Download PDF
Int J Sports Med 2016; 37(09): 714-722
DOI: 10.1055/s-0042-107250
Clinical Sciences
© Georg Thieme Verlag KG Stuttgart · New York

Investigating a Novel Measure of Brain Networking Following Sports Concussion

S. P. Broglio
1   University of Michigan, Neurotrauma Research Laboratory, Ann Arbor, United States
,
A. Rettmann
2   NeuroTrauma Research Laboratory, University of Michigan, Ann Arbor, United States
,
J. Greer
3   Michigan NeuroSport, University of Michigan, Ann Arbor, United States
,
S. Brimacombe
3   Michigan NeuroSport, University of Michigan, Ann Arbor, United States
,
B. Moore
3   Michigan NeuroSport, University of Michigan, Ann Arbor, United States
,
N. Narisetty
4   Department of Statistics, University of Michigan, Ann Arbor, United States
,
X. He
4   Department of Statistics, University of Michigan, Ann Arbor, United States
,
J. Eckner
5   Department of Physical Medicine and Rehabilitation, University of Michigan, Ann Arbor, Michigan, United States
› Author Affiliations
Further Information

Publication History



accepted after revision 04 August 2016

Publication Date:
10 June 2016 (online)

Also available at
    Permissions and Reprints

Abstract

Clinicians managing sports-related concussions are left to their clinical judgment in making diagnoses and return-to-play decisions. This study was designed to evaluate the utility of a novel measure of functional brain networking for concussion management. 24 athletes with acutely diagnosed concussion and 21 control participants were evaluated in a research laboratory. At each of the 4 post-injury time points, participants completed the Axon assessment of neurocognitive function, a self-report symptom inventory, and the auditory oddball and go/no-go tasks while electroencephalogram (EEG) readings were recorded. Brain Network Activation (BNA) scores were calculated from EEG data related to the auditory oddball and go/no-go tasks. BNA scores were unable to differentiate between the concussed and control groups or by self-report symptom severity. These findings conflict with previous work implementing electrophysiological assessments in concussed athletes, suggesting that BNA requires additional investigation and refinement before clinical implementation.

