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Sports Medicine

, Volume 35, Issue 11, pp 935–950 | Cite as

A Nonlinear Dynamic Approach for Evaluating Postural Control

New Directions for the Management of Sport-Related Cerebral Concussion
  • James T. Cavanaugh
  • Kevin M. Guskiewicz
  • Nicholas Stergiou
Review Article

Abstract

Recent research suggests that traditional biomechanical models of postural stability do not fully characterise the nonlinear properties of postural control. In sports medicine, this limitation is manifest in the postural steadiness assessment approach, which may not be sufficient for detecting the presence of subtle physiological change after injury. The limitation is especially relevant given that return-to-play decisions are being made based on assessment results. This update first reviews the theoretical foundation and limitations of the traditional postural stability paradigm. It then offers, using the clinical example of athletes recovering from cerebral concussion, an alternative theoretical proposition for measuring changes in postural control by applying a nonlinear dynamic measure known as ‘approximate entropy’. Approximate entropy shows promise as a valuable means of detecting previously unrecognised, subtle physiological changes after concussion. It is recommended as an important supplemental assessment tool for determining an athlete’s readiness to resume competitive activity.

Keywords

Postural Control Postural Stability Postural Control System Quiet Standing Sensory Organisation Test 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

Dr Cavanaugh’s dissertation work focusing on the application of approximate entropy to the analysis of centre of pressure time series in athletes with concussion was conducted in the Sports Medicine Research Laboratory at the University of North Carolina, Chapel Hill, North Carolina, USA, under the direction of Dr Guskiewicz. The work was funded in part by grants from the Injury Prevention Research Center at the University of North Carolina at Chapel Hill, the National Center for Injury Prevention and Control (USA), the National Operating Committee on Standards in Athletic Equipment (USA), and the National Athletic Trainers’ Association Research and Education Fund (USA). The authors have no conflicts of interest that are directly relevant to the content of this review.

