Assessment and rehabilitation of central sensory impairments for balance in mTBI using auditory biofeedback: a randomized clinical trial

Peter C Fino, Robert J Peterka, Timothy E Hullar, Chad Murchison, Fay B Horak, James C Chesnutt, Laurie A King, Peter C Fino, Robert J Peterka, Timothy E Hullar, Chad Murchison, Fay B Horak, James C Chesnutt, Laurie A King

Abstract

Background: Complaints of imbalance are common non-resolving signs in individuals with post-concussive syndrome. Yet, there is no consensus rehabilitation for non-resolving balance complaints following mild traumatic brain injury (mTBI). The heterogeneity of balance deficits and varied rates of recovery suggest varied etiologies and a need for interventions that address the underlying causes of poor balance function. Our central hypothesis is that most chronic balance deficits after mTBI result from impairments in central sensorimotor integration that may be helped by rehabilitation. Two studies are described to 1) characterize balance deficits in people with mTBI who have chronic, non-resolving balance deficits compared to healthy control subjects, and 2) determine the efficacy of an augmented vestibular rehabilitation program using auditory biofeedback to improve central sensorimotor integration, static and dynamic balance, and functional activity in patients with chronic mTBI.

Methods: Two studies are described. Study 1 is a cross-sectional study to take place jointly at Oregon Health and Science University and the VA Portland Health Care System. The study participants will be individuals with non-resolving complaints of balance following mTBI and age- and gender-matched controls who meet all inclusion criteria. The primary outcome will be measures of central sensorimotor integration derived from a novel central sensorimotor integration test. Study 2 is a randomized controlled intervention to take place at Oregon Health & Science University. In this study, participants from Study 1 with mTBI and abnormal central sensorimotor integration will be randomized into two rehabilitation interventions. The interventions will be 6 weeks of vestibular rehabilitation 1) with or 2) without the use of an auditory biofeedback device. The primary outcome measure is the daily activity of the participants measured using an inertial sensor.

Discussion: The results of these two studies will improve our understanding of the nature of balance deficits in people with mTBI by providing quantitative metrics of central sensorimotor integration, balance, and vestibular and ocular motor function. Study 2 will examine the potential for augmented rehabilitation interventions to improve central sensorimotor integration.

Trial registration: This trial is registered at clinicaltrials.gov ( NCT02748109 ).

Keywords: Balance; Biofeedback; Concussion; Gait; Sensorimotor integration; mTBI.

Figures

Fig. 1
Fig. 1
Sensory systems contributing to static and dynamic balance
Fig. 2
Fig. 2
CSMI methods with example data and analysis. (a) A feedback control model forms the basis for identifying model parameters (Table 2) that account for experimentally evoked body-in-space (BS) sway, representing angular tilt of the body center-of-mass (CoM), evoked by support surface (SS) and/or visual surround (VS) rotations. (b) An example of one cycle of a pseudorandom surface-tilt stimulus that evoked the CoM body sway (averaged across 5 stimulus cycles) shown in (c) for a Control subject and TBI subject. (d) Frequency domain analysis of stimulus/response data in (b) and (c) yields frequency response functions (FRFs) expressed as gain (ratio of CoM response amplitude to stimulus amplitude) and phase (timing of response relative to stimulus) measures as a function of frequency components in the pseudorandom stimulus. Parameters of the model in (a) are calculated by a fit procedure that finds parameters that optimally account for the FRF gain and phase data
Fig. 3
Fig. 3
Flowchart illustrating the study design. Study 1 is a cross-sectional design. Study 2 recruits subjects from Study 1 for a randomized intervention

