Skip to main content
SpringerLink
Log in

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

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Objective

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.

Methods

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.

Results

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.

Conclusions

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Availability of data and material (data transparency)

The data that support the findings of this study are available on request from the corresponding author, upon reasonable request.

Code availability

Not applicable.

References

  1. Mirelman A, Bonato P, Camicioli R et al (2019) Gait impairments in Parkinson’s disease. Lancet Neurol 18:697–708

    Article  PubMed  Google Scholar 

  2. 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

    CAS  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

  4. Limousin P, Foltynie T (2019) Long-term outcomes of deep brain stimulation in Parkinson disease. Nat Rev Neurol 15:234–242

    Article  PubMed  Google Scholar 

  5. 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

    Article  Google Scholar 

  6. 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)

    Article  PubMed  PubMed Central  Google Scholar 

  7. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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

    Article  CAS  PubMed  Google Scholar 

  9. 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

    Article  PubMed  Google Scholar 

  10. 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

    Article  Google Scholar 

  11. 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

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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

    Article  PubMed  PubMed Central  Google Scholar 

  13. 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

    Article  CAS  Google Scholar 

  14. 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

    Article  Google Scholar 

  15. 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

    Article  Google Scholar 

  16. 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

    Article  Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. Deuschl G, Paschen S, Witt K (2013) Clinical outcome of deep brain stimulation for Parkinson’s disease. Handb Clin Neurol 116:107–128

    Article  PubMed  Google Scholar 

  19. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. World Medical Association (2013) World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 310:2191–2194

    Article  Google Scholar 

  21. 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

    Article  CAS  Google Scholar 

  22. Fahn S, Marsden C, Calne D, Goldstein M (1987) Recent developments in Parkinson’s disease. Macmillan Health Care Information, Florham Park

    Google Scholar 

  23. 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

    Article  PubMed  PubMed Central  Google Scholar 

  24. 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

    Article  Google Scholar 

  25. 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

    Article  CAS  Google Scholar 

  26. 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

    Article  Google Scholar 

  27. 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

    Article  Google Scholar 

  28. 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

    Article  PubMed  PubMed Central  Google Scholar 

  29. 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

    Article  PubMed  PubMed Central  Google Scholar 

  30. 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

    Article  PubMed  Google Scholar 

  31. 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

    Article  Google Scholar 

  32. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 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

    Article  PubMed  PubMed Central  Google Scholar 

  34. 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

    Article  CAS  PubMed  Google Scholar 

  35. Peterson DS, Mancini M, Fino PC, Horak F, Smulders K (2020) Speeding up gait in Parkinson’s disease. J Park Dis 10:245–253

    Google Scholar 

  36. 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

    Article  PubMed  Google Scholar 

  37. 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

    Article  PubMed  Google Scholar 

  38. 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

    Article  Google Scholar 

  39. 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

    Article  PubMed  Google Scholar 

  40. 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.

  41. 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

    Article  PubMed  Google Scholar 

  42. 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

    Article  PubMed  Google Scholar 

  43. 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

    Article  PubMed  Google Scholar 

  44. 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.

  45. 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

    Article  PubMed  Google Scholar 

  46. 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

    Google Scholar 

Download references

Acknowledgements

This study was partially supported by Italian Ministry of Health—Ricerca Corrente Annual Program 2023.

Funding

No funding reported.