References

  1. 1.
    Palmieri RM, Ingersoll CD, Stone MB, et al. Center-of-pressure parameters used in the assessment of postural control. J Sport Rehabil 2002; 11: 51–66Google Scholar
  2. 2.
    Guskiewicz K. Balance and mild head injury in athletes. Orthop Phys Ther Clin N Am 2002; 11 (1): 143–157Google Scholar
  3. 3.
    Romberg M. Manual of nervous diseases of man. London: Sydenham Society, 1853: 395–401Google Scholar
  4. 4.
    Riemann BL, Guskiewicz K. Effects of mild head injury on postural stability as measured through clinical balance testing. J Athl Train 2000; 35 (1): 19–25PubMedGoogle Scholar
  5. 5.
    Guskiewicz KM, Ross SE, Marshall SM. Postural stability and neuropsychological deficits after concussion in collegiate athletes. J Athl Train 2001; 36 (3): 263–273PubMedGoogle Scholar
  6. 6.
    Ingersoll CD, Armstrong CW. The effects of closed-head injury on postural sway. Med Sci Sports Exerc 1992; 24 (7): 739–743PubMedGoogle Scholar
  7. 7.
    Duarte M, Zatsiorsky VM. On the fractal properties of natural human standing. Neurosci Lett 2000; 283: 173–176PubMedCrossRefGoogle Scholar
  8. 8.
    Gagey P-M, Martinerie J, Pezard L, et al. Balance in static conditions is controlled by a non-linear dynamic system. Ann Otolaryngol Chir Cervicofac 1998; 115: 161–168PubMedGoogle Scholar
  9. 9.
    Myklebust JB, Prieto TE, Myklebust BM. Evaluation of nonolinear dynamics in postural steadiness time series. Ann Biomed Eng 1995; 23: 711–719PubMedCrossRefGoogle Scholar
  10. 10.
    Blaszczyk JW, Klonowski W. Postural stability and fractal dynamics. Acta Neurobiol Exp (Wars) 2001; 61: 105–112Google Scholar
  11. 11.
    Cavanaugh JT, Mercer VS, Guskiewicz K. Response stability estimates for the Sensory Organization Test: equilibrium scores and approximate entropy values in healthy young adults. Gait Posture 2004; 20 Suppl. 1: S55Google Scholar
  12. 12.
    Cavanaugh JT, Mercer VS, Guskiewicz K. Effect of a secondary cognitive task on the temporal structure of postural control: implications for the dual task paradigm. Gait Posture 2004; 20 Suppl. 1: S54CrossRefGoogle Scholar
  13. 13.
    Bodfish JW, Parker DE, Lewis MH, et al. Stereotypy and motor control: differences in the postural stability dynamics of persons with stereotyped and dyskinetic movement disorders. Am J Ment Retard 2001; 106 (2): 123–134PubMedCrossRefGoogle Scholar
  14. 14.
    Newell K. Degress of freedom and the development of postural center of pressure profiles. In: Newell K, Molenaar P, editors. Applications of non-linear dynamics to developmental process modeling. Mahwah (NJ): Lawrence Erlbaum Associates, 1998: 80–81Google Scholar
  15. 15.
    Cavanaugh JT, Guskiewicz K, Giuliani C, et al. Detecting altered postural control after cerebral concussion in athletes without postural instability. Br J Sports Med. In pressGoogle Scholar
  16. 16.
    Shumway-Cook A, Woollacott M. Motor control: theory and practical applications. 1st ed. Baltimore (MD): Williams & Wilkins, 1995Google Scholar
  17. 17.
    Le Veau BF. Biomechanics of human motion. 3rd ed. Philadelphia (PA): WB Saunders, 1992Google Scholar
  18. 18.
    Goldie PA, Bach TM, Evans OM. Force platform measures for evaluating postural control: reliability and validity. Arch Phys Med Rehabil 1989; 70: 510–517PubMedGoogle Scholar
  19. 19.
    Schenkman M. Interrelationship of neurological and mechanical factors in balance control. In: Duncan PW, editor. Proceedings of the APT A Symposium on Balance. Nashville (TN): APTA, 1989: 29–41Google Scholar
  20. 20.
    Bernstein NA. Coordination and regulation of movements. New York: Pergamon Press Inc, 1967Google Scholar
  21. 21.
    Onaral B, Cammarota JP. Complexity, scaling, and fractals in biomedical signals. In: Bronzino JD, editor. The biomedical engineering handbook. New York: CRC Press Inc., 1995: 933–944Google Scholar
  22. 22.
    Stergiou N, Buzzi UH, Kurz MJ, et al. Nonlinear tools in human movement. In: Stergiou N, editor. Innovative analyses of human movement. Champaign (IL): Human Kinetics, 2004Google Scholar
  23. 23.
    Nashner LM. Sensory, neuromuscular, and bio mechanical contributions to human balance. In: Duncan PW, editor. Proceedings of the APT A Symposium on Balance. Nashville (TN): APTA, 1989: 5–12Google Scholar
  24. 24.