References

    1. Langlois JA, Rutland-Brown W, Wald MM. The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil. 2006;21(5):375–378. doi: 10.1097/00001199-200609000-00001.
    1. Hoge CW, McGurk D, Thomas JL, Cox AL, Engel CC, Castro CA. Mild traumatic brain injury in U.S. Soldiers returning from Iraq. N Engl J Med. 2008;358(5):453–463. doi: 10.1056/NEJMoa072972.
    1. Coronado VG, McGuire LC, Sarmiento K, Bell J, Lionbarger MR, Jones CD, Geller AI, Khoury N, Xu L. Trends in Traumatic Brain Injury in the U.S. and the public health response: 1995-2009. J Saf Res. 2012;43(4):299–307. doi: 10.1016/j.jsr.2012.08.011.
    1. Boake C, McCauley SR, Levin HS, Pedroza C, Contant CF, Song JX, Brown SA, Goodman H, Brundage SI, Diaz-Marchan PJ. Diagnostic criteria for postconcussional syndrome after mild to moderate traumatic brain injury. J Neuropsychiatry Clin Neurosci. 2005;17(3):350–356. doi: 10.1176/jnp.17.3.350.
    1. Ingebrigtsen T, Waterloo K, Marup-Jensen S, Attner E, Romner B. Quantification of post-concussion symptoms 3 months after minor head injury in 100 consecutive patients. J Neurol. 1998;245(9):609–612. doi: 10.1007/s004150050254.
    1. Fife TD, Kalra D. Persistent vertigo and dizziness after mild traumatic brain injury. Ann N Y Acad Sci. 2015;1343:97–105. doi: 10.1111/nyas.12678.
    1. Guskiewicz KM, Weaver NL, Padua DA, Garrett WE. Epidemiology of concussion in collegiate and high school football players. Am J Sports Med. 2000;28(5):643–650. doi: 10.1177/03635465000280050401.
    1. Daneshvar DH, Riley DO, Nowinski CJ, McKee AC, Stern RA, Cantu RC. Long-term consequences: effects on normal development profile after concussion. Phys Med Rehabil Clin N Am. 2011;22(4):683–700. doi: 10.1016/j.pmr.2011.08.009.
    1. Giza CC, Kutcher JS, Ashwal S, Barth J, Getchius TS, Gioia GA, Gronseth GS, Guskiewicz K, Mandel S, Manley G. 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(24):2250–2257. doi: 10.1212/WNL.0b013e31828d57dd.
    1. Montgomery E, Fenton G, McClelland R, MacFlynn G, Rutherford W. The psychobiology of minor head injury. Psychol Med. 1991;21(02):375–384. doi: 10.1017/S0033291700020481.
    1. McGowan JC, Yang JH, Plotkin RC, Grossman RI, Umile EM, Cecil KM, Bagley LJ. Magnetization transfer imaging in the detection of injury associated with mild head trauma. Am J Neuroradiol. 2000;21(5):875–880.
    1. Grossman EJ, Ge Y, Jensen JH, Babb JS, Miles L, Reaume J, Silver JM, Grossman RI, Inglese M. Thalamus and cognitive impairment in mild traumatic brain injury: a diffusional kurtosis imaging study. J Neurotrauma. 2012;29(13):2318–2327. doi: 10.1089/neu.2011.1763.
    1. Peskind ER, Petrie EC, Cross DJ, Pagulayan K, McCraw K, Hoff D, Hart K, Yu C-E, Raskind MA, Cook DG, et al. Cerebrocerebellar hypometabolism associated with repetitive blast exposure mild traumatic brain injury in 12 Iraq war Veterans with persistent post-concussive symptoms. NeuroImage. 2011;54, Supplement 1:S76–S82. doi: 10.1016/j.neuroimage.2010.04.008.
    1. Basta D, Todt I, Scherer H, Clarke A, Ernst A. Postural control in otolith disorders. Hum Mov Sci. 2005;24(2):268–279. doi: 10.1016/j.humov.2005.04.002.
    1. Davies RA, Luxon LM. Dizziness following head injury: A neuro-otological study. J Neurol. 1995;242(4):222–230. doi: 10.1007/BF00919595.
