Skip to main content
Top
Published in: Sports Medicine 5/2018

01-05-2018 | Review Article

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

Authors: David R. Howell, Robert C. Lynall, Thomas A. Buckley, Daniel C. Herman

Published in: Sports Medicine | Issue 5/2018

Login to get access

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.
Literature
1.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
2.
go back to reference 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. 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.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
4.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
5.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
7.
go back to reference Stache S, Howell D, Meehan WP. Concussion management practice patterns among sports medicine physicians. Clin J Sport Med. 2016;26:381–5.PubMedCrossRef Stache S, Howell D, Meehan WP. Concussion management practice patterns among sports medicine physicians. Clin J Sport Med. 2016;26:381–5.PubMedCrossRef
8.
go back to reference Broglio SP, Macciocchi SN, Ferrara MS. Sensitivity of the concussion assessment battery. Neurosurgery. 2007;60:1050–7 (discussion 1057–8).PubMedCrossRef Broglio SP, Macciocchi SN, Ferrara MS. Sensitivity of the concussion assessment battery. Neurosurgery. 2007;60:1050–7 (discussion 1057–8).PubMedCrossRef
9.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
10.
go back to reference Broglio SP, Macciocchi SN, Ferrara MS. Neurocognitive performance of concussed athletes when symptom free. J Athl Train. 2007;42:504–8.PubMedPubMedCentral Broglio SP, Macciocchi SN, Ferrara MS. Neurocognitive performance of concussed athletes when symptom free. J Athl Train. 2007;42:504–8.PubMedPubMedCentral
11.
12.
go back to reference Buckley TA, Oldham JR, Caccese JB. Postural control deficits identify lingering post-concussion neurological deficits. J Sport Health Sci. 2016;5:61–9.CrossRef Buckley TA, Oldham JR, Caccese JB. Postural control deficits identify lingering post-concussion neurological deficits. J Sport Health Sci. 2016;5:61–9.CrossRef
13.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
14.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
15.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
16.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
17.
go back to reference Powers KC, Kalmar JM, Cinelli ME. Recovery of static stability following a concussion. Gait Posture. 2014;39:611–4.PubMedCrossRef Powers KC, Kalmar JM, Cinelli ME. Recovery of static stability following a concussion. Gait Posture. 2014;39:611–4.PubMedCrossRef
18.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
19.
go back to reference Guskiewicz KM. Balance assessment in the management of sport-related concussion. Clin Sports Med. 2011;30:89–102.PubMedCrossRef Guskiewicz KM. Balance assessment in the management of sport-related concussion. Clin Sports Med. 2011;30:89–102.PubMedCrossRef
20.
go back to reference Riemann BL, Guskiewicz KM, Shields EW. Relationship between clinical and forceplate measures of postural stability. Hum Kinet J. 1999;8:71–2. Riemann BL, Guskiewicz KM, Shields EW. Relationship between clinical and forceplate measures of postural stability. Hum Kinet J. 1999;8:71–2.
21.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
22.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
24.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
25.
go back to reference 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.PubMedPubMedCentral 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.PubMedPubMedCentral
26.
go back to reference Broglio SP, Ferrara MS, Sopiarz K, et al. Reliable change of the sensory organization test. Clin J Sport Med. 2008;18:148–54.PubMedCrossRef Broglio SP, Ferrara MS, Sopiarz K, et al. Reliable change of the sensory organization test. Clin J Sport Med. 2008;18:148–54.PubMedCrossRef
27.
go back to reference 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.PubMedPubMedCentral 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.PubMedPubMedCentral
28.
go back to reference Riemann BL, Lephart SM. The sensorimotor system, part I: the physiologic basis of functional joint stability. J Athl Train. 2002;37:71–9.PubMedPubMedCentral Riemann BL, Lephart SM. The sensorimotor system, part I: the physiologic basis of functional joint stability. J Athl Train. 2002;37:71–9.PubMedPubMedCentral
29.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
30.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
31.
go back to reference Parker TM, Osternig LR, Van Donkelaar P, et al. Gait stability following concussion. Med Sci Sports Exerc. 2006;38:1032–40.PubMedCrossRef Parker TM, Osternig LR, Van Donkelaar P, et al. Gait stability following concussion. Med Sci Sports Exerc. 2006;38:1032–40.PubMedCrossRef
32.
