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Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Review Article

Surgical Advances in Parkinson’s Disease

Author(s): Victor S. Hvingelby and Nicola Pavese*

Volume 22, Issue 6, 2024

Published on: 27 April, 2023

Page: [1033 - 1046] Pages: 14

DOI: 10.2174/1570159X21666221121094343

Price: $65

Abstract

While symptomatic pharmacological therapy remains the main therapeutic strategy for Parkinson’s disease (PD), over the last two decades, surgical approaches have become more commonly used to control levodopa-induced motor complications and dopamine-resistant and non-motor symptoms of PD. In this paper, we discuss old and new surgical treatments for PD and the many technological innovations in this field. We have initially reviewed the relevant surgical anatomy as well as the pathological signaling considered to be the underlying cause of specific symptoms of PD. Subsequently, early attempts at surgical symptom control will be briefly reviewed. As the most well-known surgical intervention for PD is deep brain stimulation, this subject is discussed at length. As deciding on whether a patient stands to benefit from DBS can be quite difficult, the different proposed paradigms for precisely this are covered. Following this, the evidence regarding different targets, especially the subthalamic nucleus and internal globus pallidus, is reviewed as well as the evidence for newer proposed targets for specific symptoms. Due to the rapidly expanding nature of knowledge and technological capabilities, some of these new and potential future capabilities are given consideration in terms of their current and future use. Following this, we have reviewed newer treatment modalities, especially magnetic resonance-guided focused ultrasound and other potential surgical therapies, such as spinal cord stimulation for gait symptoms and others. As mentioned, the field of surgical alleviation of symptoms of PD is undergoing a rapid expansion, and this review provides a general overview of the current status and future directions in the field.

Graphical Abstract

[1]
Tolosa, E.; Martí, M.J.; Valldeoriola, F.; Molinuevo, J.L. History of levodopa and dopamine agonists in Parkinson’s disease treatment. Neurology, 1998, 50(Suppl. 6), S2-S10.
[http://dx.doi.org/10.1212/WNL.50.6_Suppl_6.S2] [PMID: 9633679]
[2]
Güngör, A.; Baydın, Ş.S; Holanda, V.M.; Middlebrooks, E.H.; Isler, C.; Tugcu, B.; Foote, K.; Tanriover, N. Microsurgical anatomy of the subthalamic nucleus: correlating fiber dissection results with 3-T magnetic resonance imaging using neuronavigation. J. Neurosurg., 2019, 130(3), 716-732.
[http://dx.doi.org/10.3171/2017.10.JNS171513] [PMID: 29726781]
[3]
Kerl, H.U.; Gerigk, L.; Pechlivanis, I.; Al-Zghloul, M.; Groden, C.; Nölte, I. The subthalamic nucleus at 3.0 Tesla: choice of optimal sequence and orientation for deep brain stimulation using a standard installation protocol. J. Neurosurg., 2012, 117(6), 1155-1165.
[http://dx.doi.org/10.3171/2012.8.JNS111930] [PMID: 23039154]
[4]
Patil, P.G.; Conrad, E.C.; Aldridge, J.W.; Chenevert, T.L.; Chou, K.L. The anatomical and electrophysiological subthalamic nucleus visualized by 3-T magnetic resonance imaging. Neurosurgery, 2012, 71(6), 1089-1095.
[http://dx.doi.org/10.1227/NEU.0b013e318270611f] [PMID: 22948201]
[5]
Plaha, P.; Ben-Shlomo, Y.; Patel, N.K.; Gill, S.S. Stimulation of the caudal zona incerta is superior to stimulation of the subthalamic nucleus in improving contralateral parkinsonism. Brain, 2006, 129(7), 1732-1747.
[http://dx.doi.org/10.1093/brain/awl127] [PMID: 16720681]
[6]
Holanda, V.M.; Okun, M.S.; Middlebrooks, E.H.; Gungor, A.; Barry, M.E.; Forder, J.; Foote, K.D. Postmortem dissections of common targets for lesion and deep brain stimulation surgeries. Neurosurgery, 2020, 86(6), 860-872.
[http://dx.doi.org/10.1093/neuros/nyz318] [PMID: 31504849]
[7]
Wichmann, T.; DeLong, M.R. Functional and pathophysiological models of the basal ganglia. Curr. Opin. Neurobiol., 1996, 6(6), 751-758.
[http://dx.doi.org/10.1016/S0959-4388(96)80024-9] [PMID: 9000030]
[8]
Obeso, J.A.; Rodríguez-Oroz, M.C.; Benitez-Temino, B.; Blesa, F.J.; Guridi, J.; Marin, C.; Rodriguez, M. Functional organization of the basal ganglia: Therapeutic implications for Parkinson’s disease. Mov. Disord., 2008, 23(Suppl. 3), S548-S559.
[http://dx.doi.org/10.1002/mds.22062] [PMID: 18781672]
[9]
van Albada, S.J.; Robinson, P.A. Mean-field modeling of the basal ganglia-thalamocortical system. I Firing rates in healthy and parkinsonian states. J. Theor. Biol., 2009, 257(4), 642-663.
[http://dx.doi.org/10.1016/j.jtbi.2008.12.018] [PMID: 19168074]
[10]
Wichmann, T.; Soares, J. Neuronal firing before and after burst discharges in the monkey basal ganglia is predictably patterned in the normal state and altered in parkinsonism. J. Neurophysiol., 2006, 95(4), 2120-2133.
