Cognitive impairment is associated with gait variability and fall risk in amyotrophic lateral sclerosis.
amyotrophic lateral sclerosis
cognition
falls
gait analysis
wearable sensors
Journal
European journal of neurology
ISSN: 1468-1331
Titre abrégé: Eur J Neurol
Pays: England
ID NLM: 9506311
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
revised:
08
06
2023
received:
05
04
2023
accepted:
13
06
2023
medline:
8
9
2023
pubmed:
19
6
2023
entrez:
19
6
2023
Statut:
ppublish
Résumé
In amyotrophic lateral sclerosis (ALS), gait abnormalities contribute to poor mobility and represent a relevant risk for falls. To date, gait studies in ALS patients have focused on the motor dimension of the disease, underestimating the cognitive aspects. Using a wearable gait analysis device, we compared gait patterns in ambulatory ALS patients with mild cognitive impairment (ALS MCI+; n = 18), and without MCI (ALS MCI-; n = 24), and healthy subjects (HS; n = 16) under two conditions: (1) normal gait (single task) and (2) walking while counting backward (dual task). Finally, we examined if the occurrence and number of falls in the 3 months following the baseline test were related to cognition. In the single task condition, ALS patients, regardless of cognition, displayed higher gait variability than HS, especially for stance and swing time (p < 0.001). The dual task condition revealed additional differences in gait variability parameters between ALS MCI+ and ALS MCI- for cadence (p = 0.005), stance time (p = 0.04), swing time (p = 0.04) and stability index (p = 0.02). Moreover, ALS MCI+ showed a higher occurrence (p = 0.001) and number of falls (p < 0.001) at the follow-up. Regression analyses demonstrated that MCI condition predicted the occurrence of future falls (β = 3.649; p = 0.01) and, together with executive dysfunction, was associated with the number of falls (cognitive impairment: β = 0.63; p < 0.001; executive dysfunction: β = 0.39; p = 0.03), regardless of motor impairment at clinical examination. In ALS, MCI is associated with exaggerated gait variability and predicts the occurrence and number of short-term falls.
Sections du résumé
BACKGROUND
In amyotrophic lateral sclerosis (ALS), gait abnormalities contribute to poor mobility and represent a relevant risk for falls. To date, gait studies in ALS patients have focused on the motor dimension of the disease, underestimating the cognitive aspects.
METHODS
Using a wearable gait analysis device, we compared gait patterns in ambulatory ALS patients with mild cognitive impairment (ALS MCI+; n = 18), and without MCI (ALS MCI-; n = 24), and healthy subjects (HS; n = 16) under two conditions: (1) normal gait (single task) and (2) walking while counting backward (dual task). Finally, we examined if the occurrence and number of falls in the 3 months following the baseline test were related to cognition.
RESULTS
In the single task condition, ALS patients, regardless of cognition, displayed higher gait variability than HS, especially for stance and swing time (p < 0.001). The dual task condition revealed additional differences in gait variability parameters between ALS MCI+ and ALS MCI- for cadence (p = 0.005), stance time (p = 0.04), swing time (p = 0.04) and stability index (p = 0.02). Moreover, ALS MCI+ showed a higher occurrence (p = 0.001) and number of falls (p < 0.001) at the follow-up. Regression analyses demonstrated that MCI condition predicted the occurrence of future falls (β = 3.649; p = 0.01) and, together with executive dysfunction, was associated with the number of falls (cognitive impairment: β = 0.63; p < 0.001; executive dysfunction: β = 0.39; p = 0.03), regardless of motor impairment at clinical examination.
CONCLUSION
In ALS, MCI is associated with exaggerated gait variability and predicts the occurrence and number of short-term falls.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3056-3067Informations de copyright
© 2023 The Authors. European Journal of Neurology published by John Wiley & Sons Ltd on behalf of European Academy of Neurology.
