Gait asymmetry and symptom laterality in Parkinson's disease: two of a kind?
Asymmetry
Gait
Lateralization
Parkinson’s disease
Turning
Journal
Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161
Informations de publication
Date de publication:
23 Apr 2024
23 Apr 2024
Historique:
received:
15
03
2024
accepted:
08
04
2024
revised:
07
04
2024
medline:
23
4
2024
pubmed:
23
4
2024
entrez:
23
4
2024
Statut:
aheadofprint
Résumé
The laterality of motor symptoms is considered a key feature of Parkinson's disease (PD). Here, we investigated whether gait and turning asymmetry coincided with symptom laterality as determined by the MDS-UPRDS part III and whether it was increased compared to healthy controls (HC). We analyzed the asymmetry of gait and turning with and without a cognitive dual task (DT) using motion capture systems and wearable sensors in 97 PD patients mostly from Hoehn & Yahr stage II and III and 36 age-matched HC. We also assessed motor symptom asymmetry using the bilateral sub-items of the MDS-UPDRS-III. Finally, we examined the strength of the association between gait asymmetry and symptom laterality. Participants with PD had increased gait but not more turning asymmetry compared to HC (p < 0.05). Only 53.7% of patients had a shorter step length on the more affected body side as determined by the MDS-UPDRS-III. Also, 54% took more time and 29% more steps during turns toward the more affected side. The degree of asymmetry in the different domains did not correlate with each other and was not influenced by DT-load. We found a striking mismatch between the side and the degree of asymmetry in different motor domains, i.e., in gait, turning, and distal symptom severity in individuals with PD. We speculate that motor execution in different body parts relies on different neural control mechanisms. Our findings warrant further investigation to understand the complexity of gait asymmetry in PD.
Sections du résumé
BACKGROUND
BACKGROUND
The laterality of motor symptoms is considered a key feature of Parkinson's disease (PD). Here, we investigated whether gait and turning asymmetry coincided with symptom laterality as determined by the MDS-UPRDS part III and whether it was increased compared to healthy controls (HC).
METHODS
METHODS
We analyzed the asymmetry of gait and turning with and without a cognitive dual task (DT) using motion capture systems and wearable sensors in 97 PD patients mostly from Hoehn & Yahr stage II and III and 36 age-matched HC. We also assessed motor symptom asymmetry using the bilateral sub-items of the MDS-UPDRS-III. Finally, we examined the strength of the association between gait asymmetry and symptom laterality.
RESULTS
RESULTS
Participants with PD had increased gait but not more turning asymmetry compared to HC (p < 0.05). Only 53.7% of patients had a shorter step length on the more affected body side as determined by the MDS-UPDRS-III. Also, 54% took more time and 29% more steps during turns toward the more affected side. The degree of asymmetry in the different domains did not correlate with each other and was not influenced by DT-load.
CONCLUSIONS
CONCLUSIONS
We found a striking mismatch between the side and the degree of asymmetry in different motor domains, i.e., in gait, turning, and distal symptom severity in individuals with PD. We speculate that motor execution in different body parts relies on different neural control mechanisms. Our findings warrant further investigation to understand the complexity of gait asymmetry in PD.
