Advertisement

Effects of deep brain stimulation on the kinematics of gait and balance in patients with idiopathic Parkinson's disease

      Highlights

      • Advanced Parkinson's disease is associated with gait alterations and postural instability.
      • Effects of subthalamic nucleus deep brain stimulation on gait and balance remain a matter of debate.
      • We have analysed gait of Parkinson's disease patients with stimulation of the subthalamic nucleus.
      • Subthalamic nucleus deep brain stimulation improved gait and balance in these patients.
      • Our results highlight the major role of the subthalamic nucleus in motor control mechanisms.

      Abstract

      Background

      Advanced stages of idiopathic Parkinson's disease are often characterised by gait alterations and postural instability. Despite improvements in patients' motor symptoms after deep brain stimulation of the subthalamic nucleus, its effects on gait and balance remain a matter of debate. This study investigated the effects of deep brain stimulation on balance and kinematic parameters of gait.

      Methods

      The gait of 26 patients with advanced idiopathic Parkinson's disease was analysed before and after (between 3 and 6 months) after bilateral deep brain stimulation of the subthalamic nucleus. Computerised analysis was used to study cadence, number of cycles with the correct support sequence, number of cycles, duration of the cycle stages, and knee and ankle goniometry. Balance, postural instability, and mobility were assessed using the Tinetti and Timed Up and Go test.

      Findings

      After stimulation, the following changes were significant (p < 0.01): number of cycles with the correct support sequence, number of total cycles, and foot contact. Patients improved significantly (p < 0.01) in the Tinetti and Timed Up and Go tests, the risk factors for falls changed from high (median 17) to low (median 25), and they improved from minor dependence (statistical median 14) to normality (statistical median 8.70).

