom.2016.10.029.
  • Pearce AJ. The neurophysiological response following sub-concussive Soccer heading. EBioMedicine. 2016;13:3–4. doi:10.1016/j.ebiom.2016.10.043.
  • Bryden M. Measuring handedness with questionnaires. Neuropsychologia. 1977;15(4):617–24. doi:10.1016/0028-3932(77)90067-7.
  • AFL Medical Officers Association. The management of concussion in Australian football. Melbourne, Australia: Australian Football League; 2011.
  • Pearce AJ, Hoy K, Rogers MA, Corp DT, Davies CB, Maller JJ, Fitzgerald PB. Acute motor, neurocognitive and neurophysiological change following concussion injury in Australian amateur football. A prospective multimodal investigation. J Sci Med Sport. 2015;18:500–06. doi:10.1016/j.jsams.2014.07.010.
  • Gloss DS, Wardle MG. Use of a test of psychomotor ability in an expanded role. Percept Mot Skills. 1981;53(2):659–62. doi:10.2466/pms.1981.53.2.659.
  • Yancosek KE, Howell D. A narrative review of dexterity assessments. J Hand Ther. 2009;22(3):258–70. doi:10.1016/j.jht.2008.11.004.
  • Corlett E, Salvendy G, Seymour W. Selecting operators for fine manual tasks: a study of the O’Connor finger dexterity test and the purdue pegboard. Occup Psychol. 1971;45:57–65.
  • Berger MAM, Krul AJ, Daanen HAM. Task specificity of finger dexterity tests. Appl Ergon. 2009;40:145–47. doi:10.1016/j.apergo.2008.01.014.
  • Sandberg MA. Cambridge neuropsychological testing automated battery, in encyclopedia of clinical neuropsychology. In: Kreutzer J, editor. New York: Springer; 2011. p. 480–82.
  • Owen AM, Downes JJ, Sahakian BJ, Polkey CE, Robbins TW. Planning and spatial working memory following frontal lobe lesions in man. Neuropsychologia. 1990;28(10):1021–34. doi:10.1016/0028-3932(90)90137-D.
  • Hallett M. Transcranial magnetic stimulation and the human brain. Nature. 2000;406:147–50. doi:10.1038/35018000.
  • Wilson SA, Thickbroom GW, Mastaglia FL. Topography of excitatory and inhibitory muscle responses evoked by transcranial magnetic stimulation in the human motor cortex. Neurosci Lett. 1993;154:52–56.
  • Pearce AJ, Kidgell DJ. Corticomotor excitability during precision motor tasks. J Sci Med Sport. 2009;12:280–83. doi:10.1016/j.jsams.2007.12.005.
  • Pearce AJ, Kidgell DJ. Comparison of corticomotor excitability during visuomotor dynamic and static tasks. J Sci Med Sport. 2010;13:167–71. doi:10.1016/j.jsams.2008.12.632.
  • Hermens HJ, Freriks B, Merletti R, Stegeman D, Blok J, Rau G, Disselhorst-Klug C, Hägg G. European recommendations for surface electromyography. Enschede, The Netherlands: Roessingh Research and Development; 1999.
  • Pearce AJ, Thickbroom GW, Byrnes ML, Mastaglia FL. The corticomotor representation of elite racquet sport athletes. Exp Brain Res. 2000;130:238–43. doi:10.1007/s002219900236.
  • Ziemann U, Lönnecker S, Steinhoff B, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol. 1996;40(3):367–78. doi:10.1002/ana.410400306.
  • Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol. 2003;2(3):145–56. doi:10.1016/S1474-4422(03)00321-1.
  • Wilson SA, Lockwood RJ, Thickbroom GW, Mastaglia FL. The muscle silent period following transcranial magnetic cortical stimulation. J Neurol Sci. 1993;114(2):216–22. doi:10.1016/0022-510X(93)90301-E.
  • Pearce AJ, Clark RA, Kidgell DJ. A comparison of two methods in acquiring stimulus–response curves with transcranial magnetic stimulation. Brain Stimul. 2013;6(3):306–09. doi:10.1016/j.brs.2012.05.010.
  • Rossini P, Berardelli A, Deuschl G, Hallett M, Maertens de Noordhout A, Paulus W, Pauri F. Applications of magnetic cortical stimulation. Electroencephalogr Clin Neurophysiol Suppl. 1999;52:171–85.
  • Ziemann U. Pharmaco-transcranial magnetic stimulation studies of motor excitability. In: Lozano AM, Hallett M, editors. Handbook of clinical neurology. Amsterdam, The Netherlands: Elsevier; 2013. p. 387–97.
  • Kidgell DJ, Pearce AJ. Corticospinal properties following short-term strength training of an intrinsic hand muscle. Hum Mov Sci. 2010;29(5):631–41. doi:10.1016/j.humov.2010.01.004.
  • Cantello R, Gianelli M, Civardi C, Mutani R. Magnetic brain stimulation The silent period after the motor evoked potential. Neurology. 1992;42(10):1951–1951. doi:10.1212/WNL.42.10.1951.