[http://dx.doi.org/10.1152/jn.01013.2005] [PMID: 16371459]
[11]
Alexander, G.E.; DeLong, M.R.; Strick, P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci., 1986, 9(1), 357-381.
[http://dx.doi.org/10.1146/annurev.ne.09.030186.002041] [PMID: 3085570]
[12]
Alexander, G.E.; Crutcher, M.D.; DeLong, M.R. Basal gangliathalamocortical circuits: Parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog. Brain Res., 1991, 85, 119-146.
[http://dx.doi.org/10.1016/S0079-6123(08)62678-3] [PMID: 2094891]
[13]
Fazl, A.; Fleisher, J. Anatomy, physiology, and clinical syndromes of the basal ganglia: a brief review. Semin. Pediatr. Neurol., 2018, 25, 2-9.
[http://dx.doi.org/10.1016/j.spen.2017.12.005] [PMID: 29735113]
[14]
Galvan, A.; Wichmann, T. Pathophysiology of Parkinsonism. Clin. Neurophysiol., 2008, 119(7), 1459-1474.
[http://dx.doi.org/10.1016/j.clinph.2008.03.017] [PMID: 18467168]
[15]
Brown, P.; Oliviero, A.; Mazzone, P.; Insola, A.; Tonali, P.; Di Lazzaro, V. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease. J. Neurosci., 2001, 21(3), 1033-1038.
[http://dx.doi.org/10.1523/JNEUROSCI.21-03-01033.2001] [PMID: 11157088]
[16]
Priori, A.; Foffani, G.; Pesenti, A.; Tamma, F.; Bianchi, A.; Pellegrini, M.; Locatelli, M.; Moxon, K.; Villani, R. Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson’s disease. Exp. Neurol., 2004, 189(2), 369-379.
[http://dx.doi.org/10.1016/j.expneurol.2004.06.001] [PMID: 15380487]
[17]
Sommerauer, M.; Fedorova, T.D.; Hansen, A.K.; Knudsen, K.; Otto, M.; Jeppesen, J.; Frederiksen, Y.; Blicher, J.U.; Geday, J.; Nahimi, A.; Damholdt, M.F.; Brooks, D.J.; Borghammer, P. Evaluation of the noradrenergic system in Parkinson’s disease: an 11C-MeNER PET and neuromelanin MRI study. Brain, 2018, 141(2), 496-504.
[http://dx.doi.org/10.1093/brain/awx348] [PMID: 29272343]
[18]
Pasquini, J.; Brooks, D.J.; Pavese, N. The cholinergic brain in Parkinson’s disease. Mov. Disord. Clin. Pract. (Hoboken), 2021, 8(7), 1012-1026.
[http://dx.doi.org/10.1002/mdc3.13319] [PMID: 34631936]
[19]
Oliver, L.C. Parkinson’s disease and its surgical treatment; H. K. Lewis & Co.: London, 1953.
[20]
Gardner, W.J. Surgical aspect of Parkinson’s syndrome. Postgrad. Med., 1949, 5(2), 107-111.
[http://dx.doi.org/10.1080/00325481.1949.11693763] [PMID: 18123618]
[21]
Cooper, I.S. The neurosurgical alleviation of Parkinsonism. Springfield: Irving California,; Charles C. Thomas: Ill, 1956.
[22]
Meyers, R. Surgical experiments in the therapy of certain ‘extrapyramidal’ diseases: a current evaluation. Acta Psychiatr. Neurol. Suppl., 1951, 67, 1-42.
[PMID: 14837767]
[23]
Schuepbach, W.M.; Rau, J.; Knudsen, K.; Volkmann, J.; Krack, P.; Timmermann, L.; Hälbig, T.D.; Hesekamp, H.; Navarro, S.M.; Meier, N.; Falk, D.; Mehdorn, M.; Paschen, S.; Maarouf, M.; Barbe, M.T.; Fink, G.R.; Kupsch, A.; Gruber, D.; Schneider, G.H.; Seigneuret, E.; Kistner, A.; Chaynes, P.; Ory-Magne, F.; Brefel Courbon, C.; Vesper, J.; Schnitzler, A.; Wojtecki, L.; Houeto, J.L.; Bataille, B.; Maltête, D.; Damier, P.; Raoul, S.; Sixel-Doering, F.; Hellwig, D.; Gharabaghi, A.; Krüger, R.; Pinsker, M.O.; Amtage, F.; Régis, J.M.; Witjas, T.; Thobois, S.; Mertens, P.; Kloss, M.; Hartmann, A.; Oertel, W.H.; Post, B.; Speelman, H.; Agid, Y.; Schade-Brittinger, C.; Deuschl, G. Neurostimulation for Parkinson's disease with early motor complications. N. Engl. J. Med., 2013, 368(7), 610-622.
[http://dx.doi.org/10.1056/NEJMoa1205158] [PMID: 23406026]
[24]
Deuschl, G.; Schade-Brittinger, C.; Krack, P.; Volkmann, J.; Schäfer, H.; Bötzel, K.; Daniels, C.; Deutschländer, A.; Dillmann, U.; Eisner, W.; Gruber, D.; Hamel, W.; Herzog, J.; Hilker, R.; Klebe, S.; Kloß, M.; Koy, J.; Krause, M.; Kupsch, A.; Lorenz, D.; Lorenzl, S.; Mehdorn, H.M.; Moringlane, J.R.; Oertel, W.; Pinsker, M.O.; Reichmann, H.; Reuß, A.; Schneider, G.H.; Schnitzler, A.; Steude, U.; Sturm, V.; Timmermann, L.; Tronnier, V.; Trottenberg, T.; Wojtecki, L.; Wolf, E.; Poewe, W.; Voges, J. A randomized trial of deep-brain stimulation for Parkinson’s disease. N. Engl. J. Med., 2006, 355(9), 896-908.