      Interpretation

      Deep brain stimulation to inhibit hyperactivity of the subthalamic nucleus was associated with an improvement in the space-time variables of gait and balance in patients with Parkinson's disease for up to 3–6 months. These results highlight the major role of the subthalamic nucleus in motor control mechanisms during locomotion and balance.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Clinical Biomechanics
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Agostini V.
        • Balestra G.
        • Knaflitz M.
        Segmentation and classification of gait cycles.
        IEEE Trans. Neural Syst. Rehabil. Eng. 2014; 22: 946-952https://doi.org/10.1109/TNSRE.2013.2291907
        • Agostini V.
        • Ganio D.
        • Facchin K.
        • Cane L.
        • Moreira Carneiro S.
        • Knaflitz M.
        Gait parameters and muscle activation patterns at 3, 6 and 12 months after total hip arthroplasty.
        J. Arthroplast. 2014; 29: 1265-1272https://doi.org/10.1016/j.arth.2013.12.018
        • Agostini V.
        • Lanotte M.
        • Carlone M.
        • Campagnoli M.
        • Azzolin I.
        • Scarafia R.
        • Massazza G.
        • Knaflitz M.
        Instrumented gait analysis for an objective pre−/postassessment of tap test in normal pressure hydrocephalus.
        Arch. Phys. Med. Rehabil. 2015; 96: 1235-1241https://doi.org/10.1016/j.apmr.2015.02.014
        • Agostini V.
        • Nascimbeni A.
        • Gaffuri A.
        • Knaflitz M.
        Multiple gait patterns within the same winters class in children with hemiplegic cerebral palsy.
        Clin Biomech (Bristol, Avon). 2015; 30: 908-914https://doi.org/10.1016/j.clinbiomech.2015.07.010
        • Benabid A.-L.
        • Deuschl G.
        • Lang A.E.
        • Lyons K.E.
        • Rezai A.R.
        Deep brain stimulation for Parkinson’s disease.
        Mov. Disord. 2006; 21: S168-S170https://doi.org/10.1002/mds.20954
        • Benabid A.L.
        • Chabardes S.
        • Mitrofanis J.
        • Pollak P.
        Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson’s disease.
        Lancet Neurol. 2009; 8: 67-81https://doi.org/10.1016/S1474-4422(08)70291-6
        • Benedetti M.G.
        • Agostini V.
        • Knaflitz M.
        • Gasparroni V.
        • Boschi M.
        • Piperno R.
        Self-reported gait unsteadiness in mildly impaired neurological patients: an objective assessment through statistical gait analysis.
        J Neuroeng Rehabil. 2012; 9: 64https://doi.org/10.1186/1743-0003-9-64
        • Bloem B.R.
        • Hausdorff J.M.
        • Visser J.E.
        • Giladi N.
        Falls and freezing of gait in Parkinson’s disease: a review of two interconnected, episodic phenomena.
        Mov. Disord. 2004; 19: 871-884https://doi.org/10.1002/mds.20115
        • Cantiniaux S.
        • Vaugoyeau M.
        • Robert D.
        • Horrelou-Pitek C.
        • Mancini J.
        • Witjas T.
        • Azulay J.-P.
        Comparative analysis of gait and speech in Parkinson’s disease: hypokinetic or dysrhythmic disorders?.
        J. Neurol. Neurosurg. Psychiatry. 2010; 81: 177-184https://doi.org/10.1136/jnnp.2009.174375
        • Fasano A.
        • Aquino C.C.
        • Krauss J.K.
        • Honey C.R.
        • Bloem B.R.
        Axial disability and deep brain stimulation in patients with Parkinson disease.
        Nat. Rev. Neurol. 2015; 11: 98-110https://doi.org/10.1038/nrneurol.2014.252
        • Ferrarin M.
        • Rizzone M.
        • Bergamasco B.
        • Lanotte M.
        • Recalcati M.
        • Pedotti A.
        • Lopiano L.
        Effects of bilateral subthalamic stimulation on gait kinematics and kinetics in Parkinson’s disease.
        Exp. Brain Res. 2005; 160: 517-527https://doi.org/10.1007/s00221-004-2036-5
        • Flora E.D.
        • Perera C.L.
        • Cameron A.L.
        • Maddern G.J.
        Deep brain stimulation for essential tremor: a systematic review.
        Mov. Disord. 2010; 25: 1550-1559https://doi.org/10.1002/mds.23195
        • Giladi N.
        Medical treatment of freezing of gait.
        Mov. Disord. 2008; 23: S482-S488https://doi.org/10.1002/mds.21914
        • Giladi N.
        • Treves T.A.
        • Simon E.S.
        • Shabtai H.
        • Orlov Y.
        • Kandinov B.
        • Paleacu D.
        • Korczyn A.D.
        Freezing of gait in patients with advanced Parkinson’s disease.
        J. Neural Transm. 2001; 108: 53-61
        • Hariz M.I.
        • Rehncrona S.
        • Quinn N.P.
        • Speelman J.D.
        • Wensing C.
        • Multicentre Advanced Parkinson’s Disease Deep Brain Stimulation Group
