Objective biomarkers of balance and gait for Parkinson's disease using body-worn sensors
Corresponding Author
Fay B. Horak PhD, PT
Department of Neurology, Oregon Health & Science University, Portland, Oregon
Correspondence to: Dr. Fay B. Horak, Professor of Neurology, Parkinson Center of Oregon (OP32), 3181 SW Sam Jackson Park Road, Portland, OR 97239; [email protected], [email protected]Search for more papers by this authorMartina Mancini PhD
Department of Neurology, Oregon Health & Science University, Portland, Oregon
Search for more papers by this authorCorresponding Author
Fay B. Horak PhD, PT
Department of Neurology, Oregon Health & Science University, Portland, Oregon
Correspondence to: Dr. Fay B. Horak, Professor of Neurology, Parkinson Center of Oregon (OP32), 3181 SW Sam Jackson Park Road, Portland, OR 97239; [email protected], [email protected]Search for more papers by this authorMartina Mancini PhD
Department of Neurology, Oregon Health & Science University, Portland, Oregon
Search for more papers by this authorFunding agencies: This work was supported by the National Institutes on Aging, the National Center of Medical Rehabilitation Research, the Kinetics Foundation, and Oregon Health & Science University.
Relevant conflicts of interest/financial disclosures: Dr Fay Horak and OHSU have significant financial interests in APDM, a company that might have a commercial interest in the results of this research and technology. This potential conflict of interest has been reviewed and managed by OHSU and the Integrity Oversight Council.
Full financial disclosures and author roles may be found in the online version of this article.
ABSTRACT
Balance and gait impairments characterize the progression of Parkinson's disease (PD), predict the risk of falling, and are important contributors to reduced quality of life. Advances in technology of small, body-worn, inertial sensors have made it possible to develop quick, objective measures of balance and gait impairments in the clinic for research trials and clinical practice. Objective balance and gait metrics may eventually provide useful biomarkers for PD. In fact, objective balance and gait measures are already being used as surrogate endpoints for demonstrating clinical efficacy of new treatments, in place of counting falls from diaries, using stop-watch measures of gait speed, or clinical balance rating scales. This review summarizes the types of objective measures available from body-worn sensors. The metrics are organized based on the neural control system for mobility affected by PD: postural stability in stance, postural responses, gait initiation, gait (temporal-spatial lower and upper body coordination and dynamic equilibrium), postural transitions, and freezing of gait. However, the explosion of metrics derived by wearable sensors during prescribed balance and gait tasks, which are abnormal in individuals with PD, do not yet qualify as behavioral biomarkers, because many balance and gait impairments observed in PD are not specific to the disease, nor have they been related to specific pathophysiologic biomarkers. In the future, the most useful balance and gait biomarkers for PD will be those that are sensitive and specific for early PD and are related to the underlying disease process. © 2013 International Parkinson and Movement Disorder Society
References
- 1 Biomarkers Definitions Working Group. Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin Pharmacol Ther 2001; 69: 89–95.
- 2 MacPherson JM, Horak FB. Posture. Chapter 41. In: E Kandel, J Schwartz, T Jessell, S Siegelbaum, AJ Hudspeth, eds. Principles of Neural Science. 5th ed. New York: McGraw-Hill; 2012: 935–959.
- 3
Winter D. Biomechanics and Motor Control of Human Movement. 4th ed. Hoboken, NJ: John Wiley & Sons, Inc.; 2009.
10.1002/9780470549148 Google Scholar
- 4 Schoneburg B, Mancini M, Horak F, Nutt JG. Framework for understanding balance dysfunction in Parkinson's disease [published online ahead of print 7 August 2013]. Mov Disord 2013.
- 5 Nutt JG, Horak FB, Bloem BR. Milestones in gait, balance, and falling. Mov Disord 2011; 26: 1166–1174.
- 6 Gerlach M, Maetzler W, Broich K, et al. Biomarker candidates of neurodegeneration in Parkinson's disease for the evaluation of disease-modifying therapeutics. J Neural Transm 2012; 119: 39–52.
- 7 Horak FB, Frank J, Nutt J. Effects of dopamine on postural control in parkinsonian subjects: scaling, set, and tone. J Neurophysiol 1996; 75: 2380–2396.
- 8 Rocchi L, Carlson-Kuhta P, Chiari L, Burchiel KJ, Hogarth P, Horak FB. Effects of deep brain stimulation in the subthalamic nucleus or globus pallidus internus on step initiation in Parkinson disease: laboratory investigation. J Neurosurg 2012; 117: 1141–1149.
- 9 St George RJ, Carlson-Kuhta P, Burchiel KJ, Hogarth P, Frank N, Horak FB. The effects of subthalamic and pallidal deep brain stimulation on postural responses in patients with Parkinson disease. J Neurosurg 2012; 116: 1347–1356.