go back to reference Studenski S, Perera S, Wallace D, et al. Physical performance measures in the clinical setting. J Am Geriatr Soc. 2003;51:314–22.PubMedCrossRef Studenski S, Perera S, Wallace D, et al. Physical performance measures in the clinical setting. J Am Geriatr Soc. 2003;51:314–22.PubMedCrossRef
33.
go back to reference Sutherland DH, Olshen R, Cooper L, et al. The development of mature gait. J Bone Joint Surg Am. 1980;62:336–53.PubMedCrossRef Sutherland DH, Olshen R, Cooper L, et al. The development of mature gait. J Bone Joint Surg Am. 1980;62:336–53.PubMedCrossRef
34.
go back to reference Adolph KE, Vereijken B, Shrout PE. What changes in infant walking and why. Child Dev. 2003;74:475–97.PubMedCrossRef Adolph KE, Vereijken B, Shrout PE. What changes in infant walking and why. Child Dev. 2003;74:475–97.PubMedCrossRef
35.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
37.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
38.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
39.
40.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
41.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
42.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
43.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
44.
45.
go back to reference Yogev-Seligmann G, Hausdorff JM, Giladi N. The role of executive function and attention in gait. Mov Disord. 2008;23:329–42.PubMedCrossRef Yogev-Seligmann G, Hausdorff JM, Giladi N. The role of executive function and attention in gait. Mov Disord. 2008;23:329–42.PubMedCrossRef
46.
go back to reference 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.PubMedCentralCrossRef 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.PubMedCentralCrossRef
47.
go back to reference Weiss K, Whatman C. Biomechanics associated with patellofemoral pain and ACL injuries in sports. Sports Med. 2015;45:1325–37.PubMedCrossRef Weiss K, Whatman C. Biomechanics associated with patellofemoral pain and ACL injuries in sports. Sports Med. 2015;45:1325–37.PubMedCrossRef
48.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
50.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
51.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
52.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
53.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
54.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
55.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
56.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
57.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
58.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
59.
go back to reference Gilbert FC, Burdette GT, Joyner AB, et al. Association between concussion and lower extremity injuries in collegiate athletes. Sports Health. 2016;8:561–7.PubMedPubMedCentralCrossRef Gilbert FC, Burdette GT, Joyner AB, et al. Association between concussion and lower extremity injuries in collegiate athletes. Sports Health. 2016;8:561–7.PubMedPubMedCentralCrossRef
60.
go back to reference 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. 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.
61.
go back to reference 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. 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.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
63.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
64.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
65.
go back to reference 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. 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.
66.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
67.
go back to reference Arnason A, Sigurdsson SB, Gudmundsson A, et al. Risk factors for injuries in football. Am J Sports Med. 2004;32(1 Suppl.):5S–16S.PubMedCrossRef Arnason A, Sigurdsson SB, Gudmundsson A, et al. Risk factors for injuries in football. Am J Sports Med. 2004;32(1 Suppl.):5S–16S.PubMedCrossRef
68.
go back to reference Beynnon BD, Murphy DF, Alosa DM. Predictive factors for lateral ankle sprains: a literature review. J Athl Train. 2002;37:376–80.PubMedPubMedCentral Beynnon BD, Murphy DF, Alosa DM. Predictive factors for lateral ankle sprains: a literature review. J Athl Train. 2002;37:376–80.PubMedPubMedCentral
69.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
70.
go back to reference Martini DN, Sabin MJ, DePesa SA, et al. The chronic effects of concussion on gait. Arch Phys Med Rehabil. 2011;92:585–9.PubMedCrossRef Martini DN, Sabin MJ, DePesa SA, et al. The chronic effects of concussion on gait. Arch Phys Med Rehabil. 2011;92:585–9.PubMedCrossRef
71.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
72.
73.
go back to reference 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.CrossRef 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.CrossRef
74.
go back to reference Catena RD, Donkelaar P, Chou L-S. Cognitive task effects on gait stability following concussion. Exp Brain Res. 2006;176:23–31.PubMedCrossRef Catena RD, Donkelaar P, Chou L-S. Cognitive task effects on gait stability following concussion. Exp Brain Res. 2006;176:23–31.PubMedCrossRef