  • Connors B, Malenka R, Silva L. Two inhibitory postsynaptic potentials, and GABAa and GABAb receptor‐mediated responses in neocortex of rat and cat. J Physiol. 1988;406(1):443–68. doi:10.1113/jphysiol.1988.sp017390.
  • Kujirai T, Caramia M, Rothwell J, Day B, Thompson P, Ferbert A, Wroe S, Asselman P, Marsden C. Corticocortical inhibition in human motor cortex. J Physiol. 1993;471(1):501–19. doi:10.1113/jphysiol.1993.sp019912.
  • McGinley M, Hoffman RL, Russ DW, Thomas JS, Clark BC. Older adults exhibit more intracortical inhibition and less intracortical facilitation than young adults. Exp Neurol. 2010;45(9):671–78. doi:10.1016/j.exger.2010.04.005.
  • Hammond G, Vallence A-M. Modulation of long-interval intracortical inhibition and the silent period by voluntary contraction. Brain Res. 2007;1158:63–70. doi:10.1016/j.brainres.2007.05.014.
  • Benwell NM, Mastaglia FL, Thickbroom GW. Differential changes in long-interval intracortical inhibition and silent period duration during fatiguing hand exercise. Exp Brain Res. 2007;179(2):255–62. doi:10.1007/s00221-006-0790-2.
  • Cohen J. Statistical power analysis for the behavioral sciences. Hillsdale, NJ: Erlbaum; 1988.
  • Finch CF, Clapperton AJ, McCrory P. Increasing incidence of hospitalisation for sport-related concussion in Victoria, Australia. Med J Aust. 2013;198(8):427–30. doi:10.5694/mja12.11217.
  • De Beaumont L, Brisson B, Lassonde M, Jolicoeur P. Long-term electrophysiological changes in athletes with a history of multiple concussions. Brain Inj. 2007;21(6):631–44. doi:10.1080/02699050701426931.
  • De Beaumont L, Lassonde M, Leclerc S, Théoret H. Long‐term and cumulative rffects of sports concussion on motor cortex inhibition. Neurosurgery. 2007;61(2):329–37. doi:10.1227/01.NEU.0000280000.03578.B6.
  • Sandbrink F.The MEP in clinical neurodiagnosis. In: Wasserman EM, Epstein CM, Ziemann U, Walsh V, Paus T, Lisanby SH, editors.The oxford handbook of transcranial stimulation. Oxford: Oxford University Press; 2008. p. 237–83.
  • Mills K. Magnetic stimulation of the human nervous system. New York, NY: Oxford University Press; 1999.
  • Livingston SC, Goodkin HP, Ingersoll CD. The influence of gender, hand dominance, and upper extremity length on motor evoked potentials. J Clin Monit Comput. 2010;24:427–36. doi:10.1007/s10877-010-9267-8.
  • Ghezzi A, Callea L, Zaffaroni M, Zibetti A, Montanini R. Study of central and peripheral motor conduction in normal subjects. Acta Neurol Scand. 1991;84(6):503–06. doi:10.1111/j.1600-0404.1991.tb05003.x.
  • Rabadi MH, Jordan BD. The cumulative effect of repetitive concussion in sports. Clin J Sport Med. 2001;11(3):194–98. doi:10.1097/00042752-200107000-00011.
  • McCrory P, Meeuwisse W, Dvorak J, Aubry M, Bailes J, Broglio S, Cantu RC, Cassidy D, Echemendia RJ, Castellani RJ, et al. Consensus statement on concussion in sport—the 5th international conference on concussion in sport held in Berlin, October 2016. Br J Sports Med. 2017;51:838–47. doi:10.1136/bjsports-2017-097699.
  • Chen R, Lozano AM, Ashby P. Mechanism of the silent period following transcranial magnetic stimulation evidence from epidural recordings. Exp Brain Res. 1999;128(4):539–42. doi:10.1007/s002210050.
  • Davies CH, Starkey SJ, Pozza MF, Collingridge GL. GABAb autoreceptors regulate the induction of LTP. Nature. 1991;349:609–11. doi:10.1038/349609a0.
  • Mott DD, Lewis DV. Facilitation of the induction of long-term potentiation by GABAb receptors. Science. 1991;252:1718–20. doi:10.1126/science.1675489.
  • Sale MV, Semmler JG. Age-related differences in corticospinal control during functional isometric contractions in left and right hands. J Appl Physiol. 2005;99:1483–93. doi:10.1152/japplphysiol.00371.2005.
  • Oliviero A, Profice P, Tonali PA, Pilato F, Saturno E, Dileone M, Ranieri F, Di Lazzaro V. Effects of aging on motor cortex excitability. Neurosci Res. 2006;55(1):74–77. doi:10.1016/j.neures.2006.02.002.
  • Wolters A, Ziemann U, Benecke R. The cortical silent period. In: Wasserman EM, Epstein CM, Ziemann U, Walsh V, Paus T, Lisanby SH, editors.The Oxford Handbook of Transcranial Stimulation. London: Oxford University Press; 2008. p. 91–102.