Key Words

concussion - brain network activation (BNA) - electrophysiology
 

  • References

  • 1 Bazarian JJ, Zhu T, Blyth B, Borrino A, Zhong J. Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion. Magn Reson Imaging 2011; 30: 171-180
    PubMedSearch in Google Scholar
  • 2 Bazarian JJ, Zhu T, Zhong J, Janigro D, Rozen E, Roberts A, Javien H, Merchant-Borna K, Abar B, Blackman EG. Persistent, long-term cerebral white matter changes after sports-related repetitive head impacts. PLoS One 2014; 9: e94734
    CrossrefPubMedSearch in Google Scholar
  • 3 Breedlove EL, Robinson M, Talavage TM, Morigaki KE, Yoruk U, O'Keefe K, King J, Leverenz LJ, Gilger JW, Nauman EA. Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football. J Biomech 2012; 45: 1265-1272
    CrossrefPubMedSearch in Google Scholar
  • 4 Broglio SP, Cantu RC, Gioia GA, Guskiewicz KM, Kutcher JS, Palm M, Valovich-Mcleod T. National Athletic Trainers’ Association position statement: management of sport concussion. J Athl Train 2014; 49: 245-265
    CrossrefPubMedSearch in Google Scholar
  • 5 Broglio SP, Ferrara MS, Macciocchi SN, Baumgartner TA, Elliott R. Test-retest reliability of computerized concussion assessment programs. J Athl Train 2007; 42: 509-514
    PubMedSearch in Google Scholar
  • 6 Broglio SP, Macciocchi SN, Ferrara MS. Sensitivity of the concussion assessment battery. Neurosurgery 2007; 60: 1050-1057
    CrossrefPubMedSearch in Google Scholar
  • 7 Broglio SP, Moore RD, Hillman CH. A history of sport-related concussion on event-related brain potential correlates of cognition. Int J Psychophysiol 2011; 82: 16-23
    CrossrefPubMedSearch in Google Scholar
  • 8 Broglio SP, Pontifex MB, O’Connor P, Hillman CH. The persistent effects of concussion on neuroelectic indices of attention. J Neurotrauma 2009; 26: 1463-1470
    CrossrefPubMedSearch in Google Scholar
  • 9 Broglio SP, Zhu W, Sopiarz K, Park Y. Generalizability theory analysis of balance error scoring system reliability in healthy young adults. J Athl Train 2009; 44: 497-502
    CrossrefPubMedSearch in Google Scholar
  • 10 Chen JK, Johnston KM, Collie A, McCrory P, Ptito A. A validation of the post concussion symptom scale in the assessment of complex concussion using cognitive testing and functional MRI. J Neurol Neurosurg Psychiatry 2007; 78: 1231-1238
    CrossrefPubMedSearch in Google Scholar
  • 11 Chen JK, Johnston KM, Frey S, Petrides M, Worsley K, Ptito A. Functional abnormalities in symptomatic concussed athletes: an fMRI study. Neuroimage 2004; 22: 68-82
    CrossrefPubMedSearch in Google Scholar
  • 12 Collie A, Makdissi M, Maruff P, Bennell KL, McCrory P. Cognition in the days following concussion: comparison of symptomatic versus asymptomatic athletes. J Neurol Neurosurg Psychiatry 2006; 77: 241-245
    CrossrefPubMedSearch in Google Scholar
  • 13 Collie A, Maruff P, Makdissi M, McCrory P, McStephen M, Darby D. CogSport: Reliability and correlation with conventional cognitive tests used in postconcussion medical evaluations. Clin J Sport Med 2003; 13: 28-32
    CrossrefPubMedSearch in Google Scholar
  • 14 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: 631-644
    CrossrefPubMedSearch in Google Scholar
  • 15 De Beaumont L, Theoret 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: 695-708
    CrossrefPubMedSearch in Google Scholar
  • 16 Dupuis F, Johnston KM, Lavoie M, Lepore F, Lassonde M. Concussion in athletes produce brain dysfunction as revealed by event-related potentials. Neuroreport 2000; 11: 4087-4092
    CrossrefPubMedSearch in Google Scholar
  • 17 Echemendia RJ, Bruce JM, Bailey CM, Sanders JF, Arnett P, Vargas G. The utility of post-concussion neuropsychological data in identifying cognitive change following sports-related MTBI in the absence of baseline data. Clin Neuropsychol 2012; 26: 1077-1091
    CrossrefPubMedSearch in Google Scholar
  • 18 Fedor A, Gunstad J. Limited knowledge of concussion symptoms in college athletes. Appl Neuropsychol Adult 2015; 22: 108-113
    PubMedSearch in Google Scholar
  • 19 Field M, Collins MW, Lovell MR, Maroon JC. Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. J Pediatr 2003; 142: 546-553
    CrossrefPubMedSearch in Google Scholar
  • 20 Gaetz M, Weinberg H. Electrophysiological indices of persistent post-concussion symptoms. Brain Inj 2000; 14: 815-832
    CrossrefPubMedSearch in Google Scholar
  • 21 Gibson TB, Herring SA, Kutcher JS, Broglio SP. Analyzing the effect of state legislation on health care utilization for children with concussion. JAMA Pediatr 2015; 169: 163-168
    CrossrefPubMedSearch in Google Scholar
  • 22 Giza CC, Hovda DA. The new neurometabolic cascade of concussion. Neurosurgery 2014; 75 (Suppl. 04) S24-S33
    CrossrefPubMedSearch in Google Scholar
