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Gait characteristics, balance performance and falls in ambulant adults with cerebral palsy an observational study

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Accepted Manuscript Title: Gait characteristics, balance performance and falls in ambulant adults with cerebral palsy: An observational study Author: P Morgan A Murphy A Opheim J McGinley PII: DOI: Reference: S0966-6362(16)30094-7 http://dx.doi.org/doi:10.1016/j.gaitpost.2016.06.015 GAIPOS 4802 To appear in: Gait & Posture Received date: Revised date: Accepted date: 21-12-2015 7-4-2016 11-6-2016 Please cite this article as: Morgan P, Murphy A, Opheim A, McGinley J.Gait characteristics, balance performance and falls in ambulant adults with cerebral palsy: An observational study.Gait and Posture http://dx.doi.org/10.1016/j.gaitpost.2016.06.015 This is a PDF file of an unedited manuscript that has been accepted for publication As a service to our customers we are providing this early version of the manuscript The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain Gait characteristics, balance performance and falls in ambulant adults with cerebral palsy: an observational study Morgan Pa, Murphy Ab, Opheim Ac,d, McGinley Je a Department of Physiotherapy, Monash University, Australia prue.morgan@monash.edu b Clinical Research Centre for Movement Disorders & Gait, Monash Health, Australia annat.murphy@monashhealth.org c Sunnaas Rehabilitation Hospital, Nesoddtangen, Norway, d University of Gothenburg, Institution of Neuroscience and Physiology, Rehabilitation Medicine, Gothenburg, Sweden arve.opheim@sunnaas.no e Physiotherapy, Melbourne School of Health Sciences, University of Melbourne, Australia mcginley@unimelb.edu.au Corresponding author: Dr Prue Morgan Physiotherapy Department School of Primary Health Care Faculty of Medicine, Nursing and Health Science Monash University PO Box 527 Frankston Vic 3199 Australia Prue.morgan@monash.edu Phone: 61 9904 4826 Highlights  Adults with CP demonstrate slow gait speeds and short stride length  Adults with CP demonstrate relatively high cadence to optimise gait speed  Those with a falls history took shorter strides at preferred and fast speeds  Faster gait speed was associated with better performance on BESTest total Gait characteristics, balance performance and falls in ambulant adults with cerebral palsy: an observational study The relationship between spatiotemporal gait parameters, balance performance and falls history was investigated in ambulant adults with cerebral palsy (CP) Participants completed a single assessment of gait using an instrumented walkway at preferred and fast speeds, balance testing (Balance Evaluation Systems Test; BESTest), and reported falls history Seventeen ambulatory adults with CP, mean age 37 years, participated Gait speed was typically slow at both preferred and fast speeds (mean 0.97 and 1.21 m/sec, respectively), with short stride length and high cadence relative to speed There was a significant, large positive relationship between preferred gait speed and BESTest total score (rho=0.573; p Relationship between gait and balance variables Relationships between gait variables and balance, as assessed by BESTest were explored (Table 2) A significant large positive relationship between fast gait speed and BESTest total score was evident (rho=0.647; p100 steps/min)[23] , but stride length was considerably shorter, with a mean of 0.7 m at preferred speed in comparison to normative values of >1.2 m [23] A selected gait pattern at any preferred speed typically reflects strategies to optimise energy expenditure, balance, between-step variability, and attentional demand [26] Higher than anticipated cadence and shorter stride lengths at low gait speeds have previously been described in hemiparetic patients following stroke [27] and in those with Parkinsons’ disease [28] It is possible that the relatively higher cadence proportional to stride length is a strategy to accommodate spasticity and/or contracture-induced restrictions in stride length in ambulant adults with CP, whilst concurrently keeping walking speed acceptable Greater cadence is achieved through a range of biomechanical work production strategies, potentially resulting in higher energy expenditure to achieve selected speed