Identifiants
pubmed: 38652262
doi: 10.1007/s00415-024-12379-0
pii: 10.1007/s00415-024-12379-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Bohnen NI, Kanel P, van Emde BM, Roytman S, Kerber KA (2022) Vestibular sensory conflict during postural control, freezing of gait, and falls in Parkinson’s disease. Mov Disord 37:2257–2262
doi: 10.1002/mds.29189
pubmed: 36373942
pmcid: 9673158
Booth T, Nathan M, Waldman A, Quigley A-M, Schapira A, Buscombe J (2015) The role of functional dopamine-transporter SPECT imaging in parkinsonian syndromes, part 1. Am J Neuroradiol 36:229–235
doi: 10.3174/ajnr.A3970
pubmed: 24904053
pmcid: 7965655
Conradsson D, Paquette C, Franzen E (2018) Turning stability in individuals with parkinson disease. J Neurol Phys Ther 42:241–247
doi: 10.1097/NPT.0000000000000242
pubmed: 30138233
Courtine G, Schieppati M (2003) Human walking along a curved path. II. Gait features and EMG patterns. Eur J Neurosci 18:191–205
doi: 10.1046/j.1460-9568.2003.02737.x
pubmed: 12859352
Del Din S, Godfrey A, Galna B, Lord S, Rochester L (2016) Free-living gait characteristics in ageing and Parkinson’s disease: impact of environment and ambulatory bout length. J Neuroeng Rehabil 13:1–12
Djaldetti R, Ziv I, Melamed E (2006) The mystery of motor asymmetry in Parkinson’s disease. Lancet Neurol 5:796–802
doi: 10.1016/S1474-4422(06)70549-X
pubmed: 16914408
Fasano A, Schlenstedt C, Herzog J, Plotnik M, Rose FEM, Volkmann J, Deuschl G (2016) Split-belt locomotion in Parkinson’s disease links asymmetry, dyscoordination and sequence effect. Gait Posture 48:6–12
doi: 10.1016/j.gaitpost.2016.04.020
pubmed: 27477701
Fietzek UM, Stuhlinger L, Plate A, Ceballos-Baumann A, Botzel K (2017) Spatial constraints evoke increased number of steps during turning in Parkinson’s disease. Clin Neurophysiol 128:1954–1960
doi: 10.1016/j.clinph.2017.07.399
pubmed: 28829978
Fling BW, Curtze C, Horak FB (2018) Gait asymmetry in People With Parkinson’s Disease is linked to reduced integrity of callosal sensorimotor regions. Front Neurol 9:215
doi: 10.3389/fneur.2018.00215
pubmed: 29670573
pmcid: 5893803
Frazzitta G, Pezzoli G, Bertotti G, Maestri R (2013) Asymmetry and freezing of gait in parkinsonian patients. J Neurol 260:71–76
doi: 10.1007/s00415-012-6585-4
pubmed: 22752088
Hicheur H, Vieilledent S, Berthoz A (2005) Head motion in humans alternating between straight and curved walking path: combination of stabilizing and anticipatory orienting mechanisms. Neurosci Lett 383:87–92
doi: 10.1016/j.neulet.2005.03.046
pubmed: 15936517
Hulbert S, Ashburn A, Robert L, Verheyden G (2015) A narrative review of turning deficits in people with Parkinson’s disease. Disabil Rehabil 37:1382–1389
doi: 10.3109/09638288.2014.961661
pubmed: 25255298
Hulzinga F, Seuthe J, D’Cruz N, Ginis P, Nieuwboer A, Schlenstedt C (2022) Split-belt treadmill training to improve gait adaptation in Parkinson’s disease. Mov Disord 38(1):92–103
doi: 10.1002/mds.29238
pubmed: 36239376
Janeh O, Fründt O, Schönwald B, Gulberti A, Buhmann C, Gerloff C, Steinicke F, Pötter-Nerger M (2019) Gait training in virtual reality: short-term effects of different virtual manipulation techniques in Parkinson’s disease. Cells 8:419
doi: 10.3390/cells8050419
pubmed: 31064145
pmcid: 6562780
Kennedy PM, Cressman EK, Carlsen AN, Chua R (2005) Assessing vestibular contributions during changes in gait trajectory. NeuroReport 16:1097–1100
doi: 10.1097/00001756-200507130-00013
pubmed: 15973155
Lee M, Youm C, Noh B, Park H, Cheon S-M (2020) Gait characteristics under imposed challenge speed conditions in patients with Parkinson’s disease during overground walking. Sensors 20:2132
doi: 10.3390/s20072132
pubmed: 32290054
pmcid: 7181203
Maidan I, Bernad-Elazari H, Giladi N, Hausdorff JM, Mirelman A (2017) When is higher level cognitive control needed for locomotor tasks among patients with Parkinson’s disease? Brain Topogr 30:531–538
doi: 10.1007/s10548-017-0564-0
pubmed: 28439757
Marinus J, van Hilten JJ (2015) The significance of motor (a) symmetry in Parkinson’s disease. Mov Disord 30:379–385
