Deep brain stimulation of the subthalamic nucleus in severe Parkinson's disease: relationships between dual-contact topographic setting and 1-year worsening of speech and gait.
DBS
Gait
Parkinson’s disease
STN
Speech
Symmetry
Journal
Acta neurochirurgica
ISSN: 0942-0940
Titre abrégé: Acta Neurochir (Wien)
Pays: Austria
ID NLM: 0151000
Informations de publication
Date de publication:
27 Oct 2023
27 Oct 2023
Historique:
received:
17
01
2023
accepted:
24
06
2023
medline:
27
10
2023
pubmed:
27
10
2023
entrez:
27
10
2023
Statut:
aheadofprint
Résumé
Subthalamic nucleus (STN) deep brain stimulation (DBS) alleviates severe motor fluctuations and dyskinesia in Parkinson's disease, but may result in speech and gait disorders. Among the suspected or demonstrated causes of these adverse effects, we focused on the topography of contact balance (CB; individual, right and left relative dual positions), a scantly studied topic, analyzing the relationships between symmetric or non-symmetric settings, and the worsening of these signs. An observational monocentric study was conducted on a series of 92 patients after ethical approval. CB was specified by longitudinal and transversal positions and relation to the STN (CB sub-aspects) and totalized at the patient level (patient CB). CB was deemed symmetric when the two contacts were at the same locations relative to the STN. CB was deemed asymmetric when at least one sub-aspect differed in the patient CB. Baseline and 1-year characteristics were routinely collected: (i) general, namely, Unified Parkinson's Disease Rating Scores (UPDRS), II, III motor and IV, daily levodopa equivalent doses, and Parkinson's Disease Questionnaire of Quality of Life (PDQ39) scores; (ii) specific, namely scores for speech (II-5 and III-18) and axial signs (II-14, III-28, III-29, and III-30). Only significant correlations were considered (p < 0.05). Baseline characteristics were comparable (symmetric versus asymmetric). CB settings were related to deteriorations of speech and axial signs: communication PDQ39 and UPDRS speech and gait scores worsened exclusively with symmetric settings; the most influential CB sub-aspect was symmetric longitudinal position. Our findings suggest that avoiding symmetric CB settings, whether by electrode positioning or shaping of electric fields, could reduce worsening of speech and gait.
Sections du résumé
BACKGROUND
BACKGROUND
Subthalamic nucleus (STN) deep brain stimulation (DBS) alleviates severe motor fluctuations and dyskinesia in Parkinson's disease, but may result in speech and gait disorders. Among the suspected or demonstrated causes of these adverse effects, we focused on the topography of contact balance (CB; individual, right and left relative dual positions), a scantly studied topic, analyzing the relationships between symmetric or non-symmetric settings, and the worsening of these signs.
METHOD
METHODS
An observational monocentric study was conducted on a series of 92 patients after ethical approval. CB was specified by longitudinal and transversal positions and relation to the STN (CB sub-aspects) and totalized at the patient level (patient CB). CB was deemed symmetric when the two contacts were at the same locations relative to the STN. CB was deemed asymmetric when at least one sub-aspect differed in the patient CB. Baseline and 1-year characteristics were routinely collected: (i) general, namely, Unified Parkinson's Disease Rating Scores (UPDRS), II, III motor and IV, daily levodopa equivalent doses, and Parkinson's Disease Questionnaire of Quality of Life (PDQ39) scores; (ii) specific, namely scores for speech (II-5 and III-18) and axial signs (II-14, III-28, III-29, and III-30). Only significant correlations were considered (p < 0.05).
RESULTS
RESULTS
Baseline characteristics were comparable (symmetric versus asymmetric). CB settings were related to deteriorations of speech and axial signs: communication PDQ39 and UPDRS speech and gait scores worsened exclusively with symmetric settings; the most influential CB sub-aspect was symmetric longitudinal position.
CONCLUSION
CONCLUSIONS
Our findings suggest that avoiding symmetric CB settings, whether by electrode positioning or shaping of electric fields, could reduce worsening of speech and gait.