75.
go back to reference Howell DR, Osternig LR, Chou L-S. Monitoring recovery of gait balance control following concussion using an accelerometer. J Biomech. 2015;48:3364–8.PubMedCrossRef Howell DR, Osternig LR, Chou L-S. Monitoring recovery of gait balance control following concussion using an accelerometer. J Biomech. 2015;48:3364–8.PubMedCrossRef
76.
go back to reference 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.CrossRef 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.CrossRef
77.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
78.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
79.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
80.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
81.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
82.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
83.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
84.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
85.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
86.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
87.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
88.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
89.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
90.
go back to reference 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.CrossRef 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.CrossRef
91.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
92.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
93.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
94.
go back to reference 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.CrossRef 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.CrossRef
95.
go back to reference Holste KG, Yasen AL, Hill MJ, et al. Motor cortex inhibition is increased during a secondary cognitive task. Motor Control. 2016;20:380–94.PubMedCrossRef Holste KG, Yasen AL, Hill MJ, et al. Motor cortex inhibition is increased during a secondary cognitive task. Motor Control. 2016;20:380–94.PubMedCrossRef
96.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
97.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
98.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
99.
go back to reference Powers KC, Cinelli ME, Kalmar JM. Cortical hypoexcitability persists beyond the symptomatic phase of a concussion. Brain Inj. 2014;28:465–71.PubMedCrossRef Powers KC, Cinelli ME, Kalmar JM. Cortical hypoexcitability persists beyond the symptomatic phase of a concussion. Brain Inj. 2014;28:465–71.PubMedCrossRef
100.
101.
go back to reference Livingston SC, Goodkin HP, Hertel JN, et al. Differential rates of recovery after acute sport-related concussion. J Clin Neurophysiol. 2012;29:23–32.PubMedCrossRef Livingston SC, Goodkin HP, Hertel JN, et al. Differential rates of recovery after acute sport-related concussion. J Clin Neurophysiol. 2012;29:23–32.PubMedCrossRef
102.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
103.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
104.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
106.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
107.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
108.
go back to reference DiScala C, Lescohier I, Barthel M, et al. Injuries to children with attention deficit hyperactivity disorder. Pediatrics. 1998;102:1415–21.PubMedCrossRef DiScala C, Lescohier I, Barthel M, et al. Injuries to children with attention deficit hyperactivity disorder. Pediatrics. 1998;102:1415–21.PubMedCrossRef
109.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
111.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
112.
go back to reference Patel DR, Luckstead EF. Sport participation, risk taking, and health risk behaviors. Adolesc Med. 2000;11:141–55.PubMed Patel DR, Luckstead EF. Sport participation, risk taking, and health risk behaviors. Adolesc Med. 2000;11:141–55.PubMed
113.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
114.
go back to reference Wilkerson GB. Neurocognitive reaction time predicts lower extremity sprains and strains. Int J Athl Ther Train. 2012;17:4–9.CrossRef Wilkerson GB. Neurocognitive reaction time predicts lower extremity sprains and strains. Int J Athl Ther Train. 2012;17:4–9.CrossRef
115.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
116.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
Metadata
Title
Neuromuscular Control Deficits and the Risk of Subsequent Injury after a Concussion: A Scoping Review
Authors
David R. Howell
Robert C. Lynall
Thomas A. Buckley
Daniel C. Herman
Publication date
01-05-2018
Publisher
Springer International Publishing
Published in
Sports Medicine / Issue 5/2018
Print ISSN: 0112-1642
Electronic ISSN: 1179-2035
DOI
https://doi.org/10.1007/s40279-018-0871-y

Other articles of this Issue 5/2018

Sports Medicine 5/2018 Go to the issue