Increasing fatigue has been reported as a consequence of ageing with CP [29] Effortful gait strategies may contribute to experienced fatigue Considerable individual variation in muscle activation strategies to modulate gait speed has been described in patients with stroke [27], and in a cohort of ambulant adults with CP [15] This warrants further exploration in this population This study demonstrated a positive correlation between balance as measured by the BESTest total and gait speed Although a strong relationship between gait speed and balance measures in the general population has not consistently been demonstrated [30], this relationship is more evident in those with acquired neurological dysfunction such as Parkinson’s disease and stroke [9, 31] In the current study, those with better balance performance typically walked faster at preferred speeds, with shorter double support time, reinforcing the notion of enhanced motor control and dynamic balance being integral elements of gait The mean double support time as percentage of the gait cycle, which if increased has been shown to be indicative of poorer balance ability, was in this study 31%, much higher than 22-25% reported in an older adult population [32] This is probably indicative of the generally poorer balance in this group It was interesting that no significant correlations were identified between stride length and BESTest scores In older adults, gait becomes slower and strides shorten with ageing [21]; both are thought to improve stability against balance challenges For those ageing with CP, there may be limited adaptability in impairments contributing to their gait pattern to accommodate balance decline Of particular interest were significant relationships between gait speed and anticipatory postural adjustments (III), reactive postural responses (IV), and stability in gait (VI) components of the BESTest in this study Whereas the strong association between stability in gait (VI) and gait speed was not surprising as this component includes measures of speed-sensitive gait performance, the strong relationship between gait speed and anticipatory and reactive postural responses confirms construct validity of the BESTest in this population Opheim and colleagues [14] previously found anticipatory (III) and reactive (IV) postural responses to score lowest from the BESTest in a group of adults with spastic bilateral CP These findings may suggest that anticipatory and reactive postural responses are more sensitive measures of balance than other BESTest components in this population, and a potential target for therapeutic intervention to improve balance [16] Nine of seventeen participants reported one or more falls in the past twelve months, in line with previous reports of frequent falls in this population [13] In this study, fallers took shorter strides at both preferred and fast gait speeds than non-fallers, possibly reflective of more impaired lower limb function Reduced stride length has been proposed as a strategy to reduce trip risk in older adults [33) Importantly, reduced stride length per se has not consistently been demonstrated to independently relate to falls frequency in older adults [34] The link between shorter stride length and falls may reflect longstanding physical features in lower limbs of adults with CP such as spasticity, contractures, and altered skeletal alignment, making them more vulnerable to balance disturbances and foot clearance errors, for example Of note, there was a trend towards greater step length variability in the shorter step at faster gait speeds in those with falls history (p=0.061), supporting the notion of increased demand on an impaired motor output with increasing speed generation There was also a trend towards lower performance on BESTest components I and VI in those who have fallen in this study The significance of stride length outcome, step length variability and BESTest performance require further investigation to assist in prospective identification of falls risk in this population There was a trend towards slower gait speeds in fallers in this study In older adults, slower gait speed has been associated with an increased risk of falls [2] However in the stroke population, a ‘U’ shaped curve has been proposed suggesting that those who walk at preferred speeds either