Review
Moving forward on gait measurement: Toward a more refined approach
Sue Lord PhD,
Brook Galna PhD,
Lynn Rochester PhD,
Sue Lord PhD
Institute for Ageing and Health, Clinical Ageing Research Unit, Newcastle University, United Kingdom
Search for more papers by this authorBrook Galna PhD
Institute for Ageing and Health, Clinical Ageing Research Unit, Newcastle University, United Kingdom
Search for more papers by this authorCorresponding Author
Lynn Rochester PhD
Institute for Ageing and Health, Clinical Ageing Research Unit, Newcastle University, United Kingdom
Correspondence to: Dr. Lynn Rochester, Professor of Human Movement Science, Institute for Ageing and Health, Newcastle University, Clinical Ageing Research Unit, Campus for Ageing and Vitality, Newcastle upon Tyne, NE4 5PL United Kingdom; [email protected]Search for more papers by this authorSue Lord PhD,
Brook Galna PhD,
Lynn Rochester PhD,
Sue Lord PhD
Institute for Ageing and Health, Clinical Ageing Research Unit, Newcastle University, United Kingdom
Search for more papers by this authorBrook Galna PhD
Institute for Ageing and Health, Clinical Ageing Research Unit, Newcastle University, United Kingdom
Search for more papers by this authorCorresponding Author
Lynn Rochester PhD
Institute for Ageing and Health, Clinical Ageing Research Unit, Newcastle University, United Kingdom
Correspondence to: Dr. Lynn Rochester, Professor of Human Movement Science, Institute for Ageing and Health, Newcastle University, Clinical Ageing Research Unit, Campus for Ageing and Vitality, Newcastle upon Tyne, NE4 5PL United Kingdom; [email protected]Search for more papers by this authorRelevant conflicts of interest/financial disclosures: Nothing to report.
Full financial disclosures and author roles may be found in the online version of this article.
Funding agencies: This research was supported by the National Institute for Health Research (NIHR) Newcastle Biomedical Research Centre based at Newcastle upon Tyne Hospitals National Health Service Foundation Trust and Newcastle University. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health.
ABSTRACT
Gait is emerging as a powerful measurement tool in neurodegenerative disorders to identify markers of incipient pathology, inform diagnostic algorithms and disease progression, and measure the efficacy of interventions. However, it is unclear which of the many gait outcomes is most appropriate for each of these purposes. In this review, we summarise key topics relating to gait measurement. We draw on literature from Parkinson's disease, ageing, and neurodegenerative disease to address the issue of variable selection with the goal of moving toward a structured approach to measurement. Findings from this review identify a wide range of spatiotemporal and dynamic characteristics; however, their suitability differs according to the aim of measurement. Gait speed is useful as a global characteristic of performance but may not capture the nature of underlying pathology. Inconsistent application, reporting, and interpretation of gait outcomes currently preclude a prescriptive approach. Conceptual models of gait may facilitate a reasoned approach to outcome selection. We also recommend harmonisation of protocols, longitudinal cohort studies, and use of novel technologies and methods of analysis to provide a complete picture of gait. Gait characteristics are “fit for purpose” when selected according to a clear rationale and in accordance with their clinimetric properties. Evidence supports the use of gait as a biomarker of disease and to complement diagnosis and inform disease management. A structured approach to measurement is urgently required to fully realise the contribution gait can make to our understanding of neurodegenerative disease. © 2013 International Parkinson and Movement Disorder Society
References
- 1
Studenski S,
Perera S,
Patel K, et al. Gait speed and survival in older adults. JAMA 2011; 305: 50–58.
- 2
Pickering RM,
Grimbergen YA,
Rigney U, et al. A meta-analysis of six prospective studies of falling in Parkinson's disease. Mov Disord 2007; 22: 1892–1900.
- 3
Speelman AD,
van de Warrenburg BP,
van Nimwegen M,
Petzinger GM,
Munneke M,
Bloem BR. How might physical activity benefit patients with Parkinson disease? Nat Rev Neurol 2011; 7: 528–534.
- 4
Nutt J,
Marsden C,
Thompson P. Human walking and higher-level gait disorders, particularly in the elderly. Neurology 1993; 43: 269–279.
- 5
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.
- 6
Verghese J,
Wang C,
Lipton RB,
Holtzer R,
Xue X. Quantitative gait dysfunction and risk of cognitive decline and dementia. J Neurol Neurosurg Psychiatry 2007; 78: 929–935.