Références
Montero-Odasso M, Verghese J, Beauchet O, Hausdorff JM. Gait and cognition: a complementary approach to understanding brain function and the risk of falling. J Am Geriatr Soc. 2012;60(11):2127-2136.
Morris R, Lord S, Bunce J, Burn D, Rochester L. Gait and cognition: mapping the global and discrete relationships in ageing and neurodegenerative disease. Neurosci Biobehav Rev. 2016;64:326-345.
Bahureksa L, Najafi B, Saleh A, et al. The impact of mild cognitive impairment on gait and balance: a systematic review and meta-analysis of studies using instrumented assessment. Gerontology. 2016;63(1):67-83.
Stolze H, Klebe S, Zechlin C, Baecker C, Friege L, Deuschl G. Falls in frequent neurological diseases: prevalence, risk factors and aetiology. J Neurol. 2004;251(1):79-84.
Gil J, Funalot B, Verschueren A, et al. Causes of death amongst French patients with amyotrophic lateral sclerosis: a prospective study. Eur J Neurol. 2008;15(11):1245-1251.
Goldfarb B, Simon S. Gait patterns in patients with amyotrophic lateral sclerosis. Arch Phys Med Rehabil. 1984;65(2):61-65.
Schell WE, Mar VS, Da Silva CP. Correlation of falls in patients with amyotrophic lateral sclerosis with objective measures of balance, strength, and spasticity. NeuroRehabilitation. 2019;44(1):85-93.
Montes J, Cheng B, Diamond B, Doorish C, Mitsumoto H, Gordon PH. The Timed Up and Go test: predicting falls in ALS. Amyotroph Lateral Scler. 2007;8(5):292-295.
Feron M, Couillandre A, Mseddi E, et al. Extrapyramidal deficits in ALS: a combined biomechanical and neuroimaging study. J Neurol. 2018 Sep;265(9):2125-2136.
Elamin M, Phukan J, Bede P, et al. Executive dysfunction is a negative prognostic indicator in patients with ALS without dementia. Neurology. 2011;76(14):1263-1269.
Elamin M, Bede P, Byrne S, et al. Cognitive changes predict functional decline in ALS: a population-based longitudinal study. Neurology. 2013;80(17):1590-1597.
Olney RK, Murphy J, Forshew D, et al. The effects of executive and behavioral dysfunction on the course of ALS. Neurology. 2005;65(11):1774-1777.
Amboni M, Barone P, Hausdorff JM. Cognitive contributions to gait and falls: evidence and implications. Mov Disord. 2013;28(11):1520-1533.
Segev-Jacubovski O, Herman T, Yogev-Seligmann G, Mirelman A, Giladi N, Hausdorff JM. The interplay between gait, falls and cognition: can cognitive therapy reduce fall risk? Expert Rev Neurother. 2011;11(7):1057-1075.
Sheridan PL, Solomont J, Kowall N, Hausdorff JM. Influence of executive function on locomotor function: divided attention increases gait variability in Alzheimer's disease. J Am Geriatr Soc. 2003;51(11):1633-1637.
Sheridan PL, Hausdorff JM. The role of higher-level cognitive function in gait: executive dysfunction contributes to fall risk in Alzheimer's disease. Dement Geriatr Cogn Disord. 2007;24(2):125-137.
Mirelman A, Herman T, Brozgol M, et al. Executive function and falls in older adults: new findings from a five-year prospective study link fall risk to cognition. PLoS One. 2012;7(6):1-8.
Mak MK, Wong A, Pang MY. Impaired executive function can predict recurrent falls in Parkinson's disease. Arch Phys Med Rehabil. 2014;95(12):2390-2395.
Muir-Hunter SW, Wittwer JE. Dual-task testing to predict falls in community-dwelling older adults: a systematic review. Physiotherapy. 2016;102(1):29-40.
Montero-Odasso MM, Sarquis-Adamson Y, Speechley M, et al. Association of dual-task gait with incident dementia in mild cognitive impairment: results from the Gait and Brain Study. JAMA Neurol. 2017;74(7):857-865.