very slowly (1.3m/second) are at greater risk of falls [5] Given overall low preferred gait speeds, and few persons walking at fast speeds evident in ambulant adults with CP, further investigation of this relationship could be warranted There were several limitations associated with this study Firstly, this study attracted a small convenience sample of adults with CP who likely had prior concern regarding mobility and/or falls Further, 12 month falls history was obtained using recall rather than prospective falls diary methodology However, we would suggest that under-reporting is prevalent in both methodologies, and dichotomising of data into fall/no fall simplified falls recall process Limited significant findings were returned regarding measures of gait variability and BESTest, and gait variability and falls history, possibly impacted by large standard deviations in some measures Despite these limitations, this study has provided useful baseline information to inform future investigation into predictive value of gait speed, stride length, step length variability and BESTest on falls risk identification in this population In conclusion, this study examined the relationship between gait variables, balance performance and falls history Ambulant adults with CP typically demonstrated slow gait speeds, short stride length likely predetermined by characteristics of lifelong neuromuscular dysfunction, and relatively high cadence to optimise gait speed Those with prior history of falls took shorter strides at both preferred and fast gait speed Faster gait speed was associated with better performance on BESTest total and anticipatory and postural responses components, suggesting both better gross motor function in those walking faster, and potential therapeutic training targets either focused on optimising balance responses or enhancing gait speed Future exploration of implications of low walking speed and reduced stride length on falls and community engagement, and predictive value of stride length for falls risk identification is recommended Acknowledgement This study was supported by a 2013 Lions John Cockayne Memorial Fellowship Trust Fund Conflict of Interest Statement The authors report no conflict of interest References [1] Studenski S, Perera S, Wallace D, Chandler JM, Duncan PW, Rooney E, et al Physical Performance Measures in the Clinical Setting J Am Geriatr Soc 2003;51(3):314-22 [2] Verghese J, Holtzer R, Lipton RB, Wang C Quantitative Gait Markers and Incident Fall Risk in Older Adults J Gerontol Series A: Biol Sci Med Sci 2009;64A(8):896-901 [3] Cesari M, Kritchevsky SB, Penninx BW, Nicklas BJ, Simonsick EM, Newman AB, et al Prognostic value of usual gait speed in well-functioning older people results from the Health, Aging and Body Composition Study J Am Geriatr Soc 2005;53(10):1675-80 Epub 2005/09/27 [4] Brach JS, Berthold R, Craik R, VanSwearingen JM, Newman AB Gait variability in community- dwelling older adults J Am Geriatr Soc 2001;49(12):1646-50 Epub 2002/02/15 [5] Quach L, Galica AM, Jones RN, Procter-Gray E, Manor B, Hannan MT, et al The Non-linear Relationship between Gait Speed and Falls: The MOBILIZE Boston Study J Am Geriatr Soc 2011;59(6):1069-73 [6] Hausdorff J Gait variability: methods, modeling and meaning J NeuroEng Rehabil 2005;2:19 [7] Callisaya J, Blizzard L, Schmidt M, Martin K, McGinley J, Sanders L, et al Gait, gait variability and the risk of multiple incident falls in older people: a population-based study Age Ageing 2011; 40:481-487 [8] Brach J, Berlin J, VanSwearingen J, Newman A, Studenski S Too much or too little step width variability is associated with a fall history in older persons who walk at or normal gait speed J NeuroEng Rehabil 2005; 2:21 [9] Yang Y-R, Lee Y-Y, Cheng S-J, Lin P-Y, Wang R-Y Relationships between gait and dynamic balance in early Parkinson's disease Gait & Posture 2008;27(4):611-5 [10] Hausdorff J Gait dynamics, fractals and falls: Finding meaning in the stride-to-stride fluctuations of human walking Human Mov Sci 2007; 555–589 [11] Milne SC, Hocking DR, Georgiou-Karistianis N, Murphy A, Delatycki MB, Corben LA Sensitivity of spatiotemporal gait parameters in measuring disease severity in Friedreich ataxia Cerebellum (London, England) 2014;13(6):677-88 Epub 2014/07/16 [12] Socie M, Sosnoff J Gait variability and