Identifiants
pubmed: 37889334
doi: 10.1007/s00701-023-05843-9
pii: 10.1007/s00701-023-05843-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.
Références
Aldridge D, Theodoros D, Angwin A, Vogel AP (2016) Speech outcomes in Parkinson’s disease after subthalamic nucleus deep brain stimulation: a systematic review. Parkinsonism Relat Disord 33:3–11
pubmed: 27693195
doi: 10.1016/j.parkreldis.2016.09.022
Alvarez L (2005) Bilateral subthalamotomy in Parkinson’s disease: initial and long-term response. Brain 128(3):570–583
pubmed: 15689366
doi: 10.1093/brain/awh397
Antonini A, Moro E, Godeiro C, Reichmann H (2018) Medical and surgical management of advanced Parkinson’s disease. Mov Disord 33(6):900–908
pubmed: 29570862
doi: 10.1002/mds.27340
Askari A, Greif TR, Lam J, Maher AC, Persad CC, Patil PG (2022) Decline of verbal fluency with lateral superior frontal gyrus penetration in subthalamic nucleus deep brain stimulation for Parkinson disease. J Neurosurg 137(3):729–734
doi: 10.3171/2021.11.JNS211528
Barbe MT, Tonder L, Krack P et al (2020) Deep brain stimulation for freezing of gait in Parkinson’s disease with early motor complications. Mov Disord 35(1):82–90
pubmed: 31755599
doi: 10.1002/mds.27892
Bender R, Lange S (2001) Adjusting for multiple testing—when and how? J Clin Epidemiol 54(4):343–349
pubmed: 11297884
doi: 10.1016/S0895-4356(00)00314-0
Bohnen NI, Yarnall AJ, Weil RS, Moro E, Moehle MS, Borghammer P, Bedard M-A, Albin RL (2022) Cholinergic system changes in Parkinson’s disease: emerging therapeutic approaches. Lancet Neurol 21(4):381–392
pubmed: 35131038
pmcid: 8985079
doi: 10.1016/S1474-4422(21)00377-X
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 97(3):1212–1246
doi: 10.1212/WNL.0000000000012246
Bruno S, Nikolov P, Hartmann CJ, Trenado C, Slotty PJ, Vesper J, Schnitzler A, Groiss SJ (2021) Directional deep brain stimulation of the thalamic ventral intermediate area for essential tremor increases therapeutic window. Neuromodulation 24(2):343–352
pubmed: 32666569
doi: 10.1111/ner.13234
Butson CR, Cooper SE, Henderson JM, McIntyre CC (2007) Patient-specific analysis of the volume of tissue activated during deep brain stimulation. Neuroimage 34(2):661–670
pubmed: 17113789
doi: 10.1016/j.neuroimage.2006.09.034
Büttner C, Maack M, Janitzky K, Witt K (2019) The evolution of quality of life after subthalamic stimulation for Parkinson’s disease: a meta-analysis. Mov Disord Clin Pract 6(7):521–530
pubmed: 31538085
pmcid: 6749804
doi: 10.1002/mdc3.12819
Cavallieri F, Budriesi C, Gessani A, Contardi S, Fioravanti V, Menozzi E, Pinto S, Moro E, Valzania F, Antonelli F (2021) Dopaminergic treatment effects on dysarthric speech: acoustic analysis in a cohort of patients with advanced Parkinson’s disease. Front Neurol 11(Article 616062):1–7
Chen CC, Brücke C, Kempf F, Kupsch A, Lu CS, Lee ST, Tisch S, Limousin P, Hariz M, Brown P (2006) Deep brain stimulation of the subthalamic nucleus: a two-edged sword. Curr Biol 16(22):R952–R953
pubmed: 17113373
doi: 10.1016/j.cub.2006.10.013
Chenausky K, MacAuslan J, Goldhor R (2011) Acoustic analysis of PD speech. Parkinsons Dis 2011:1–13
doi: 10.4061/2011/435232