        Multicenter study on deep brain stimulation in Parkinson’s disease: an independent assessment of reported adverse events at 4 years.
        Mov. Disord. 2008; 23: 416-421https://doi.org/10.1002/mds.21888
        • Hausdorff J.M.
        • Cudkowicz M.E.
        • Firtion R.
        • Wei J.Y.
        • Goldberger A.L.
        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: 428-437https://doi.org/10.1002/mds.870130310
        • Hausdorff J.M.
        • Gruendlinger L.
        • Scollins L.
        • O’Herron S.
        • Tarsy D.
        Deep brain stimulation effects on gait variability in Parkinson’s disease.
        Mov. Disord. 2009; 24: 1688-1692https://doi.org/10.1002/mds.22554
        • Johnsen E.L.
        • Mogensen P.H.
        • Sunde N.A.
        • Østergaard K.
        Improved asymmetry of gait in Parkinson’s disease with DBS: gait and postural instability in Parkinson’s disease treated with bilateral deep brain stimulation in the subthalamic nucleus.
        Mov. Disord. 2009; 24: 590-597https://doi.org/10.1002/mds.22419
        • Kegelmeyer D.A.
        • Kloos A.D.
        • Thomas K.M.
        • Kostyk S.K.
        Reliability and validity of the Tinetti mobility test for individuals with Parkinson disease.
        Phys. Ther. 2007; 87: 1369-1378https://doi.org/10.2522/ptj.20070007
        • Kelly V.E.
        • Israel S.M.
        • Samii A.
        • Slimp J.C.
        • Goodkin R.
        • Shumway-Cook A.
        Assessing the effects of subthalamic nucleus stimulation on gait and mobility in people with Parkinson disease.
        Disabil. Rehabil. 2010; 32: 929-936https://doi.org/10.3109/09638280903374139
        • Kuhner A.
        • Wiesmeier I.K.
        • Cenciarini M.
        • Maier T.L.
        • Kammermeier S.
        • Coenen V.A.
        • Burgard W.
        • Maurer C.
        Motion biomarkers showing maximum contrast between healthy subjects and Parkinson’s disease patients treated with deep brain stimulation of the subthalamic nucleus. A Pilot Study.
        Front Neurosci. 2019; 13: 1450https://doi.org/10.3389/fnins.2019.01450
        • Lubik S.
        • Fogel W.
        • Tronnier V.
        • Krause M.
        • König J.
        • Jost W.H.
        Gait analysis in patients with advanced Parkinson disease: different or additive effects on gait induced by levodopa and chronic STN stimulation.
        J. Neural Transm. (Vienna). 2006; 113: 163-173https://doi.org/10.1007/s00702-005-0310-8
        • Maetzler W.
        • Klucken J.
        • Horne M.
        A clinical view on the development of technology-based tools in managing Parkinson’s disease.
        Mov. Disord. 2016; 31: 1263-1271https://doi.org/10.1002/mds.26673
        • Magariños-Ascone C.M.
        • Regidor I.
        • Gómez-Galán M.
        • Cabañes-Martínez L.
        • Figueiras-Méndez R.
        Deep brain stimulation in the globus pallidus to treat dystonia: electrophysiological characteristics and 2 years’ follow-up in 10 patients.
        Neuroscience. 2008; 152: 558-571https://doi.org/10.1016/j.neuroscience.2008.01.001
        • McNeely M.E.
        • Earhart G.M.
        Medication and subthalamic nucleus deep brain stimulation similarly improve balance and complex gait in Parkinson disease.
        Parkinsonism Relat. Disord. 2013; 19: 86-91https://doi.org/10.1016/j.parkreldis.2012.07.013
        • McNeely M.E.
        • Hershey T.
        • Campbell M.C.
        • Tabbal S.D.
        • Karimi M.
        • Hartlein J.M.
        • Lugar H.M.
        • Revilla F.J.
        • Perlmutter J.S.
        • Earhart G.M.
        Effects of deep brain stimulation of dorsal versus ventral subthalamic nucleus regions on gait and balance in Parkinson’s disease.
        J. Neurol. Neurosurg. Psychiatry. 2011; 82: 1250-1255https://doi.org/10.1136/jnnp.2010.232900
        • Mera T.O.
        • Filipkowski D.E.
        • Riley D.E.
        • Whitney C.M.
        • Walter B.L.
        • Gunzler S.A.
        • Giuffrida J.P.
        Quantitative analysis of gait and balance response to deep brain stimulation in Parkinson’s disease.
        Gait Posture. 2013; 38: 109-114https://doi.org/10.1016/j.gaitpost.2012.10.025
        • Morris M.
        • Iansek R.
        • Matyas T.
        • Summers J.
        Abnormalities in the stride length-cadence relation in parkinsonian gait.
        Mov. Disord. 1998; 13: 61-69https://doi.org/10.1002/mds.870130115
        • Morris S.
        • Morris M.E.
        • Iansek R.
        Reliability of measurements obtained with the timed “up & go” test in people with Parkinson disease.
        Phys. Ther. 2001; 81: 810-818https://doi.org/10.1093/ptj/81.2.810
        • Nilsson M.H.
        • Törnqvist A.L.
        • Rehncrona S.