    1. Ernst A: Sensory disorders of the auditory and vestibular systems following blunt head trauma. In: IUTAM Symposium on Impact Biomechanics: From Fundamental Insights to Applications: 2005. The Netherlands: Springer. 2005:213–20.
    1. Toglia JU, Rosenberg PE, Ronis ML. Posttraumatic dizziness: Vestibular, audiologic, and medicolegal aspects. Arch Otolaryngol. 1970;92(5):485–492. doi: 10.1001/archotol.1970.04310050067010.
    1. Drew AS, Langan J, Halterman C, Osternig LR, Chou L-S, van Donkelaar P. Attentional disengagement dysfunction following mTBI assessed with the gap saccade task. Neurosci Lett. 2007;417(1):61–65. doi: 10.1016/j.neulet.2007.02.038.
    1. Suh M, Basu S, Kolster R, Sarkar R, McCandliss B, Ghajar J, Cognitive, Consortium NR Increased oculomotor deficits during target blanking as an indicator of mild traumatic brain injury. Neurosci Lett. 2006;410(3):203–207. doi: 10.1016/j.neulet.2006.10.001.
    1. Suh M, Kolster R, Sarkar R, McCandliss B, Ghajar J, Cognitive, Consortium NR Deficits in predictive smooth pursuit after mild traumatic brain injury. Neurosci Lett. 2006;401(1):108–113. doi: 10.1016/j.neulet.2006.02.074.
    1. Capó-Aponte JE, Urosevich TG, Temme LA, Tarbett AK, Sanghera NK. Visual dysfunctions and symptoms during the subacute stage of blast-induced mild traumatic brain injury. Mil Med. 2012;177(7):804–813. doi: 10.7205/MILMED-D-12-00061.
    1. Peterka RJ. Sensorimotor Integration in Human Postural Control. J Neurophysiol. 2002;88(3):1097–1118.
    1. Peterka RJ, Loughlin PJ. Dynamic Regulation of Sensorimotor Integration in Human Postural Control. J Neurophysiol. 2004;91(1):410–423. doi: 10.1152/jn.00516.2003.
    1. Peterka R, Statler K, Wrisley D, Horak F. Postural compensation for unilateral vestibular loss. Front Neurol. 2011;2:57. doi: 10.3389/fneur.2011.00057.
    1. Finnoff JT, Peterson VJ, Hollman JH, Smith J. Intrarater and interrater reliability of the Balance Error Scoring System (BESS) PM&R. 2009;1(1):50–54. doi: 10.1016/j.pmrj.2008.06.002.
    1. McCrea M, Barr WB, Guskiewicz K, 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(1):58–69. doi: 10.1017/S1355617705050083.
    1. Basford JR, Chou L-S, Kaufman KR, Brey RH, Walker A, Malec JF, Moessner AM, Brown AW. An assessment of gait and balance deficits after traumatic brain injury. Arch Phys Med Rehabil. 2003;84(3):343–349. doi: 10.1053/apmr.2003.50034.
    1. Cavanaugh J, Guskiewicz K, Giuliani C, Marshall S, Mercer V, Stergiou N. Detecting altered postural control after cerebral concussion in athletes with normal postural stability. Br J Sports Med. 2005;39(11):805–811. doi: 10.1136/bjsm.2004.015909.
    1. De Beaumont L, Mongeon D, Tremblay S, Messier J, Prince F, Leclerc S, Lassonde M, Theoret H. Persistent motor system abnormalities in formerly concussed athletes. J Athl Train. 2011;46(3):234–240.
    1. Sosnoff JJ, Broglio SP, Shin S, Ferrara MS. Previous mild traumatic brain injury and postural-control dynamics. J Athl Train. 2011;46(1):85. doi: 10.4085/1062-6050-46.1.85.
    1. Fino PC, Nussbaum MA, Brolinson PG. Decreased high-frequency center-of-pressure complexity in recently concussed asymptomatic athletes. Gait Posture. 2016;50:69–74. doi: 10.1016/j.gaitpost.2016.08.026.
    1. Catena RD, van Donkelaar P, Chou L-S. Cognitive task effects on gait stability following concussion. Exp Brain Res. 2007;176(1):23–31. doi: 10.1007/s00221-006-0596-2.