Chung SJ, Jeon SR, Kim SR, Sung YH, Lee MC (2006) Bilateral effects of unilateral subthalamic nucleus deep brain stimulation in advanced Parkinson’s disease. Eur Neurol 56(2):127–132
pubmed: 16960454
doi: 10.1159/000095704
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. Neurophysiologie Clinique/Clin Neurophysiol 45(4–5):371–388
doi: 10.1016/j.neucli.2015.07.001
Coste J, Ouchchane L, Sarry L, Derost P, Durif F, Gabrillargues J, Hemm S, Lemaire JJ (2009) New electrophysiological mapping combined with MRI in Parkinsonian’s subthalamic region. Eur J Neurosci 29(8):1627–1633
pubmed: 19419425
doi: 10.1111/j.1460-9568.2009.06698.x
De Bie RMA, Schuurman PR, Esselink RAJ, Bosch DA, Speelman JD (2002) Bilateral pallidotomy in Parkinson’s disease: a retrospective study. Mov Disord 17(3):533–538
pubmed: 12112203
doi: 10.1002/mds.10090
de Chazeron I, Pereira B, Chereau-Boudet I, Durif F, Lemaire JJ, Brousse G, Ulla M, Derost P, Debilly B, Llorca PM (2016) Impact of localisation of deep brain stimulation electrodes on motor and neurobehavioural outcomes in Parkinson’s disease. J Neurol Neurosurg Psychiatr 87(7):758–766
doi: 10.1136/jnnp-2015-310953
de Roquemaurel A, Wirth T, Vijiaratnam N, Ferreira F, Zrinzo L, Akram H, Foltynie T, Limousin P (2021) Stimulation sweet spot in subthalamic deep brain stimulation – myth or reality? A critical review of literature. Stereotact Funct Neurosurg 99(5):425–442
pubmed: 34120117
doi: 10.1159/000516098
Derost P-P, Ouchchane L, Morand D, Ulla M, Llorca P-M, Barget M, Debilly B, Lemaire J-J, Durif F (2007) Is DBS-STN appropriate to treat severe Parkinson disease in an elderly population? Neurology 68(17):1345–1355
pubmed: 17452578
doi: 10.1212/01.wnl.0000260059.77107.c2
Fabbri M, Guimarães I, Cardoso R et al (2017) Speech and voice response to a levodopa challenge in late-stage Parkinson’s disease. Front Neurol 8(Article 432):1–7
Feise RJ (2002) Do multiple outcome measures require p-value adjustment? BMC Med Res Methodol 2(1):8
pubmed: 12069695
pmcid: 117123
doi: 10.1186/1471-2288-2-8
Fenoy AJ, McHenry MA, Schiess MC (2017) Speech changes induced by deep brain stimulation of the subthalamic nucleus in Parkinson disease: involvement of the dentatorubrothalamic tract. J Neurosurg 126(6):2017–2027
pubmed: 27611200
doi: 10.3171/2016.5.JNS16243
Florence G, Sameshima K, Fonoff ET, Hamani C (2016) Deep brain stimulation: more complex than the inhibition of cells and excitation of fibers. Neuroscientist 22(4):332–345
pubmed: 26150316
doi: 10.1177/1073858415591964
Fluchere F, Witjas T, Eusebio A, Bruder N, Giorgi R, Leveque M, Peragut J-C, Azulay J-P, Regis J (2014) Controlled general anaesthesia for subthalamic nucleus stimulation in Parkinson’s disease. J Neurol Neurosurg Psychiatry 85(10):1167–1173
pubmed: 24249783
doi: 10.1136/jnnp-2013-305323
Follett KA, Weaver FM, Stern M et al (2010) Pallidal versus subthalamic deep-brain stimulation for Parkinson’s disease. N Engl J Med 362(22):2077–2091
pubmed: 20519680
doi: 10.1056/NEJMoa0907083
Fox SH, Katzenschlager R, Lim S-Y, Barton B, de Bie RMA, Seppi K, Coelho M, Sampaio C (2018) International Parkinson and movement disorder society evidence-based medicine review: update on treatments for the motor symptoms of Parkinson’s disease. Mov Disord 33(8):1248–1266