- 10 Zampieri C, Salarian A, Carlson-Kuhta P, Aminian K, Nutt JG, Horak FB. The instrumented timed up and go test: potential outcome measure for disease modifying therapies in Parkinson's disease. J Neurol Neurosurg Psychiatry 2010; 81: 171–176.
- 11 Bilney B, Morris M, Webster K. Concurrent related validity of the GAITRite walkway system for quantification of the spatial and temporal parameters of gait. Gait Posture 2003; 17: 68–74.
- 12 Mancini M, King LA, Salarian A, Holmstrom L, McNames J, Horak FB. Mobility lab to assess balance and gait with synchronized body-worn sensors. J Bioeng Biomed Sci 2012; 1: 2–7.
- 13 Baltadjieva R, Giladi N, Gruendlinger L, Peretz C, Hausdorff JM. Marked alterations in the gait timing and rhythmicity of patients with de novo Parkinson's disease. Eur J Neurosci 2006; 24: 1815–1820.
- 14 Hausdorff JM. Gait dynamics in Parkinson's disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling [serial online]. Chaos 2009; 19: 026113.
- 15 Hausdorff JM, Cudkowicz ME, Firtion R, Wei JY, Goldberger AL. Gait variability and basal ganglia disorders: stride-to-stride variations of gait cycle timing in Parkinson's disease and Huntington's disease. Mov Disord 1998; 13: 428–437.
- 16 Shany T, Redmond SJ, Marschollek M, Lovell NH. Assessing fall risk using wearable sensors: a practical discussion. A review of the practicalities and challenges associated with the use of wearable sensors for quantification of fall risk in older people. Z Gerontol Geriatr 2012; 45: 694–706.
- 17 Peterka RJ, Benolken MS. Role of somatosensory and vestibular cues in attenuating visually induced human postural sway. Exp Brain Res 1995; 105: 101–110.
- 18 Maurer C, Mergner T, Peterka RJ. Multisensory control of human upright stance. Exp Brain Res 2006; 171: 231–250.
- 19 Maurer C, Peterka RJ. A new interpretation of spontaneous sway measures based on a simple model of human postural control. J Neurophysiol 2005; 93: 189–200.
- 20 Rocchi L, Chiari L, Cappello A. Feature selection of stabilometric parameters based on principal component analysis. Med Biol Eng Comput 2004; 42: 71–79.
- 21 Merlo A, Zemp D, Zanda E, Rocchi S, Meroni F, Tettamanti M, et al. Postural stability and history of falls in cognitively able older adults: the Canton Ticino study. Gait Posture 2012; 36: 662–666.
- 22 Melzer I, Kurz I, Oddsson LI. A retrospective analysis of balance control parameters in elderly fallers and non-fallers. Clin Biomech (Bristol, Avon) 2010; 25: 984–988.
- 23 Norris JA, Marsh AP, Smith IJ, Kohut RI, Miller ME. Ability of static and statistical mechanics posturographic measures to distinguish between age and fall risk. J Biomech 2005; 38: 1263–1272.
- 24 Palmerini L, Rocchi L, Mellone S, Valzania F, Chiari L. Feature selection for accelerometer-based posture analysis in Parkinson's disease. IEEE Trans Inf Technol Biomed 2011; 15: 481–490.
- 25 Mancini M, Salarian A, Carlson-Kuhta P, Zampieri C, King L, Chiari L, et al. ISway: a sensitive, valid and reliable measure of postural control [serial online]. J Neuroeng Rehabil 2012; 9: 59.
- 26 O'Sullivan M, Blake C, Cunningham C, Boyle G, Finucane C. Correlation of accelerometry with clinical balance tests in older fallers and non-fallers. Age Ageing 2009; 38: 308–313.
- 27 Whitney SL, Roche JL, Marchetti GF, et al. A comparison of accelerometry and center of pressure measures during computerized dynamic posturography: a measure of balance. Gait Posture 2011; 33: 594–599.
- 28 Mancini M, Horak FB, Zampieri C, Carlson-Kuhta P, Nutt JG, Chiari L. Trunk accelerometry reveals postural instability in untreated Parkinson's disease. Parkinsonism Relat Disord 2011; 17: 557–562.
- 29 Maetzler W, Mancini M, Liepelt-Scarfone I, et al. Impaired trunk stability in individuals at high risk for Parkinson's disease [serial online]. PLoS One 2012; 7: e32240.
- 30 Mancini M, Carlson-Kuhta P, Zampieri C, Nutt JG, Chiari L, Horak FB. Postural sway as a marker of progression in Parkinson's disease: a pilot longitudinal study. Gait Posture 2012; 36: 471–476.
- 31 Rocchi L, Chiari L, Horak FB. Effects of deep brain stimulation and levodopa on postural sway in Parkinson's disease. J Neurol Neurosurg Psychiatry 2002; 73: 267–274.