  • Modugno N, Curra A, Giovannelli M, Priori A, Squitieri F, Ruggieri S, Manfredi M, Berardelli A. The prolonged cortical silent period in patients with Huntington’s disease. Clin Neurophysiol. 2001;112(8):1470–74. doi:10.1016/S1388-2457(01)00599-5.
  • Magnus-Haraldsson H, Ferrarelli F, Kalin NH, Tononi G. Transcranial magnetic stimulation in the investigation and treatment of schizophrenia: a review. Schizophr Res. 2004;71:1–16. doi:10.1016/j.schres.2003.10.006.
  • Bunse T, Wobrock T, Strube W, Padberg F, Palm U, Falkai P, Hasan A. Motor cortical excitability assessed by transcranial magnetic stimulation in psychiatric disorders: a systematic review. Brain Stimul. 2014;7(2):158–69. doi:10.1016/j.brs.2013.08.009.
  • Radhu N, De Jesus DR, Ravindran LN, Zanjani A, Fitzgerald PB, Daskalakis ZJ. A meta-analysis of cortical inhibition and excitability using transcranial magnetic stimulation in psychiatric disorders. Clin Neurophysiol. 2013;124(7):1309–20. doi:10.1016/j.clinph.2013.01.014.
  • Nadone R, Golaszewski S, Trinka E. Dementia. In: Aminoff MJ, Boller F, Swaab DF, editors. Handbook of clinical neurology: brain stimulation. Edinburgh: Elsevier; 2013. p. 599–611.
  • McIntosh AS, McCrory P, Comerford J. The dynamics of concussive head impacts in rugby and Australian Rules football. Med Sci Sport Exer. 2000;32(12):1980–84. doi:10.1097/00005768-200012000-00002.
  • Beckwith JG, Greenwald RM, Chu JJ, Crisco JJ, Rowson S, Duma SM, Broglio SP, McAllister TW, Guskiewicz KM, Mihalik JP. Timing of concussion diagnosis is related to head impact exposure prior to injury. Med Sci Sport Exer. 2012;45:747–54. doi:10.1249/MSS.0b013e3182793067.
  • Kerr ZY, Marshall SW, Guskiewicz KM. Reliability of concussion history in former professional football players. Med Sci Sport Exer. 2012;44(3):377–82. doi:10.1249/MSS.0b013e31823240f2.
  • Robbins CA, Daneshvar DH, Picano JD, Gavett BE, Baugh CM, Riley DO, Nowinski CJ, McKee AC, Cantu RC, Stern RA. Self-reported concussion history: impact of providing a definition of concussion. Open Access J Sports Med. 2014;5:99. doi:10.2147/OAJSM.S58005.
  • Gardner AJ, Iverson GL, Wojtowicz M, Levi CR, Kay-Lambkin F, Schofield PW, Zafonte R, Shultz SR, Lin AP, Stanwell P. MR Spectroscopy findings in retired professional rugby league players. Int J Sports Med. 2017;38(03):241–52. doi:10.1055/s-0042-120843.
  • Delaney JS, Lacroix VJ, Gagne C, Antoniou J. Concussions among university football and soccer players: a pilot study. Clin J Sport Med. 2001;11(4):234–40. doi:10.1097/00042752-200110000-00005.
  • Ward JA. The physiology of concussion. Clin Neurosurg. 1964;12:95–111.
  • Kim DH, Zaremski J, Kwon B, Jenis L, Woodard E, Bode R, Banco RJ. Risk factors for false positive transcranial motor evoked potential monitoring alerts during surgical treatment of cervical myelopathy. Spine. 2007;32(26):3041–46. doi:10.1097/BRS.0b013e31815d0072.
  • Lieberman JA, Lyon R, Feiner J, Diab M, Gregory GA. The effect of age on motor evoked potentials in children under propofol/isoflurane anesthesia. Anesth Analg. 2006;103(2):316–21. doi:10.1213/01.ane.0000226142.15746.b2.
  • Nollet H, Deprez P, Ham L, Dewulf J, Decleir A, Vanderstraeten G. Transcranial magnetic stimulation: normal values of magnetic motor evoked potentials in 84 normal horses and influence of height, weight, age and sex. Equine Vet J. 2004;36(1):51–57. doi:10.2746/0425164044864660.
  • Rijckaert J, Pardon B, Verryken K, Van Ham L, Van Loon G, Deprez P. Motor evoked potentials in standing and recumbent calves induced by magnetic stimulation at the foramen magnum. Vet J. 2016;216(Supplement C):178–82. doi:10.1016/j.tvjl.2016.08.006.
  • Keller CJ, Honey CJ, Mégevand P, Entz L, Ulbert I, Mehta AD. Mapping human brain networks with cortico-cortical evoked potentials. Philos Trans Royal Soc B. 2014;369(1653):20130528. doi:10.1098/rstb.2013.0528.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.