Abstract
Postural stability deficits are commonly observed in cases of concussion. However, the objective duration in which impairments of standing postural stability remain following a concussion is often inconclusive. The present study was conducted to determine if prior history of concussion is associated with deficits in postural stability beyond the clinical determination of recovery. It was hypothesized that concussion history would be associated with decreases in static stability compared to individuals that have never sustained a concussion. Fifty-four healthy adults were recruited based on whether they reported sustaining one or more prior concussions (n = 27) or no history of concussion (n = 27). Participants were instructed to stand on a force platform to track center-of-pressure (CoP) during standing for thirty seconds under four conditions based on stance and number of tasks: (1) bipedal, single-task, (2) bipedal, dual-task, (3) unipedal, single-task, and (4) unipedal, dual-task. Results revealed that individuals with a history of concussion demonstrate significantly reduced postural stability under dual-task conditions as evidenced by increases in average displacements and elliptical area of postural sway as well as reductions in CoP sample entropy. However, there were no significant differences in CoP displacement or elliptical area between groups under single task conditions. Overall, these findings indicate that concussion is associated with impairments of maintaining standing postural stability that remain evident approximately 7 years following clinical resolution of the initial injury. The exacerbation of these impairments under dual-task conditions indicate that concussion can result in a reduced capacity to allocate proper attention resources to multiple concurrent objectives.
Similar content being viewed by others
Abbreviations
- ANOVA:
-
Analysis of variance
- AP:
-
Anteroposterior
- B-DT:
-
Bipedal, dual-task
- B-ST:
-
Bipedal, single-task
- BESS:
-
Balance error scoring system
- CoP:
-
Center of pressure
- ML:
-
Mediolateral
- SampEn:
-
Sample entropy
- U-DT:
-
Unipedal, dual-task
- U-ST:
-
Unipedal, single task
References
Allum JH, Adkin AL, Carpenter MG et al (2001) Trunk sway measures of postural stability during clinical balance tests: effects of a unilateral vestibular deficit. Gait Posture 14:227–237
Alsalaheen BA, Whitney SL, Marchetti GF et al (2016) Relationship Between Cognitive Assessment and Balance Measures in Adolescents Referred for Vestibular Physical Therapy After Concussion. Clin J Sport Med 26:46–52. https://doi.org/10.1097/JSM.0000000000000185
Beretta VS, Barbieri FA, Orcioli-Silva D et al (2018) Can postural control asymmetry predict falls in people with Parkinson’s disease? Mot Control 22:449–461. https://doi.org/10.1123/mc.2017-0033
Berkner J, Meehan WP, Master CL, Howell DR (2017) Gait and quiet-stance performance among adolescents after concussion-symptom resolution. J Athl Train 52:1089–1095. https://doi.org/10.4085/1062-6050-52.11.23
Błaszczyk JW, Orawiec R (2011) Assessment of postural control in patients with Parkinson’s disease: sway ratio analysis. Hum Mov Sci 30:396–404. https://doi.org/10.1016/j.humov.2010.07.017
Błaszczyk JW, Orawiec R, Duda-Kłodowska D, Opala G (2007) Assessment of postural instability in patients with Parkinson’s disease. Exp Brain Res 183:107–114. https://doi.org/10.1007/s00221-007-1024-y
Broglio SP, Macciocchi SN, Ferrara MS (2007) Sensitivity of the concussion assessment battery. Neurosurgery 60:1050–1057. https://doi.org/10.1227/01.NEU.0000255479.90999.C0(discussion 1057-1058)
Buckley TA, Munkasy BA (2010) Deficits in postural stability following concussion persist beyond BESS recovery. Med Sci Sports Exerc 42:492–492
Buckley TA, Oldham JR, Caccese JB (2016) Postural control deficits identify lingering post-concussion neurological deficits. J Sport Health Sci 5:61–69. https://doi.org/10.1016/j.jshs.2016.01.007
Busa MA, van Emmerik REA (2016) Multiscale entropy: a tool for understanding the complexity of postural control. J Sport Health Sci 5:44–51. https://doi.org/10.1016/j.jshs.2016.01.018