pubmed: 29570866
doi: 10.1002/mds.27372
Fraix V, Houeto J-L, Lagrange C et al (2006) Clinical and economic results of bilateral subthalamic nucleus stimulation in Parkinson’s disease. J Neurol Neurosurg Psychiatr 77(4):443–449
doi: 10.1136/jnnp.2005.077677
Garcia-Garcia D, Guridi J, Toledo JB, Alegre M, Obeso JA, Rodríguez-Oroz MC (2016) Stimulation sites in the subthalamic nucleus and clinical improvement in Parkinson’s disease: a new approach for active contact localization. J Neurosurg 1–12
Gonzalezballester M (2002) Estimation of the partial volume effect in MRI. Med Image Anal 6(4):389–405
doi: 10.1016/S1361-8415(02)00061-0
Gonzalez-Escamilla G, Koirala N, Bange M, Glaser M, Pintea B, Dresel C, Deuschl G, Muthuraman M, Groppa S (2022) Deciphering the network effects of deep brain stimulation in Parkinson’s disease. Neurol Ther 11:265–282
pubmed: 35000133
pmcid: 8857357
doi: 10.1007/s40120-021-00318-4
Guiot G, Derome P, Trigo JC (1967) Intention tremor: the best indication for stereotaxic surgery. Presse Med 75(49):2513–2518
Harmsen IE, Elias GJB, Beyn ME, Boutet A, Pancholi A, Germann J, Mansouri A, Lozano CS, Lozano AM (2020) Clinical trials for deep brain stimulation: current state of affairs. Brain Stimul 13(2):378–385
pubmed: 31786180
doi: 10.1016/j.brs.2019.11.008
Haynes WIA, Haber SN (2013) The organization of prefrontal-subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: implications for Basal Ganglia models and deep brain stimulation. J Neurosci 33(11):4804–4814
pubmed: 23486951
pmcid: 3755746
doi: 10.1523/JNEUROSCI.4674-12.2013
Hemm S, Coste J, Gabrillargues J et al (2009) Contact position analysis of deep brain stimulation electrodes on post-operative CT images. Acta Neurochir (Wien) 151(7):823–829 (discussion 829)
pubmed: 19444372
doi: 10.1007/s00701-009-0393-3
Holiga Š, Mueller K, Möller HE, Urgošík D, Růžička E, Schroeter ML, Jech R (2015) Resting-state functional magnetic resonance imaging of the subthalamic microlesion and stimulation effects in Parkinson’s disease: Indications of a principal role of the brainstem. Neuroimage Clin 9:264–274
pubmed: 26509113
pmcid: 4576412
doi: 10.1016/j.nicl.2015.08.008
Huang L-C, Chen L-G, Wu P-A, Pang C-Y, Lin S-Z, Tsai S-T, Chen S-Y (2022) Effect of deep brain stimulation on brain network and white matter integrity in Parkinson’s disease. CNS Neurosci Ther 28(1):92–104
pubmed: 34643338
doi: 10.1111/cns.13741
Jiang J-L, Chen S-Y, Tsai S-T (2019) Quality of life in patients with Parkinson’s disease after subthalamic stimulation: an observational cohort study for outcome prediction. Ci Ji Yi Xue Za Zhi 31(2):107–112
pubmed: 31007491
Jourdain VA, Schechtmann G, Di Paolo T (2014) Subthalamotomy in the treatment of Parkinson’s disease: clinical aspects and mechanisms of action. J Neurosurg 120(1):140–151
pubmed: 24205909
doi: 10.3171/2013.10.JNS13332
Karachi C, Yelnik J, Tandé D, Tremblay L, Hirsch EC, François C (2005) The pallidosubthalamic projection: an anatomical substrate for nonmotor functions of the subthalamic nucleus in primates. Mov Disord 20(2):172–180
pubmed: 15382210
doi: 10.1002/mds.20302