    Nicholas SC, Doxey-Gasway DD, Paloski WH. A link-segment model of upright human posture for analysis of head-trunk coordination. J Vestib Res 1998; 8 (3): 187–200PubMedCrossRefGoogle Scholar
  25. 25.
    Winter DA, Patla AE, Frank JS. Assessment of balance control in humans. Med Prog Technol 1990; 16 (1–2): 31–51PubMedGoogle Scholar
  26. 26.
    Nashner LM. A model describing vestibular detection of body sway motion. Acta Otolaryngol 1971; 72: 429–436PubMedCrossRefGoogle Scholar
  27. 27.
    Sasaki O, Gagey P-M, Ouaknine AM,et al. Non-linear analysis of orthostatic posture in patients with vertigo or balance disorders. Neurosci Res 2001; 41: 185–192PubMedCrossRefGoogle Scholar
  28. 28.
    Woollacott MH, Shumway-Cook A, Nashner LM. Aging and posture control: changes in sensory organization and muscular coordination. Int J Aging Hum Dev 1986; 23 (2): 97–114PubMedCrossRefGoogle Scholar
  29. 29.
    Kuo AD, Speers RA, Peterka RJ, et al. Effect of altered sensory conditions on multivariate descriptors of human postural sway. Exp Brain Res 1998; 122: 185–195PubMedCrossRefGoogle Scholar
  30. 30.
    Speers RA, Kuo AD, Horak F. Contributions of altered sensation and feedback responses to changes in coordination of postural control due to aging. Gait Posture 2002; 16: 20–30PubMedCrossRefGoogle Scholar
  31. 31.
    Slobounov SM, Newell KM. Postural dynamics in upright and inverted stances. J Appl Biomech 1996; 12: 185–196Google Scholar
  32. 32.
    Riccio GE, Stoffregen TA. Affordances as constraints on control of stance. Hum Mov Sci 1988; 7: 265–300CrossRefGoogle Scholar
  33. 33.
    Lipsitz LA, Goldberger AL. Loss of’ complexity’ and aging: potential applications of fractals and chaos theory to senescence. JAMA 1992; 267 (13): 1806–1809PubMedCrossRefGoogle Scholar
  34. 34.
    Nashner LM. Strategies for organization of human posture. In: Igarashi M, Black O, editors. Vestibular and visual control on posture and locomotor equilibrium. 7th International Symposium, International Society Posturography; 1983; Houston (TX). Basel: Karger, 1985: 1–8Google Scholar
  35. 35.
    Hasan SS, Robin DW, Shiavi RG. Drugs and postural sway. IEEE Eng in Med Biol Mag 1992; 11 (4): 35–41CrossRefGoogle Scholar
  36. 36.
    Rogers MM, Cavanagh PR. Glossary of bio mechanical terms, concepts, and units. Phys Ther 1984; 64 (12): 23–39Google Scholar
  37. 37.
    Patla A, Winter DA, Frank JS, et al. Identification of age-related changes in the balance control system. In: Duncan PW, editor. Proceedings of the American Physical Therapy Association Symposium on Balance; 1989 Jun 13–15; Nashville. Nashville (TN): APTA, 1989: 43–55Google Scholar
  38. 38.
    Prieto TE, Myklebust JB, Myklebust BM. Characterization and modeling of postural steadiness in the elderly: a review. IEEE Trans Rehabil Eng 1993; 1 (1): 26–34CrossRefGoogle Scholar
  39. 39.
    Rocchi L, Chiari L, Cappello A. Feature selection of stabilometric parameters based on principal component analysis. Med Biol Eng Comput 2004 Jan; 42 (1): 71–79PubMedCrossRefGoogle Scholar
  40. 40.
    Chiari L, Bertani A, Cappello A. Classification of visual strategies in human postural control by stochastic parameters. Hum Mov Sci 2000; 19: 817–842CrossRefGoogle Scholar
  41. 41.
    Messier SP, Royer TD, Craven TE, et al. Long-term exercise and its effect on balance in older, osteoarthritic adults: results from the Fitness, Arthritis, and Seniors Trial (FAST). J Am Geriatr Soc 2000; 48 (2): 131–138PubMedGoogle Scholar
  42. 42.
    Cornwall MW, Murrell P. Postural sway following inversion sprain of the ankle. J Am Podiatr Med Assoc 1991; 81: 243–247PubMedGoogle Scholar
  43. 43.
    Hufschmidt A, Dichgans J, Mauritz KH, et al. Some methods and parameters of body sway quantification and their neurological applications. Arch Psychiatr Nervenkr 1980; 228: 135–150PubMedCrossRefGoogle Scholar
  44. 44.
    Rocchi L, Chiari L, Horak F. Effects of deep brain stimulation and levodopa on postural sway in Parkinson’s disease. J Neurol Neurosurg Psychiatry 2002; 73 (3): 267–274PubMedCrossRefGoogle Scholar
  45. 45.
    Geurts ACH, Ribbers GM, Knoop JA, et al. Identification of static and dynamic postural instability following traumatic brain injury. Arch Phys Med Rehabil 1996; 77: 639–644PubMedCrossRefGoogle Scholar