Büttner F, Howell DR, Ardern CL et al (2019) Concussed athletes walk slower than non-concussed athletes during cognitive-motor dual-task assessments but not during single-task assessments 2 months after sports concussion: a systematic review and meta-analysis using individual participant data. Br J Sports Med. https://doi.org/10.1136/bjsports-2018-100164
Catena RD, van Donkelaar P, Chou L-S (2011) The effects of attention capacity on dynamic balance control following concussion. J Neuroeng Rehabil 8:8. https://doi.org/10.1186/1743-0003-8-8
Catena RD, van Donkelaar P, Chou L-S (2007) Cognitive task effects on gait stability following concussion. Exp Brain Res 176:23–31. https://doi.org/10.1007/s00221-006-0596-2
Cavanaugh J (2004) Assessing changes in the regularity of center of pressure time series in collegiate athletes after cerebral concussion. ProQuest Dissertations Publishing
Cavanaugh JT, Guskiewicz KM, Giuliani C et al (2005) Detecting altered postural control after cerebral concussion in athletes with normal postural stability. Br J Sports Med 39:805–811. https://doi.org/10.1136/bjsm.2004.015909
Cavanaugh JT, Guskiewicz KM, Giuliani C et al (2006) Recovery of postural control after cerebral concussion: new insights using approximate entropy. J Athl Train 41:305–313
Chauhan NB (2014) Chronic neurodegenerative consequences of traumatic brain injury. Restor Neurol Neurosci 32:337–365. https://doi.org/10.3233/RNN-130354
Chen YJ, Nabavizadeh SA, Vossough A et al (2017) Wallerian degeneration beyond the corticospinal tracts: conventional and advanced MRI findings. J Neuroimaging 27:272–280. https://doi.org/10.1111/jon.12404
Collins MW, Iverson GL, Lovell MR et al (2003) On-field predictors of neuropsychological and symptom deficit following sports-related concussion. Clin J Sport Med 13:222–229
Covassin T, Elbin RJ, Harris W et al (2012) The role of age and sex in symptoms, neurocognitive performance, and postural stability in athletes after concussion. Am J Sports Med 40:1303–1312. https://doi.org/10.1177/0363546512444554
Davceva N, Sivevski A, Basheska N (2017) Traumatic axonal injury, a clinical-pathological correlation. J Forensic Leg Med 48:35–40. https://doi.org/10.1016/j.jflm.2017.04.004
De Beaumont L, Mongeon D, Tremblay S et al (2011) Persistent motor system abnormalities in formerly concussed athletes. J Athl Train 46:234–240. https://doi.org/10.4085/1062-6050-46.3.234
Eagle SR, Nindl BC, Johnson CD et al (2019) Does concussion affect perception-action coupling behavior? Action boundary perception as a biomarker for concussion. Clin J Sport Med. https://doi.org/10.1097/JSM.0000000000000731
Eagle SR, Kontos AP, Pepping G-J et al (2020) Increased risk of musculoskeletal injury following sport-related concussion: a perception-action coupling approach. Sports Med 50:15–23. https://doi.org/10.1007/s40279-019-01144-3
Echemendia RJ, Meeuwisse W, McCrory P et al (2017) The Sport Concussion Assessment Tool 5th edition (SCAT5): background and rationale. Br J Sports Med 51:848–850. https://doi.org/10.1136/bjsports-2017-097506
Ferguson B (2014) ACSMs guidelines for exercise testing and prescription. J Can Chiropr Assoc 58:328
Galea OA, Cottrell MA, Treleaven JM, O’Leary SP (2018) Sensorimotor and physiological indicators of impairment in mild traumatic brain injury: a meta-analysis. Neurorehabil Neural Repair 32:115–128. https://doi.org/10.1177/1545968318760728
Guskiewicz KM (2001) Postural stability assessment following concussion: one piece of the puzzle. Clin J Sport Med 11:182
Guskiewicz KM (2011) Balance assessment in the management of sport-related concussion. Clin Sports Med 30(89–102):ix. https://doi.org/10.1016/j.csm.2010.09.004
Guskiewicz KM, Perrin DH, Gansneder BM (1996) Effect of mild head injury on postural stability in athletes. J Athl Train 31:300–306
Guskiewicz KM, Marshall SW, Bailes J et al (2005) Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery 57:719–726
Howell DR, Beasley M, Vopat L, Meehan WP (2016) The effect of prior concussion history on dual-task gait following a concussion. J Neurotrauma 34:838–844. https://doi.org/10.1089/neu.2016.4609
Howell DR, Osternig LR, Chou L-S (2015) Return to activity after concussion affects dual-task gait balance control recovery. Med Sci Sports Exerc 47:673–680. https://doi.org/10.1249/MSS.0000000000000462
