Neurosurgical Review

, Volume 39, Issue 1, pp 27–35 | Cite as

Spinal cord stimulation for Parkinson’s disease: a systematic review

  • Emerson Magno de Andrade
  • Maria Gabriela Ghilardi
  • Rubens Gisbert Cury
  • Egberto Reis Barbosa
  • Romulo Fuentes
  • Manoel Jacobsen Teixeira
  • Erich Talamoni Fonoff
Review

Abstract

Axial symptoms are a late-developing phenomenon in the course of Parkinson’s disease (PD) and represent a therapeutic challenge given their poor response to levodopa therapy and deep brain stimulation. Spinal cord stimulation (SCS) may be a new therapeutic approach for the alleviation of levodopa-resistant motor symptoms of PD. Our purpose was to systematically review the effectiveness of SCS for the treatment of motor symptoms of PD and to evaluate the technical and pathophysiological mechanisms that may influence the outcome efficacy of SCS. A comprehensive literature search was conducted using electronic databases for the period from January 1966 through April 2014. The methodology utilized in this work follows a review process derived from evidence-based systematic review and meta-analysis of randomized trials described in the PRISMA statement. Reports examining SCS for the treatment of PD are limited. Eight studies with a total of 24 patients were included in this review. The overall motor score of the Unified Parkinson’s Disease Rating Scale in the on/off-stimulation condition remained unchanged in 6 patients and improved in 18 patients after SCS. SCS appears to yield positive results for PD symptoms, especially for impairments in gait function and postural stability. However, evidence is limited and long-term prospective studies will be required to identify the optimal candidates for SCS and the best parameters of stimulation and to fully characterize the effects of stimulation on motor and nonmotor symptoms of PD.

Keywords

Parkinson’s disease Spinal cord stimulation Dorsal column Gait function 

Notes

Conflict of interests

The author has no conflicts of interest to declare.