  46. 46.
    Foudriat BA, Di Fabio RP, Anderson JH. Sensory organization of balance responses in children 3–6 years of age: a normative study with diagnostic implications. Int J Pediatr Otorhinolaryngol 1993; 27 (3): 255–271PubMedCrossRefGoogle Scholar
  47. 47.
    Usui N, Maekawa K, Hirasawa Y. Development of the upright postural sway of children. Dev Med Child Neurol 1995; 37 (11): 985–996PubMedCrossRefGoogle Scholar
  48. 48.
    Teasdale N, Stelmach GE, Breunig A. Postural sway characteristics of the elderly under normal and altered visual and support surface conditions. J Gerontol 1991; 46 (6): B238–B244PubMedCrossRefGoogle Scholar
  49. 49.
    Paloski WH, Black FO, Reschke MF, et al. Vestibular ataxia following shuttle flights: effects of microgravity on otolith-mediated sensorimotor control of posture. Am J Otol 1993; 14 (1): 9–17PubMedGoogle Scholar
  50. 50.
    Collins JJ, De Luca CJ, Burrows A, et al. Age-related changes in open-loop and closed-loop postural control mechanisms. Exp Brain Res 1995; 104: 480–492PubMedCrossRefGoogle Scholar
  51. 51.
    Lajoie Y, Teasdale N, Bard C, et al. Attentional demands for static and dynamic equilibrium. Exp Brain Res 1993; 97 (1): 139–144PubMedCrossRefGoogle Scholar
  52. 52.
    Riley MA, Wong S, Mitra S, et al. Common effects of touch and vision on postural parameters. Exp Brain Res 1997; 117: 165–170PubMedCrossRefGoogle Scholar
  53. 53.
    Sabatini AM. Analysis of postural sway using entropy measures of signal complexity. Med Biol Eng Comput 2000; 38: 617–624PubMedCrossRefGoogle Scholar
  54. 54.
    Winter DA. Sagittal plane balance and posture in human walking. IEEE Eng Med Biol Mag 1987; 9: 8–11CrossRefGoogle Scholar
  55. 55.
    Karlsson A, Frykberg G. Correlations between force plate measures for assessment of balance. Clin Biomech 2000; 15: 365–369CrossRefGoogle Scholar
  56. 56.
    Baloh RW, Jacobson KM, Enrietto JA, et al. Balance disorders in older persons: quantification with posturography. Otolaryngol Head Neck Surg 1998; 119: 89–92PubMedCrossRefGoogle Scholar
  57. 57.
    Di Fabio RP. Sensitivity and specificity of platform posturography for identifying patients with vestibular function. Phys Ther 1995; 75 (4): 290–305Google Scholar
  58. 58.
    Baloh RW, Fife TD, Zwerling L, et al. Comparison of static and dynamic posturography in young and older normal people. J Am Geriatr Soc 1994; 42 (4): 405–412PubMedGoogle Scholar
  59. 59.
    Glass L, Mackey MC. From clocks to chaos: the rhythms of life. Princeton (NJ): Princeton University Press, 1988Google Scholar
  60. 60.
    Carroll JP, Freedman W. Nonstationary properties of postural sway. J Biomech 1993; 26 (4/5): 409–416PubMedCrossRefGoogle Scholar
  61. 61.
    Collins JJ, De Luca CJ. Open-loop and closed-loop control of posture: a random-walk analysis of center-of-pressure trajectories. Exp Brain Res 1993; 95 (2): 308–318PubMedCrossRefGoogle Scholar
  62. 62.
    Oie KS, Kiemel T, Jeka J. Human multisensory fusion of vision and touch: detecting non-linearity with small changes in the sensory environment. Neurosci Lett 2001; 315: 113–116PubMedCrossRefGoogle Scholar
  63. 63.
    Thurner S, Mittermaier C, Hanel R, et al. Scaling-violation phenomena and fractality in the human posture control system. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 2000; 62 (3): 4018–4024PubMedCrossRefGoogle Scholar
  64. 64.
    Pincus SM. Approximate entropy as a measure of system complexity. Proc Natl Acad Sci U S A 1991; 88 (6): 2297–2301PubMedCrossRefGoogle Scholar
  65. 65.
    Grassberger P, Procaccia I. Measuring the strangeness of strange attractors. Physica D 1983; 9: 189–208CrossRefGoogle Scholar
  66. 66.
    Vaillancourt DE, Slifkin AB, Newell KM. Regularity of force tremor in Parkinson’s disease. Clin Neurophysiol Sep 2001; 11 (9): 1594–1603CrossRefGoogle Scholar
  67. 67.
    Pincus SM. Quantifying complexity and regularity of neurobiological systems. Methods Neurosci 1995; 28: 336–363CrossRefGoogle Scholar
  68. 68.
    Slifkin AB, Newell KM. Variability and noise in continuous force production. J Mot Behav 2000 Jun; 32 (2): 141–150PubMedCrossRefGoogle Scholar
  69. 69.
    Yates FE. General introduction. In: Yates FE editor. Self- organizing control systems: the emergence of order. New York: Plenum Press, 1987: 1–14Google Scholar