- 7
Abellan van Kan G,
Rolland Y,
Andrieu S, et al. Gait speed at usual pace as a predictor of adverse outcomes in community-dwelling older people an International Academy on Nutrition and Aging (IANA) Task Force. J Nutr Health Aging 2009; 13: 881–889.
- 8
Nieuwboer A,
Kwakkel G,
Rochester L, et al. Cueing training in the home improves gait-related mobility in Parkinson's disease: the RESCUE trial. J Neurol Neurosurg Psychiatry 2007; 78: 134–140.
- 9
Hausdorff JM. Gait variability: methods, modeling and meaning [serial online]. J Neuroeng Rehabil 2005; 2: 19.
- 10
Lord S,
Galna B,
Verghese J,
Coleman S,
Burn D,
Rochester L. Independent domains of gait in older adults and associated motor and non-motor attributes: validation of a factor analysis approach [published online ahead of print 18 December 2012]. J Gerontol 2012.
- 11
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.
- 12
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.
- 13
Bohannon RW,
Andrews AW,
Thomas MW. Walking speed: reference values and correlates for older adults. J Orthop Sports Phys Ther 1996; 24: 86–90.
- 14
Lim LI,
van Wegen EE,
de Goede CJ, et al. Measuring gait and gait-related activities in Parkinson's patients own home environment: a reliability, responsiveness and feasibility study. Parkinsonism Relat Disord 2005; 11: 19–24.
- 15
Lord S,
Howe T,
Greenland J,
Simpson L,
Rochester L. Gait variability in older adults: a structured review of testing protocol and clinimetric properties. Gait Posture 2011; 34: 443–450.
- 16
Brach JS,
Perera S,
Studenski S,
Katz M,
Hall C,
Verghese J. Meaningful change in measures of gait variability in older adults. Gait Posture 2010; 31: 175–179.
- 17
Montero-Odasso M,
Wells JL,
Borrie MJ,
Speechley M. Can cognitive enhancers reduce the risk of falls in older people with mild cognitive impairment? A protocol for a randomised controlled double blind trial [serial online]. BMC Neurol 2009; 9: 42.
- 18
Graham JE,
Ostir GV,
Fisher SR,
Ottenbacher KJ. Assessing walking speed in clinical research: a systematic review. J Eval Clin Pract 2008; 14: 552–562.
- 19
Steffen T,
Seney M. Test-retest reliability and minimal detectable change on balance and ambulation tests, the 36-item short-form health survey, and the Unified Parkinson Disease Rating Scale in people with parkinsonism. Phys Ther 2008; 88: 733–746.
- 20
Galna B,
Lord S,
Rochester L. Is gait variability reliable in older adults and in Parkinson's disease? Towards an optimal testing protocol. Gait Posture 2013; 37: 580–585.
- 21
Hollman JH,
Childs KB,
McNeil ML,
Mueller AC,
Quilter CM,
Youdas JW. Number of strides required for reliable measurements of pace, rhythm and variability parameters of gait during normal and dual task walking in older individuals. Gait Posture 2010; 32: 23–28.
- 22
Beauchet O,
Freiberger E,
Annweiler C,
Kressig RW,
Herrmann FR,
Allali G. Test-retest reliability of stride time variability while dual tasking in healthy and demented adults with frontotemporal degeneration [serial online]. J Neuroeng Rehabil 2011; 8: 37.
- 23
Verghese J,
Holtzer R,
Lipton RB,
Wang C. Mobility stress test approach to predicting frailty, disability, and mortality in high-functioning older adults. J Am Geriatr Soc 2012; 60: 1901–1905.
- 24
Srygley JM,
Mirelman A,
Herman T,
Giladi N,
Hausdorff JM. When does walking alter thinking? Age and task associated findings. Brain Res 2009; 1253: 92–99.
- 25
Snijders A,
van de Warrenburg B,
Giladi N,
Bloem B. Neurological gait disorders in elderly people: clinical approach and classification. Lancet Neurol 2007; 6: 63–74.
- 26
Beauchet O,
Annweiler C,
Dubost V, et al. Stops walking when talking: a predictor of falls in older adults? Eur J Neurol 2009; 16: 786–795.