- 32 King LA, Salarian A, Mancini M, et al. Exploring outcome measures for exercise intervention in people with Parkinson's disease [published online ahead of print 30 April 2013]. Parkinsons Dis 2013.
- 33 Melzer I, Benjuya N, Kaplanski J. Postural stability in the elderly: a comparison between fallers and non-fallers. Age Ageing 2004; 33: 602–607.
- 34 King LA, St George RJ, Carlson-Kuhta P, Nutt JG, Horak FB. Preparation for compensatory forward stepping in Parkinson's disease. Arch Phys Med Rehabil 2010; 91: 1332–1338.
- 35 Jacobs JV, Horak FB, Van Tran K, Nutt JG. An alternative clinical postural stability test for patients with Parkinson's disease. J Neurol 2006; 253: 1404–1413.
- 36 Horak FB, Nutt JG, Nashner LM. Postural inflexibility in parkinsonian subjects. J Neurol Sci 1992; 111: 46–58.
- 37 Chong RK, Horak FB, Woollacott MH. Time-dependent influence of sensorimotor set on automatic responses in perturbed stance. Exp Brain Res 1999; 124: 513–519.
- 38 El-Gohary M, Smith B, Carlson-Kuhta P, Horak F. Instrumented Push and Release Test (IPUSH) for Postural Responses Using Wearable Inertial Sensors. [Abstract] San Diego, CA: Society for Neuroscience; 2013
- 39 Mancini M, Zampieri C, Carlson-Kuhta P, Chiari L, Horak FB. Anticipatory postural adjustments prior to step initiation are hypometric in untreated Parkinson's disease: an accelerometer-based approach. Eur J Neurol 2009; 16: 1028–1034.
- 40 Martinez-Mendez R, Sekine M, Tamura T. Detection of anticipatory postural adjustments prior to gait initiation using inertial wearable sensors [serial online]. J Neuroeng Rehabil 2011; 8: 17.
- 41 Rocchi L, Mancini M, Chiari L, Cappello A. Dependence of anticipatory postural adjustments for step initiation on task movement features: a study based on dynamometric and accelerometric data. Conf Proc IEEE Eng Med Biol Soc 2006; 1: 1489–1492.
- 42 Burleigh-Jacobs A, Horak FB, Nutt JG, Obeso JA. Step initiation in Parkinson's disease: influence of levodopa and external sensory triggers. Mov Disord 1997; 12: 206–215.
- 43 Breniere J DM, Bouisset S. Are dynamic phenomena prior to stepping essential to walking? J Mot Behav 1987; 19: 62–76.
- 44 Breniere Y, Do MC. Control of gait initiation. J Mot Behav 1991; 23: 235–240.
- 45 Morris ME, Iansek R, Matyas TA, Summers JJ. The pathogenesis of gait hypokinesia in Parkinson's disease. Brain 1994; 117(pt 5): 1169–1181.
- 46 Hausdorff JM, Edelberg HK, Mitchell SL, Goldberger AL, Wei JY. Increased gait unsteadiness in community-dwelling elderly fallers. Arch Phys Med Rehabil 1997; 78: 278–283.
- 47 Hausdorff JM, Rios DA, Edelberg HK. Gait variability and fall risk in community-living older adults: a 1-year prospective study. Arch Phys Med Rehabil 2001; 82: 1050–1056.
- 48 Chee R, Murphy A, Danoudis M, Georgiou-Karistianis N, Iansek R. Gait freezing in Parkinson's disease and the stride length sequence effect interaction. Brain 2009; 132(pt 8): 2151–2160.
- 49 Salarian A, Russmann H, Vingerhoets FJ, Dehollain C, Blanc Y, Burkhard PR, Aminian K. Gait assessment in Parkinson's disease: toward an ambulatory system for long-term monitoring. IEEE Trans Biomed Eng 2004; 51: 1434–1443.
- 50 O'Connor SM, Kuo AD. Direction-dependent control of balance during walking and standing. J Neurophysiol 2009; 102: 1411–1419.
- 51 Boonsinsukh R, Saengsirisuwan V, Carlson-Kuhta P, Horak FB. A cane improves postural recovery from an unpracticed slip during walking in people with Parkinson disease. Phys Ther 2012; 92: 1117–1129.
- 52 Brach JS, Berlin JE, VanSwearingen JM, Newman AB, Studenski SA. Too much or too little step width variability is associated with a fall history in older persons who walk at or near normal gait speed [serial online]. J Neuroeng Rehabil 2005; 2: 21.
- 53 Hausdorff JM. Gait dynamics, fractals and falls: finding meaning in the stride-to-stride fluctuations of human walking. Hum Mov Sci 2007; 26: 555–589.
