Long-term effects of bilateral subthalamic nucleus deep brain stimulation on gait disorders in Parkinson's disease: a clinical-instrumental study.


Journal

Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161

Informations de publication

Date de publication:
Sep 2023
Historique:
received: 10 01 2023
accepted: 12 05 2023
revised: 21 04 2023
medline: 14 8 2023
pubmed: 20 5 2023
entrez: 19 5 2023
Statut: ppublish

Résumé

To assess the long-term effects of bilateral subthalamic nucleus deep brain stimulation (STN-DBS) on gait in a cohort of advanced Parkinson's Disease (PD) patients. This observational study included consecutive PD patients treated with bilateral STN-DBS. Different stimulation and drug treatment conditions were assessed: on-stimulation/off-medication, off-stimulation/off-medication, and on-stimulation/on-medication. Each patient performed the instrumented Timed Up and Go test (iTUG). The instrumental evaluation of walking ability was carried out with a wearable inertial sensor containing a three-dimensional (3D) accelerometer, gyroscope, and magnetometer. This device could provide 3D linear acceleration, angular velocity, and magnetic field vector. Disease motor severity was evaluated with the total score and subscores of the Unified Parkinson Disease Rating Scale part III. Twenty-five PD patients with a 5-years median follow-up after surgery (range 3-7) were included (18 men; mean disease duration at surgery 10.44 ± 4.62 years; mean age at surgery 58.40 ± 5.73 years). Both stimulation and medication reduced the total duration of the iTUG and most of its different phases, suggesting a long-term beneficial effect on gait after surgery. However, comparing the two treatments, dopaminergic therapy had a more marked effect in all test phases. STN-DBS alone reduced total iTUG duration, sit-to-stand, and second turn phases duration, while it had a lower effect on stand-to-sit, first turn, forward walking, and walking backward phases duration. This study highlighted that in the long-term after surgery, STN-DBS may contribute to gait and postural control improvement when used together with dopamine replacement therapy, which still shows a substantial beneficial effect.

Identifiants

pubmed: 37208527
doi: 10.1007/s00415-023-11780-5
pii: 10.1007/s00415-023-11780-5
doi:

Types de publication

Observational Study Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

4342-4353

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany.

