Neuromuscular Control Deficits and the Risk of Subsequent Injury after a Concussion: A Scoping Review

Abstract

An emerging area of research has identified that an increased risk of musculoskeletal injury may exist upon returning to sports after a sport-related concussion. The mechanisms underlying this recently discovered phenomenon, however, remain unknown. One theorized reason for this increased injury risk includes residual neuromuscular control deficits that remain impaired despite clinical recovery. Thus, the objectives of this review were: (1) to summarize the literature examining the relationship between concussion and risk of subsequent injury and (2) to summarize the literature for one mechanism with a theorized association with this increased injury risk, i.e., neuromuscular control deficits observed during gait after concussion under dual-task conditions. Two separate reviews were conducted consistent with both specified objectives. Studies published before 9 December, 2016 were identified using PubMed, Web of Science, and Academic Search Premier (EBSCOhost). Inclusion for the objective 1 search included dependent variables of quantitative measurements of musculoskeletal injury after concussion. Inclusion criteria for the objective 2 search included dependent variables pertaining to gait, dynamic balance control, and dual-task function. A total of 32 studies were included in the two reviews (objective 1 n = 10, objective 2 n = 22). According to a variety of study designs, athletes appear to have an increased risk of sustaining a musculoskeletal injury following a concussion. Furthermore, dual-task neuromuscular control deficits may continue to exist after patients report resolution of concussion symptoms, or perform normally on other clinical concussion tests. Therefore, musculoskeletal injury risk appears to increase following a concussion and persistent motor system and attentional deficits also seem to exist after a concussion. While not yet experimentally tested, these motor system and attentional deficits may contribute to the risk of sustaining a musculoskeletal injury upon returning to full athletic participation.

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References

  1. 1.

    Broglio SP, Cantu RC, Gioia GA, et al. National Athletic Trainers’ Association position statement: management of sport concussion. J Athl Train. 2014;49:245–65.

    PubMed  PubMed Central  Article  Google Scholar 

  2. 2.

    McCrory P, Meeuwisse W, Dvorak J, 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.

  3. 3.

    McCrea M, Guskiewicz KM, Marshall SW, et al. Acute effects and recovery time following concussion in collegiate football players: the NCAA concussion study. JAMA. 2003;290:2556–63.

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Buckley TA, Burdette G, Kelly K. Concussion-management practice patterns of National Collegiate Athletic Association Division II and III athletic trainers: how the other half lives. J Athl Train. 2015;50:879–88.

    PubMed  PubMed Central  Article  Google Scholar 

  5. 5.

    Kelly KC, Jordan EM, Joyner AB, et al. National Collegiate Athletic Association Division I athletic trainers’ concussion-management practice patterns. J Athl Train. 2014;49:665–73.

    PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    Baugh CM, Kroshus E, Stamm JM, et al. Clinical practices in collegiate concussion management. Am J Sports Med. 2016;44:1391–9.

    PubMed  PubMed Central  Article  Google Scholar 

  7. 7.

    Stache S, Howell D, Meehan WP. Concussion management practice patterns among sports medicine physicians. Clin J Sport Med. 2016;26:381–5.

    PubMed  Article  Google Scholar 

  8. 8.

    Broglio SP, Macciocchi SN, Ferrara MS. Sensitivity of the concussion assessment battery. Neurosurgery. 2007;60:1050–7 (discussion 1057–8).

    PubMed  Article  Google Scholar 

  9. 9.

    McCrea M, Barr WB, Guskiewicz K, et al. Standard regression-based methods for measuring recovery after sport-related concussion. J Int Neuropsychol Soc. 2005;11:58–69.

    PubMed  Article  Google Scholar 

  10. 10.

    Broglio SP, Macciocchi SN, Ferrara MS. Neurocognitive performance of concussed athletes when symptom free. J Athl Train. 2007;42:504–8.

    PubMed  PubMed Central  Google Scholar 

  11. 11.

    Buckley TA, Munkasy BA, Tapia-Lovler TG, et al. Altered gait termination strategies following a concussion. Gait Posture. 2013;38:549–51.

    PubMed  PubMed Central  Article  Google Scholar 

  12. 12.

    Buckley TA, Oldham JR, Caccese JB. Postural control deficits identify lingering post-concussion neurological deficits. J Sport Health Sci. 2016;5:61–9.

    Article  Google Scholar 

  13. 13.