Howell DR, Brilliant A, Berkstresser B et al (2017a) The association between dual-task gait after concussion and prolonged symptom duration. J Neurotrauma 34:3288–3294. https://doi.org/10.1089/neu.2017.5191
Howell DR, Oldham JR, DiFabio M et al (2017b) Single-task and dual-task gait among collegiate athletes of different sport classifications: implications for concussion management. J Appl Biomech 33:24–31. https://doi.org/10.1123/jab.2015-0323
Huber BR, Alosco ML, Stein TD, McKee AC (2016) Potential long-term consequences of concussive and subconcussive injury. Phys Med Rehabil Clin N Am 27:503–511. https://doi.org/10.1016/j.pmr.2015.12.007
Hugentobler JA, Gupta R, Slater R et al (2016) Influence of age on postconcussive postural control measures and future implications for assessment. Clin J Sport Med 26:510–517. https://doi.org/10.1097/JSM.0000000000000286
Hurtubise J, Gorbet D, Hamandi Y et al (2016) The effect of concussion history on cognitive-motor integration in elite hockey players. Concussion 1:CNC17. https://doi.org/10.2217/cnc-2016-0006
Jacobson GP, McCaslin DL, Piker EG et al (2011) Insensitivity of the “Romberg test of standing balance on firm and compliant support surfaces” to the results of caloric and VEMP tests. Ear Hear 32:e1–5. https://doi.org/10.1097/AUD.0b013e31822802bb
Kalron A, Achiron A (2013) Postural control, falls and fear of falling in people with multiple sclerosis without mobility aids. J Neurol Sci 335:186–190. https://doi.org/10.1016/j.jns.2013.09.029
Ko J-H, Newell KM (2016) Aging and the complexity of center of pressure in static and dynamic postural tasks. Neurosci Lett 610:104–109. https://doi.org/10.1016/j.neulet.2015.10.069
Konrad C, Geburek AJ, Rist F et al (2011) Long-term cognitive and emotional consequences of mild traumatic brain injury. Psychol Med 41:1197–1211. https://doi.org/10.1017/S0033291710001728
Lynall RC, Blackburn JT, Guskiewicz KM et al (2018) Reaction time and joint kinematics during functional movement in recently concussed individuals. Arch Phys Med Rehabil 99:880–886. https://doi.org/10.1016/j.apmr.2017.12.011
Matinolli M, Korpelainen JT, Korpelainen R et al (2007) Postural sway and falls in Parkinson’s disease: a regression approach. Mov Disord 22:1927–1935. https://doi.org/10.1002/mds.21633
McAllister T, McCrea M (2017) Long-term cognitive and neuropsychiatric consequences of repetitive concussion and head-impact exposure. J Athl Train 52:309–317. https://doi.org/10.4085/1062-6050-52.1.14
McCrory P (2011) Sports concussion and the risk of chronic neurological impairment. Clin J Sport Med 21:6. https://doi.org/10.1097/JSM.0b013e318204db50
Merritt ED, Brown CN, Queen RM et al (2017) Concussion history and time since concussion do not influence static and dynamic balance in collegiate athletes. J Sport Rehabil 26:518–523. https://doi.org/10.1123/jsr.2016-0119
Moran RN, Meek J, Allen J, Robinson J (2020) Sex differences and normative data for the m-CTSIB and sensory integration on baseline concussion assessment in collegiate athletes. Brain Inj 34:20–25. https://doi.org/10.1080/02699052.2019.1669824
Morton SM, Bastian AJ (2004) Cerebellar control of balance and locomotion. Neuroscientist 10:247–259. https://doi.org/10.1177/1073858404263517
Murray N, Salvatore A, Powell D, Reed-Jones R (2014) Reliability and validity evidence of multiple balance assessments in athletes with a concussion. J Athl Train 49:540–549. https://doi.org/10.4085/1062-6050-49.3.32
Murray NG, Szekely B, Moran R et al (2019) Concussion history associated with increased postural control deficits after subsequent injury. Physiol Meas 40:024001. https://doi.org/10.1088/1361-6579/aafcd8
Nashner LM, Shupert CL, Horak FB, Black FO (1989) Organization of posture controls: an analysis of sensory and mechanical constraints. Prog Brain Res 80:411–418 (discussion 395-397)
Pellecchia GL (2003) Postural sway increases with attentional demands of concurrent cognitive task. Gait Posture 18:29–34
Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88:1097–1118. https://doi.org/10.1152/jn.2002.88.3.1097
Piirtola M, Era P (2006) Force platform measurements as predictors of falls among older people—a review. Gerontology 52:1–16. https://doi.org/10.1159/000089820
Pincus SM, Goldberger AL (1994) Physiological time-series analysis: what does regularity quantify? Am J Physiol 266:H1643–1656. https://doi.org/10.1152/ajpheart.1994.266.4.H1643