        Deep-brain stimulation in the subthalamic nuclei improves balance performance in patients with Parkinson’s disease, when tested without anti-parkinsonian medication.
        Acta Neurol. Scand. 2005; 111: 301-308https://doi.org/10.1111/j.1600-0404.2005.00394.x
        • Nilsson M.H.
        • Fransson P.-A.
        • Jarnlo G.-B.
        • Magnusson M.
        • Rehncrona S.
        The effects of high frequency subthalamic stimulation on balance performance and fear of falling in patients with Parkinson’s disease.
        J Neuroeng Rehabil. 2009; 6: 13https://doi.org/10.1186/1743-0003-6-13
        • Podsiadlo D.
        • Richardson S.
        The timed “up & go”: a test of basic functional mobility for frail elderly persons.
        J. Am. Geriatr. Soc. 1991; 39: 142-148
        • Roper J.A.
        • Kang N.
        • Ben J.
        • Cauraugh J.H.
        • Okun M.S.
        • Hass C.J.
        Deep brain stimulation improves gait velocity in Parkinson’s disease: a systematic review and meta-analysis.
        J. Neurol. 2016; 263: 1195-1203https://doi.org/10.1007/s00415-016-8129-9
        • Schaafsma J.D.
        • Giladi N.
        • Balash Y.
        • Bartels A.L.
        • Gurevich T.
        • Hausdorff J.M.
        Gait dynamics in Parkinson’s disease: relationship to Parkinsonian features, falls and response to levodopa.
        J. Neurol. Sci. 2003; 212: 47-53
        • Seger A.
        • Gulberti A.
        • Vettorazzi E.
        • Braa H.
        • Buhmann C.
        • Gerloff C.
        • Hamel W.
        • Moll C.K.E.
        • Pötter-Nerger M.
        Short pulse and conventional deep brain stimulation equally improve the Parkinsonian gait disorder.
        J. Parkinsons Dis. 2021; https://doi.org/10.3233/JPD-202492
        • Stern G.M.
        • Franklyn S.E.
        • Imms F.J.
        • Prestidge S.P.
        Quantitative assessments of gait and mobility in Parkinson’s disease.
        J. Neural Transm. Suppl. 1983; 19: 201-214
        • Tinetti M.E.
        Performance-oriented assessment of mobility problems in elderly patients.
        J. Am. Geriatr. Soc. 1986; 34: 119-126https://doi.org/10.1111/j.1532-5415.1986.tb05480.x
        • Tinetti M.E.
        • Williams T.F.
        • Mayewski R.
        Fall risk index for elderly patients based on number of chronic disabilities.
        Am. J. Med. 1986; 80: 429-434
        • Vallabhajosula S.
        • Haq I.U.
        • Hwynn N.
        • Oyama G.
        • Okun M.
        • Tillman M.D.
        • Hass C.J.
        Low-frequency versus high-frequency subthalamic nucleus deep brain stimulation on postural control and gait in Parkinson’s disease: a quantitative study.
        Brain Stimul. 2015; 8: 64-75https://doi.org/10.1016/j.brs.2014.10.011
        • Villadoniga M.
        • San Millan A.
        • Cabanes-Martinez L.
        • Aviles-Olmos I.
        • Del Alamo-De Pedro M.
        • Regidor I.
        Quantitative gait analysis in patients with advanced Parkinson’s disease.
        Rev. Neurol. 2016; 63: 97-102
        • Visser J.E.
        • Allum J.H.J.
        • Carpenter M.G.
        • Esselink R.A.
        • Speelman J.D.
        • Borm G.F.
        • Bloem B.R.
        Subthalamic nucleus stimulation and levodopa-resistant postural instability in Parkinson’s disease.
        J. Neurol. 2008; 255: 205-210https://doi.org/10.1007/s00415-008-0636-x
        • Weiss D.
        • Walach M.
        • Meisner C.
        • Fritz M.
        • Scholten M.
        • Breit S.
        • Plewnia C.
        • Bender B.
        • Gharabaghi A.
        • Wächter T.
        • Krüger R.
        Nigral stimulation for resistant axial motor impairment in Parkinson’s disease? A randomized controlled trial.
        Brain. 2013; 136: 2098-2108https://doi.org/10.1093/brain/awt122
        • Wu Z.
        • Zhong M.
        • Jiang X.
        • Shen B.
        • Zhu J.
        • Pan Y.
        • Dong J.
        • Yan J.
        • Xu P.
        • Zhang W.
        • Gao Y.
        • Zhang L.
        Can quantitative gait analysis be used to guide treatment of patients with different subtypes of Parkinson’s disease?.
        Neuropsychiatr. Dis. Treat. 2020; 16: 2335-2341https://doi.org/10.2147/NDT.S266585
        • Xie J.
        • Krack P.
        • Benabid A.L.
        • Pollak P.
        Effect of bilateral subthalamic nucleus stimulation on parkinsonian gait.
        J. Neurol. 2001; 248: 1068-1072
        • Yu K.
        • Ren Z.
        • Guo S.
        • Li J.
        • Li Y.
        Effects of pedunculopontine nucleus deep brain stimulation on gait disorders in Parkinson’s disease: a meta-analysis of the literature.
        Clin. Neurol. Neurosurg. 2020; 198106108https://doi.org/10.1016/j.clineuro.2020.106108