Estimulación de la médula espinal para los trastornos de la marcha en Enfermedad de Parkinson y parkinsonismo atípico: Una revisión sistemática de los estudios preclínicos y clínicos: Publicado originalmente en la Revista Neuromodulation 2023; 26: 1339–1361. Traducción: Dr. Sergio Sacchettoni.

Matteo Ciocca; Barry M. Seemungal; Yen F. Tai

doi:10.47924/neurotarget2024454

Authors

Matteo Ciocca Department of Brain Sciences, Imperial College London, London, UK.
Barry M. Seemungal Department of Brain Sciences, Imperial College London, London, UK.
Yen F. Tai Department of Brain Sciences, Imperial College London, London, UK.

DOI:

https://doi.org/10.47924/neurotarget2024454

Keywords:

Freezing of gait, multiple system atrophy, Parkinson’s disease, progressive supranuclear palsy, spinal cord stimulation

Abstract

Background: Falls in extrapyramidal disorders, particularly Parkinson’s disease (PD), multisystem atrophy (MSA), and progressive supranuclear palsy (PSP), are key milestones affecting patients’ quality of life, incurring increased morbidity/mortality and high healthcare costs. Unfortunately, gait and balance in parkinsonisms respond poorly to currently available treatments. A serendipitous observation of improved gait and balance in patients with PD receiving spinal cord stimulation (SCS) for back pain kindled an interest in using SCS to treat gait disorders in parkinsonisms.
Objectives: We reviewed preclinical and clinical studies of SCS to treat gait dysfunction in parkinsonisms, covering its putative mechanisms and efficacies.
Materials and Methods: Preclinical studies in animal models of PD and clinical studies in patients with PD, PSP, and MSA who received SCS for gait disorders were included. The main outcome assessed was clinical improvement in gait, together with outcome measures used and possible mechanism of actions.
Results: We identified 500 references, and 45 met the selection criteria and have been included in this study for analysis. Despite positive results in animal models, the outcomes in human studies are inconsistent.
Conclusions: The lack of blind and statistically powered studies, the heterogeneity in patient selection and study outcomes, and the poor understanding of the underlying mechanisms of action of SCS are some of the limiting factors in the field. Addressing these limitations will allow us to draw more reliable conclusions on the effects of SCS on gait and balance in extrapiramidal disorders.

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References

Tysnes OB, Storstein A. Epidemiology of Parkinson’s disease. J Neural Transm (Vienna). 2017;124:901–905.

Postuma RB, Berg D, Stern M, et al. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2015;30:1591–1601.

Bloem BR, Hausdorff JM, Visser JE, Giladi N. Falls and freezing of gait in Parkinson’s disease: a review of two interconnected, episodic phenomena. Mov Disord. 2004;19:871–884.

Matinolli M, Korpelainen JT, Sotaniemi KA, Myllylä VV, Korpelainen R. Recurrent falls and mortality in Parkinson’s disease: a prospective two-year follow-up study. Acta Neurol Scand. 2011;123:193–200.

Weir S, Samnaliev M, Kuo TC, et al. Short- and long-term cost and utilization of health care resources in Parkinson’s disease in the UK. Mov Disord. 2018;33:974–981.

Fasano A, Canning CG, Hausdorff JM, Lord S, Rochester L. Falls in Parkinson’s disease: a complex and evolving picture. Mov Disord. 2017;32:1524–1536.

O’Sullivan SS, Massey LA, Williams DR, et al. Clinical outcomes of progressive supranuclear palsy and multiple system atrophy. Brain. 2008;131:1362–1372.

Zwergal A, la Fougère C, Lorenzl S, et al. Postural imbalance and falls in PSP correlate with functional pathology of the thalamus. Neurology. 2011;77:101–109.

Sdrulla AD, Guan Y, Raja SN. Spinal cord stimulation: clinical efficacy and potential mechanisms. Pain Pract. 2018;18:1048–1067.

Agari T, Date I. Spinal cord stimulation for the treatment of abnormal posture and gait disorder in patients with Parkinson’s disease. Neurol Med Chir (Tokyo). 2012;52:470–474.

Samotus O, Parrent A, Jog M. Spinal cord stimulation therapy for gait dysfunction in advanced Parkinson’s disease patients. Mov Disord. 2018;33:783–792.