References

  1. 1.
    Agari T, Date I (2012) Spinal cord stimulation for the treatment of abnormal posture and gait disorder in patients with Parkinson’s disease. Neurol Med Chir (Tokyo) 52(7):470–474CrossRefGoogle Scholar
  2. 2.
    Babu R, Hazzard MA, Huang KT, Ugiliweneza B, Patil CG, Boakye M, Lad SP (2013) Outcomes of percutaneous and paddle lead implantation for spinal cord stimulation: a comparative analysis of complications, reoperation rates, and health-care costs. Neuromodulation 16(5):418–427PubMedCrossRefGoogle Scholar
  3. 3.
    Barolat G (1993) Experience with 509 plate electrodes implanted epidurally from C1 to L1. Stereotact Funct Neurosurg 61(2):60–79PubMedCrossRefGoogle Scholar
  4. 4.
    Barolat G (1998) Epidural spinal cord stimulation: anatomical and electrical properties of the intraspinal structures relevant to spinal cord stimulation and clinical correlations. Neuromodulation 1(2):63–71PubMedCrossRefGoogle Scholar
  5. 5.
    Benarroch EE (2013) Pedunculopontine nucleus: functional organization and clinical implications. Neurology 80(12):1148–1155PubMedCrossRefGoogle Scholar
  6. 6.
    Brown P (2007) Abnormal oscillatory synchronisation in the motor system leads to impaired movement. Curr Opin Neurobiol 17(6):656–664PubMedCrossRefGoogle Scholar
  7. 7.
    Connor DE Jr, Nixon M, Nanda A, Guthikonda B (2012) Vagal nerve stimulation for the treatment of medically refractory epilepsy: a review of the current literature. Neurosurg Focus 32(3):E12PubMedCrossRefGoogle Scholar
  8. 8.
    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(9):896–908PubMedCrossRefGoogle Scholar
  9. 9.
    Fénelon G, Goujon C, Gurruchaga J-M, Cesaro P, Jarraya B, Palfi S, Lefaucheur J-P (2012) Spinal cord stimulation for chronic pain improved motor function in a patient with Parkinson’s disease. Parkinsonism Relat Disord 18(2):213–214PubMedCrossRefGoogle Scholar
  10. 10.
    Ferraye MU, Debû B, Fraix V et al (2010) Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson’s disease. Brain J Neurol 133(Pt 1):205–214CrossRefGoogle Scholar
  11. 11.
    Ferraye MU, Debû B, Pollak P (2008) Deep brain stimulation effect on freezing of gait. Mov Disord Off J Mov Disord Soc 23(Suppl 2):S489–S494CrossRefGoogle Scholar
  12. 12.
    Foreman RD (2000) Integration of viscerosomatic sensory input at the spinal level. Prog Brain Res 122:209–221PubMedCrossRefGoogle Scholar
  13. 13.
    Fuentes R, Petersson P, Nicolelis MAL (2010) Restoration of locomotive function in Parkinson’s disease by spinal cord stimulation: mechanistic approach. Eur J Neurosci 32(7):1100–1108PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Fuentes R, Petersson P, Siesser WB, Caron MG, Nicolelis MAL (2009) Spinal cord stimulation restores locomotion in animal models of Parkinson’s disease. Science 323(5921):1578–1582PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Garcia-Rill E (1991) The pedunculopontine nucleus. Prog Neurobiol 36(5):363–389PubMedCrossRefGoogle Scholar
  16. 16.
    Gildenberg PL (1978) Treatment of spasmodic torticollis by dorsal column stimulation. Appl Neurophysiol 41(1–4):113–121PubMedGoogle Scholar
  17. 17.
    Goetz CG, Poewe W, Rascol O, Sampaio C (2005) Evidence-based medical review update: pharmacological and surgical treatments of Parkinson’s disease: 2001 to 2004. Mov Disord 20(5):523–539PubMedCrossRefGoogle Scholar
  18. 18.
    Grabli D, Karachi C, Welter M-L, Lau B, Hirsch EC, Vidailhet M, François C (2012) Normal and pathological gait: what we learn from Parkinson’s disease. J Neurol Neurosurg Psychiatry 83(10):979–985PubMedCrossRefGoogle Scholar
  19. 19.
    Hamani C, Richter E, Schwalb JM, Lozano AM (2008) Bilateral subthalamic nucleus stimulation for Parkinson’s disease: a systematic review of the clinical literature. Neurosurgery 62(Suppl 2):863–874PubMedGoogle Scholar
  20. 20.
    Hassan S, Amer S, Alwaki A, Elborno A (2013) A patient with Parkinson’s disease benefits from spinal cord stimulation. J Clin Neurosci Off J Neurosurg Soc Austral 20(8):1155–1156Google Scholar
  21. 21.
    Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117(4):500–544PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Holgado AJN, Terry JR, Bogacz R (2010) Conditions for the generation of beta oscillations in the subthalamic nucleus-globus pallidus network. J Neurosci 30(37):12340–12352PubMedCrossRefGoogle Scholar
  23. 23.
    Holsheimef J, Barolat G (1998) Spinal geometry and paresthesia coverage in spinal cord stimulation. Neuromodulation 1(3):129–136PubMedCrossRefGoogle Scholar