Author information

Authors and Affiliations

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

    Francesco Cavallieri, Valentina Fioravanti, Giulia Di Rauso, Jessica Rossi & Franco Valzania

  2. Clinical and Experimental Medicine PhD Program, University of Modena and Reggio Emilia, Reggio Emilia, Italy

    Francesco Cavallieri & Jessica Rossi

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

    Isabella Campanini, Benedetta Damiano, Sara Scaltriti, Noemi Guagnano & Andrea Merlo

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

    Annalisa Gessani, Carla Budriesi, Giulia Di Rauso, Elisa Bardi, Maria Giulia Corni, Francesca Antonelli & Maria Angela Molinari

  5. Department of Neurosciences, Biomedicine, and Movement Sciences, Institute of Neurosurgery, University of Verona, Verona, Italy

    Alberto Feletti

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

    Alberto Feletti, Annette Puzzolante & Giacomo Pavesi

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

    Francesca Cavalleri

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

    Sara Contardi

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

    Elisa Menozzi

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

    Giuseppe Vannozzi & Elena Bergamini

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

    Sara Meoni, Valérie Fraix & Elena Moro

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

    Alessandro Fraternali & Annibale Versari

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

    Mirco Lusuardi

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

    Giuseppe Biagini

Authors
  1. Francesco Cavallieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isabella Campanini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Annalisa Gessani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carla Budriesi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Valentina Fioravanti
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Giulia Di Rauso
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alberto Feletti
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Benedetta Damiano
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sara Scaltriti
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Noemi Guagnano
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Elisa Bardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Maria Giulia Corni
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Jessica Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Francesca Antonelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Francesca Cavalleri
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Maria Angela Molinari
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Sara Contardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Elisa Menozzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Annette Puzzolante
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Giuseppe Vannozzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Elena Bergamini
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Giacomo Pavesi
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Sara Meoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Valérie Fraix
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Alessandro Fraternali
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Annibale Versari
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. Mirco Lusuardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  28. Giuseppe Biagini
    View author publications

    You can also search for this author in PubMed Google Scholar

  29. Andrea Merlo
    View author publications

    You can also search for this author in PubMed Google Scholar

  30. Elena Moro
    View author publications

    You can also search for this author in PubMed Google Scholar

  31. Franco Valzania
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FC: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; IC: design of the study, data collection and analysis, manuscript preparation: writing of the first draft and review and critique; AG: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; CB: design of the study, data collection and analysis, manuscript preparation: writing of the first draft and review and critique; VFi: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; GDR: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; AF: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; BD: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; SS: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; NG: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; EB: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; MGC: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; JR: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; FA: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; FCa: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; MAM: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; SC: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; EM: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; AP: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; GV: design of the study, data collection and analysis, manuscript preparation: review and critique; EB: design of the study, data collection and analysis, manuscript preparation: review and critique; GP: design of the study, data collection and analysis, manuscript preparation: review and critique; SM: data collection and analysis, manuscript preparation: review and critique; VFr: data collection and analysis, manuscript preparation: review and critique; AF: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; AV: design of the study, data collection and analysis, manuscript preparation: writing of the first draft; ML: data collection and analysis, manuscript preparation: review and critique; GB: design of the study, data collection and analysis, manuscript preparation: review and critique; AM: design of the study, data collection and analysis, manuscript preparation: writing of the first draft and review and critique; EM: data collection and analysis, manuscript preparation: review and critique; FV: design of the study, data collection and analysis, manuscript preparation: writing of the first draft and review and critique. All the authors. All the authors approve the final version for publication.

Corresponding author

Correspondence to Isabella Campanini.

Ethics declarations

Conflicts of interest

E. Moro has received honoraria from Medtronic, Abbott and Kyowa for consulting services. She has also received grant support from Ipsen and Boston Medical. VF receiving honoraria for lecturing Boston Scientific and Medtronic. All the other authors declare no financial disclosures. The authors declare that they have no conflict of interest.

Ethical approval

The study was approved by the local ethics committee (protocol number: 2019/0056629).

Consent for publication

Written informed consent was obtained from participants according to the Declaration of Helsinki.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1648 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cavallieri, F., Campanini, I., Gessani, A. et al. Long-term effects of bilateral subthalamic nucleus deep brain stimulation on gait disorders in Parkinson’s disease: a clinical-instrumental study. J Neurol 270, 4342–4353 (2023). https://doi.org/10.1007/s00415-023-11780-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-023-11780-5

Keywords

Search

Navigation