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Neuromodulatory procedures for gait disorders in Parkinson’s disease

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Abstract

The neurophysiology of gait is complex and involves numerous structures in the central nervous system. Gait disorders occur frequently in Parkinson’s disease (PD), and their management may become cumbersome, especially in the more advanced stages. Neuromodulatory treatments, including deep brain stimulation, cortical stimulation and spinal cord stimulation, are reviewed with respect to their effectiveness to improve gait in PD patients. Although positive effects have been reported for all of these procedures, many issues remain in view of methodological heterogeneity, variability in outcome measures and sample size. Gait in PD remains a difficult issue with a tremendous impact on quality of life, for which future research is badly needed.

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References

  1. Smulders K, Dale ML, Carlson-Kuhta P, Nutt JG, Horak FB (2016) Pharmacological treatment in Parkinson’s disease: effects on gait. Parkinsonism Relat Disord 31:3–13. https://doi.org/10.1016/j.parkreldis.2016.07.006

    Article  PubMed  PubMed Central  Google Scholar 

  2. Stuart S, Lord S, Hill E, Rochester L (2016) Gait in Parkinson’s disease: a visuo-cognitive challenge. Neurosci Biobehav Rev 62:76–88. https://doi.org/10.1016/j.neubiorev.2016.01.002

    Article  PubMed  Google Scholar 

  3. Galna B, Lord S, Burn DJ, Rochester L (2015) Progression of gait dysfunction in incident Parkinson’s disease: impact of medication and phenotype. Mov Disord 30:359–367. https://doi.org/10.1002/mds.26110

    Article  CAS  PubMed  Google Scholar 

  4. Thenganatt MA, Jankovic J (2014) Parkinson disease subtypes. JAMA Neurol 71:499–504. https://doi.org/10.1001/jamaneurol.2013.6233

    Article  PubMed  Google Scholar 

  5. Wu T, Hallett M, Chan P (2015) Motor automaticity in Parkinson’s disease. Neurobiol Dis 82:226–234. https://doi.org/10.1016/j.nbd.2015.06.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Curtze C, Nutt JG, Carlson-Kuhta P, Mancini M, Horak FB (2015) Levodopa is a double-edged sword for balance and gait in people with Parkinson’s disease. Mov Disord 30:1361–1370. https://doi.org/10.1002/mds.26269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Giladi N (2008) Medical treatment of freezing of gait. Mov Disord 23(Suppl 2):S482–S488. https://doi.org/10.1002/mds.21914

    Article  PubMed  Google Scholar 

  8. Giladi N, Nieuwboer A (2008) Understanding and treating freezing of gait in parkinsonism, proposed working definition, and setting the stage. Mov Disord 23(Suppl 2):S423–S425. https://doi.org/10.1002/mds.21927

    Article  PubMed  Google Scholar 

  9. Perez-Lloret S, Negre-Pages L, Damier P, Delval A, Derkinderen P, Destée A, Meissner WG, Schelosky L, Tison F, Rascol O (2014) Prevalence, determinants, and effect on quality of life of freezing of gait in Parkinson disease. JAMA Neurol 71(7):884–890. https://doi.org/10.1001/jamaneurol.2014.753

    Article  PubMed  Google Scholar 

  10. Takakusaki K (2013) Neurophysiology of gait: from the spinal cord to the frontal lobe. Mov Disord 28(11):1483–1491. https://doi.org/10.1002/mds.25669

    Article  PubMed  Google Scholar 

  11. Moro E, Schüpbach M, Wächter T, Allert N, Eleopra R, Honey CR, Rueda M, Schiess MC, Shimo Y, Valkovic P, Whone A, Stoevelaar H (2016) Referring Parkinson’s disease patients for deep brain stimulation: a RAND/UCLA appropriateness study. J Neurol 263:112–119. https://doi.org/10.1007/s00415-015-7942-x

    Article  PubMed  Google Scholar 

  12. 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. https://doi.org/10.1007/s00415-016-8129-9

    Article  CAS  PubMed  Google Scholar 

  13. Collomb-Clerc A, Welter ML (2015) Effects of deep brain stimulation on balance and gait in patients with Parkinson’s disease: a systematic neurophysiological review. Neurophysiol Clin 45:371–388. https://doi.org/10.1016/j.neucli.2015.07.001

    Article  CAS  PubMed  Google Scholar 

  14. Vercruysse S, Vandenberghe W, Münks L, Nuttin B, Devos H, Nieuwboer A (2014) Effects of deep brain stimulation of the subthalamic nucleus on freezing of gait in Parkinson’s disease: a prospective controlled study. J Neurol Neurosurg Psychiatry 85:871–877. https://doi.org/10.1136/jnnp-2013-306336