  24. 24.
    Holsheimer J (1998) Computer modelling of spinal cord stimulation and its contribution to therapeutic efficacy. Spinal Cord 36(8):531–540PubMedCrossRefGoogle Scholar
  25. 25.
    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(3):181–184PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Ichikawa T, Oshima M, Fuminura Y, Nishida Y (2013) Effect of spinal cord stimulation on gait with patients with PSP. Mov Disord 28(1):S431–S432Google Scholar
  27. 27.
    Jenkinson N, Nandi D, Muthusamy K, Ray NJ, Gregory R, Stein JF, Aziz TZ (2009) Anatomy, physiology, and pathophysiology of the pedunculopontine nucleus. Mov Disord 24(3):319–328PubMedCrossRefGoogle Scholar
  28. 28.
    Khan S, Gill SS, Mooney L, White P, Whone A, Brooks DJ, Pavese N (2012) Combined pedunculopontine-subthalamic stimulation in Parkinson disease. Neurology 78(14):1090–1095PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Landi A, Trezza A, Pirillo D, Vimercati A, Antonini A, Sganzerla EP (2013) Spinal cord stimulation for the treatment of sensory symptoms in advanced Parkinson’s disease. Neuromodulation 16(3):276–279PubMedCrossRefGoogle Scholar
  30. 30.
    Levy R, Ashby P, Hutchison WD, Lang AE, Lozano AM, Dostrovsky JO (2002) Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson’s disease. Brain J Neurol 125(Pt 6):1196–1209CrossRefGoogle Scholar
  31. 31.
    Levy R, Dostrovsky JO, Lang AE, Sime E, Hutchison WD, Lozano AM (2001) Effects of apomorphine on subthalamic nucleus and globus pallidus internus neurons in patients with Parkinson’s disease. J Neurophysiol 86(1):249–260PubMedGoogle Scholar
  32. 32.
    Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol 62(10):e1–e34PubMedCrossRefGoogle Scholar
  33. 33.
    Linderoth B (2009) Spinal cord stimulation: a brief update on mechanisms of action. Eur J Pain Suppl 3(2):89–93CrossRefGoogle Scholar
  34. 34.
    Magill PJ, Bolam JP, Bevan MD (2000) Relationship of activity in the subthalamic nucleus-globus pallidus network to cortical electroencephalogram. J Neurosci 20(2):820–833PubMedGoogle Scholar
  35. 35.
    Magill PJ, Bolam JP, Bevan MD (2001) Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus-globus pallidus network. Neuroscience 106(2):313–330PubMedCrossRefGoogle Scholar
  36. 36.
    McCarthy MM, Moore-Kochlacs C, Gu X, Boyden ES, Han X, Kopell N (2011) Striatal origin of the pathologic beta oscillations in Parkinson’s disease. Proc Natl Acad Sci U S A 108(28):11620–11625PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Melzack R, Wall PD (1965) Pain mechanisms: a new theory. Science 150(3699):971–979PubMedCrossRefGoogle Scholar
  38. 38.
    Mitsuyama T, Goto S, Sasaki T, Taira T, Okada Y (2013) Spinal cord stimulation for chronic lumbar pain in patients with parkinson’s disease. Stereotact Funct Neurosurg 91(1):273Google Scholar
  39. 39.
    Moro E, Hamani C, Poon Y-Y, Al-Khairallah T, Dostrovsky JO, Hutchison WD, Lozano AM (2010) Unilateral pedunculopontine stimulation improves falls in Parkinson’s disease. Brain J Neurol 133(Pt 1):215–224CrossRefGoogle Scholar
  40. 40.
    North RB, Kidd DH, Olin JC, Sieracki JM (2002) Spinal cord stimulation electrode design: prospective, randomized, controlled trial comparing percutaneous and laminectomy electrodes-part I: technical outcomes. Neurosurgery 51(2):381–389, discussion 389–390 PubMedGoogle Scholar
  41. 41.
    Oakley JC, Prager JP (2002) Spinal cord stimulation: mechanisms of action. Spine 27(22):2574–2583PubMedCrossRefGoogle Scholar
  42. 42.
    Pahapill PA, Lozano AM (2000) The pedunculopontine nucleus and Parkinson’s disease. Brain J Neurol 123(Pt 9):1767–1783CrossRefGoogle Scholar
  43. 43.
    Plenz D, Kital ST (1999) A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400(6745):677–682PubMedCrossRefGoogle Scholar
  44. 44.
    Post B, Muslimovic D, van Geloven N, Speelman JD, Schmand B, de Haan RJ, CARPA-study group (2011) Progression and prognostic factors of motor impairment, disability and quality of life in newly diagnosed Parkinson’s disease. Mov Disord 26(3):449–456PubMedCrossRefGoogle Scholar
  45. 45.
    Qin C, Farber JP, Foreman RD (2007) Spinal cord stimulation modulates activity of lumbosacral spinal neurons receiving input from urinary bladder in rats. Neurosci Lett 428(1):38–42PubMedCrossRefGoogle Scholar
  46. 46.