[http://dx.doi.org/10.1056/NEJMoa060281] [PMID: 16943402]
[25]
Hitti, F.L.; Ramayya, A.G.; McShane, B.J.; Yang, A.I.; Vaughan, K.A.; Baltuch, G.H. Long-term outcomes following deep brain stimulation for Parkinson’s disease. J. Neurosurg., 2019, 1-6.
[PMID: 30660117]
[26]
Witt, K.; Daniels, C.; Volkmann, J. Factors associated with neuropsychiatric side effects after STN-DBS in Parkinson’s disease. Parkinsonism Relat. Disord., 2012, 18(Suppl. 1), S168-S170.
[http://dx.doi.org/10.1016/S1353-8020(11)70052-9] [PMID: 22166423]
[27]
Sidtis, J.J.; Van Lancker Sidtis, D.; Ramdhani, R.; Tagliati, M. Speech intelligibility during clinical and low frequency. Brain Sci., 2020, 10(1), 26.
[http://dx.doi.org/10.3390/brainsci10010026] [PMID: 31906549]
[28]
Defer, G-L.; Widner, H.; Marié, R-M.; Rémy, P.; Levivier, M. Core assessment program for surgical interventional therapies in Parkinson’s disease (CAPSIT-PD). Mov. Disord., 1999, 14(4), 572-584.
[http://dx.doi.org/10.1002/1531-8257(199907)14:4<572:AID-MDS1005>3.0.CO;2-C] [PMID: 10435493]
[29]
Moro, E.; Allert, N.; Eleopra, R.; Houeto, J.L.; Phan, T.M.; Stoevelaar, H. A decision tool to support appropriate referral for deep brain stimulation in Parkinson’s disease. J. Neurol., 2009, 256(1), 83-88.
[http://dx.doi.org/10.1007/s00415-009-0069-1] [PMID: 19221846]
[30]
Okun, M.S.; Fernandez, H.H.; Pedraza, O.; Misra, M.; Lyons, K.E.; Pahwa, R.; Tarsy, D.; Scollins, L.; Corapi, K.; Friehs, G.M.; Grace, J.; Romrell, J.; Foote, K.D. Development and initial validation of a screening tool for Parkinson disease surgical candidates. Neurology, 2004, 63(1), 161-163.
[http://dx.doi.org/10.1212/01.WNL.0000133122.14824.25] [PMID: 15249630]
[31]
Wächter, T.; Mínguez-Castellanos, A.; Valldeoriola, F.; Herzog, J.; Stoevelaar, H. A tool to improve pre-selection for deep brain stimulation in patients with Parkinson’s disease. J. Neurol., 2011, 258(4), 641-646.
[http://dx.doi.org/10.1007/s00415-010-5814-y] [PMID: 21088849]
[32]
Pal, G.D.; Persinger, V.; Bernard, B.; Ouyang, B.; Goetz, C.G.; Verhagen, M.L. The core assessment program for surgical interventional therapies in parkinson’s disease (CAPSIT-PD): Tolerability of preoperative neuropsychological testing for deep brain stimulation in Parkinson’s disease. Mov. Disord. Clin. Pract. (Hoboken), 2015, 2(4), 379-383.
[http://dx.doi.org/10.1002/mdc3.12213] [PMID: 30363547]
[33]
Artusi, C.A.; Lopiano, L.; Morgante, F. Deep brain stimulation selection criteria for Parkinson’s disease: time to Go beyond CAPSIT-PD. J. Clin. Med., 2020, 9(12), 3931.
[http://dx.doi.org/10.3390/jcm9123931] [PMID: 33291579]
[34]
Anderson, V.C.; Burchiel, K.J.; Hogarth, P.; Favre, J.; Hammerstad, J.P. Pallidal vs. subthalamic nucleus deep brain stimulation in Parkinson disease. Arch. Neurol., 2005, 62(4), 554-560.
[http://dx.doi.org/10.1001/archneur.62.4.554] [PMID: 15824252]
[35]
Xie, C.L.; Shao, B.; Chen, J.; Zhou, Y.; Lin, S.Y.; Wang, W.W. Effects of neurostimulation for advanced Parkinson’s disease patients on motor symptoms: A multiple-treatments meta-analysas of randomized controlled trials. Sci. Rep., 2016, 6(1), 25285.
[http://dx.doi.org/10.1038/srep25285] [PMID: 27142183]
[36]
Mansouri, A.; Taslimi, S.; Badhiwala, J.H.; Witiw, C.D.; Nassiri, F.; Odekerken, V.J.J.; De Bie, R.M.A.; Kalia, S.K.; Hodaie, M.; Munhoz, R.P.; Fasano, A.; Lozano, A.M. Deep brain stimulation for Parkinson’s disease: meta-analysis of results of randomized trials at varying lengths of follow-up. J. Neurosurg., 2018, 128(4), 1199-1213.
[http://dx.doi.org/10.3171/2016.11.JNS16715] [PMID: 28665252]
[37]
Mao, Z.; Ling, Z.; Pan, L.; Xu, X.; Cui, Z.; Liang, S.; Yu, X. Comparison of efficacy of deep brain stimulation of different targets in Parkinson’s disease: a network meta-analysis. Front. Aging Neurosci., 2019, 11, 23.