doi: 10.1002/mds.26107
pubmed: 25546239
Miller-Patterson C, Buesa R, McLaughlin N, Jones R, Akbar U, Friedman JH (2018) Motor asymmetry over time in Parkinson’s disease. J Neurol Sci 393:14–17
doi: 10.1016/j.jns.2018.08.001
pubmed: 30096567
Noh B, Youm C, Lee M, Cheon S-M (2020) Gait characteristics in individuals with Parkinson’s disease during 1-minute treadmill walking. PeerJ 8:e9463
doi: 10.7717/peerj.9463
pubmed: 32655998
pmcid: 7331622
Park H, Youm C, Lee M, Noh B, Cheon S-M (2020) Turning characteristics of the more-affected side in Parkinson’s disease patients with freezing of gait. Sensors 20:3098
doi: 10.3390/s20113098
pubmed: 32486303
pmcid: 7309092
Patla AE, Adkin A, Ballard T (1999) Online steering: coordination and control of body center of mass, head and body reorientation. Exp Brain Res 129:629–634
doi: 10.1007/s002210050932
pubmed: 10638436
Pillai L, Glover A, Virmani T (2022) A study of turn bias in people with idiopathic Parkinson’s disease. Exp Brain Res 240:1673–1685
doi: 10.1007/s00221-022-06378-8
pubmed: 35551430
pmcid: 9205174
Plotnik M, Arad E, Grinberg A, Salomon M, Bahat Y, Hassin-Baer S, Zeilig G (2023) Differential gait adaptation patterns in Parkinson’s disease–a split belt treadmill pilot study. BMC Neurol 23:279
doi: 10.1186/s12883-023-03321-4
pubmed: 37495943
pmcid: 10369736
Plotnik M, Giladi N, Balash Y, Peretz C, Hausdorff JM (2005) Is freezing of gait in Parkinson’s disease related to asymmetric motor function? Ann Neurol 57:656–663
doi: 10.1002/ana.20452
pubmed: 15852404
Roemmich RT, Hack N, Akbar U, Hass CJ (2014) Effects of dopaminergic therapy on locomotor adaptation and adaptive learning in persons with Parkinson’s disease. Behav Brain Res 268:31–39
doi: 10.1016/j.bbr.2014.03.041
pubmed: 24698798
pmcid: 4034129
Roemmich RT, Nocera JR, Stegemoller EL, Hassan A, Okun MS, Hass CJ (2014) Locomotor adaptation and locomotor adaptive learning in Parkinson’s disease and normal aging. Clin Neurophysiol 125:313–319
doi: 10.1016/j.clinph.2013.07.003
pubmed: 23916406
RStudio Team (2018) RStudio: Integrated Development for R. In: RStudio, Inc.
Sadeghi H, Allard P, Prince F, Labelle H (2000) Symmetry and limb dominance in able-bodied gait: a review. Gait Posture 12:34–45
doi: 10.1016/S0966-6362(00)00070-9
pubmed: 10996295
Sasikumar S, Sorrento G, Lang AE, Strafella AP, Fasano A (2023) Cognition affects gait adaptation after split-belt treadmill training in Parkinson’s disease. Neurobiol Dis 181:106109
doi: 10.1016/j.nbd.2023.106109
pubmed: 37019221
Seuthe J, D’Cruz N, Ginis P, Becktepe JS, Weisser B, Nieuwboer A, Schlenstedt C (2020) The effect of one session split-belt treadmill training on gait adaptation in people with Parkinson’s disease and freezing of gait. Neurorehabil Neural Repair 34:954–963
doi: 10.1177/1545968320953144
pubmed: 32940131
Spildooren J, Vercruysse S, Meyns P, Vandenbossche J, Heremans E, Desloovere K, Vandenberghe W, Nieuwboer A (2012) Turning and unilateral cueing in Parkinson’s disease patients with and without freezing of gait. Neuroscience 207:298–306
doi: 10.1016/j.neuroscience.2012.01.024
pubmed: 22285883
Stack E, Ashburn A (2008) Dysfunctional turning in Parkinson’s disease. Disabil Rehabil 30:1222–1229
doi: 10.1080/09638280701829938
pubmed: 18608364
van der Hoorn A, Burger H, Leenders KL, de Jong BM (2012) Handedness correlates with the dominant Parkinson side: a systematic review and meta-analysis. Mov Disord 27:206–210
doi: 10.1002/mds.24007
pubmed: 21994149
Viteckova S, Kutilek P, Svoboda Z, Krupicka R, Kauler J, Szabo Z (2018) Gait symmetry measures: a review of current and prospective methods. Biomed Signal Process Control 42:89–100
doi: 10.1016/j.bspc.2018.01.013
Yogev G, Plotnik M, Peretz C, Giladi N, Hausdorff JM (2007) Gait asymmetry in patients with Parkinson’s disease and elderly fallers: when does the bilateral coordination of gait require attention? Exp Brain Res 177:336–346
doi: 10.1007/s00221-006-0676-3
pubmed: 16972073