    Article  CAS  PubMed  Google Scholar 

  15. Xie J, Krack P, Benabid AL, Pollak P (2001) Effect of bilateral subthalamic nucleus stimulation on parkinsonian gait. J Neurol 248:1068–1072

    Article  CAS  PubMed  Google Scholar 

  16. Ferraye MU, Debû B, Fraix V, Xie-Brustolin J, Chabardès S, Krack P, Benabid AL, Pollak P (2008) Effects of subthalamic nucleus stimulation and levodopa on freezing of gait in Parkinson disease. Neurology 70:1431–1437. https://doi.org/10.1212/01.wnl.0000310416.90757.85

    Article  CAS  PubMed  Google Scholar 

  17. Farris SM, Giroux ML (2016) Rapid assessment of gait and speech after subthalamic deep brain stimulation. Surg Neurol Int 7(Suppl 19):S545–S550. https://doi.org/10.4103/2152-7806.187532

    Article  PubMed  PubMed Central  Google Scholar 

  18. Schlenstedt C, Shalash A, Muthuraman M, Falk D, Witt K, Deuschl G (2017) Effect of high-frequency subthalamic neurostimulation on gait and freezing of gait in Parkinson’s disease: a systematic review and meta-analysis. Eur J Neurol 24:18–26. https://doi.org/10.1111/ene.13167

    Article  CAS  PubMed  Google Scholar 

  19. Fleury V, Pollak P, Gere J, Tommasi G, Romito L, Combescure C, Bardinet E, Chabardes S, Momjian S, Krainik A, Burkhard P, Yelnik J, Krack P (2016) Subthalamic stimulation may inhibit the beneficial effects of levodopa on akinesia and gait. Mov Disord 31:1389–1397. https://doi.org/10.1002/mds.26545

    Article  CAS  PubMed  Google Scholar 

  20. Weiss D, Breit S, Wächter T, Plewnia C, Gharabaghi A, Krüger R (2011) Combined stimulation of the substantia nigra pars reticulata and the subthalamic nucleus is effective in hypokinetic gait disturbance in Parkinson’s disease. J Neurol 258:1183–1185. https://doi.org/10.1007/s00415-011-5906-3

    Article  PubMed  Google Scholar 

  21. Weiss D, Walach M, Meisner C, Fritz M, Scholten M, Breit S, Plewnia C, Bender B, Gharabaghi A, Wächter T, Krüger R (2013) Nigral stimulation for resistant axial motor impairment in Parkinson’s disease? A randomized controlled trial. Brain 136(Pt 7):2098–2108. https://doi.org/10.1093/brain/awt122

    Article  PubMed  PubMed Central  Google Scholar 

  22. Blumenfeld Z, Brontë-Stewart H (2015) High frequency deep brain stimulation and neural rhythms in Parkinson’s disease. Neuropsychol Rev 25:384–397. https://doi.org/10.1007/s11065-015-9308-7

    Article  PubMed  Google Scholar 

  23. Moro E, Esselink RJ, Xie J, Hommel M, Benabid AL, Pollak P (2002) The impact on Parkinson’s disease of electrical parameter settings in STN stimulation. Neurology 59:706–713

    Article  CAS  PubMed  Google Scholar 

  24. Moreau C, Defebvre L, Destée A, Bleuse S, Clement F, Blatt JL, Krystkowiak P, Devos D (2008) STN-DBS frequency effects on freezing of gait in advanced Parkinson disease. Neurology 71:80–84. https://doi.org/10.1212/01.wnl.0000303972.16279.46

    Article  CAS  PubMed  Google Scholar 

  25. Khoo HM, Kishima H, Hosomi K, Maruo T, Tani N, Oshino S, Shimokawa T, Yokoe M, Mochizuki H, Saitoh Y, Yoshimine T (2014) Low-frequency subthalamic nucleus stimulation in Parkinson’s disease: a randomized clinical trial. Mov Disord 29:270–274. https://doi.org/10.1002/mds.25810

    Article  PubMed  Google Scholar 

  26. Ricchi V, Zibetti M, Angrisano S, Merola A, Arduino N, Artusi CA, Rizzone M, Lopiano L, Lanotte M (2012) Transient effects of 80 Hz stimulation on gait in STN DBS treated PD patients: a 15 months follow-up study. Brain Stimul 5:388–392. https://doi.org/10.1016/j.brs.2011.07.001

    Article  PubMed  Google Scholar 

  27. Zibetti M, Moro E, Krishna V, Sammartino F, Picillo M, Munhoz RP, Lozano AM, Fasano A (2016) Low-frequency subthalamic stimulation in Parkinson’s disease: long-term outcome and predictors. Brain Stimul 9:774–779. https://doi.org/10.1016/j.brs.2016.04.017