[http://dx.doi.org/10.3389/fnagi.2019.00023] [PMID: 30853908]
[38]
Liu, Y.; Zhang, L.; Chen, W.; Ling, Y.; Xu, M.; Li, Y.; Yang, C.; Liu, J.; Chen, L.; Jiang, N. Subthalamic nucleus deep brain stimulation improves sleep in Parkinson’s disease patients: a retrospective study and a meta-analysis. Sleep Med., 2020, 74, 301-306.
[http://dx.doi.org/10.1016/j.sleep.2020.07.042] [PMID: 32882663]
[39]
Xu, H.; Zheng, F.; Krischek, B.; Ding, W.; Xiong, C.; Wang, X.; Niu, C. Subthalamic nucleus and globus pallidus internus stimulation for the treatment of Parkinson’s disease: A systematic review. J. Int. Med. Res., 2017, 45(5), 1602-1612.
[http://dx.doi.org/10.1177/0300060517708102] [PMID: 28701061]
[40]
Weaver, F.M.; Follett, K.; Stern, M.; Hur, K.; Harris, C.; Marks, W.J., Jr; Rothlind, J.; Sagher, O.; Reda, D.; Moy, C.S.; Pahwa, R.; Burchiel, K.; Hogarth, P.; Lai, E.C.; Duda, J.E.; Holloway, K.; Samii, A.; Horn, S.; Bronstein, J.; Stoner, G.; Heemskerk, J.; Huang, G.D. Bilateral deep brain stimulation vs. best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA, 2009, 301(1), 63-73.
[http://dx.doi.org/10.1001/jama.2008.929] [PMID: 19126811]
[41]
Weaver, F.M.; Follett, K.A.; Stern, M.; Luo, P.; Harris, C.L.; Hur, K.; Marks, W.J., Jr; Rothlind, J.; Sagher, O.; Moy, C.; Pahwa, R.; Burchiel, K.; Hogarth, P.; Lai, E.C.; Duda, J.E.; Holloway, K.; Samii, A.; Horn, S.; Bronstein, J.M.; Stoner, G.; Starr, P.A.; Simpson, R.; Baltuch, G.; De Salles, A.; Huang, G.D.; Reda, D.J. Randomized trial of deep brain stimulation for Parkinson disease: Thirty-six-month outcomes. Neurology, 2012, 79(1), 55-65.
[http://dx.doi.org/10.1212/WNL.0b013e31825dcdc1] [PMID: 22722632]
[42]
Odekerken, V.J.J.; van Laar, T.; Staal, M.J.; Mosch, A.; Hoffmann, C.F.E.; Nijssen, P.C.G.; Beute, G.N.; van Vugt, J.P.P.; Lenders, M.W.P.M.; Contarino, M.F.; Mink, M.S.J.; Bour, L.J.; van den Munckhof, P.; Schmand, B.A.; de Haan, R.J.; Schuurman, P.R.; de Bie, R.M.A. Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson’s disease (NSTAPS study): a randomised controlled trial. Lancet Neurol., 2013, 12(1), 37-44.
[http://dx.doi.org/10.1016/S1474-4422(12)70264-8] [PMID: 23168021]
[43]
Odekerken, V.J.J.; Boel, J.A.; Schmand, B.A.; de Haan, R.J.; Figee, M.; van den Munckhof, P.; Schuurman, P.R.; de Bie, R.M.A. GPi vs STN deep brain stimulation for Parkinson disease: Three-year follow-up. Neurology, 2016, 86(8), 755-761.
[http://dx.doi.org/10.1212/WNL.0000000000002401] [PMID: 26819458]
[44]
Harati, A.; Müller, T. Neuropsychological effects of deep brain stimulation for Parkinson's disease. Surg. Neurol. Int., 2013, 4(7)(Suppl. 6), 443.
[http://dx.doi.org/10.4103/2152-7806.121637] [PMID: 24349868]
[45]
Obeso, J.A.; Olanow, C.W.; Rodriguez-Oroz, M.C.; Krack, P.; Kumar, R.; Lang, A.E. Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson’s disease. N. Engl. J. Med., 2001, 345(13), 956-963.
[http://dx.doi.org/10.1056/NEJMoa000827] [PMID: 11575287]
[46]
Moro, E.; Lozano, A.M.; Pollak, P.; Agid, Y.; Rehncrona, S.; Volkmann, J.; Kulisevsky, J.; Obeso, J.A.; Albanese, A.; Hariz, M.I.; Quinn, N.P.; Speelman, J.D.; Benabid, A.L.; Fraix, V.; Mendes, A.; Welter, M.L.; Houeto, J.L.; Cornu, P.; Dormont, D.; Tornqvist, A.L.; Ekberg, R.; Schnitzler, A.; Timmermann, L.; Wojtecki, L.; Gironell, A.; Rodriguez-Oroz, M.C.; Guridi, J.; Bentivoglio, A.R.; Contarino, M.F.; Romito, L.; Scerrati, M.; Janssens, M.; Lang, A.E. Long-term results of a multicenter study on subthalamic and pallidal stimulation in Parkinson’s disease. Mov. Disord., 2010, 25(5), 578-586.
[http://dx.doi.org/10.1002/mds.22735] [PMID: 20213817]
[47]
Hamani, C.; Richter, E.O.; Andrade-Souza, Y.; Hutchison, W.; Saint-Cyr, J.A.; Lozano, A.M. Correspondence of microelectrode mapping with magnetic resonance imaging for subthalamic nucleus procedures. Surg. Neurol., 2005, 63(3), 249-253.