Miller JP, Eldabe S, Buchser E, Johanek LM, Guan Y, Linderoth B. Parameters of spinal cord stimulation and their role in electrical charge delivery: a review. Neuromodulation. 2016;19:373–384.

Linderoth B, Foreman RD. Conventional and novel spinal stimulation algorithms: hypothetical mechanisms of action and comments on outcomes. Neuromodulation. 2017;20:525–533.

Fénelon G, Goujon C, Gurruchaga JM, et al. Spinal cord stimulation for chronic pain improved motor function in a patient with Parkinson’s disease. Parkinsonism Relat Disord. 2012;18:213–214.

Landi A, Trezza A, Pirillo D, Vimercati A, Antonini A, Sganzerla EP. Spinal cord stimulation for the treatment of sensory symptoms in advanced Parkinson’s disease. Neuromodulation. 2013;16:276–279.

Hassan S, Amer S, Alwaki A, Elborno A. A patient with Parkinson’s disease benefits from spinal cord stimulation. J Clin Neurosci. 2013;20:1155–1156.

Akiyama H, Nukui S, Akamatu M, Hasegawa Y, Nishikido O, Inoue S. Effectiveness of spinal cord stimulation for painful camptocormia with Pisa syndrome in Parkinson’s disease: a case report. BMC Neurol. 2017;17:148.

Kobayashi R, Kenji S, Taketomi A, Murakami H, Ono K, Otake H. New mode of burst spinal cord stimulation improved mental status as well as motor function in a patient with Parkinson’s disease. Parkinsonism Relat Disord. 2018;57:82–83.

Mazzone P, Viselli F, Ferraina S, et al. High cervical spinal cord stimulation: a one year follow-up study on motor and non-motor functions in Parkinson’s disease. Brain Sci. 2019;9:78.

Furusawa Y, Matsui A, Kobayashi-Noami K, et al. Burst spinal cord stimulation for pain and motor function in Parkinson’s disease: a case series. Clin Park Relat Disord. 2020;3;100043.

Chakravarthy KV, Chaturvedi R, Agari T, Iwamuro H, Reddy R, Matsui A. Single arm prospective multicenter case series on the use of burst stimulation to improve pain and motor symptoms in Parkinson’s disease. Bioelectron Med. 2020;6:18.

Thevathasan W, Mazzone P, Jha A, et al. Spinal cord stimulation failed to relieve akinesia or restore locomotion in Parkinson disease. Neurology. 2010;74:1325–1327.

Pinto de Souza C, Hamani C, Oliveira Souza C, et al. Spinal cord stimulation improves gait in patients with Parkinson’s disease previously treated with Deep brain stimulation. Mov Disord. 2017;32:278–282.

de Lima-Pardini AC, Coelho DB, Souza CP, et al. Effects of spinal cord stimulation on postural control in Parkinson’s disease patients with freezing of gait. Elife. 2018;7;e37727.

Hubsch C, D’Hardemare V, Ben Maacha M, et al. Tonic spinal cord stimulation as therapeutic option in Parkinson disease with axial symptoms: effects on walking and quality of life. Parkinsonism Relat Disord. 2019;63:235–237.

Prasad S, Aguirre-Padilla DH, Poon YY, Kalsi-Ryan S, Lozano AM, Fasano A. Spinal cord stimulation for very advanced Parkinson’s disease: a 1-year prospective trial. Mov Disord. 2020;35:1082–1083.

Samotus O, Parrent A, Jog M. Long-term update of the effect of spinal cord stimulation in advanced Parkinson’s disease patients. Brain Stimul. 2020;13:1196–1197.

Samotus O, Parrent A, Jog M. Spinal cord stimulation therapy for gait dysfunction in progressive supranuclear palsy patients. J Neurol. 2021;268:989–996.

Samotus O, Parrent A, Jog M. Spinal cord stimulation therapy for gait dysfunction in two corticobasal syndrome patients. Can J Neurol Sci. 2021;48:278–280.

Zhou PB, Bao M. Spinal cord stimulation treatment for freezing of gait in Parkinson’s disease: a case report. Brain Stimul. 2022;15:76–77.

Rohani M, Kalsi-Ryan S, Lozano AM, Fasano A. Spinal cord stimulation in primary progressive freezing of gait. Mov Disord. 2017;32:1336–1337.

Zhang Y, Song T, Zhuang P, et al. Spinal cord stimulation improves freezing of gait in a patient with multiple system atrophy with predominant parkinsonism. Brain Stimul. 2020;13:653–654.