multiple sclerosis Multiple Sclerosis International 2013 http://dx.doi.org/10.1155/2013/645197 [13] Morgan P, McGinley J Performance of adults with cerebral palsy related to falls, balance and function: a preliminary report Dev Neurorehabil 2013;16(2):113-20 Epub 2013/03/13 [14] Opheim A, Jahnsen R, Olsson E, Stanghelle JK Balance in Relation to Walking Deterioration in Adults With Spastic Bilateral Cerebral Palsy Phys Ther 2012;92(2):279-88 [15] Opheim A, McGinley JL, Olsson E, Stanghelle JK, Jahnsen R Walking deterioration and gait analysis in adults with spastic bilateral cerebral palsy Gait & Posture 2013;37(2):165-71 [16] Morgan P, Murphy A, Opheim A, Pogrebnoy D, Kravtsov S, McGinley J The safety and feasibility of an intervention to improve balance dysfunction in ambulant adults with cerebral palsy: A pilot randomized controlled trial Clin Rehabil 2014 Epub 2014/11/22 [17] SCPE Collaborative Group Surveillance of cerebral palsy in Europe: a collaboration of cerebral palsy surveys and registers Surveillance of Cerebral Palsy in Europe (SCPE) Devl Med Child Neurol 2000;42(12):816-24 Epub 2000/12/29 [18] Palisano R, Rosenbaum P, Bartlett D, Livingston M Gross motor function classification system - Expanded and Revised 2007 Hamilton, Canada: CanChild Centre for Childhood Disability Research Retrieved from http://motorgrowth.canchild.ca/en/GMFCS/resources/GMFCS-ER.pdf [19] Menz HB, Latt MD, Tiedemann A, Mun San Kwan M, Lord SR Reliability of the GAITRite® walkway system for the quantification of temporo-spatial parameters of gait in young and older people Gait & Posture 2004;20(1):20-5 [20] Kuys SS, Brauer SG, Ada L Test-retest reliability of the GAITRite system in people with stroke undergoing rehabilitation Disabil Rehabil 2011;33(19-20):1848-53 [21] Horak FB, Wrisley DM, Frank J The Balance Evaluation Systems Test (BESTest) to Differentiate Balance Deficits Phys Ther 2009;89(5):484-98 [22] Cohen J Statistic power analysis for the behavioural sciences 2nd ed Hillsdale, NJ: Lawrence Erlbaum Associates; 1988 [23] Oberg T, Karsznia A, Oberg K Basic gait parameters: reference data for normal subjects, 10- 79 years of age J Rehabil Res Dev 1993;30(2):210-23 Epub 1993/01/01 [24] Taylor NF, Dodd KJ, Baker RJ, Willoughby K, Thomason P, Graham HK Progressive resistance training and mobility-related function in young people with cerebral palsy: a randomized controlled trial Dev Med Child Neurol 2013;55(9):806-12 Epub 2013/06/25 [25] Salbach NM, O'Brien K, Brooks D, Irvin E, Martino R, Takhar P, et al Speed and distance requirements for community ambulation: a systematic review Arch Phys Med Rehabil 2014;95(1):117-28 e11 Epub 2013/07/04 [26] Kuo AD, Donelan JM Dynamic Principles of Gait and Their Clinical Implications Phys Ther 2010;90(2):157-74 [27] Jonsdottir J, Recalcati M, Rabuffetti M, Casiraghi A, Boccardi S, Ferrarin M Functional resources to increase gait speed in people with stroke: Strategies adopted compared to healthy controls Gait & Posture 2009;29(3):355-9 [28] Morris M, Iansek R, McGinley J, Matyas T, Huxham F Three-dimensional gait biomechanics in Parkinson's disease: Evidence for a centrally mediated amplitude regulation disorder Mov Disord 2005;20(1):40-50 [29] Jahnsen R, Villien L, Stanghelle JK, Holm I Fatigue in adults with cerebral palsy in Norway compared with the general population Dev Med Child Neurol 2003;45(05):296-303 [30] Ringsberg K, Gerdhem P, Johansson J, Obrant KJ Is there a relationship between balance, gait performance and muscular strength in 75-year-old women? Age Ageing 1999;28(3):289-93 [31] Patterson SL, Forrester LW, Rodgers MM, Ryan AS, Ivey FM, Sorkin JD, et al Determinants of walking function after stroke: differences by deficit severity Arch Phys Med Rehabil 2007;88(1):1159 Epub 2007/01/09 [32] Callisaya ML, Blizzard L, Schmidt MD, McGinley JL, Srikanth VK Ageing and gait variability—a population-based study of older people Age Ageing 2010;39(2):191-7 [33] Espy DD, Yang F, Bhatt T, Pai YC Independent influence of gait speed and step length on stability and fall risk Gait & Posture 2010;32(3):378-82 [34] Thaler-Kall K, Peters A, Thorand B, Grill E, Autenrieth CS, Horsch A, et al Description of spatio-temporal gait parameters in elderly people and their association with history of falls: results of the population-based cross-sectional