Kim MJ, Chang KW, Park SH, Chang WS, Jung HH, Chang JW (2021) Stimulation-induced side effects of deep brain stimulation in the ventralis intermedius and posterior subthalamic area for essential tremor. Front Neurol 12:678592
pubmed: 34177784
pmcid: 8220085
doi: 10.3389/fneur.2021.678592
Kim R, Kim H-J, Shin C, Park H, Kim A, Paek SH, Jeon B (2019) Long-term effect of subthalamic nucleus deep brain stimulation on freezing of gait in Parkinson’s disease. J Neurosurg 131(6):1797–1804
pubmed: 30641837
doi: 10.3171/2018.8.JNS18350
Kluin KJ, Mossner JM, Costello JT, Chou KL, Patil PG (2022) Motor speech effects in subthalamic deep brain stimulation for Parkinson’s disease. J Neurosurg 137(3):722–728
doi: 10.3171/2021.12.JNS211729
Knight EJ, Testini P, Min H-K et al (2015) Motor and nonmotor circuitry activation induced by subthalamic nucleus deep brain stimulation in patients with Parkinson disease: intraoperative functional magnetic resonance imaging for deep brain stimulation. Mayo Clin Proc 90(6):773–785
pubmed: 26046412
doi: 10.1016/j.mayocp.2015.03.022
Knowles T, Adams SG, Jog M (2021) Speech rate mediated vowel and stop voicing distinctiveness in Parkinson’s disease. J Speech Lang Hear Res 64(11):4096–4123
pubmed: 34582276
doi: 10.1044/2021_JSLHR-21-00160
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(20):1925–1934
pubmed: 14614167
doi: 10.1056/NEJMoa035275
Lemaire J-J, Coste J, Ouchchane L et al (2007) Brain mapping in stereotactic surgery: a brief overview from the probabilistic targeting to the patient-based anatomic mapping. Neuroimage 37(Suppl 1):S109-115
pubmed: 17644002
doi: 10.1016/j.neuroimage.2007.05.055
Lemaire J-J, De Salles A, Coll G, El Ouadih Y, Chaix R, Coste J, Durif F, Makris N, Kikinis R (2019) MRI atlas of the human deep brain. Front Neurol. https://doi.org/10.3389/fneur.2019.00851
doi: 10.3389/fneur.2019.00851
pubmed: 31507507
pmcid: 6718608
Lemaire J-J, Pereira B, Derost P et al (2016) Subthalamus stimulation in Parkinson disease: Accounting for the bilaterality of contacts. Surg Neurol Int 7(Suppl 35):S837–S847
pubmed: 27990316
pmcid: 5134117
doi: 10.4103/2152-7806.194066
Lemaire J, Sakka L, Ouchchane L, Caire F, Gabrillargues J, Bonny J (2010) Anatomy of the human thalamus based on spontaneous contrast and microscopic voxels in high-field magnetic resonance imaging. Neurosurgery 66(3 Suppl Operative):161–172
pubmed: 20173566
Lezcano E, Gómez-Esteban JC, Tijero B et al (2016) Long-term impact on quality of life of subthalamic nucleus stimulation in Parkinson’s disease. J Neurol 263(5):895–905
pubmed: 26964542
doi: 10.1007/s00415-016-8077-4
Lhommée E, Wojtecki L, Czernecki V et al (2018) Behavioural outcomes of subthalamic stimulation and medical therapy versus medical therapy alone for Parkinson’s disease with early motor complications (EARLYSTIM trial): secondary analysis of an open-label randomised trial. Lancet Neurol 17(3):223–231
pubmed: 29452685
doi: 10.1016/S1474-4422(18)30035-8
Limousin P, Foltynie T (2019) Long-term outcomes of deep brain stimulation in Parkinson disease. Nat Rev Neurol 15(4):234–242
pubmed: 30778210
doi: 10.1038/s41582-019-0145-9
Lin Z, Zhang C, Li D, Sun B (2021) Lateralized effects of deep brain stimulation in Parkinson’s disease: evidence and controversies. npj Parkinsons Dis 7(1):64