[http://dx.doi.org/10.1016/j.surneu.2004.05.036] [PMID: 15734516]
[48]
Schlaier, J.R.; Habermeyer, C.; Janzen, A.; Fellner, C.; Hochreiter, A.; Proescholdt, M.; Brawanski, A.; Lange, M. The influence of intraoperative microelectrode recordings and clinical testing on the location of final stimulation sites in deep brain stimulation for Parkinson’s disease. Acta Neurochir. (Wien), 2013, 155(2), 357-366.
[http://dx.doi.org/10.1007/s00701-012-1592-x] [PMID: 23275071]
[49]
Gross, R.E.; Krack, P.; Rodriguez-Oroz, M.C.; Rezai, A.R.; Benabid, A.L. Electrophysiological mapping for the implantation of deep brain stimulators for Parkinson’s disease and tremor. Mov. Disord., 2006, 21(S14)(Suppl. 14), S259-S283.
[http://dx.doi.org/10.1002/mds.20960] [PMID: 16810720]
[50]
Rolston, J.D.; Englot, D.J.; Starr, P.A.; Larson, P.S. An unexpectedly high rate of revisions and removals in deep brain stimulation surgery: Analysis of multiple databases. Parkinsonism Relat. Disord., 2016, 33, 72-77.
[http://dx.doi.org/10.1016/j.parkreldis.2016.09.014] [PMID: 27645504]
[51]
Ho, A.L.; Ali, R.; Connolly, I.D.; Henderson, J.M.; Dhall, R.; Stein, S.C.; Halpern, C.H. Awake versus asleep deep brain stimulation for Parkinson’s disease: a critical comparison and meta-analysis. J. Neurol. Neurosurg. Psychiatry, 2018, 89(7), 687-691.
[http://dx.doi.org/10.1136/jnnp-2016-314500] [PMID: 28250028]
[52]
Brodsky, M.A.; Anderson, S.; Murchison, C.; Seier, M.; Wilhelm, J.; Vederman, A.; Burchiel, K.J. Clinical outcomes of asleep vs. awake deep brain stimulation for Parkinson disease. Neurology, 2017, 89(19), 1944-1950.
[http://dx.doi.org/10.1212/WNL.0000000000004630] [PMID: 28986415]
[53]
Verhagen Metman, L.; Slavin, K.V.; Rosenow, J.M.; Vitek, J.L.; Munckhof, P. More than just the level of consciousness: comparing asleep and awake deep brain stimulation. Mov. Disord., 2021, 36(12), 2763-2766.
[http://dx.doi.org/10.1002/mds.28806] [PMID: 34585783]
[54]
Patriat, R.; Cooper, S.E.; Duchin, Y.; Niederer, J.; Lenglet, C.; Aman, J.; Park, M.C.; Vitek, J.L.; Harel, N. Individualized tractography-based parcellation of the globus pallidus pars interna using 7T MRI in movement disorder patients prior to DBS surgery. Neuroimage, 2018, 178, 198-209.
[http://dx.doi.org/10.1016/j.neuroimage.2018.05.048] [PMID: 29787868]
[55]
Sweet, J.A.; Walter, B.L.; Gunalan, K.; Chaturvedi, A.; McIntyre, C.C.; Miller, J.P. Fiber tractography of the axonal pathways linking the basal ganglia and cerebellum in Parkinson disease: implications for targeting in deep brain stimulation. J. Neurosurg., 2014, 120(4), 988-996.
[http://dx.doi.org/10.3171/2013.12.JNS131537] [PMID: 24484226]
[56]
Avecillas-Chasin, J.M.; Alonso-Frech, F.; Parras, O.; del Prado, N.; Barcia, J.A. Assessment of a method to determine deep brain stimulation targets using deterministic tractography in a navigation system. Neurosurg. Rev., 2015, 38(4), 739-751.
[http://dx.doi.org/10.1007/s10143-015-0643-1] [PMID: 25962557]
[57]
Muller, J.; Alizadeh, M.; Mohamed, F.B.; Riley, J.; Pearce, J.J.; Trieu, B.; Liang, T.W.; Romo, V.; Sharan, A.; Wu, C. Clinically applicable delineation of the pallidal sensorimotor region in patients with advanced Parkinson’s disease: Study of probabilistic and deterministic tractography. J. Neurosurg., 2018, 1-12.
[PMID: 30554176]
[58]
Cacciola, A.; Milardi, D.; Bertino, S.; Basile, G.A.; Calamuneri, A.; Chillemi, G.; Rizzo, G.; Anastasi, G.; Quartarone, A. Structural connectivity-based topography of the human globus pallidus: Implications for therapeutic targeting in movement disorders. Mov. Disord., 2019, 34(7), 987-996.
[http://dx.doi.org/10.1002/mds.27712] [PMID: 31077436]
[59]
Low, H.L.; Ismail, M.N.M.; Taqvi, A.; Deeb, J.; Fuller, C.; Misbahuddin, A. Comparison of posterior subthalamic area deep brain stimulation for tremor using conventional landmarks versus directly targeting the dentatorubrothalamic tract with tractography. Clin. Neurol. Neurosurg., 2019, 185, 105466.
[http://dx.doi.org/10.1016/j.clineuro.2019.105466] [PMID: 31466022]
[60]
Ranjan, M.; Elias, G.J.B.; Boutet, A.; Zhong, J.; Chu, P.; Germann, J.; Devenyi, G.A.; Chakravarty, M.M.; Fasano, A.; Hynynen, K.; Lipsman, N.; Hamani, C.; Kucharczyk, W.; Schwartz, M.L.; Lozano, A.M.; Hodaie, M. Tractography-based targeting of the ventral intermediate nucleus: accuracy and clinical utility in MRgFUS thalamotomy. J. Neurosurg., 2019, 1-8.