Powers KC, Kalmar JM, Cinelli ME (2014) Recovery of static stability following a concussion. Gait Posture 39:611–614. https://doi.org/10.1016/j.gaitpost.2013.05.026
Purkayastha S, Adair H, Woodruff A et al (2019) Balance testing following concussion: postural sway versus complexity index. PM R. https://doi.org/10.1002/pmrj.12129
Resch JE, May B, Tomporowski PD, Ferrara MS (2011) Balance performance with a cognitive task: a continuation of the dual-task testing paradigm. J Athl Train 46:170–175. https://doi.org/10.4085/1062-6050-46.2.170
Riemann BL, Guskiewicz KM (2000) Effects of mild head injury on postural stability as measured through clinical balance testing. J Athl Train 35:19–25
Roerdink M, Hlavackova P, Vuillerme N (2011) Center-of-pressure regularity as a marker for attentional investment in postural control: a comparison between sitting and standing postures. Hum Mov Sci 30:203–212. https://doi.org/10.1016/j.humov.2010.04.005
Shumway-Cook A, Woollacott M (2000) Attentional demands and postural control: the effect of sensory context. J Gerontol A Biol Sci Med Sci 55:M10–16
Slobounov S, Cao C, Sebastianelli W et al (2008) Residual deficits from concussion as revealed by virtual time-to-contact measures of postural stability. Clin Neurophysiol 119:281–289. https://doi.org/10.1016/j.clinph.2007.10.006
Sosnoff JJ, Broglio SP, Shin S, Ferrara MS (2011) Previous mild traumatic brain injury and postural-control dynamics. J Athl Train 46:85–91. https://doi.org/10.4085/1062-6050-46.1.85
Spira JL, Lathan CE, Bleiberg J, Tsao JW (2014) The impact of multiple concussions on emotional distress, post-concussive symptoms, and neurocognitive functioning in active duty United States marines independent of combat exposure or emotional distress. J Neurotrauma 31:1823–1834. https://doi.org/10.1089/neu.2014.3363
Stein TD, Alvarez VE, McKee AC (2015) Concussion in chronic traumatic encephalopathy. Curr Pain Headache Rep. https://doi.org/10.1007/s11916-015-0522-z
Stern RA, Riley DO, Daneshvar DH et al (2011) Long-term consequences of repetitive brain trauma: chronic traumatic encephalopathy. PM R 3:S460–467. https://doi.org/10.1016/j.pmrj.2011.08.008
Takakusaki K, Takahashi M, Obara K, Chiba R (2017) Neural substrates involved in the control of posture. Adv Robot 31:2–23. https://doi.org/10.1080/01691864.2016.1252690
Vuillerme N, Nougier V, Teasdale N (2000) Effects of a reaction time task on postural control in humans. Neurosci Lett 291:77–80. https://doi.org/10.1016/S0304-3940(00)01374-4
Westwood C, Killelea C, Faherty M, Sell T (2019) Postural stability under dual-task conditions: development of a post-concussion assessment for lower extremity injury risk. J Sport Rehabil. https://doi.org/10.1123/jsr.2018-0358
Winter D (1995) Human balance and posture control during standing and walking. Gait Posture 3:193–214. https://doi.org/10.1016/0966-6362(96)82849-9
Winter DA, Patla AE, Prince F et al (1998) Stiffness control of balance in quiet standing. J Neurophysiol 80:1211–1221. https://doi.org/10.1152/jn.1998.80.3.1211
Young CC, Jacobs BA, Clavette K et al (1997) Serial sevens: not the most effective test of mental status in high school athletes. Clin J Sport Med 7:196–198
Author information
Authors and Affiliations
Contributions
NR conceptualized the study design and research question, developed the methodology, conducted data collection and analyses, and contributed to drafting and editing the manuscript. JP contributed to the study design, conducted data collections and analyses, and edited the final manuscript for submission. JM conducted data collection and analyses and contributed edits toward the final manuscript. ES helped design the methodology, contributed toward data analyses and edits of the final manuscript. All authors read and approved the present manuscript for submission.
Corresponding author
Additional information
Communicated by Bill J. Yates.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Reilly, N., Prebor, J., Moxey, J. et al. Chronic impairments of static postural stability associated with history of concussion. Exp Brain Res 238, 2783–2793 (2020). https://doi.org/10.1007/s00221-020-05934-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-020-05934-4