Références

Mirelman A, Bonato P, Camicioli R et al (2019) Gait impairments in Parkinson’s disease. Lancet Neurol 18:697–708
pubmed: 30975519 doi: 10.1016/S1474-4422(19)30044-4
Kemoun G, Defebvre L (2001) Gait disorders in Parkinson disease. Clinical description, analysis of posture, initiation of stabilized gait. Presse Medicale Paris Fr 1983 30:452–459
Deuschl G, Schade-Brittinger C, Krack P et al (2006) A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med 355:896–908
pubmed: 16943402 doi: 10.1056/NEJMoa060281
Limousin P, Foltynie T (2019) Long-term outcomes of deep brain stimulation in Parkinson disease. Nat Rev Neurol 15:234–242
pubmed: 30778210 doi: 10.1038/s41582-019-0145-9
Rodriguez-Oroz MC, Moro E, Krack P (2012) Long-term outcomes of surgical therapies for Parkinson’s disease. Mov Disord Off J Mov Disord Soc 27:1718–1728
doi: 10.1002/mds.25214
Bove F, Mulas D, Cavallieri F et al (2021) Long-term outcomes (15 years) after subthalamic nucleus deep brain stimulation in patients with Parkinson disease. Neurology. https://doi.org/10.1212/WNL.0000000000012246 . (Epub 2021 Jun 2)
doi: 10.1212/WNL.0000000000012246 pubmed: 34484932 pmcid: 8377877
Weaver FM, Follett K, Stern M et al (2009) Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA 301:63–73
pubmed: 19126811 pmcid: 2814800 doi: 10.1001/jama.2008.929
Cavallieri F, Fraix V, Bove F et al (2021) Predictors of long-term outcome of subthalamic stimulation in Parkinson disease. Ann Neurol 89:587–597
pubmed: 33349939 doi: 10.1002/ana.25994
Bove F, Fraix V, Cavallieri F et al (2020) Dementia and subthalamic deep brain stimulation in Parkinson disease: a long-term overview. Neurology 95:e384–e392
pubmed: 32611633 doi: 10.1212/WNL.0000000000009822
Zampogna A, Cavallieri F, Bove F et al (2022) Axial impairment and falls in Parkinson’s disease: 15 years of subthalamic deep brain stimulation. NPJ Park Dis 8:121
doi: 10.1038/s41531-022-00383-y
Di Rauso G, Cavallieri F, Campanini I et al (2022) Freezing of gait in Parkinson’s disease patients treated with bilateral subthalamic nucleus deep brain stimulation: a long-term overview. Biomedicines 10:2214
pubmed: 36140318 pmcid: 9496255 doi: 10.3390/biomedicines10092214
Rocchi L, Carlson-Kuhta P, Chiari L, Burchiel KJ, Hogarth P, Horak FB (2012) Effects of deep brain stimulation in the subthalamic nucleus or globus pallidus internus on step initiation in Parkinson disease: laboratory investigation. J Neurosurg 117:1141–1149
pubmed: 23039143 pmcid: 3990225 doi: 10.3171/2012.8.JNS112006
Collomb-Clerc A, Welter M-L (2015) Effects of deep brain stimulation on balance and gait in patients with Parkinson’s disease: a systematic neurophysiological review. Neurophysiol Clin Clin Neurophysiol 45:371–388
doi: 10.1016/j.neucli.2015.07.001
Hausdorff JM, Gruendlinger L, Scollins L, O’Herron S, Tarsy D (2009) Deep brain stimulation effects on gait variability in Parkinson’s disease. Mov Disord Off J Mov Disord Soc 24:1688–1692
doi: 10.1002/mds.22554
Vallabhajosula S, Haq IU, Hwynn N et al (2015) Low-frequency versus high-frequency subthalamic nucleus deep brain stimulation on postural control and gait in Parkinson’s disease: a quantitative study. Brain Stimulat 8:64–75
doi: 10.1016/j.brs.2014.10.011
Bakker M, Esselink RAJ, Munneke M, Limousin-Dowsey P, Speelman HD, Bloem BR (2004) Effects of stereotactic neurosurgery on postural instability and gait in Parkinson’s disease. Mov Disord Off J Mov Disord Soc 19:1092–1099
doi: 10.1002/mds.20116
Krack P, Batir A, Van Blercom N et al (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:1925–1934
pubmed: 14614167 doi: 10.1056/NEJMoa035275
Deuschl G, Paschen S, Witt K (2013) Clinical outcome of deep brain stimulation for Parkinson’s disease. Handb Clin Neurol 116:107–128
pubmed: 24112889 doi: 10.1016/B978-0-444-53497-2.00010-3
Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184
pubmed: 1564476 pmcid: 1014720 doi: 10.1136/jnnp.55.3.181
World Medical Association (2013) World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 310:2191–2194
doi: 10.1001/jama.2013.281053
Defer GL, Widner H, Marié RM, Rémy P, Levivier M (1999) Core assessment program for surgical interventional therapies in Parkinson’s disease (CAPSIT-PD). Mov Disord Off J Mov Disord Soc 14:572–584
doi: 10.1002/1531-8257(199907)14:4<572::AID-MDS1005>3.0.CO;2-C
Fahn S, Marsden C, Calne D, Goldstein M (1987) Recent developments in Parkinson’s disease. Macmillan Health Care Information, Florham Park
Campanini I, Mastrangelo S, Bargellini A et al (2018) Feasibility and predictive performance of the Hendrich Fall Risk Model II in a rehabilitation department: a prospective study. BMC Health Serv Res 18:18
pubmed: 29325560 pmcid: 5765700 doi: 10.1186/s12913-017-2815-x
Stebbins GT, Goetz CG, Burn DJ, Jankovic J, Khoo TK, Tilley BC (2013) How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson’s disease rating scale: comparison with the unified Parkinson’s disease rating scale. Mov Disord Off J Mov Disord Soc 28:668–670
doi: 10.1002/mds.25383