Springer S, Giladi N, Peretz C, Yogev G, Simon ES, Hausdorff JM. Dual-tasking effects on gait variability: the role of aging, falls, and executive function. Mov Disord. 2006;21(7):950-957.
Pieruccini-Faria F, Black SE, Masellis M, et al. Gait variability across neurodegenerative and cognitive disorders: results from the Canadian Consortium of Neurodegeneration in Aging (CCNA) and the gait and brain study. Alzheimers Dementia. 2021;17(8):1317-1338.
Yogev G, Giladi N, Peretz C, Springer S, Simon ES, Hausdorff JM. Dual tasking, gait rhythmicity, and Parkinson's disease: which aspects of gait are attention demanding? Eur J Neurosci. 2005;22(5):1248-1256.
Radovanović S, Milićev M, Perić S, Basta I, Kostić V, Stević Z. Gait in amyotrophic lateral sclerosis: is gait pattern differently affected in spinal and bulbar onset of the disease during dual task walking? Amyotroph Lateral Scler Frontotemporal Degener. 2014;15(7-8):488-493.
Montero-Odasso M, Muir SW, Speechley M. Dual-task complexity affects gait in people with mild cognitive impairment: the interplay between gait variability, dual tasking, and risk of falls. Arch Phys Med Rehabil. 2012;93(2):293-299.
Hausdorff JM, Lertratanakul A, Cudkowicz ME, et al. Dynamic markers of altered gait rhythm in amyotrophic lateral sclerosis. J Appl Physiol. 2000;88(6):2045-2053.
Brooks BR, Miller RG, Swash M, Munsat TL. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2000;1(5):293-299.
Strong MJ, Abrahams S, Goldstein LH, et al. Amyotrophic lateral sclerosis - frontotemporal spectrum disorder (ALS-FTSD): revised diagnostic criteria. Amyotroph Lateral Scler Frontotemporal Degener. 2017;18(3-4):153-174.
Dyck PJ, Boes CJ, Mulder D, et al. History of standard scoring, notation, and summation of neuromuscular signs. A current survey and recommendation. J Peripher Nerv Syst. 2005;10(2):158-173.
Cedarbaum JM, Stambler N, Malta E, et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS study group (phase III). J Neurol Sci. 1999;169(1-2):13-21.
Quinn C, Edmundson C, Dahodwala N, Elman L. Reliable and efficient scale to assess upper motor neuron disease burden in amyotrophic lateral sclerosis. Muscle Nerve. 2020;61(4):508-511.
Zhou J, Manor B, Yu W, et al. Targeted tDCS mitigates dual-task costs to gait and balance in older adults. Ann Neurol. 2021;90(3):428-439.
Kahya M, Gouskova NA, Lo OY, et al. Brain activity during dual-task standing in older adults. J Neuroeng Rehabil. 2022;19(1):123. doi:10.1186/s12984-022-01095-3
Maidan I, Nieuwhof F, Bernad-Elazari H, et al. Evidence for differential effects of 2 forms of exercise on prefrontal plasticity during walking in Parkinson's disease. Neurorehabil Neural Repair. 2018;32(3):200-208.
Cohen M, Herman T, Ganz N, Badichi I, Gurevich T, Hausdorff JM. Multidisciplinary intensive rehabilitation program for people with Parkinson's disease: gaps between the clinic and real-world mobility. Int J Environ Res Public Health. 2023;20(5):1-12. doi:10.3390/ijerph20053806
Poole VN, Dawe RJ, Lamar M, et al. Dividing attention during the Timed Up and Go enhances associations of several subtask performances with MCI and cognition. PLoS One. 2022;17:e0269398. doi:10.1371/journal.pone.0269398
Park G, Woo Y. Comparison between a center of mass and a foot pressure sensor system for measuring gait parameters in healthy adults. J Phys Ther Sci. 2015;27(10):3199-3202.