- 27
Kelly VE,
Eusterbrock AJ,
Shumway-Cook A. A review of dual-task walking deficits in people with Parkinson's disease: motor and cognitive contributions, mechanisms, and clinical implications [serial online]. Parkinsons Dis 2012; 2012: 918719.
- 28
Al-Yahya E,
Dawes H,
Smith L,
Dennis A,
Howells K,
Cockburn J. Cognitive motor interference while walking: a systematic review and meta-analysis. Neurosci Biobehav Rev 2011; 35: 715–728.
- 29
Smulders K,
Esselink RA,
Weiss A,
Kessels RP,
Geurts AC,
Bloem BR. Assessment of dual tasking has no clinical value for fall prediction in Parkinson's disease. J Neurol 2012; 259: 1840–1847.
- 30
Lord S,
Rochester L,
Baker K,
Nieuwboer A. Concurrent validity of accelerometry to measure gait in Parkinsons disease. Gait Posture 2008; 27: 357–359.
- 31
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.
- 32
Paterson KL,
Lythgo ND,
Hill KD. Gait variability in younger and older adult women is altered by overground walking protocol. Age Ageing 2009; 38: 745–748.
- 33
Jahn K,
Zwergal A,
Schniepp R. [Gait disturbances in old age classification, diagnosis, and treatment from a neurological perspective.] Deutsches Arzteblatt Int 2010; 107: 306–339.
- 34Frenkel-Toledo S, Giladi N, Peretz C, Herman T, Gruendlinger L, Hausdorff JM. Treadmill walking as an external pacemaker to improve gait rhythm and stability in Parkinson's disease. Mov Disord 2005; 20: 1109–1114.
- 35
Ebersbach G,
Sojer M,
Valldeoriola F, et al. Comparative analysis of gait in Parkinson's disease, cerebellar ataxia and subcortical arteriosclerotic encephalopathy. Brain 1999; 122(pt 7): 1349–1355.
- 36
Morris M,
Iansek R,
Matyas T,
Summers J. Abnormalities in the stride length-cadence relation in parkinsonian gait. Mov Disord 1998; 13: 61–69.
- 37
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.
- 38
Stolze H,
Kuhtz-Buschbeck JP,
Drucke H,
Johnk K,
Illert M,
Deuschl G. Comparative analysis of the gait disorder of normal pressure hydrocephalus and Parkinson's disease. J Neurol Neurosurg Psychiatry 2001; 70: 289–297.
- 39
Serrao M,
Pierelli F,
Ranavolo A, et al. Gait pattern in inherited cerebellar ataixa. Cerebellum 2012; 11: 194–211.
- 40
Rao AK,
Muratori L,
Louis ED,
Moskowitz CB,
Marder KS. Spectrum of gait impairments in presymptomatic and symptomatic Huntington's disease. Mov Disord 2008; 23: 1100–1107.
- 41
Rao AK,
Mazzoni P,
Wasserman P,
Marder K. Longitudinal change in gait and motor function in pre-manifest Huntington's disease [serial online]. PLoS Curr 2011; 3: RRN1268.
- 42
Mak MK,
Pang MY. Fear of falling is independently associated with recurrent falls in patients with Parkinson's disease: a 1-year prospective study. J Neurol 2009; 256: 1689–1695.
- 43
Wade D. Measurement in Neurological Rehabilitation. Oxford, United Kingdom: Oxford University Press; 1992.
- 44
Mehrholz J,
Friis R,
Kugler J,
Twork S,
Storch A,
Pohl M. Treadmill training for patients with Parkinson's disease. Cochrane Database Syst Rev 2010(1): CD007830.
- 45
Tomlinson CL,
Patel S,
Meek C, et al. Physiotherapy intervention in Parkinson's disease: systematic review and meta-analysis [serial online]. BMJ 2012; 345: e5004.
- 46
Blin O,
Ferrandez AM,
Pailhous J,
Serratrice G. Dopa-sensitive and dopa-resistant gait parameters in Parkinson's disease. J Neurol Sci 1991; 103: 51–54.
- 47
O'Sullivan JD,
Said CM,
Dillon LC,
Hoffman M,
Hughes AJ. Gait analysis in patients with Parkinson's disease and motor fluctuations: influence of levodopa and comparison with other measures of motor function. Mov Disord 1998; 13: 900–906.
- 48
Rochester L,
Baker K,
Nieuwboer A,
Burn D. Targeting dopa-sensitive and dopa-resistant gait dysfunction in Parkinson's disease: selective responses to internal and external cues. Mov Disord 2011; 26: 430–435.