  • 23 Giza CC, Kutcher JS, Ashwal S, Barth J, Getchius TS, Gioia GA, Gronseth GS, Guskiewicz KM, Mandel S, Manley G, McKeag DB, Thurman DJ, Zafonte R. Summary of evidence-based guideline update: Evaluation and management of concussion in sports: Report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology 2013; 80: 2250-2257
    CrossrefPubMedSearch in Google Scholar
  • 24 Gosselin N, Theriault M, Leclerc S, Montplaisir J, Lassonde M. Neurophysiological anomalies in symptomatic and asymptomatic concussed athletes. Neurosurgery 2006; 58: 1151-1161
    CrossrefPubMedSearch in Google Scholar
  • 25 Harmon KG, Drezner J, Gammons M, Guskiewicz KM, Halstead M, Herring SA, Kutcher JS, Pana A, Putukian M, Roberts W. American Medical Society for Sports Medicine. American Medical Society for Sports Medicine position statement: concussion in sport. Clin J Sport Med 2013; 23: 1-18
    CrossrefPubMedSearch in Google Scholar
  • 26 Harriss DJ, Atkinson G. Ethical Standards in Sport and Exercise Science Research: 2016 Update. Int J Sports Med 2015; 36: 1121-1124
    Search in Google Scholar
  • 27 Henry LC, Elbin RJ, Collins MW, Marchetti G, Kontos AP. Examining recovery trajectories after sport-related concussion with a multimodal clinical assessment approach. Neurosurgery 2016; 78: 232-241
    CrossrefPubMedSearch in Google Scholar
  • 28 Herring SA, Cantu RC, Guskiewicz KM, Putukian M, Kibler WB, Bergfeld JA, Boyajian-O’Neill LA, Franks RR, Indelicato PA. American College of Sports Medicine. Concussion (mild traumatic brain injury) and the team physician: a consensus statement−2011 update. Med Sci Sports Exerc 2011; 43: 2412-2422
    CrossrefPubMedSearch in Google Scholar
  • 29 Iverson GL, Lange RT. Examination of “postconcussion-like” symptoms in a healthy sample. Appl Neuropsychol 2003; 10: 137-144
    CrossrefPubMedSearch in Google Scholar
  • 30 Kiefer AW, Barber Foss K, Reches A, Gadd B, Gordon M, Rushford K, Laufer I, Weiss M, Myer GD. Brain network activation as a novel biomarker for the return-to-play pathway following sport-related brain injury. Front Neurol 2015; 6: 243
    PubMedSearch in Google Scholar
  • 31 Kontos AP, Reches A, Elbin RJ, Dickman D, Laufer I, Geva AB, Shacham G, DeWolf R, Collins MW. Preliminary evidence of reduced brain network activation in patients with post-traumatic migraine following concussion. Brain Imaging Behav in press
    PubMed
  • 32 Langlois JA, Rutland-Brown W, Wald MM. The epidemiology and impact of traumatic brain injury: A brief overview. J Head Trauma Rehabil 2006; 21: 375-378
    CrossrefPubMedSearch in Google Scholar
  • 33 Leahy S. Peyton Manning admits to tanking NFL’s baseline concussion test. In: USA Today. 4/27/2011 ed
    PubMed
  • 34 Llewellyn T, Burdette GT, Joyner AB, Buckley TA. Concussion reporting rates at the conclusion of an intercollegiate athletic career. Clin J Sport Med 2014; 24: 76-79
    CrossrefPubMedSearch in Google Scholar
  • 35 Lovell MR, Iverson GL, Collins MW, Podell K, Johnston KM, Pardini JE, Pardini JE, Norwig J, Maroon JC. Measurement of symptoms following sports-related concussion: reliability and normative data for the post-concussion scale. Appl Neuropsychol 2006; 13: 166-174
    CrossrefPubMedSearch in Google Scholar
  • 36 McAllister TW, Ford JC, Flashman LA, Maerlender A, Greenwald RM, Beckwith JG, Bolander RP, Tosteson TD, Turco JH, Raman R, Jain S. Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes. Neurology 2014; 82: 63-69
    CrossrefPubMedSearch in Google Scholar
  • 37 McCrea M, Barr WB, Guskiewicz KM, Randolph C, Marshall SW, Cantu R, Onate JA, Kelly JP. Standard regression-based methods for measuring recovery after sport-related concussion. J Int Neuropsychol Soc 2005; 11: 58-69
    PubMedSearch in Google Scholar
  • 38 McCrea M, Broshek DK, Barth JT. Sports concussion assessment and management: future research directions. Brain Inj 2015; 29: 276-282
    CrossrefPubMedSearch in Google Scholar
  • 39 McCrea M, Guskiewicz KM, Marshall SW, Barr W, Randolph C, Cantu RC, Onate JA, Yang J, Kelly JP. Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study. JAMA 2003; 290: 2556-2563
    CrossrefPubMedSearch in Google Scholar
  • 40 McCrea M, Guskiewicz KM, Randolph C, Barr WB, Hammeke TA, Marshall SW, Powell MR, Woo AK, Wang Y, Kelly JP. Incidence, clinical course, and predictors of prolonged recovery time following sport-related concussion in high school and college athletes. J Int Neuropsychol Soc 2013; 19: 22-33
    CrossrefPubMedSearch in Google Scholar
  • 41 McCrea M, Hammeke T, Olsen G, Leo P, Guskiewicz K. Unreported concussion in high school football players: implications for prevention. Clin J Sport Med 2004; 14: 13-17
    CrossrefPubMedSearch in Google Scholar
  • 42 McCrory P, Meeuwisse W, Johnston K, Dvorak J, Aubry M, Molloy M, Cantu R. Consensus statement on concussion in sport: the 3rd International Conference on Concussion in Sport held in Zurich, November 2008. Br J Sports Med 2009; 43: i76-i90