Wang L, Zhu R, Pan Y, et al. Effects of high cervical spinal cord stimulation on gait disturbance and Dysarthropneumophonia in Parkinson’s disease and Parkinson variant of multiple system atrophy: a case series. Brain Sci. 2022;12:1222.

Li J, Mei S, Zhang X, et al. Case report: combined therapy of bilateral subthalamic nucleus deep brain stimulation and spinal cord stimulation significantly improves motor function in a patient with multiple system atrophy with predominant parkinsonism. Front Neurosci. 2022;16;929273.

Squair JW, Berney M, Castro Jimenez M, et al. Implanted system for orthostatic hypotension in multiple-system atrophy. N Engl J Med. 2022;386:1339–1344.

Fuentes R, Petersson P, Siesser WB, Caron MG, Nicolelis MA. Spinal cord stimulation restores locomotion in animal models of Parkinson’s disease. Science. 2009;323:1578–1582.

Santana MB, Halje P, Simplício H, et al. Spinal cord stimulation alleviates motor deficits in a primate model of Parkinson disease. Neuron. 2014;84:716–722.

Brys I, Bobela W, Schneider BL, Aebischer P, Fuentes R. Spinal cord stimulation improves forelimb use in an alpha-synuclein animal model of Parkinson’s disease. Int J Neurosci. 2017;127:28–36.

Yadav AP, Fuentes R, Zhang H, et al. Chronic spinal cord electrical stimulation protects against 6-hydroxydopamine lesions. Sci Rep. 2014;4:3839.

Zhong H, Zhu C, Minegishi Y, et al. Epidural spinal cord stimulation improves motor function in rats with chemically induced parkinsonism. Neurorehabil Neural Repair. 2019;33:1029–1039.

Shinko A, Agari T, Kameda M, et al. Spinal cord stimulation exerts neuroprotective effects against experimental Parkinson’s disease. PLoS One. 2014;9;e101468.

Kuwahara K, Sasaki T, Yasuhara T, et al. Long-term continuous cervical spinal cord stimulation exerts neuroprotective effects in experimental Parkinson’s disease. Front Aging Neurosci. 2020;12:164.

Ichiyama RM, Gerasimenko YP, Zhong H, Roy RR, Edgerton VR. Hindlimb stepping movements in complete spinal rats induced by epidural spinal cord stimulation. Neurosci Lett. 2005;383:339–344.

Meuwissen KPV, de Vries LE, Gu JW, Zhang TC, Joosten EAJ. Burst and tonic spinal cord stimulation both activate spinal GABAergic mechanisms to attenuate pain in a rat model of chronic neuropathic pain. Pain Pract. 2020;20:75–87.

Wagner FB, Mignardot JB, Le Goff-Mignardot CG, et al. Targeted neurotechnology restores walking in humans with spinal cord injury. Nature. 2018;563:65–71. CIOCCA ET AL www.neuromodulationjournal.org © 2023 The Authors. Published by Elsevier Inc. on behalf of the International Neuromodulation Society. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Neuromodulation 2023; 26: 1339–1361

Jara JS, Agger S, Hollis 2nd ER. Functional electrical stimulation and the modulation of the axon regeneration program. Front Cell Dev Biol. 2020;8:736.

Takakusaki K. Neurophysiology of gait: from the spinal cord to the frontal lobe. Mov Disord. 2013;28:1483–1491.

Takakusaki K. Functional neuroanatomy for posture and gait control. J Mov Disord. 2017;10:1–17.

Grillner S. Neuroscience. Human locomotor circuits conform. Science. 2011;334:912–913.

Bocci T, De Carolis G, Paroli M, et al. Neurophysiological comparison among tonic, high frequency, and burst spinal cord stimulation: novel insights into spinal and brain mechanisms of action. Neuromodulation. 2018;21:480–488.

Jacobs JV, Lou JS, Kraakevik JA, Horak FB. The supplementary motor area contributes to the timing of the anticipatory postural adjustment during step initiation in participants with and without Parkinson’s disease. Neuroscience. 2009;164:877–885.

Cury RG, Carra RB, Capato TTC, Teixeira MJ, Barbosa ER. Spinal cord stimulation for Parkinson’s disease: dynamic habituation as a mechanism of failure? Mov Disord. 2020;35:1882–1883.