    1. Howell DR, Osternig LR, Chou L-S. Dual-Task Effect on Gait Balance Control in Adolescents With Concussion. Arch Phys Med Rehabil. 2013;94(8):1513–1520. doi: 10.1016/j.apmr.2013.04.015.
    1. Parker TM, Osternig LR, Van Donkelaar P, Chou L. Gait stability following concussion. Med Sci Sports Exerc. 2006;38(6):1032. doi: 10.1249/01.mss.0000222828.56982.a4.
    1. 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(9):1983–1988. doi: 10.1016/j.jbiomech.2016.05.004.
    1. Alberts JL, Hirsch JR, Koop MM, Schindler DD, Kana DE, Linder SM, Campbell S, Thota AK. Using accelerometer and gyroscopic measures to quantify postural stability. J Athl Train. 2015;50(6):578–588. doi: 10.4085/1062-6050-50.2.01.
    1. Alberts JL, Thota A, Hirsch J, Ozinga S, Dey T, Schindler DD, Koop MM, Burke D, Linder SM. Quantification of the Balance Error Scoring System with Mobile Technology. Med Sci Sports Exerc. 2015;47(10):2233–2240. doi: 10.1249/MSS.0000000000000656.
    1. Howell D, Osternig L, Chou L-S. Monitoring recovery of gait balance control following concussion using an accelerometer. J Biomech. 2015;48(12):3364–3368. doi: 10.1016/j.jbiomech.2015.06.014.
    1. King LA, Horak FB, Mancini M, Pierce D, Priest KC, Chesnutt J, Sullivan P, Chapman JC. Instrumenting the Balance Error Scoring System for Use With Patients Reporting Persistent Balance Problems After Mild Traumatic Brain Injury. Arch Phys Med Rehabil. 2014;95(2):353–9.
    1. Horak F, King L, Mancini M. Role of body-worn movement monitor technology for balance and gait rehabilitation. Phys Ther. 2015;95(3):461–470. doi: 10.2522/ptj.20140253.
    1. Mancini M, Horak FB. The relevance of clinical balance assessment tools to differentiate balance deficits. Eur J Phys Rehabil Med. 2010;46(2):239.
    1. Dozza M, Chiari L, Horak FB. Audio-biofeedback improves balance in patients with bilateral vestibular loss. Arch Phys Med Rehabil. 2005;86(7):1401–1403. doi: 10.1016/j.apmr.2004.12.036.
    1. Dozza M, Horak FB, Chiari L. Auditory biofeedback substitutes for loss of sensory information in maintaining stance. Exp Brain Res. 2007;178(1):37–48. doi: 10.1007/s00221-006-0709-y.
    1. Kansagara D, Maya Elin ON, Carlson K, Storzbach D, Brenner L, Freeman M, Quiñones A, Motu’apuaka M: Complications of Mild Traumatic Brain Injury in Veterans and Military Personnel: A Systematic Review. 2013.
    1. Katzman R, Brown T, Fuld P, Peck A, Schechter R, Schimmel H. Validation of a short Orientation-Memory-Concentration Test of cognitive impairment. Am J Psychiatry. 1983;140(6):734–739. doi: 10.1176/ajp.140.6.734.
    1. Pintelon R, Schoukens J. Measurement of frequency response functions using periodic excitations, corrupted by correlated input/output errors. IEEE Trans Instrum Meas. 2001;50(6):1753–1760. doi: 10.1109/19.982976.
    1. Peterka RJ. Simplifying the complexities of maintaining balance. IEEE Eng Med Biol Mag. 2003;22(2):63–68. doi: 10.1109/MEMB.2003.1195698.
    1. Mancini M, King L, Salarian A, Holmstrom L, McNames J, Horak FB. Mobility lab to assess balance and gait with synchronized body-worn sensors. J Bioeng Biomed Sci. 2011;Suppl 1:007.
    1. Baron RM, Kenny DA. The moderator–mediator variable distinction in social psychological research: Conceptual, strategic, and statistical considerations. J Pers Soc Psychol. 1986;51(6):1173. doi: 10.1037/0022-3514.51.6.1173.