pubmed: 34294724
pmcid: 8298477
doi: 10.1038/s41531-021-00209-3
Lizarraga KJ, Jagid JR, Luca CC (2016) Comparative effects of unilateral and bilateral subthalamic nucleus deep brain stimulation on gait kinematics in Parkinson’s disease: a randomized, blinded study. J Neurol 263(8):1652–1656
pubmed: 27278062
doi: 10.1007/s00415-016-8191-3
Lozano AM, Lipsman N, Bergman H et al (2019) Deep brain stimulation: current challenges and future directions. Nat Rev Neurol 15(3):148–160
pubmed: 30683913
pmcid: 6397644
doi: 10.1038/s41582-018-0128-2
Mueller K, Jech R, Růžička F et al (2018) Brain connectivity changes when comparing effects of subthalamic deep brain stimulation with levodopa treatment in Parkinson’s disease. Neuroimage Clin 19:1025–1035
pubmed: 30035027
pmcid: 6051673
doi: 10.1016/j.nicl.2018.05.006
Ni Z, Kim SJ, Phielipp N et al (2018) Pallidal deep brain stimulation modulates cortical excitability and plasticity. Ann Neurol 83(2):352–362
pubmed: 29369401
doi: 10.1002/ana.25156
Obeso JA, Rodríguez-Oroz MC, Benitez-Temino B, Blesa FJ, Guridi J, Marin C, Rodriguez M (2008) Functional organization of the basal ganglia: therapeutic implications for Parkinson’s disease. Mov Disord 23(Suppl 3):S548-559
pubmed: 18781672
doi: 10.1002/mds.22062
Okun MS, Gallo BV, Mandybur G et al (2012) Subthalamic deep brain stimulation with a constant-current device in Parkinson’s disease: an open-label randomised controlled trial. Lancet Neurol 11(2):140–149
pubmed: 22239915
doi: 10.1016/S1474-4422(11)70308-8
Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev 20(1):91–127
pubmed: 7711769
doi: 10.1016/0165-0173(94)00007-C
Pieruccini-Faria F, Ehgoetz Martens K, Silveira C, Jones J (2015) Side of basal ganglia degeneration influences freezing of gait in Parkinson’s disease. Behav Neurosci 129(2):214–218
pubmed: 25730121
doi: 10.1037/bne0000039
Piña-Fuentes D, van Dijk JMC, van Zijl JC, Moes HR, van Laar T, Oterdoom DLM, Little S, Brown P, Beudel M (2020) Acute effects of adaptive deep brain stimulation in Parkinson’s disease. Brain Stimul 13(6):1507–1516
pubmed: 32738409
pmcid: 7116216
doi: 10.1016/j.brs.2020.07.016
Prenger MTM, Madray R, Van Hedger K, Anello M, MacDonald PA (2020) Social symptoms of Parkinson’s disease. Parkinsons Dis 2020:1–10
doi: 10.1155/2020/8846544
Prent N, Potters WV, Boon LI, Caan MWA, de Bie RMA, van den Munckhof P, Schuurman PR, van Rootselaar A-F (2019) Distance to white matter tracts is associated with deep brain stimulation motor outcome in Parkinson’s disease. J Neurosurg 133(2):433–442
doi: 10.3171/2019.5.JNS1952
Rodriguez-Rojas R, Pineda-Pardo JA, Mañez-Miro J, Sanchez-Turel A, Martinez-Fernandez R, Del Alamo M, DeLong M, Obeso JA (2022) Functional topography of the human subthalamic nucleus: relevance for subthalamotomy in Parkinson’s disease. Mov Disord 37(2):279–290
pubmed: 34859498
doi: 10.1002/mds.28862
Rossi M, Bruno V, Arena J, Cammarota Á, Merello M (2018) Challenges in PD patient management after DBS: a pragmatic review. Mov Disord Clin Pract 5(3):246–254
pubmed: 30363375
pmcid: 6174419
doi: 10.1002/mdc3.12592
Rothman KJ (1990) No adjustments are needed for multiple comparisons. Epidemiology 1(1):43–46