Grisanti S, Ferri L, Cavallieri F et al (2022) Increased stroke risk in patients with Parkinson’s disease with LRRK2 mutations. Mov Disord Off J Mov Disord Soc 37:1117–1118
doi: 10.1002/mds.28996
Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord Off J Mov Disord Soc 25:2649–2653
doi: 10.1002/mds.23429
Palmerini L, Mellone S, Avanzolini G, Valzania F, Chiari L (2013) Quantification of motor impairment in Parkinson’s disease using an instrumented timed up and go test. IEEE Trans Neural Syst Rehabil Eng Publ IEEE Eng Med Biol Soc 21:664–673
doi: 10.1109/TNSRE.2012.2236577
van Lummel RC, Walgaard S, Hobert MA et al (2016) Intra-rater, inter-rater and test-retest reliability of an instrumented timed up and go (iTUG) test in patients with Parkinson’s disease. PLoS One 11:e0151881
pubmed: 26999051 pmcid: 4801645 doi: 10.1371/journal.pone.0151881
Vervoort D, Vuillerme N, Kosse N, Hortobágyi T, Lamoth CJC (2016) Multivariate analyses and classification of inertial sensor data to identify aging effects on the timed-up-and-go test. PLoS One 11:e0155984
pubmed: 27271994 pmcid: 4894562 doi: 10.1371/journal.pone.0155984
Hurt CP, Kuhman DJ, Guthrie BL, Lima CR, Wade M, Walker HC (2020) Walking speed reliably measures clinically significant changes in gait by directional deep brain stimulation. Front Hum Neurosci 14:618366
pubmed: 33584227 doi: 10.3389/fnhum.2020.618366
Pötter-Nerger M, Volkmann J (2013) Deep brain stimulation for gait and postural symptoms in Parkinson’s disease. Mov Disord Off J Mov Disord Soc 28:1609–1615
doi: 10.1002/mds.25677
St George RJ, Nutt JG, Burchiel KJ, Horak FB (2010) A meta-regression of the long-term effects of deep brain stimulation on balance and gait in PD. Neurology 75:1292–1299
pubmed: 20921515 pmcid: 3013496 doi: 10.1212/WNL.0b013e3181f61329
Navratilova D, Krobot A, Otruba P et al (2020) Deep brain stimulation effects on gait pattern in advanced Parkinson’s disease patients. Front Neurosci 14:814
pubmed: 32922256 pmcid: 7456806 doi: 10.3389/fnins.2020.00814
Roper JA, Kang N, Ben J, Cauraugh JH, Okun MS, Hass CJ (2016) Deep brain stimulation improves gait velocity in Parkinson’s disease: a systematic review and meta-analysis. J Neurol 263:1195–1203
pubmed: 27126451 doi: 10.1007/s00415-016-8129-9
Peterson DS, Mancini M, Fino PC, Horak F, Smulders K (2020) Speeding up gait in Parkinson’s disease. J Park Dis 10:245–253
Mak MKY, Levin O, Mizrahi J, Hui-Chan CWY (2003) Joint torques during sit-to-stand in healthy subjects and people with Parkinson’s disease. Clin Biomech Bristol Avon 18:197–206
pubmed: 12620782 doi: 10.1016/S0268-0033(02)00191-2
Inkster LM, Eng JJ (2004) Postural control during a sit-to-stand task in individuals with mild Parkinson’s disease. Exp Brain Res 154:33–38
pubmed: 12961057 doi: 10.1007/s00221-003-1629-8
Mak MKY, Hui-Chan CWY (2005) The speed of sit-to-stand can be modulated in Parkinson’s disease. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 116:780–789
doi: 10.1016/j.clinph.2004.12.017
Weiss A, Herman T, Plotnik M et al (2010) Can an accelerometer enhance the utility of the Timed Up & Go Test when evaluating patients with Parkinson’s disease? Med Eng Phys 32:119–125
pubmed: 19942472 doi: 10.1016/j.medengphy.2009.10.015
Fatmehsari YR, Bahrami F (2011) Sit-to-stand or stand-to-sit: Which movement can classify better Parkinsonian patients from healthy elderly subjects? 2011 18th Iran Conf Biomed Eng ICBME. Tehran, Iran: IEEE; pp 48–53. http://ieeexplore.ieee.org/document/6168583/ . Accessed Nov 13, 2022.
Weiss A, Herman T, Mirelman A et al (2019) The transition between turning and sitting in patients with Parkinson’s disease: a wearable device detects an unexpected sequence of events. Gait Posture 67:224–229
pubmed: 30380506 doi: 10.1016/j.gaitpost.2018.10.018
Raffegeau TE, Krehbiel LM, Kang N et al (2019) A meta-analysis: Parkinson’s disease and dual-task walking. Parkinsonism Relat Disord 62:28–35
pubmed: 30594454 doi: 10.1016/j.parkreldis.2018.12.012
Vance RC, Healy DG, Galvin R, French HP (2015) Dual tasking with the timed “up & go” test improves detection of risk of falls in people with Parkinson disease. Phys Ther 95:95–102
pubmed: 25147186 doi: 10.2522/ptj.20130386
Byl N, Henry R, Rizzo R, Blum D (2018) Is the timed up and go (TUG) sensitive to differentiating patients with mild to moderate PD compared to age matched controls: a descriptive pilot study. Int Phys Med Rehabil J. 3. https://medcraveonline.com/IPMRJ/is-the-timed-up-and-go-tug-sensitive-to-differentiating-patients-with-mild-to-moderate-pd-compared-to-age-matched-controls-a-descriptive-pilot-study.html . Accessed Dec 5, 2022.
Zampieri C, Salarian A, Carlson-Kuhta P, Aminian K, Nutt JG, Horak FB (2010) The instrumented timed up and go test: potential outcome measure for disease modifying therapies in Parkinson’s disease. J Neurol Neurosurg Psychiatry 81:171–176
pubmed: 19726406 doi: 10.1136/jnnp.2009.173740
Dibilio V, Nicoletti A, Mostile G et al (1996) Dopaminergic and non-dopaminergic gait components assessed by instrumented timed up and go test in Parkinson’s disease. J Neural Transm Vienna Austria 2017(124):1539–1546