    Article  PubMed  Google Scholar 

  28. Gut NK, Winn P (2016) The pedunculopontine tegmental nucleus—a functional hypothesis from the comparative literature. Mov Disord 31:615–624. https://doi.org/10.1002/mds.26556

    Article  PubMed  PubMed Central  Google Scholar 

  29. Golestanirad L, Elahi B, Graham SJ, Das S, Wald LL (2016) Efficacy and safety of pedunculopontine nuclei (PPN) deep brain stimulation in the treatment of gait disorders: a meta-analysis of clinical studies. Can J Neurol Sci 43:120–126. https://doi.org/10.1017/cjn.2015.318

    Article  PubMed  Google Scholar 

  30. Mestre TA, Sidiropoulos C, Hamani C, Poon YY, Lozano AM, Lang AE, Moro E (2016) Long-term double-blinded unilateral pedunculopontine area stimulation in Parkinson’s disease. Mov Disord 31:1570–1574. https://doi.org/10.1002/mds.26710

    Article  PubMed  Google Scholar 

  31. Defebvre LJ, Krystkowiak P, Blatt JL, Duhamel A, Bourriez JL, Périna M, Blond S, Guieu JD, Destée A (2002) Influence of pallidal stimulation and levodopa on gait and preparatory postural adjustments in Parkinson’s disease. Mov Disord 17:76–83

    Article  PubMed  Google Scholar 

  32. Bakker M, Esselink RA, 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 19:1092–1099

    Article  PubMed  Google Scholar 

  33. Bastian AJ, Kelly VE, Perlmutter JS, Mink JW (2003) Effects of pallidotomy and levodopa on walking and reaching movements in Parkinson’s disease. Mov Disord 18:1008–1017

    Article  PubMed  Google Scholar 

  34. Bronte-Stewart HM, Minn AY, Rodrigues K, Buckley EL, Nashner LM (2002) Postural instability in idiopathic Parkinson’s disease: the role of medication and unilateral pallidotomy. Brain 125:2100–2114

    Article  PubMed  Google Scholar 

  35. Roberts-Warrior D, Overby A, Jankovic J, Olson S, Lai EC, Krauss JK, Grossman R (2000) Postural control in Parkinson’s disease after unilateral posteroventral pallidotomy. Brain 123:2141–2149

    Article  PubMed  Google Scholar 

  36. Turnbull GI (2006) Changes in gait and symptoms after bilateral pallidotomy: a client with Parkinson’s disease. Physiother Res Int 11:173–179

    Article  PubMed  Google Scholar 

  37. Alvarez L, Macias R, Lopez G, Alvarez E, Pavon N, Rodriguez-Oroz MC, Juncos JL, Maragoto C, Guridi J, Litvan I, Tolosa ES, Koller W, Vitek J, DeLong MR, Obeso JA (2005) Bilateral subthalamotomy in Parkinson’s disease: initial and long-term response. Brain 128:570–583

    Article  CAS  PubMed  Google Scholar 

  38. Chung CL, Mak MK (2016) Effect of repetitive transcranial magnetic stimulation on physical function and motor signs in Parkinson’s disease: a systematic review and meta-analysis. Brain Stimul 9:475–487. https://doi.org/10.1016/j.brs.2016.03.017

    Article  CAS  PubMed  Google Scholar 

  39. Santana MB, Halje P, Simplício H, Richter U, Freire MA, Petersson P, Fuentes R, Nicolelis MA (2014) Spinal cord stimulation alleviates motor deficits in a primate model of Parkinson disease. Neuron 84:716–722. https://doi.org/10.1016/j.neuron.2014.08.061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Pinto de Souza C, Hamani C, Oliveira Souza C, Lopez Contreras WO, Dos Santos Ghilardi MG, Cury RG, Reis Barbosa E, Jacobsen Teixeira M, Talamoni Fonoff E (2017) Spinal cord stimulation improves gait in patients with Parkinson’s disease previously treated with deep brain stimulation. Mov Disord 32:278–282. https://doi.org/10.1002/mds.26850

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Neurology, Ghent University Hospital, De Pintelaan 185, 9000, Ghent, Belgium

    Patrick Santens

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  1. Patrick Santens
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Correspondence to Patrick Santens.

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The author is a senior clinical researcher at the FWO-Flanders.

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The author has received speaker’s honorarium from Medtronic Inc. at various occasions.

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Since this is a review article, no new studies with animals or humans were involved in the preparation of this manuscript.

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Santens, P. Neuromodulatory procedures for gait disorders in Parkinson’s disease. Acta Neurol Belg 118, 13–19 (2018). https://doi.org/10.1007/s13760-017-0862-z

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  • DOI: https://doi.org/10.1007/s13760-017-0862-z

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