    Qin C, Lehew RT, Khan KA, Wienecke GM, Foreman RD (2007) Spinal cord stimulation modulates intraspinal colorectal visceroreceptive transmission in rats. Neurosci Res 58(1):58–66PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Ramasubbu C, Flagg A 2nd, Williams K (2013) Principles of electrical stimulation and dorsal column mapping as it relates to spinal cord stimulation: an overview. Curr Pain Headache Rep 17(2):315PubMedCrossRefGoogle Scholar
  48. 48.
    Rutecki P (1990) Anatomical, physiological, and theoretical basis for the antiepileptic effect of vagus nerve stimulation. Epilepsia 31(Suppl 2):S1–S6PubMedCrossRefGoogle Scholar
  49. 49.
    Rye DB, Lee HJ, Saper CB, Wainer BH (1988) Medullary and spinal efferents of the pedunculopontine tegmental nucleus and adjacent mesopontine tegmentum in the rat. J Comp Neurol 269(3):315–341PubMedCrossRefGoogle Scholar
  50. 50.
    Schuepbach WMM, Rau J, Knudsen K et al (2013) Neurostimulation for Parkinson’s disease with early motor complications. N Engl J Med 368(7):610–622PubMedCrossRefGoogle Scholar
  51. 51.
    Shealy CN, Mortimer JT, Reswick JB (1967) Electrical inhibition of pain by stimulation of the dorsal columns: preliminary clinical report. Anesth Analg 46(4):489–491PubMedCrossRefGoogle Scholar
  52. 52.
    Soltani F, Lalkhen A (2013) Improvement of parkinsonian symptoms with spinal cord stimulation: consequence or coincidence? J Neurol Neurosurg Psychiatry 84(11):e2CrossRefGoogle Scholar
  53. 53.
    Stefani A, Lozano AM, Peppe A, Stanzione P, Galati S, Tropepi D, Pierantozzi M, Brusa L, Scarnati E, Mazzone P (2007) Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson’s disease. Brain J Neurol 130(Pt 6):1596–1607CrossRefGoogle Scholar
  54. 54.
    Stein E, Bar-Gad I (2013) β oscillations in the cortico-basal ganglia loop during parkinsonism. Exp Neurol 245:52–59PubMedCrossRefGoogle Scholar
  55. 55.
    Takakusaki K, Habaguchi T, Ohtinata-Sugimoto J, Saitoh K, Sakamoto T (2003) Basal ganglia efferents to the brainstem centers controlling postural muscle tone and locomotion: a new concept for understanding motor disorders in basal ganglia dysfunction. Neuroscience 119(1):293–308PubMedCrossRefGoogle Scholar
  56. 56.
    Thevathasan W, Mazzone P, Jha A, Djamshidian A, Dileone M, Di Lazzaro V, Brown P (2010) Spinal cord stimulation failed to relieve akinesia or restore locomotion in Parkinson disease. Neurology 74(16):1325–1327PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Tulgar M, He J, Barolat G, Ketcik B, Struijk H, Holsheimer J (1993) Analysis of parameters for epidural spinal cord stimulation. 3. topographical distribution of paresthesiae—a preliminary analysis of 266 combinations with contacts implanted in the midcervical and midthoracic vertebral levels. Stereotact Funct Neurosurg 61(3):146–155PubMedCrossRefGoogle Scholar
  58. 58.
    Weise D, Winkler D, Meixensberger J, Classen J (2010) Effects of spinal cord stimulation in a patient with Parkinson’s disease and chronic back pain. J Neurol 257(1):S217Google Scholar
  59. 59.
    Williams A, Gill S, Varma T et al (2010) Deep brain stimulation plus best medical therapy versus best medical therapy alone for advanced Parkinson’s disease (PD SURG trial): a randomised, open-label trial. Lancet Neurol 9(6):581–591PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Wu C, Sharan AD (2013) Neurostimulation for the treatment of epilepsy: a review of current surgical interventions. Neuromodulation 16(1):10–24PubMedCrossRefGoogle Scholar
  61. 61.
    Yakhnitsa V, Linderoth B, Meyerson BA (1999) Spinal cord stimulation attenuates dorsal horn neuronal hyperexcitability in a rat model of mononeuropathy. Pain 79(2–3):223–233PubMedCrossRefGoogle Scholar
  62. 62.
    Yampolsky C, Hem S, Bendersky D (2012) Dorsal column stimulator applications. Surg Neurol Int 3(Suppl 4):S275–S289PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Zabara J (1992) Inhibition of experimental seizures in canines by repetitive vagal stimulation. Epilepsia 33(6):1005–1012PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Emerson Magno de Andrade
    • 1
  • Maria Gabriela Ghilardi
    • 1
  • Rubens Gisbert Cury
    • 1
    • 2
  • Egberto Reis Barbosa
    • 2
  • Romulo Fuentes
    • 3
  • Manoel Jacobsen Teixeira
    • 1
    • 2
  • Erich Talamoni Fonoff
    • 1
    • 2
  1. 1.Division of Functional Neurosurgery, Department of NeurologyUniversity of São Paulo Medical School (FMUSP)São PauloBrazil
  2. 2.Department of NeurologyUniversity of São Paulo Medical School (FMUSP)Sao PauloBrazil
  3. 3.Edmond and Lily Safra International Institute of Neuroscience of Natal (ELS-IINN)NatalBrazil

Personalised recommendations