pubmed: 2081237
doi: 10.1097/00001648-199001000-00010
Sandström L, Hägglund P, Johansson L, Blomstedt P, Karlsson F (2015) Speech intelligibility in Parkinson’s disease patients with zona incerta deep brain stimulation. Brain Behav 5(10):e00394
pubmed: 26516614
pmcid: 4614054
doi: 10.1002/brb3.394
Sanger TD (2018) A computational model of deep-brain stimulation for acquired dystonia in children. Front Comput Neurosci 12:77
pubmed: 30294268
pmcid: 6158364
doi: 10.3389/fncom.2018.00077
Schnitzler A, Mir P, Brodsky MA et al (2022) Directional deep brain stimulation for Parkinson’s disease: results of an international crossover study with randomized, double-blind primary endpoint. Neuromodulation: Technol Neural Interface 25(6):817–828
doi: 10.1111/ner.13407
Schuepbach WMM, Rau J, Knudsen K et al (2013) Neurostimulation for Parkinson’s disease with early motor complications. N Engl J Med 368(7):610–622
pubmed: 23406026
doi: 10.1056/NEJMoa1205158
Shen L, Jiang C, Hubbard CS et al (2020) Subthalamic nucleus deep brain stimulation modulates 2 distinct neurocircuits. Ann Neurol 88(6):1178–1193
pubmed: 32951262
pmcid: 8087166
doi: 10.1002/ana.25906
Stefani A, Cerroni R, Mazzone P, Liguori C, Di Giovanni G, Pierantozzi M, Galati S (2019) Mechanisms of action underlying the efficacy of deep brain stimulation of the subthalamic nucleus in Parkinson’s disease: central role of disease severity. Eur J Neurosci 49(6):805–816
pubmed: 30044030
doi: 10.1111/ejn.14088
Strotzer QD, Kohl Z, Anthofer JM, Faltermeier R, Schmidt NO, Torka E, Greenlee MW, Fellner C, Schlaier JR, Beer AL (2022) Structural connectivity patterns of side effects induced by subthalamic deep brain stimulation for Parkinson’s disease. Brain Connect 12:brain.2021.0051
doi: 10.1089/brain.2021.0051
Tanaka Y, Tsuboi T, Watanabe H et al (2020) Longitudinal speech change after subthalamic nucleus deep brain stimulation in Parkinson’s disease patients: a 2-year prospective study. J Parkinsons Dis 10(1):131–140
pubmed: 31884493
doi: 10.3233/JPD-191798
Thobois S, Ardouin C, Lhommee E et al (2010) Non-motor dopamine withdrawal syndrome after surgery for Parkinson’s disease: predictors and underlying mesolimbic denervation. Brain 133(4):1111–1127
pubmed: 20237128
doi: 10.1093/brain/awq032
Timmermann L, Jain R, Chen L et al (2015) Multiple-source current steering in subthalamic nucleus deep brain stimulation for Parkinson’s disease (the VANTAGE study): a non-randomised, prospective, multicentre, open-label study. Lancet Neurol 14(7):693–701
pubmed: 26027940
doi: 10.1016/S1474-4422(15)00087-3
Tir M, Devos D, Blond S et al (2007) Exhaustive, one-year follow-up of subthalamic nucleus deep brain stimulation in a large, single-center cohort of Parkinsonian patients. Neurosurgery 61(2):297–304 (discussion 304-305)
pubmed: 17762742
doi: 10.1227/01.NEU.0000307964.21298.FD
Tripoliti E, Limousin P, Foltynie T, Candelario J, Aviles-Olmos I, Hariz MI, Zrinzo L (2014) Predictive factors of speech intelligibility following subthalamic nucleus stimulation in consecutive patients with Parkinson’s disease: speech intelligibility after STN-DBS. Mov Disord 29(4):532–538
pubmed: 24532491
pmcid: 8759591
doi: 10.1002/mds.25816