[PMID: 31561221]
[61]
Avecillas-Chasin, J.M.; Alonso-Frech, F.; Nombela, C.; Villanueva, C.; Barcia, J.A. Stimulation of the tractography-defined subthalamic nucleus regions correlates with clinical outcomes. Neurosurgery, 2019, 85(2), E294-E303.
[http://dx.doi.org/10.1093/neuros/nyy633] [PMID: 30690487]
[62]
Hariz, M.I.; Shamsgovara, P.; Johansson, F.; Hariz, G.M.; Fodstad, H. Tolerance and tremor rebound following long-term chronic thalamic stimulation for Parkinsonian and essential tremor. Stereotact. Funct. Neurosurg., 1999, 72(2-4), 208-218.
[http://dx.doi.org/10.1159/000029728] [PMID: 10853080]
[63]
Cury, R.G.; Fraix, V.; Castrioto, A.; Pérez Fernández, M.A.; Krack, P.; Chabardes, S.; Seigneuret, E.; Alho, E.J.L.; Benabid, A.L.; Moro, E. Thalamic deep brain stimulation for tremor in Parkinson disease, essential tremor, and dystonia. Neurology, 2017, 89(13), 1416-1423.
[http://dx.doi.org/10.1212/WNL.0000000000004295] [PMID: 28768840]
[64]
Ondo, W.; Jankovic, J.; Schwartz, K.; Almaguer, M.; Simpson, R.K. Unilateral thalamic deep brain stimulation for refractory essential tremor and Parkinson’s disease tremor. Neurology, 1998, 51(4), 1063-1069.
[http://dx.doi.org/10.1212/WNL.51.4.1063] [PMID: 9781530]
[65]
Akram, H.; Dayal, V.; Mahlknecht, P.; Georgiev, D.; Hyam, J.; Foltynie, T.; Limousin, P.; De Vita, E.; Jahanshahi, M.; Ashburner, J.; Behrens, T.; Hariz, M.; Zrinzo, L. Connectivity derived thalamic segmentation in deep brain stimulation for tremor. Neuroimage Clin., 2018, 18, 130-142.
[http://dx.doi.org/10.1016/j.nicl.2018.01.008] [PMID: 29387530]
[66]
Fukuda, M.; Barnes, A.; Simon, E.S.; Holmes, A.; Dhawan, V.; Giladi, N.; Fodstad, H.; Ma, Y.; Eidelberg, D. Thalamic stimulation for parkinsonian tremor: correlation between regional cerebral blood flow and physiological tremor characteristics. Neuroimage, 2004, 21(2), 608-615.
[http://dx.doi.org/10.1016/j.neuroimage.2003.09.068] [PMID: 14980563]
[67]
Fransson, P.-A.; Nilsson, M.H.; Rehncrona, S.; Tjernström, F.; Magnusson, M.; Johansson, R.; Patel, M. Deep brain stimulation in the subthalamic nuclei alters postural alignment and adaptation in Parkinson’s disease. PLoS One, 2021, 16(12), e0259862.
[http://dx.doi.org/10.1371/journal.pone.0259862] [PMID: 34905546]
[68]
Roediger, J.; Artusi, C.A.; Romagnolo, A.; Boyne, P.; Zibetti, M.; Lopiano, L.; Espay, A.J.; Fasano, A.; Merola, A. Effect of subthalamic deep brain stimulation on posture in Parkinson’s disease: A blind computerized analysis. Parkinsonism Relat. Disord., 2019, 62, 122-127.
[http://dx.doi.org/10.1016/j.parkreldis.2019.01.003] [PMID: 30638820]
[69]
Weiss, D.; Walach, M.; Meisner, C.; Fritz, M.; Scholten, M.; Breit, S.; Plewnia, C.; Bender, B.; Gharabaghi, A.; Wächter, T.; Krüger, R. Nigral stimulation for resistant axial motor impairment in Parkinson’s disease? A randomized controlled trial. Brain, 2013, 136(7), 2098-2108.
[http://dx.doi.org/10.1093/brain/awt122] [PMID: 23757762]
[70]
Horn, M.A.; Gulberti, A.; Hidding, U.; Gerloff, C.; Hamel, W.; Moll, C.K.E.; Pötter-Nerger, M. Comparison of shod and unshod gait in patients with Parkinson’s disease with subthalamic and nigral stimulation. Front. Hum. Neurosci., 2022, 15, 751242.
[http://dx.doi.org/10.3389/fnhum.2021.751242] [PMID: 35095446]
[71]
Nandi, D.; Aziz, T.Z.; Giladi, N.; Winter, J.; Stein, J.F. Reversal of akinesia in experimental parkinsonism by GABA antagonist microinjections in the pedunculopontine nucleus. Brain, 2002, 125(11), 2418-2430.
[http://dx.doi.org/10.1093/brain/awf259] [PMID: 12390969]
[72]
Ferraye, M.U.; Debû, B.; Fraix, V.; Goetz, L.; Ardouin, C.; Yelnik, J.; Henry-Lagrange, C.; Seigneuret, E.; Piallat, B.; Krack, P.; Le Bas, J.F.; Benabid, A.L.; Chabardès, S.; Pollak, P. Effects of pedunculopontine nucleus area stimulation on gait disorders in Parkinson’s disease. Brain, 2010, 133(1), 205-214.
[http://dx.doi.org/10.1093/brain/awp229] [PMID: 19773356]
[73]
Thevathasan, W.; Coyne, T.J.; Hyam, J.A.; Kerr, G.; Jenkinson, N.; Aziz, T.Z.; Silburn, P.A. Pedunculopontine nucleus stimulation improves gait freezing in Parkinson disease. Neurosurgery, 2011, 69(6), 1248-1254.
[http://dx.doi.org/10.1227/NEU.0b013e31822b6f71] [PMID: 21725254]
[74]
Thevathasan, W.; Debu, B.; Aziz, T.; Bloem, B.R.; Blahak, C.; Butson, C.; Czernecki, V.; Foltynie, T.; Fraix, V.; Grabli, D.; Joint, C.; Lozano, A.M.; Okun, M.S.; Ostrem, J.; Pavese, N.; Schrader, C.; Tai, C.H.; Krauss, J.K.; Moro, E. Pedunculopontine nucleus deep brain stimulation in Parkinson’s disease: A clinical review. Mov. Disord., 2018, 33(1), 10-20.
[http://dx.doi.org/10.1002/mds.27098] [PMID: 28960543]
[75]
Yamamoto, T.; Katayama, Y.; Kano, T.; Kobayashi, K.; Oshima, H.; Fukaya, C. Deep brain stimulation for the treatment of parkinsonian, essential, and poststroke tremor: a suitable stimulation method and changes in effective stimulation intensity. J. Neurosurg., 2004, 101(2), 201-209.
[http://dx.doi.org/10.3171/jns.2004.101.2.0201] [PMID: 15309909]
[76]
Mongardi, L.; Rispoli, V.; Scerrati, A.; Giordano, F.; Capone, J.G.; Vaudano, A.E.; De Bonis, P.; Morgante, F.; Picillo, M.; Cavallo, M.A.; Sensi, M. Deep brain stimulation of the ventralis oralis anterior thalamic nucleus is effective for dystonic tremor. Parkinsonism Relat. Disord., 2020, 81, 8-11.
[http://dx.doi.org/10.1016/j.parkreldis.2020.09.040] [PMID: 33035802]
[77]
Alonso-Frech, F.; Fernandez-Garcia, C.; Gómez-Mayordomo, V.; Monje, M.H.G.; Delgado-Suarez, C.; Villanueva-Iza, C.; Catalan-Alonso, M.J. Non-motor adverse effects avoided by directional stimulation in Parkinson’s disease: a case report. Front. Neurol., 2022, 12, 786166.
[http://dx.doi.org/10.3389/fneur.2021.786166] [PMID: 35173666]
[78]
Steigerwald, F.; Müller, L.; Johannes, S.; Matthies, C.; Volkmann, J. Directional deep brain stimulation of the subthalamic nucleus: A pilot study using a novel neurostimulation device. Mov. Disord., 2016, 31(8), 1240-1243.
[http://dx.doi.org/10.1002/mds.26669] [PMID: 27241197]
[79]
Dembek, T.A.; Reker, P.; Visser-Vandewalle, V.; Wirths, J.; Treuer, H.; Klehr, M.; Roediger, J.; Dafsari, H.S.; Barbe, M.T.; Timmermann, L. Directional DBS increases side-effect thresholds-A prospective, double-blind trial. Mov. Disord., 2017, 32(10), 1380-1388.
[http://dx.doi.org/10.1002/mds.27093] [PMID: 28843009]
[80]
Steffen, J.K.; Reker, P.; Mennicken, F.K.; Dembek, T.A.; Dafsari, H.S.; Fink, G.R.; Visser-Vandewalle, V.; Barbe, M.T. Bipolar directional deep brain stimulation in essential and Parkinsonian Tremor. Neuromodulation, 2020, 23(4), 543-549.
[http://dx.doi.org/10.1111/ner.13109] [PMID: 32040883]
[81]
Rammo, R.A.; Ozinga, S.J.; White, A.; Nagel, S.J.; Machado, A.G.; Pallavaram, S.; Cheeran, B.J.; Walter, B.L. Directional Stimulation in Parkinson’s Disease and Essential Tremor: The Cleveland Clinic Experience. Neuromodulation, 2022, 25(6), 829-835.
[http://dx.doi.org/10.1111/ner.13374] [PMID: 33733515]
[82]
Pavese, N.; Tai, Y.F.; Yousif, N.; Nandi, D.; Bain, P.G. Traditional trial and error versus neuroanatomic 3-dimensional image software-assisted deep brain stimulation programming in patients with Parkinson disease. World Neurosurg., 2020, 134, e98-e102.
[http://dx.doi.org/10.1016/j.wneu.2019.09.106] [PMID: 31568905]
[83]
Kluin, K.J.; Mossner, J.M.; Costello, J.T.; Chou, K.L.; Patil, P.G. Motor speech effects in subthalamic deep brain stimulation for Parkinson’s disease. J. Neurosurg., 2022, 137(3), 722-728.
[http://dx.doi.org/10.3171/2021.12.JNS211729] [PMID: 35090126]
[84]
Guidetti, M.; Marceglia, S.; Loh, A.; Harmsen, I.E.; Meoni, S.; Foffani, G.; Lozano, A.M.; Moro, E.; Volkmann, J.; Priori, A. Clinical perspectives of adaptive deep brain stimulation. Brain Stimul., 2021, 14(5), 1238-1247.
[http://dx.doi.org/10.1016/j.brs.2021.07.063] [PMID: 34371211]
[85]
Gagliardo, C.; Ragonese, P.; Iacopino, G.D.; Salemi, G.; Midiri, M.; D’Amelio, M. Transcranial magnetic resonance-guided focused ultrasound thalamotomy as a safe treatment option in multiple sclerosis patients with essential tremor. Neurol. Sci., 2021, 42(3), 1139-1143.
[http://dx.doi.org/10.1007/s10072-020-04841-4] [PMID: 33094429]
[86]
Bond, A.; Dallapiazza, R.; Huss, D.; Warren, A.; Sperling, S.; Gwinn, R. A randomized, sham-controlled trial of transcranial MR guided focused ultrasound thalamotomy trial for the treatment of tremor-dominant, idiopathic Parkinson’s disease. J. Ther. Ultrasound, 2016, 4(1)
[87]
Sperling, S.A.; Shah, B.B.; Barrett, M.J.; Bond, A.E.; Huss, D.S.; Gonzalez, M.J.A.; Elias, W.J. Focused ultrasound thalamotomy in Parkinson disease. Neurology, 2018, 91(14), e1275-e1284.
[http://dx.doi.org/10.1212/WNL.0000000000006279] [PMID: 30158160]
[88]
Martínez-Fernández, R.; Máñez-Miró, J.U.; Rodríguez-Rojas, R.; del Álamo, M.; Shah, B.B.; Hernández-Fernández, F.; Pineda-Pardo, J.A.; Monje, M.H.G.; Fernández-Rodríguez, B.; Sperling, S.A.; Mata-Marín, D.; Guida, P.; Alonso-Frech, F.; Obeso, I.; Gasca-Salas, C.; Vela-Desojo, L.; Elias, W.J.; Obeso, J.A. Randomized trial of focused ultrasound subthalamotomy for Parkinson’s disease. N. Engl. J. Med., 2020, 383(26), 2501-2513.
[http://dx.doi.org/10.1056/NEJMoa2016311] [PMID: 33369354]
[89]
Jung, N.Y.; Park, C.K.; Kim, M.; Lee, P.H.; Sohn, Y.H.; Chang, J.W. The efficacy and limits of magnetic resonance-guided focused ultrasound pallidotomy for Parkinson’s disease: a Phase I clinical trial. J. Neurosurg., 2018, 1-9.
[PMID: 30095337]
[90]
Eisenberg, H.M.; Krishna, V.; Elias, W.J.; Cosgrove, G.R.; Gandhi, D.; Aldrich, C.E.; Fishman, P.S. MR-guided focused ultrasound pallidotomy for Parkinson’s disease: safety and feasibility. J. Neurosurg., 2020, 135(3), 1-7.
[PMID: 33481557]
[91]
de Andrade, E.M.; Ghilardi, M.G.; Cury, R.G.; Barbosa, E.R.; Fuentes, R.; Teixeira, M.J.; Fonoff, E.T. Spinal cord stimulation for Parkinson’s disease: a systematic review. Neurosurg. Rev., 2016, 39(1), 27-35.
[http://dx.doi.org/10.1007/s10143-015-0651-1] [PMID: 26219854]
[92]
Zhou, P.B.; Bao, M. Spinal cord stimulation treatment for freezing of gait in Parkinson’s disease: A case report. Brain Stimul., 2022, 15(1), 76-77.
[http://dx.doi.org/10.1016/j.brs.2021.11.011] [PMID: 34798352]
[93]
Pinto de Souza, C.; Hamani, C.; Oliveira Souza, C.; Lopez Contreras, W.O.; dos Santos Ghilardi, M.G.; Cury, R.G.; Reis Barbosa, E.; Jacobsen Teixeira, M.; Talamoni, F.E. Spinal cord stimulation improves gait in patients with Parkinson’s disease previously treated with deep brain stimulation. Mov. Disord., 2017, 32(2), 278-282.
[http://dx.doi.org/10.1002/mds.26850] [PMID: 27862267]
[94]
Fénelon, G.; Goujon, C.; Gurruchaga, J.M.; Cesaro, P.; Jarraya, B.; Palfi, S.; Lefaucheur, J.P. Spinal cord stimulation for chronic pain improved motor function in a patient with Parkinson’s disease. Parkinsonism Relat. Disord., 2012, 18(2), 213-214.
[http://dx.doi.org/10.1016/j.parkreldis.2011.07.015] [PMID: 21865071]
[95]
Samotus, O.; Parrent, A.; Jog, M. Spinal cord stimulation therapy for gait dysfunction in advanced Parkinson’s disease patients. Mov. Disord., 2018, 33(5), 783-792.
[http://dx.doi.org/10.1002/mds.27299] [PMID: 29442369]
[96]
Prasad, S.; Aguirre-Padilla, D.H.; Poon, Y.Y.; Kalsi-Ryan, S.; Lozano, A.M.; Fasano, A. Spinal cord stimulation for very advanced Parkinson’s disease: a 1-year prospective trial. Mov. Disord., 2020, 35(6), 1082-1083.
[http://dx.doi.org/10.1002/mds.28065] [PMID: 32311155]
[97]
Hvingelby, V.S.; Højholt Terkelsen, M.; Johnsen, E.L.; Møller, M.; Danielsen, E.H.; Henriksen, T.; Glud, A.N.; Tai, Y.; Møller Andersen, A.S.; Meier, K.; Borghammer, P.; Moro, E.; Sørensen, J.C.H.; Pavese, N. Spinal cord stimulation therapy for patients with Parkinson’s disease and gait problems (STEP-PD): Study protocol for an exploratory, double-blind, randomised, placebo-controlled feasibility trial. BMJ Neurology Open, 2022, 4(2), e000333.
[http://dx.doi.org/10.1136/bmjno-2022-000333] [PMID: 36101543]

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