- 54 Callisaya ML, Blizzard L, Schmidt MD, Martin KL, McGinley JL, Sanders LM, Srikanth VK. Gait, gait variability and the risk of multiple incident falls in older people: a population-based study. Age Ageing 2011; 40: 481–487.
- 55 Rebula JR, Ojeda LV, Adamczyk PG, Kuo AD. Measurement of foot placement and its variability with inertial sensors [published online ahead of print 26 June 2013]. Gait Posture 2013.
- 56 Bryant MS, Rintala DH, Hou JG, et al. Gait variability in Parkinson's disease: influence of walking speed and dopaminergic treatment. Neurol Res 2011; 33: 959–964.
- 57 Lord S, Baker K, Nieuwboer A, Burn D, Rochester L. Gait variability in Parkinson's disease: an indicator of non-dopaminergic contributors to gait dysfunction? J Neurol 2011; 258: 566–572.
- 58 Mirelman A, Gurevich T, Giladi N, Bar-Shira A, Orr-Urtreger A, Hausdorff JM. Gait alterations in healthy carriers of the LRRK2 G2019S mutation. Ann Neurol 2011; 69: 193–197.
- 59 Greene BR, Doheny EP, Walsh C, Cunningham C, Crosby L, Kenny RA. Evaluation of falls risk in community-dwelling older adults using body-worn sensors. Gerontology 2012; 58: 472–480.
- 60 Weiss A, Herman T, Plotnik M, Brozgol M, Giladi N, Hausdorff JM. An instrumented timed up and go: the added value of an accelerometer for identifying fall risk in idiopathic fallers. Physiol Meas 2011; 32: 2003–2018.
- 61 King LA, Mancini M, Priest K, Salarian A, Rodrigues-de-Paula F, Horak F. Do clinical scales of balance reflect turning abnormalities in people with Parkinson's disease? J Neurol Phys Ther 2012; 36: 25–31.
- 62 Palmerini L, Mellone S, Avanzolini G, Valzania F, Chiari L. Quantification of motor impairment in Parkinson's disease using an instrumented timed up and go test. IEEE Trans Neural Syst Rehabil Eng 2013; 21: 664–673.
- 63 Weiss A, Herman T, Plotnik M, et al. Can an accelerometer enhance the utility of the Timed Up & Go Test when evaluating patients with Parkinson's disease? Med Eng Phys 2010; 32: 119–125.
- 64
Adame MR,
Al-Jawad A,
Romanovas M,
Hobert MA,
Maetzler W,
Moller K,
Manoli Y. TUG Test Instrumentation for Parkinson's disease patients using Inertial Sensors and Dynamic Time Warping [published online ahead of print 30 August 2012]. Biomed Tech (Berl) 2012.
10.1515/bmt-2012-4426 Google Scholar
- 65 Moore ST, MacDougall HG, Ondo WG. Ambulatory monitoring of freezing of gait in Parkinson's disease. J Neurosci Methods 2008; 167: 340–348.
- 66 Hausdorff JM, Balash Y, Giladi N. Time series analysis of leg movements during freezing of gait in Parkinson's disease: akinesia, rhyme or reason? Physica A 2003; 321(3-4): 565–570.
- 67 Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A. Freezing of gait: moving forward on a mysterious clinical phenomenon. Lancet Neurol 2011; 10: 734–744.
- 68 Mancini M, Priest KC, Nutt JG, Horak FB. Quantifying freezing of gait in Parkinson's disease during the instrumented timed up and go test. Conf Proc IEEE Eng Med Biol Soc 2012;2012: 1198–1201.
- 69 Mancini M, Horak FB. The relevance of clinical balance assessment tools to differentiate balance deficits. Eur J Phys Rehabil Med 2010; 46: 239–248.
- 70 Cavanaugh JT, Ellis TD, Earhart GM, Ford MP, Foreman KB, Dibble LE. Capturing ambulatory activity decline in Parkinson's disease. J Neurol Phys Ther 2012; 36: 51–57.
- 71 Rochester L, Chastin SF, Lord S, Baker K, Burn DJ. Understanding the impact of deep brain stimulation on ambulatory activity in advanced Parkinson's disease. J Neurol 2012; 259: 1081–1086.
- 72 Weiss A, Sharifi S, Plotnik M, van Vugt JP, Giladi N, Hausdorff JM. Toward automated, at-home assessment of mobility among patients with Parkinson disease, using a body-worn accelerometer. Neurorehabil Neural Repair 2011; 25: 810–818.
- 73 Jahn K, Deutschlander A, Stephan T, et al. Imaging human supraspinal locomotor centers in brainstem and cerebellum. Neuroimage 2008; 39: 786–792.
- 74 Fling BW, Cohen RG, Mancini M, Nutt JG, Fair DA, Horak FB. Asymmetric pedunculopontine network connectivity in parkinsonian patients with freezing of gait. Brain 2013; 136(pt 8): 2405–2418.