Tripoliti E, Zrinzo L, Martinez-Torres I et al (2011) Effects of subthalamic stimulation on speech of consecutive patients with Parkinson disease. Neurology 76(1):80–86
pubmed: 21068426
doi: 10.1212/WNL.0b013e318203e7d0
van Hartevelt TJ, Cabral J, Deco G, Møller A, Green AL, Aziz TZ, Kringelbach ML (2014) Neural plasticity in human brain connectivity: the effects of long term deep brain stimulation of the subthalamic nucleus in Parkinson’s disease. PLoS ONE 9(1):e86496
pubmed: 24466120
pmcid: 3899266
doi: 10.1371/journal.pone.0086496
Vizcarra JA, Situ-Kcomt M, Artusi CA, Duker AP, Lopiano L, Okun MS, Espay AJ, Merola A (2019) Subthalamic deep brain stimulation and levodopa in Parkinson’s disease: a meta-analysis of combined effects. J Neurol 266(2):289–297
pubmed: 29909467
doi: 10.1007/s00415-018-8936-2
Vu TC, Nutt JG, Holford NHG (2012) Progression of motor and nonmotor features of Parkinson’s disease and their response to treatment. Br J Clin Pharmacol 74(2):267–283
pubmed: 22283961
pmcid: 3630747
doi: 10.1111/j.1365-2125.2012.04192.x
Wang J-W, Zhang Y-Q, Zhang X-H, Wang Y-P, Li J-P, Li Y-J (2017) Deep brain stimulation of pedunculopontine nucleus for postural instability and gait disorder after Parkinson disease: a meta-analysis of individual patient data. World Neurosurg 102:72–78
pubmed: 28279773
doi: 10.1016/j.wneu.2017.02.110
Weintraub D, Duda JE, Carlson K, Luo P, Sagher O, Stern M, Follett KA, Reda D, Weaver FM (2013) Suicide ideation and behaviours after STN and GPi DBS surgery for Parkinson’s disease: results from a randomised, controlled trial. J Neurol Neurosurg Psychiatry 84(10):1113–1118
pubmed: 23667214
doi: 10.1136/jnnp-2012-304396
Welter M-L, Schüpbach M, Czernecki V et al (2014) Optimal target localization for subthalamic stimulation in patients with Parkinson disease. Neurology 82(15):1352–1361
pubmed: 24647024
pmcid: 4001189
doi: 10.1212/WNL.0000000000000315
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):581–591
pubmed: 20434403
pmcid: 2874872
doi: 10.1016/S1474-4422(10)70093-4
Witt K, Granert O, Daniels C, Volkmann J, Falk D, van Eimeren T, Deuschl G (2013) Relation of lead trajectory and electrode position to neuropsychological outcomes of subthalamic neurostimulation in Parkinson’s disease: results from a randomized trial. Brain 136(Pt 7):2109–2119
pubmed: 23801735
doi: 10.1093/brain/awt151
Xie T, Kang UJ, Warnke P (2012) Effect of stimulation frequency on immediate freezing of gait in newly activated STN DBS in Parkinson’s disease. J Neurol Neurosurg Psychiatry 83(10):1015–1017
pubmed: 22696586
doi: 10.1136/jnnp-2011-302091
Yamamoto T, Uchiyama T, Higuchi Y, Asahina M, Hirano S, Yamanaka Y, Weibing L, Kuwabara S (2017) Long term follow-up on quality of life and its relationship to motor and cognitive functions in Parkinson’s disease after deep brain stimulation. J Neurol Sci 379:18–21
pubmed: 28716237
doi: 10.1016/j.jns.2017.05.037
Zerroug A, Gabrillargues J, Coll G et al (2016) Personalized mapping of the deep brain with a white matter attenuated inversion recovery (WAIR) sequence at 1.5-tesla: experience based on a series of 156 patients. Neurochirurgie 62(4):183–9
pubmed: 27236731
doi: 10.1016/j.neuchi.2016.01.009