KORA-Age study BMC Geriatrics 2015;15:32 Epub 2015/04/17 Figure 1: Scatter-plot of participants’ preferred gait speed (X-axis) vs fast gait speed (Y-axis) The solid line indicates no change between preferred and fast gait speeds The dashed lines indicate a threshold walking speed of 1.0 m/second [3] Fast gait speed m/sec Preferred gait speed m/sec Table 1: Gait characteristics at preferred and fast speed Preferred gait speed Fast gait speed (n=17) (n-16)* Mean (SD) range Mean (SD) range Gait speed (m/sec) 0.97 (0.26) 0.45-1.48 1.21 (0.37) 0.44-1.93 Stride length (m) 0.69 (0.28) 0.35-1.38 0.77 (0.33) 0.39-1.47 Step length – longer step (m) 0.59 (0.14) 0.32-0.83 0.63 (0.15) 0.36-0.97 Step length – shorter step (m) 0.54 (0.14) 0.33-0.80 0.59 (0.15) 0.35-0.93 Step width (m) 0.14 (0.07) 0.02-0.29 0.14 (0.06) 0.02-0.28 Cadence (steps/min) 102.8 (21.2) 47-140 117.5 (27.3) 47-168 Double support time (% of 31.4 (8.0) 21.5-46.1 28.4 (9.4) 17.3-52.0 0.01-0.07 0.03 (0.02) 0.01-0.08 0.03 (0.01) 0.01-0.05 0.03 (0.01) 0.01-0.06 Step width variability (m) 0.02 (0.01) 0.01-0.04 0.02 (0.01) 0.01-0.03 Double support time 3.2 (2.1) 1.5 – 10.9 2.9 (2.0) 1.2 – 9.1 gait cycle) Step length variability – longer 0.03 (0.02) step (m) Step length variability – shorter step (m) variability (% of gait cycle) *data from one participant unavailable Table 2: Correlations between gait parameters and BESTest scores Gait speed (m/sec) Stride length (m) Step width (m) Cadence Double support time Double support time Speed (steps/min) (% gait cycle) variability increase Pref Fast Pref Fast Pref Fast Pref Fast Pref Fast Pref Fast (m/sec) BESTest n=17 n=16 n=17 n=16 n=17 n=16 n=17 n=16 n=17 n=16 n=17 n=16 n=16 Total 0.573* 0.647** 0.255 0.269 -0.081 -0.021 0.275 0.485 -0.608** -0.671** -0.474 -0.495 0.776** I biomechanical constraints 0.528* 0.561* 0.322 0.348 0.052 0.057 0.307 0.491 -0.646** -0.712** -0.620** -0.514* 0.671** II stability limits/verticality 0.297 0.404 0.014 -0.041 -0.171 0.050 0.314 0.449 -0.425 -0.388 -0.383 -0.345 0.588* III anticipatory postural adjustments 0.648** 0.735** 0.440 0.426 -0.088 0.040 0.238 0.456 -0.670** -0.683** -0.423 -0.503* 0.822** IV postural responses 0.611** 0.638** 0.258 0.290 -0.066 -0.026 0.217 0.406 -0.622** -0.709** -0.398 -0.445 0.628** V sensory orientation 0.245 0.368 0.027 0.020 -0.001 -0.077 0.246 0.286 -0.323 -0.469 -0.459 -0.455 0.576* VI stability in gait 0.832** 0.886** 0.255 0.269 -0.143 0.019 0.332 0.485 -0.822** -0.788** -0.444 -0.511* 0.845** *Correlation is significant at the 0.05 level; **correlation is significant at the 0.01 level Table 3: The relationship between balance, gait variables and past year falls history No falls ≥1 fall N=8 N= Mean (SD) Mean (SD) Level I n=2 n=0 Level II n=5 n=5 Level III n=1 n=4 BESTest total, %, mean (SD) 57.9 (29.6) 46.9 (15.3) 0.343 I biomechanical constraints 59.2 (27.0) 43.7 (18.9) 0.187 II stability limits/verticality 73.2 (19.2) 73.5 (17.0) 0.970 III anticipatory postural adjustments 50.7 (30.8) 37.0 (12.7) 0.240 IV postural responses 48.6 (41.0) 26.5 (29.4) 0.218 V sensory orientation 57.5 (36.5) 60.0 (27.9) 0.875 VI stability in gait 58.3 (33.5) 40.7 (14.3) 0.171 Preferred 1.08 (0.26) 0.89 (0.21) 0.114 Fast 1.36 (0.41) 1.10 (0.31) 0.154 Preferred 0.14 (0.05) 0.13 (0.08) 0.745 Fast 0.15 (0.04) 0.13 (0.08) 0.565 Preferred 0.85 (0.34) 0.56 (0.13) 0.032* Fast 0.97 (0.39) 0.61 (0.16) 0.025* Preferred 98.3 (11.2) 106.7 (27.5) 0.429 Fast 113.8 (18.2) 120.4 (33.6) 0.648 Double support time Preferred 28.8 (7.5) 34.0 (7.8) 0.150 (% of gait cycle) Fast 25.1 (7.8) 31.0 (10.1) 0.221 0.28 (0.15) 0.21 (0.11) 0.267 GMFCS E&R Level Gait speed (m/sec) Step width (m) Stride length (m) Cadence (steps/min) Speed increase (m/sec) p-value NT 24 Step length variability – longer step Preferred 0.02 (0.01) 0.03 (0.02) 0.227 (m) Fast 0.02 (0.01) 0.04 (0.02) 0.289 Step length variability – shorter step Preferred 0.03 (0.01) 0.03 (0.01) 0.375 (m) Fast 0.02 (0.01) 0.03 (0.01) 0.061 Step width variability (m) Preferred 0.03 (0.01) 0.02 (0.01) 0.308 Fast 0.02 (0.01) 0.02 (0.01) 0.334 Double support time variability Preferred 2.4 (0.75) 3.9 (2.75) 0.163 (% of gait cycle) Fast 2.1 (1.22) 3.4 (2.29) 0.186 NT = not tested; *significant difference between no falls and falls group, with p

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