- 49
Holtzer R,
Verghese J,
Xue X,
Lipton RB. Cognitive processes related to gait velocity: results from the Einstein Aging Study. Neuropsychology 2006; 20: 215–223.
- 50
Holtzer R,
Wang C,
Verghese J. The relationship between attention and gait in aging: facts and fallacies. Motor Control 2012; 16: 64–80.
- 51
Lord S,
Rochester L,
Hetherington V,
Allcock LM,
Burn D. Executive dysfunction and attention contribute to gait interference in “off” state Parkinson's disease. Gait Posture 2010; 31: 169–174.
- 52
Yogev-Seligmann G,
Hausdorff JM,
Giladi N. The role of executive function and attention in gait. Mov Disord 2008; 23: 329–342.
- 53
Rosano C,
Aizenstein H,
Brach J,
Allison L,
Studenski S,
Newman A. Gait measures indicate underlying focal gray matter atrophy in the brain of older adults. J Gerontol Med Sci 2008; 63A: 1380–1388.
- 54
de Laat KF,
Tuladhar AM,
van Norden AG,
Norris DG,
Zwiers MP,
de Leeuw FE. Loss of white matter integrity is associated with gait disorders in cerebral small vessel disease. Brain 2011; 134(pt 1): 73–83.
- 55
Rochester L,
Yarnall AJ,
Baker MR, et al. Cholinergic dysfunction contributes to gait disturbance in early Parkinson's disease. Brain 2012; 135: 2779–2788.
- 56
Lord S,
Galna B,
Coleman S,
Burn D,
Rochester L. Mild depressive symptoms are associated with gait impairment in early Parkinson's disease [published online ahead of print 6 February 2013]. Mov Disord 2013.
- 57
Verghese J,
Holtzer R,
Lipton R,
Wang C. Quantitative gait markers and incident fall risk in older adults. J Gerontol A Bio Sci Med Sci 2009; 64A: 896–901.
- 58
Verghese J,
Robbins T,
Holtzer R, et al. Gait dysfunction in mild cognitive impairment syndromes. J Am Geriatr Soc 2008; 56: 1244–1251.
- 59
Hollman J,
McDade E,
Peterson R. Normative spatiotemporal gait parameters in older adults. Gait Posture 2011; 34: 111–118.
- 60
Cavanaugh JT,
Kochi N,
Stergiou N. Nonlinear analysis of ambulatory activity patterns in community-dwelling older adults. J Gerontol A Biol Sci Med Sci 2010; 65: 197–203.
- 61
Dalton A,
Khalil H,
Busse M,
Rosser A,
van Deursen R,
Olaighin G. Analysis of gait and balance through a single triaxial accelerometer in presymptomatic and symptomatic Huntington's disease. Gait Posture 2013; 37: 49–54.
- 62
Lord S,
Chastin SF,
McInnes L,
Little L,
Briggs P,
Rochester L. Exploring patterns of daily physical and sedentary behaviour in community-dwelling older adults. Age Ageing 2011; 40: 205–210.
- 63
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.
- 64
Weiss A,
Brozgol M,
Dorfman M, et al. Does the evaluation of gait quality during daily-life provide insight into fall risk? A novel approach using 3 day accelerometer recordings. Neurorehabil Neural Repair In press.
- 65
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.
- 66
Pierrynowski MR,
Gross A,
Miles M,
Galea V,
McLaughlin L,
McPhee C. Reliability of the long-range power-law correlations obtained from the bilateral stride intervals in asymptomatic volunteers whilst treadmill walking. Gait Posture 2005; 22: 46–50.
- 67
van Schooten KS,
Rispens SM,
Pijnappels M,
Daffertshofer A,
van Dieen JH. Assessing gait stability: the influence of state space reconstruction on inter- and intra-day reliability of local dynamic stability during over-ground walking. J Biomech 2013; 46: 137–141.
- 68
Lord S,
Galna B,
Khoo T, et al. Gait is associated with decline in attention at 18 months in an incident cohort of Parkinson's disease. Paper for presentation at: 17th International Congress of Parkinson's Disease and Movement Disorders; June 16–20, 2013; Sydney, Australia.
- 69
Chastin SF,
Granat MH. Methods for objective measure, quantification and analysis of sedentary behaviour and inactivity. Gait Posture 2010; 31: 82–86.