Auteurs

Francesco Cavallieri (F)

Neuromotor and Rehabilitation Department, Neurology Unit, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia, Italy.
Clinical and Experimental Medicine PhD Program, University of Modena and Reggio Emilia, Reggio Emilia, Italy.

Isabella Campanini (I)

LAM-Motion Analysis Laboratory, Neuromotor and Rehabilitation Department, Azienda USL-IRCCS Di Reggio Emilia, S. Sebastiano Hospital, Correggio, Italy. Isabella.Campanini@ausl.re.it.

Annalisa Gessani (A)

Department of Neuroscience, Neurology Unit, S. Agostino Estense Hospital, AziendaOspedaliero-Universitaria di Modena, Modena, Italy.

Carla Budriesi (C)

Department of Neuroscience, Neurology Unit, S. Agostino Estense Hospital, AziendaOspedaliero-Universitaria di Modena, Modena, Italy.

Valentina Fioravanti (V)

Neuromotor and Rehabilitation Department, Neurology Unit, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia, Italy.

Giulia Di Rauso (G)

Neuromotor and Rehabilitation Department, Neurology Unit, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia, Italy.
Department of Neuroscience, Neurology Unit, S. Agostino Estense Hospital, AziendaOspedaliero-Universitaria di Modena, Modena, Italy.

Alberto Feletti (A)

Department of Neurosciences, Biomedicine, and Movement Sciences, Institute of Neurosurgery, University of Verona, Verona, Italy.
Neurosurgery Unit, Azienda Ospedaliero-Universitaria of Modena, Ospedale Civile Baggiovara (OCB) Hospital, Modena, Italy.

Benedetta Damiano (B)

LAM-Motion Analysis Laboratory, Neuromotor and Rehabilitation Department, Azienda USL-IRCCS Di Reggio Emilia, S. Sebastiano Hospital, Correggio, Italy.