    Howell DR, Osternig LR, Christie AD, et al. Return to physical activity timing and dual-task gait stability are associated 2 months following concussion. J Head Trauma Rehabil. 2016;31:262–8.

    PubMed  Article  Google Scholar 

  14. 14.

    Slobounov S, Sebastianelli W, Hallett M. Residual brain dysfunction observed one year post-mild traumatic brain injury: combined EEG and balance study. Clin Neurophysiol. 2012;123:1755–61.

    PubMed  PubMed Central  Article  Google Scholar 

  15. 15.

    Gao J, Hu J, Buckley T, et al. Shannon and Renyi entropies to classify effects of mild traumatic brain injury on postural sway. PloS One. 2011;6:e24446.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. 16.

    Slobounov S, Cao C, Sebastianelli W. Differential effect of first versus second concussive episodes on wavelet information quality of EEG. Clin Neurophysiol. 2009;120:862–7.

    PubMed  PubMed Central  Article  Google Scholar 

  17. 17.

    Powers KC, Kalmar JM, Cinelli ME. Recovery of static stability following a concussion. Gait Posture. 2014;39:611–4.

    PubMed  Article  Google Scholar 

  18. 18.

    Kamins J, Bigler E, Covassin T, et al. What is the physiological time to recovery after concussion? A systematic review. Br J Sports Med. 2017;51:935–40.

    PubMed  Article  Google Scholar 

  19. 19.

    Guskiewicz KM. Balance assessment in the management of sport-related concussion. Clin Sports Med. 2011;30:89–102.

    PubMed  Article  Google Scholar 

  20. 20.

    Riemann BL, Guskiewicz KM, Shields EW. Relationship between clinical and forceplate measures of postural stability. Hum Kinet J. 1999;8:71–2.

    Google Scholar 

  21. 21.

    Burk JM, Munkasy BA, Joyner AB, et al. Balance error scoring system performance changes after a competitive athletic season. Clin J Sport Med. 2013;23:312–7.

    PubMed  Article  Google Scholar 

  22. 22.

    Rahn C, Munkasy BA, Joyner AB, et al. Sideline performance of the balance error scoring system during a live sporting event. Clin J Sport Med. 2015;25:248–53.

    PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Bell DR, Guskiewicz KM, Clark MA, et al. Systematic review of the balance error scoring system. Sports Health. 2011;3:287–95.

    PubMed  PubMed Central  Article  Google Scholar 

  24. 24.

    Valovich McLeod TC, Perrin DH, et al. Serial administration of clinical concussion assessments and learning effects in healthy young athletes. Clin J Sport Med. 2004;14:287–95.

    PubMed  Article  Google Scholar 

  25. 25.

    Onate JA, Beck BC, Van Lunen BL. On-field testing environment and balance error scoring system performance during preseason screening of healthy collegiate baseball players. J Athl Train. 2007;42:446–51.

    PubMed  PubMed Central  Google Scholar 

  26. 26.

    Broglio SP, Ferrara MS, Sopiarz K, et al. Reliable change of the sensory organization test. Clin J Sport Med. 2008;18:148–54.

    PubMed  Article  Google Scholar 

  27. 27.

    Cavanaugh JT, Guskiewicz KM, Giuliani C, et al. Recovery of postural control after cerebral concussion: new insights using approximate entropy. J Athl Train. 2006;41:305–13.

    PubMed  PubMed Central  Google Scholar 

  28. 28.

    Riemann BL, Lephart SM. The sensorimotor system, part I: the physiologic basis of functional joint stability. J Athl Train. 2002;37:71–9.

    PubMed  PubMed Central  Google Scholar 

  29. 29.

    Howell DR, Osternig LR, Chou L-S. Dual-task effect on gait balance control in adolescents with concussion. Arch Phys Med Rehabil. 2013;94:1513–20.

    PubMed  Article  Google Scholar 

  30. 30.

    Howell DR, Osternig LR, Chou L-S. Return to activity after concussion affects dual-task gait balance control recovery. Med Sci Sports Exerc. 2015;47:673–80.

    PubMed  Article  Google Scholar 

  31. 31.

    Parker TM, Osternig LR, Van Donkelaar P, et al. Gait stability following concussion. Med Sci Sports Exerc. 2006;38:1032–40.

    PubMed  Article  Google Scholar 

  32. 32.

    Studenski S, Perera S, Wallace D, et al. Physical performance measures in the clinical setting. J Am Geriatr Soc. 2003;51:314–22.

    PubMed  Article  Google Scholar 

  33. 33.

    Sutherland DH, Olshen R, Cooper L, et al. The development of mature gait. J Bone Joint Surg Am. 1980;62:336–53.

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Adolph KE, Vereijken B, Shrout PE. What changes in infant walking and why. Child Dev. 2003;74:475–97.

    PubMed  Article  Google Scholar 

  35. 35.

    Wang J, Wai Y, Weng Y, et al. Functional MRI in the assessment of cortical activation during gait-related imaginary tasks. J Neural Transm. 2009;116:1087–92.

    PubMed  Article  Google Scholar 

  36. 36.

    Godde B, Voelcker-Rehage C. More automation and less cognitive control of imagined walking movements in high- versus low-fit older adults. Front Aging Neurosci. 2010;2:pii: 139. https://doi.org/10.3389/fnagi.2010.00139.

  37. 37.

    Howell DR, Osternig LR, Chou L-S. Consistency and cost of dual-task gait balance measure in healthy adolescents and young adults. Gait Posture. 2016;49:176–80.

    PubMed  Article  Google Scholar 

  38. 38.

    Howell DR, Oldham JR, DiFabio M, et al. Single-task and dual-task gait among collegiate athletes of different sport classifications: implications for concussion management. J Appl Biomech. 2017;33:24–31.

    PubMed  Article  Google Scholar 

  39. 39.

    Oldham JR, Munkasy BA, Evans KM, et al. Altered dynamic postural control during gait termination following concussion. Gait Posture. 2016;49:437–42.

    PubMed  PubMed Central  Article  Google Scholar 

  40. 40.

    Buckley TA, Oldham JR, Munkasy BA, et al. Decreased anticipatory postural adjustments during gait initiation acutely post-concussion. Arch Phys Med Rehabil. 2017;98(10):1962–8.

    PubMed  Article  Google Scholar 

  41. 41.

    Register-Mihalik JK, Littleton AC, Guskiewicz KM. Are divided attention tasks useful in the assessment and management of sport-related concussion? Neuropsychol Rev. 2013;23:300–13.

    PubMed  Article  Google Scholar 

  42. 42.

    Howell DR, Osternig L, van Donkelaar P, et al. Effects of concussion on attention and executive function in adolescents. Med Sci Sports Exerc. 2013;45:1030–7.

    PubMed  Article  Google Scholar 

  43. 43.

    Halterman CI, Langan J, Drew A, et al. Tracking the recovery of visuospatial attention deficits in mild traumatic brain injury. Brain. 2006;129:747–53.

    PubMed  Article  Google Scholar 

  44. 44.

    Mayr U, Laroux C, Rolheiser T, et al. Executive dysfunction assessed with a task-switching task following concussion. PloS One. 2014;9:e91379.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  45. 45.

    Yogev-Seligmann G, Hausdorff JM, Giladi N. The role of executive function and attention in gait. Mov Disord. 2008;23:329–42.

    PubMed  Article  Google Scholar 

  46. 46.

    Herman D, Zaremski JL, Vincent HK, et al. Effect of neurocognition and concussion on musculoskeletal injury risk. Curr Sports Med Rep. 2015;14:194–9.

    PubMed Central  Article  Google Scholar 

  47. 47.

    Weiss K, Whatman C. Biomechanics associated with patellofemoral pain and ACL injuries in sports. Sports Med. 2015;45:1325–37.

    PubMed  Article  Google Scholar 

  48. 48.

    Read PJ, Oliver JL, De Ste Croix MBA, et al. Neuromuscular risk factors for knee and ankle ligament injuries in male youth soccer players. Sports Med. 2016;46:1059–66.

    PubMed  PubMed Central  Article  Google Scholar 

  49. 49.

    Guy JA, Knight LM, Wang Y, et al. Factors associated with musculoskeletal injuries in children and adolescents with attention-deficit/hyperactivity disorder. Prim Care Companion CNS Disord. 2016 Jun 23;18(3). https://doi.org/10.4088/pcc.16m01937.

  50. 50.

    Howell DR, Osternig LR, Koester MC, et al. The effect of cognitive task complexity on gait stability in adolescents following concussion. Exp Brain Res. 2014;232:1773–82.

    PubMed  Article  Google Scholar 

  51. 51.

    Fino PC. A preliminary study of longitudinal differences in local dynamic stability between recently concussed and healthy athletes during single and dual-task gait. J Biomech. 2016;49:1983–8.

    PubMed  Article  Google Scholar 

  52. 52.

    Fait P, Swaine B, Cantin J-F, et al. Altered integrated locomotor and cognitive function in elite athletes 30 days postconcussion: a preliminary study. J Head Trauma Rehabil. 2013;28:293–301.

    PubMed  Article  Google Scholar 

  53. 53.

    Sambasivan K, Grilli L, Gagnon I. Balance and mobility in clinically recovered children and adolescents after a mild traumatic brain injury. J Pediatr Rehabil Med. 2015;8:335–44.

    PubMed  Article  Google Scholar 

  54. 54.

    Brooks MA, Peterson K, Biese K, et al. Concussion increases odds of sustaining a lower extremity musculoskeletal injury after return to play among collegiate athletes. Am J Sports Med. 2016;44:742–7.

    PubMed  Article  Google Scholar 

  55. 55.

    Herman DC, Jones D, Harrison A, et al. Concussion may increase the risk of subsequent lower extremity musculoskeletal injury in collegiate athletes. Sports Med. 2017;47:1003–10.

    PubMed  Article  Google Scholar 

  56. 56.

    Lynall RC, Mauntel TC, Padua DA, et al. Acute lower extremity injury rates increase after concussion in college athletes. Med Sci Sports Exerc. 2015;47:2487–92.

    PubMed  Article  Google Scholar 

  57. 57.

    Cross M, Kemp S, Smith A, et al. Professional Rugby Union players have a 60% greater risk of time loss injury after concussion: a 2-season prospective study of clinical outcomes. Br J Sports Med. 2016;50:926–31.

    PubMed  Article  Google Scholar 

  58. 58.

    Nordström A, Nordström P, Ekstrand J. Sports-related concussion increases the risk of subsequent injury by about 50% in elite male football players. Br J Sports Med. 2014;48:1447–50.

    PubMed  Article  Google Scholar 

  59. 59.

    Gilbert FC, Burdette GT, Joyner AB, et al. Association between concussion and lower extremity injuries in collegiate athletes. Sports Health. 2016;8:561–7.

    PubMed  PubMed Central  Article  Google Scholar 

  60. 60.

    Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(264–9):W64.

    Google Scholar 

  61. 61.

    McCrory P, Meeuwisse WH, Aubry M, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Br J Sports Med. 2013;47:250–8.

  62. 62.

    Makdissi M, McCrory P, Ugoni A, et al. A prospective study of postconcussive outcomes after return to play in Australian football. Am J Sports Med. 2009;37:877–83.

    PubMed  Article  Google Scholar 

  63. 63.

    Pietrosimone B, Golightly YM, Mihalik JP, et al. Concussion frequency associates with musculoskeletal injury in retired NFL players. Med Sci Sports Exerc. 2015;47:2366–72.

    PubMed  Article  Google Scholar 

  64. 64.

    Burman E, Lysholm J, Shahim P, et al. Concussed athletes are more prone to injury both before and after their index concussion: a data base analysis of 699 concussed contact sports athletes. BMJ Open Sport Exerc Med. 2016;2:e000092.

    PubMed  PubMed Central  Article  Google Scholar 

  65. 65.

    Nyberg G, Mossberg KH, Lysholm J, et al. Subsequent traumatic injuries after a concussion in elite ice hockey: a study over 28 years. Curr Res Concussion. 2015;2:109–12.

    Google Scholar 

  66. 66.

    Hägglund M, Waldén M, Ekstrand J. Previous injury as a risk factor for injury in elite football: a prospective study over two consecutive seasons. Br J Sports Med. 2006;40:767–72.

    PubMed  PubMed Central  Article  Google Scholar 

  67. 67.

    Arnason A, Sigurdsson SB, Gudmundsson A, et al. Risk factors for injuries in football. Am J Sports Med. 2004;32(1 Suppl.):5S–16S.

    PubMed  Article  Google Scholar 

  68. 68.

    Beynnon BD, Murphy DF, Alosa DM. Predictive factors for lateral ankle sprains: a literature review. J Athl Train. 2002;37:376–80.

    PubMed  PubMed Central  Google Scholar 

  69. 69.

    Hewett TE, Myer GD, Ford KR. Anterior cruciate ligament injuries in female athletes: part 1, mechanisms and risk factors. Am J Sports Med. 2006;34:299–311.

    PubMed  Article  Google Scholar 

  70. 70.

    Martini DN, Sabin MJ, DePesa SA, et al. The chronic effects of concussion on gait. Arch Phys Med Rehabil. 2011;92:585–9.

    PubMed  Article  Google Scholar 

  71. 71.

    Martini DN, Goulet GC, Gates DH, et al. Long-term effects of adolescent concussion history on gait, across age. Gait Posture. 2016;49:264–70.

    PubMed  Article  Google Scholar 

  72. 72.

    Catena RD, van Donkelaar P, Chou L-S. The effects of attention capacity on dynamic balance control following concussion. J Neuroeng Rehabil. 2011;8:8.

    PubMed  PubMed Central  Article  Google Scholar 

  73. 73.

    Parker TM, Osternig LR, Lee H-J, et al. The effect of divided attention on gait stability following concussion. Clin Biomech. 2005;20:389–95.

    Article  Google Scholar 

  74. 74.

    Catena RD, Donkelaar P, Chou L-S. Cognitive task effects on gait stability following concussion. Exp Brain Res. 2006;176:23–31.

    PubMed  Article  Google Scholar 

  75. 75.

    Howell DR, Osternig LR, Chou L-S. Monitoring recovery of gait balance control following concussion using an accelerometer. J Biomech. 2015;48:3364–8.

    PubMed  Article  Google Scholar 

  76. 76.

    Catena R, van Donkelaar P, Chou LS. Different gait tasks distinguish immediate vs. long-term effects of concussion on balance control. J Neuroeng Rehabil. 2009;6:1–7.

    Article  Google Scholar 

  77. 77.

    Catena RD, van Donkelaar P, Chou L-S. Altered balance control following concussion is better detected with an attention test during gait. Gait Posture. 2007;25:406–11.

    PubMed  Article  Google Scholar 

  78. 78.

    Chiu S-L, Osternig L, Chou L-S. Concussion induces gait inter-joint coordination variability under conditions of divided attention and obstacle crossing. Gait Posture. 2013;38:717–22.

    PubMed  Article  Google Scholar 

  79. 79.

    Parker TM, Osternig LR, van Donkelaar P, et al. Balance control during gait in athletes and non-athletes following concussion. Med Eng Phys. 2008;30:959–67.

    PubMed  Article  Google Scholar 

  80. 80.

    Howell DR, Osternig LR, Chou L-S. Adolescents demonstrate greater gait balance control deficits after concussion than young adults. Am J Sports Med. 2015;43:625–32.

    PubMed  Article  Google Scholar 

  81. 81.

    Howell DR, Beasley M, Vopat L, et al. The effect of prior concussion history on dual-task gait following a concussion. J Neurotrauma. 2017;34:838–44.

    PubMed  Article  Google Scholar 

  82. 82.

    Plisky PJ, Rauh MJ, Kaminski TW, et al. Star Excursion Balance Test as a predictor of lower extremity injury in high school basketball players. J Orthop Sports Phys Ther. 2006;36:911–9.

    PubMed  Article  Google Scholar 

  83. 83.

    McGuine TA, Greene JJ, Best T, et al. Balance as a predictor of ankle injuries in high school basketball players. Clin J Sport Med. 2000;10:239–44.

    CAS  PubMed  Article  Google Scholar 

  84. 84.

    Smith CA, Chimera NJ, Warren M. Association of Y balance test reach asymmetry and injury in Division I athletes. Med Sci Sports Exerc. 2015;47:136–41.

    PubMed  Article  Google Scholar 

  85. 85.

    Zazulak BT, Hewett TE, Reeves NP, et al. Deficits in neuromuscular control of the trunk predict knee injury risk: a prospective biomechanical-epidemiologic study. Am J Sports Med. 2007;35:1123–30.

    PubMed  Article  Google Scholar 

  86. 86.

    Hewett TE, Myer GD, Ford KR, et al. Biomechanical measures of neuromuscular control and valgus loading of the knee predict anterior cruciate ligament injury risk in female athletes: a prospective study. Am J Sports Med. 2005;33:492–501.

    PubMed  Article  Google Scholar 

  87. 87.

    Padua DA, DiStefano LJ, Beutler AI, et al. The landing error scoring system as a screening tool for an anterior cruciate ligament injury-prevention program in elite-youth soccer athletes. J Athl Train. 2015;50:589–95.

    PubMed  PubMed Central  Article  Google Scholar 

  88. 88.

    Dubose DF, Herman DC, Jones DL, et al. Lower extremity stiffness changes after concussion in collegiate football players. Med Sci Sports Exerc. 2017;49:167–72.

    PubMed  PubMed Central  Article  Google Scholar 

  89. 89.

    Howell DR, Osternig LR, Chou L-S. Single-task and dual-task tandem gait test performance after concussion. J Sci Med Sport. 2017;20:622–6.

    PubMed  Article  Google Scholar 

  90. 90.

    Kim AS, Needle AR, Thomas SJ, et al. A sex comparison of reactive knee stiffness regulation strategies under cognitive loads. Clin Biomech (Bristol, Avon). 2016;35:86–92.

    Article  Google Scholar 

  91. 91.

    Kipp K, Brown TN, McLean SG, et al. Decision making and experience level influence frontal plane knee joint biomechanics during a cutting maneuver. J Appl Biomech. 2013;29:756–62.

    PubMed  Article  Google Scholar 

  92. 92.

    Brown TN, O’Donovan M, Hasselquist L, et al. Soldier-relevant loads impact lower limb biomechanics during anticipated and unanticipated single-leg cutting movements. J Biomech. 2014;47:3494–501.

    PubMed  Article  Google Scholar 

  93. 93.

    Kim JH, Lee K-K, Ahn KO, et al. Evaluation of the interaction between contact force and decision making on lower extremity biomechanics during a side-cutting maneuver. Arch Orthop Trauma Surg. 2016;136:821–8.

    PubMed  Article  Google Scholar 

  94. 94.

    Collins JD, Almonroeder TG, Ebersole KT, et al. The effects of fatigue and anticipation on the mechanics of the knee during cutting in female athletes. Clin Biomech (Bristol, Avon). 2016;35:62–7.

    Article  Google Scholar 

  95. 95.

    Holste KG, Yasen AL, Hill MJ, et al. Motor cortex inhibition is increased during a secondary cognitive task. Motor Control. 2016;20:380–94.

    PubMed  Article  Google Scholar 

  96. 96.

    Corp DT, Rogers MA, Youssef GJ, et al. The effect of dual-task difficulty on the inhibition of the motor cortex. Exp Brain Res. 2016;234:443–52.

    PubMed  Article  Google Scholar 

  97. 97.

    Fino PC, Nussbaum MA, Brolinson PG. Locomotor deficits in recently concussed athletes and matched controls during single and dual-task turning gait: preliminary results. J Neuroeng Rehabil. 2016;13:65.

    PubMed  PubMed Central  Article  Google Scholar 

  98. 98.

    Cossette I, Ouellet M-C, McFadyen BJ. A preliminary study to identify locomotor-cognitive dual tasks that reveal persistent executive dysfunction after mild traumatic brain injury. Arch Phys Med Rehabil. 2014;95:1594–7.

    PubMed  Article  Google Scholar 

  99. 99.

    Powers KC, Cinelli ME, Kalmar JM. Cortical hypoexcitability persists beyond the symptomatic phase of a concussion. Brain Inj. 2014;28:465–71.

    PubMed  Article  Google Scholar 

  100. 100.

    De Beaumont L, Mongeon D, Tremblay S, et al. Persistent motor system abnormalities in formerly concussed athletes. J Athl Train. 2011;46:234–40.

    PubMed  PubMed Central  Article  Google Scholar 

  101. 101.

    Livingston SC, Goodkin HP, Hertel JN, et al. Differential rates of recovery after acute sport-related concussion. J Clin Neurophysiol. 2012;29:23–32.

    PubMed  Article  Google Scholar 

  102. 102.

    Livingston SC, Saliba EN, Goodkin HP, et al. A preliminary investigation of motor evoked potential abnormalities following sport-related concussion. Brain Inj. 2010;24:904–13.

    PubMed  Article  Google Scholar 

  103. 103.

    Miller NR, Yasen AL, Maynard LF, et al. Acute and longitudinal changes in motor cortex function following mild traumatic brain injury. Brain Inj. 2014;28:1270–6.

    PubMed  Article  Google Scholar 

  104. 104.