    CrossrefPubMedSearch in Google Scholar
  • 43 McCrory P, Meeuwisse WH, Aubry M, Cantu RC, Dvorak J, Echemendia RJ, Engebretsen L, Johnston K, Kutcher JS, Raftery M, Sills A, Benson BW, Davis GA, Ellenbogen RG, Guskiewicz KM, Herring SA, Iverson GL, Jordan BD, Kissick J, McCrea M, McIntosh AS, Maddocks D, Makdissi M, Purcell L, Putukian M, Schneider K, Tator CH, Turner M. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Br J Sports Med 2013; 47: 250-258
    CrossrefPubMedSearch in Google Scholar
  • 44 Meier TB, Brummel BJ, Singh R, Nerio CJ, Polanski DW, Bellgowan PS. The underreporting of self-reported symptoms following sports-related concussion. J Sci Med Sport 2015; 18: 507-511
    CrossrefPubMedSearch in Google Scholar
  • 45 Moore RD, Broglio SP, Hillman CH. Sport-related concussion and sensory function in young adults. J Athl Train 2014; 49: 36-41
    CrossrefPubMedSearch in Google Scholar
  • 46 Moore RD, Hillman CH, Broglio SP. The persistent influence of concussive injuries on cognitive control and neuroelectric function. J Athl Train 2014; 49: 24-35
    CrossrefPubMedSearch in Google Scholar
  • 47 Pontifex MB, O’Connor PM, Broglio SP, Hillman CH. The association between mild traumatic brain injury history and cognitive control. Neuropsychologia 2009; 47: 3210-3216
    CrossrefPubMedSearch in Google Scholar
  • 48 Randolph C. Baseline neuropsychological testing in managing sport-related concussion: does it modify risk?. Curr Sports Med Rep 2011; 10: 21-26
    CrossrefPubMedSearch in Google Scholar
  • 49 Randolph C, McCrea M, Barr WB. Is neuropsychological testing useful in the management of sport-related concussion?. J Athl Train 2005; 40: 139-154
    PubMedSearch in Google Scholar
  • 50 Reches A, Kerem D, Gal N, Laufer I, Shani-Hershkovitch R, Dickman D, Geva A. A novel ERP pattern analysis method for revealing invariant reference brain network models. Funct Neurol Rehabil Ergon 2013; 3: 295-317
    PubMedSearch in Google Scholar
  • 51 Reches A, Laufer I, Ziv K, Cukierman G, McEvoy K, Ettinger M, Knight RT, Gazzaley A, Geva AB. Network dynamics predict improvement in working memory performance following donepezil administration in healthy young adults. Neuroimage 2013; 88C: 228-241
    PubMedSearch in Google Scholar
  • 52 Reches A, Levy-Cooperman N, Laufer I, Shani-Hershkovitch R, Ziv K, Kerem D, Gal N, Stern Y, Cukierman G, Romach MK, Sellers EM, Geva AB. Brain Network Activation (BNA) reveals scopolamine-induced impairment of visual working memory. J Mol Neurosci 2014; 54: 59-70
    CrossrefPubMedSearch in Google Scholar
  • 53 Resch J, Driscoll A, McCaffrey N, Brown C, Ferrara MS, Macciocchi S, Baumgartner T, Walpert K. ImPact test-retest reliability: reliably unreliable?. J Athl Train 2013; 48: 506-511
    CrossrefPubMedSearch in Google Scholar
  • 54 Schmidt JD, Register-Mihalik JK, Mihalik JP, Kerr ZY, Guskiewicz KM. Identifying impairments after concussion: normative data versus individualized baselines. Med Sci Sports Exerc 2012; 44: 1621-1628
    CrossrefPubMedSearch in Google Scholar
  • 55 Sefton JM, Pirog K, Capitao A, Harackiewicz D, Cordova ML. An examination of factors that influence knowledge and reporting of mild brain injuries in collegiate football. J Athl Train 2004; 39: S52-S53
    PubMedSearch in Google Scholar
  • 56 Shahaf G, Reches A, Pinchuk N, Fisher T, Ben Bashat G, Kanter A, Tauber I, Kerem D, Laufer I, Aharon-Peretz J, Pratt H, Geva AB. Introducing a novel approach of network oriented analysis of ERPs, demonstrated on adult attention deficit hyperactivity disorder. Clin Neurophysiol 2012; 123: 1568-1580
    CrossrefPubMedSearch in Google Scholar
  • 57 Sim A, Terrberry-Spohr L, Wilson KR. Prolonged recovery of memory functioning after mild traumatic brain injury in adolescent athletes. J Neurosurg 2008; 108: 511-516
    CrossrefPubMedSearch in Google Scholar
  • 58 Straume-Naesheim TM, Andersen TE, Bahr R. Reproducibility of computer based neuropsychological testing among Norwegian elite football players. Br J Sports Med 2005; 39: i64-i69
    CrossrefPubMedSearch in Google Scholar
  • 59 Talavage TM, Nauman EA, Breedlove EL, Yoruk U, Dye AE, Morigaki KE, Feuer H, Leverenz LJ. Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. J Neurotrauma 2014; 31: 327-338
    CrossrefPubMedSearch in Google Scholar
  • 60 Theriault M, De Beaumont L, Gosselin N, Filipinni M, Lassonde M. Electrophysiological abnormalities in well functioning multiple concussed athletes. Brain Inj 2009; 23: 899-906
    CrossrefPubMedSearch in Google Scholar
  • 61 Williams RM, Puetz TW, Giza CC, Broglio SP. Concussion recovery time among high school and collegiate athletes: a systematic review and meta-analysis. Sports Med 2015; 45: 893-903
    CrossrefPubMedSearch in Google Scholar