    1. Herdman SJ. Role of vestibular adaptation in vestibular rehabilitation. Otolaryngol Head Neck Surg. 1998;119(1):49–54. doi: 10.1016/S0194-5998(98)70195-0.
    1. Shepard NT, Telian SA. Programmatic vestibular rehabilitation. Otolaryngol Head Neck Surg. 1995;112(1):173–182. doi: 10.1016/S0194-5998(95)70317-9.
    1. Weightman MM, Bolgla R, McCulloch KL, Peterson MD. Physical therapy recommendations for service members with mild traumatic brain injury. J Head Trauma Rehabil. 2010;25(3):206–218. doi: 10.1097/HTR.0b013e3181dc82d3.
    1. Mayagoitia RE, Nene AV, Veltink PH. Accelerometer and rate gyroscope measurement of kinematics: an inexpensive alternative to optical motion analysis systems. J Biomech. 2002;35(4):537–542. doi: 10.1016/S0021-9290(01)00231-7.
    1. Jacobson GP, Newman CW. The development of the dizziness handicap inventory. Arch Otolaryngol Head Neck Surg. 1990;116(4):424–427. doi: 10.1001/archotol.1990.01870040046011.
    1. Weathers FW, Litz BT, Herman DS, Huska JA, Keane TM: The PTSD Checklist (PCL): Reliability, validity, and diagnostic utility. In: annual convention of the international society for traumatic stress studies: 1993: International Society for Traumatic Stress Studies San Antonio; 1993.
    1. Bennett RM, Friend R, Marcus D, Bernstein C, Han BK, Yachoui R, Deodhar A, Kaell A, Bonafede P, Chino A. Criteria for the diagnosis of fibromyalgia: validation of the modified 2010 preliminary American College of Rheumatology criteria and the development of alternative criteria. Arthritis Res. 2014;66(9):1364–1373. doi: 10.1002/acr.22301.
    1. Friend R, Bennett RM. Distinguishing fibromyalgia from rheumatoid arthritis and systemic lupus in clinical questionnaires: an analysis of the revised Fibromyalgia Impact Questionnaire (FIQR) and its variant, the Symptom Impact Questionnaire (SIQR), along with pain locations. Arthritis Res Ther. 2011;13(2):1. doi: 10.1186/ar3311.
    1. McCrory P, Meeuwisse WH, Aubry M, Cantu B, Dvořák J, Echemendia RJ, Engebretsen L, Johnston K, Kutcher JS, Raftery 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(5):250–258. doi: 10.1136/bjsports-2013-092313.
    1. Beck AT, Steer RA, Brown GK. Beck depression inventory-II. San Antonio: The Psychological Corporation. 1996:78204–2498.
    1. McHorney CA, Ware JE, Lu J, Sherbourne CD. The MOS 36-item short-form health survey (SF-36) Med Care. 1994;32(1):40–66. doi: 10.1097/00005650-199401000-00004.
    1. Cicerone KD, Kalmar K. Persistent postconcussion syndrome: The structure of subjective complaints after mild traumatic brain injury. J Head Trauma Rehabil. 1995;10(3):1–17. doi: 10.1097/00001199-199510030-00002.
    1. Reeves DL, Winter KP, Bleiberg J, Kane RL. ANAM® Genogram: Historical perspectives, description, and current endeavors. Arch Clin Neuropsychol. 2007;22:15–37. doi: 10.1016/j.acn.2006.10.013.
    1. Eckner JT, Kutcher JS, Richardson JK. Pilot evaluation of a novel clinical test of reaction time in National Collegiate Athletic Association Division I football players. J Athl Train. 2010;45(4):327–332. doi: 10.4085/1062-6050-45.4.327.
    1. Shumway-Cook A, Horak FB. Assessing the influence of sensory interaction on balance. Phys Ther. 1986;66(10):1548–1550.
    1. Nashner LM, Peters JF. Dynamic posturography in the diagnosis and management of dizziness and balance disorders. Neurol Clin. 1990;8(2):331–49.

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