  70. 70.
    Pincus SM. Greater signal regularity may indicate increased system isolation. Math Biosci 1994; 122: 161–181PubMedCrossRefGoogle Scholar
  71. 71.
    Pincus SM, Keefe DL. Quantification of hormone pulsatility via an approximate entropy algorithm. Am J Physiol 1992; 262 (5 Pt 1): E741–E754PubMedGoogle Scholar
  72. 72.
    Pincus SM, Goldberger AL. Physiological time-series analysis: what does regularity quantify? Am J Physiol 1994; 266 (4 Pt 2): H1643–H1656PubMedGoogle Scholar
  73. 73.
    Newell KM, van Emmerik REA, Sprague RL. Sterotypy and variability. In: Newell KM, Corcos DM, editors. Variability and motor control. Champaign (IL): Human Kinetics Publishers, 1993: 475–496Google Scholar
  74. 74.
    Harbourne RT, Stergiou N. Nonlinear analysis of the development of sitting postural control. Dev Psychobiol 2003; 42: 368–377PubMedCrossRefGoogle Scholar
  75. 75.
    Thurman DJ, Branche CM, Sniezek JE. The epidemiology of sports-related traumatic brain injuries in the United States: recent developments. J Head Trauma Rehabil 1998; 13 (2): 1–8PubMedCrossRefGoogle Scholar
  76. 76.
    Guskiewicz KM, Weaver NL, Padua DA, et al. Epidemiology of concussion in collegiate and high school football players. Am J Sports Med 2000; 28 (5): 643–650PubMedGoogle Scholar
  77. 77.
    Guskiewicz KM, McCrea M, Marshall SW, et al. Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. JAMA 2003 Nov 19; 290 (19): 2549–2555PubMedCrossRefGoogle Scholar
  78. 78.
    Salcido R, Costich JF. Recurrent traumatic brain injury. Brain Inj 1992; 6 (3): 293–298PubMedCrossRefGoogle Scholar
  79. 79.
    Gronwall D, Wrightson P. Cumulative effect of concussion. Lancet 1975; II (7943): 995–997CrossRefGoogle Scholar
  80. 80.
    Saunders RL, Harbaugh RE. The second impact in catastrophic contact-sports head trauma. JAMA 1984; 252 (4): 538–539PubMedCrossRefGoogle Scholar
  81. 81.
    McCrory PR, Berkovic SF. Concussion: the history of clinical and pathophysiological concepts and misconceptions. Neurology 2001; 57 (12): 2283–2289PubMedCrossRefGoogle Scholar
  82. 82.
    Shaw N. The neurophysiology of concussion. Prog Neurobiol 2002; 67 (4): 281–344PubMedCrossRefGoogle Scholar
  83. 83.
    Mallinson AI, Longridge NS. Dizziness from whiplash and head injury: differences between whiplash and head injury. Am J Otol 1998; 19 (6): 814–818PubMedGoogle Scholar
  84. 84.
    Wojtys EM, Hovda D, Landry G, et al. Current concepts: concussion in sports. Am J Sports Med 1999; 27 (5): 676–687PubMedGoogle Scholar
  85. 85.
    McCrory P, Johnston KM, Mohtadi NG, et al. Evidence-based review of sport-related concussion: basic science. Clin J Sport Med 2001; 11 (3): 160–165PubMedCrossRefGoogle Scholar
  86. 86.
    Salenius S, Hari R. Synchronous cortical oscillatory activity during motor action. Curr Opin Neurobiol Dec 2003; 13 (6): 678–684CrossRefGoogle Scholar
  87. 87.
    Guskiewicz KM, Perrin DH, Gansneder BM. Effect of mild head injury on postural stability in athletes. J Athl Train 1996; 31 (4): 300–306PubMedGoogle Scholar
  88. 88.
    Guskiewicz KM, Riemann BL, Perrin DH, et al. Alternative approaches to the assessment of mild head injury in athletes. Med Sci Sports Exerc 1997; 29 (7 Suppl.): S213–S221PubMedGoogle Scholar
  89. 89.
    Mrazik M, Ferrara MS, Peterson CL, et al. Injury severity and neuropsychological and balance outcomes of four college athletes. Brain Inj 2000; 14 (10): 921–931PubMedCrossRefGoogle Scholar
  90. 90.
    Cavanaugh J, Guskiewicz K, Stergiou N. New insights into the recovery of postural control after cerebral concussion. J Orthop Sport Phys Ther 2005; 35 (1): A77–A78Google Scholar

Copyright information

© Adis Data Information BV 2005

Authors and Affiliations

  • James T. Cavanaugh
    • 1
    • 2
  • Kevin M. Guskiewicz
    • 3
  • Nicholas Stergiou
    • 4
  1. 1.Geriatric Research, Education and Clinical Center, Department of Veterans Affairs Medical CenterDurhamUSA
  2. 2.Department of Physical and Occupational TherapyDuke University Medical CenterDurhamUSA
  3. 3.Department of Exercise and Sport ScienceUniversity of North CarolinaChapel HillUSA
  4. 4.HPER Biomechanics LaboratoryUniversity of Nebraska at OmahaOmahaUSA

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