    Teel EF, Ray WJ, Geronimo AM, et al. Residual alterations of brain electrical activity in clinically asymptomatic concussed individuals: an EEG study. Clin Neurophysiol. 2014;125:703–7.

    CAS  PubMed  Article  Google Scholar 

  105. 105.

    Howell DR, Oldham JR, Meehan WP, et al. Dual-task tandem gait and average walking speed in healthy collegiate athletes. Clin J Sport Med. 2017. https://doi.org/10.1097/jsm.0000000000000509 (Epub ahead of print).

  106. 106.

    Gardner RM, Yengo-Kahn A, Bonfield CM, et al. Comparison of baseline and post-concussion ImPACT test scores in young athletes with stimulant-treated and untreated ADHD. Phys Sportsmed. 2017;45:1–10.

    PubMed  Article  Google Scholar 

  107. 107.

    Elbin RJ, Kontos AP, Kegel N, et al. Individual and combined effects of LD and ADHD on computerized neurocognitive concussion test performance: evidence for separate norms. Arch Clin Neuropsychol. 2013;28:476–84.

    CAS  PubMed  Article  Google Scholar 

  108. 108.

    DiScala C, Lescohier I, Barthel M, et al. Injuries to children with attention deficit hyperactivity disorder. Pediatrics. 1998;102:1415–21.

    CAS  PubMed  Article  Google Scholar 

  109. 109.

    Clendenin AA, Businelle MS, Kelley ML. Screening ADHD problems in the sports behavior checklist: factor structure, convergent and divergent validity, and group differences. J Atten Disord. 2005;8:79–87.

    PubMed  Article  Google Scholar 

  110. 110.

    Osborn ZH, Blanton PD, Schwebel DC. Personality and injury risk among professional hockey players. J Inj Violence Res. 2009;1:15–9.

    PubMed  PubMed Central  Article  Google Scholar 

  111. 111.

    Lysens RJ, Ostyn MS, Vanden Auweele Y, et al. The accident-prone and overuse-prone profiles of the young athlete. Am J Sports Med. 1989;17:612–9.

    CAS  PubMed  Article  Google Scholar 

  112. 112.

    Patel DR, Luckstead EF. Sport participation, risk taking, and health risk behaviors. Adolesc Med. 2000;11:141–55.

    CAS  PubMed  Google Scholar 

  113. 113.

    Swanik CB, Covassin T, Stearne DJ, et al. The relationship between neurocognitive function and noncontact anterior cruciate ligament injuries. Am J Sports Med. 2007;35:943–8.

    PubMed  Article  Google Scholar 

  114. 114.

    Wilkerson GB. Neurocognitive reaction time predicts lower extremity sprains and strains. Int J Athl Ther Train. 2012;17:4–9.

    Article  Google Scholar 

  115. 115.

    Herman DC, Barth JT. Drop-jump landing varies with baseline neurocognition: implications for anterior cruciate ligament injury risk and prevention. Am J Sports Med. 2016;44:2347–53.

    PubMed  Article  Google Scholar 

  116. 116.

    Dretsch MN, Silverberg N, Gardner AJ, et al. Genetics and other risk factors for past concussions in active-duty soldiers. J Neurotrauma. 2017;34:869–75.

    PubMed  Article  Google Scholar 

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Correspondence to David R. Howell.

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Funding

David R. Howell has received research support through a research contract between Boston Children’s Hospital, Cincinnati Children’s Hospital Medical Center, and ElMindA Ltd. Thomas A. Buckley is funded, in part, by a grant from the National Collegiate Athletic Association and the Department of Defense. Daniel C. Herman is supported in part by National Institutes of Health Grant No. 5K12HD001097-17 (Rehabilitation Medical Scientist Training Program), and grants through the Foundation for Physical Medicine and Rehabilitation, American Medical Society for Sports Medicine Foundation, and American College of Sports Medicine Foundation.

Conflict of interest

David R. Howell, Robert C. Lynall, Thomas A. Buckley, and Daniel C. Herman have no conflicts of interest directly relevant to the content of this review.

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Howell, D.R., Lynall, R.C., Buckley, T.A. et al. Neuromuscular Control Deficits and the Risk of Subsequent Injury after a Concussion: A Scoping Review. Sports Med 48, 1097–1115 (2018). https://doi.org/10.1007/s40279-018-0871-y

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