De Ridder R, Lebleu J, Willems T, De Blaiser C, Detrembleur C, Roosen P. Concurrent validity of a commercial wireless trunk triaxial accelerometer system for gait analysis. J Sport Rehabil. 2019;28(6):4-7.
Schneider N, Dagan M, Katz R, et al. Combining transcranial direct current stimulation with a motor-cognitive task: the impact on dual-task walking costs in older adults. J Neuroeng Rehabil. 2021;18(1):1-13.
Moretta P, Spisto M, Ausiello FP, et al. Alteration of interoceptive sensitivity: expanding the spectrum of behavioural disorders in amyotrophic lateral sclerosis. Neurol Sci. 2022;43(9):5403-5410.
De Lucia N, Ausiello FP, Spisto M, Manganelli F, Salvatore E, Dubbioso R. The emotional impact of COVID-19 outbreak in amyotrophic lateral sclerosis patients: evaluation of depression, anxiety and interoceptive awareness. Neurol Sci. 2020;41(9):2339-2341.
Folstein M, Folstein S, McHugh P. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189-198.
Abrahams S, Newton J, Niven E, Foley J, Bak TH. Screening for cognition and behaviour changes in ALS. Amyotroph Lateral Scler Frontotemporal Degener. 2014;15:9-14.
Dubois B, Slachevsky A, Litvan I, Pillon B. The FAB: a frontal assessment battery at bedside. Neurology. 2000;55(11):1621-1626.
Carlesimo C, Caltagirone C, Gainotti G. The Mental Deterioration Battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. The Group for the Standardization of the Mental Deterioration Battery. Eur Neurol. 1996;36(6):378-384.
Milner B. Effects of different brain lesions on card sorting the role of the frontal lobes. Arch Neurol. 1963;9(1):90-100.
Barbarotto R, Laiacona M, Frosio R, Vecchio M, Farinato A, Capitani E. A normative study on visual reaction times and two Stroop colour-word tests. Neurol Sci. 1998;19(3):161-170.
Monaco M, Costa A, Caltagirone C, Carlesimo GA. Forward and backward span for verbal and visuo-spatial data: standardization and normative data from an Italian adult population. Neurol Sci. 2013;34(5):749-754.
Mondini S, Mapelli D, Vestri A, Arcara G, Bisiacchi PS. Una batteria di test per lo screening neuropsicologico. In: Esame neuropsicologico breve. Raffaello Cortina Editore; 2003:49-51.
Caffarra P, Vezzadini G, Dieci F, Zonato F, Venneri A. Rey-Osterrieth complex figure: normative values in an Italian population sample. Neurol Sci. 2002;22(6):443-447.
Litvan I, Goldman JG, Tröster AI, et al. Diagnostic criteria for mild cognitive impairment in Parkinson's disease: Movement Disorder Society Task Force guidelines. Mov Disord. 2012;27(3):349-356.
Miller RG, Jackson CE, Kasarskis EJ, et al. Practice parameter update: the care of the patient with amyotrophic lateral sclerosis: drug, nutritional, and respiratory therapies (an evidence-based review): report of the quality standards subcommittee of the American Academy of Neurology. Neurology. 2009;73:1218-1226.
Boulgarides LK, McGinty SM, Willett JA, Barnes CW. Use of clinical and impairment-based tests to predict falls by community-dwelling older adults. Phys Ther. 2003;83(4):328-339.
Muir SW, Speechley M, Wells J, Borrie M, Gopaul K, Montero-Odasso M. Gait assessment in mild cognitive impairment and Alzheimer's disease: the effect of dual-task challenges across the cognitive spectrum. Gait Posture. 2012;35(1):96-100.
Desai J, Swash M. Extrapyramidal involvement in amyotrophic lateral sclerosis: backward falls and retropulsion. J Neurol Neurosurg Psychiatry. 1999;67(2):214-216.