Sara Scaltriti (S)

LAM-Motion Analysis Laboratory, Neuromotor and Rehabilitation Department, Azienda USL-IRCCS Di Reggio Emilia, S. Sebastiano Hospital, Correggio, Italy.

Noemi Guagnano (N)

LAM-Motion Analysis Laboratory, Neuromotor and Rehabilitation Department, Azienda USL-IRCCS Di Reggio Emilia, S. Sebastiano Hospital, Correggio, Italy.

Elisa Bardi (E)

Department of Neuroscience, Neurology Unit, S. Agostino Estense Hospital, AziendaOspedaliero-Universitaria di Modena, Modena, Italy.

Maria Giulia Corni (MG)

Department of Neuroscience, Neurology Unit, S. Agostino Estense Hospital, AziendaOspedaliero-Universitaria di Modena, Modena, Italy.

Jessica Rossi (J)

Neuromotor and Rehabilitation Department, Neurology Unit, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia, Italy.
Clinical and Experimental Medicine PhD Program, University of Modena and Reggio Emilia, Reggio Emilia, Italy.

Francesca Antonelli (F)

Department of Neuroscience, Neurology Unit, S. Agostino Estense Hospital, AziendaOspedaliero-Universitaria di Modena, Modena, Italy.

Francesca Cavalleri (F)

Division of Neuroradiology, Department of Neuroscience, Nuovo Ospedale Civile S. Agostino Estense, Modena, Italy.

Maria Angela Molinari (MA)

Department of Neuroscience, Neurology Unit, S. Agostino Estense Hospital, AziendaOspedaliero-Universitaria di Modena, Modena, Italy.

Sara Contardi (S)

IRCCS Istituto delle Scienze Neurologiche di Bologna, Neurologia e Rete Stroke Metropolitana, Ospedale Maggiore, Bologna, Italy.

Elisa Menozzi (E)

Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, UK.

Annette Puzzolante (A)

Neurosurgery Unit, Azienda Ospedaliero-Universitaria of Modena, Ospedale Civile Baggiovara (OCB) Hospital, Modena, Italy.

Giuseppe Vannozzi (G)

Laboratory of Bioengineering and Neuromechanics, Department of Movement, Human and Health Sciences, University of Rome "Foro Italico", Rome, Italy.

Elena Bergamini (E)

Laboratory of Bioengineering and Neuromechanics, Department of Movement, Human and Health Sciences, University of Rome "Foro Italico", Rome, Italy.

Giacomo Pavesi (G)

Neurosurgery Unit, Azienda Ospedaliero-Universitaria of Modena, Ospedale Civile Baggiovara (OCB) Hospital, Modena, Italy.

Sara Meoni (S)

Division of Neurology, Grenoble Alpes University, Centre HospitalierUniversitaire de Grenoble, Grenoble Institute of Neuroscience, Grenoble, France.

Valérie Fraix (V)

Division of Neurology, Grenoble Alpes University, Centre HospitalierUniversitaire de Grenoble, Grenoble Institute of Neuroscience, Grenoble, France.

Alessandro Fraternali (A)

Nuclear Medicine Unit, Azienda Unità Sanitaria Locale IRCCS, Reggio Emilia, Italy.

Annibale Versari (A)

Nuclear Medicine Unit, Azienda Unità Sanitaria Locale IRCCS, Reggio Emilia, Italy.

Mirco Lusuardi (M)

Neuromotor and Rehabilitation Department, Azienda USL-IRCCS di Reggio Emilia, 42015, Reggio Emilia, Italy.

Giuseppe Biagini (G)

Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy.

Andrea Merlo (A)

LAM-Motion Analysis Laboratory, Neuromotor and Rehabilitation Department, Azienda USL-IRCCS Di Reggio Emilia, S. Sebastiano Hospital, Correggio, Italy.

Elena Moro (E)

Division of Neurology, Grenoble Alpes University, Centre HospitalierUniversitaire de Grenoble, Grenoble Institute of Neuroscience, Grenoble, France.

Franco Valzania (F)

Neuromotor and Rehabilitation Department, Neurology Unit, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia, Italy.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH