Abstract
Background
Parkinson’s disease (PD) is the second most common neurodegenerative disorder, affecting both motor and non-motor systems. Deep brain stimulation of the subthalamic nucleus (STN-DBS) has been an approved treatment for PD for more than 30 years, but few data are available regarding its long-term effectiveness.
Objective
The aim of this study is to evaluate patients’ outcome, both from a motor and non-motor perspective, 9 to 14 years after DBS implantation. We have investigated patients with advanced PD and treated with STN-DBS, in relation to key clinical features of PD.
Methods
18 patients were assessed both retrospectively and prospectively. They underwent motor examination, neuropsychological evaluation and questionnaires on the quality of life, preoperatively, as well as 1, 9 and 14 years after DBS surgery. All patients were implanted with STN-DBS at San Raffaele Hospital between 2004 and 2010.
Results
13 males and five females underwent DBS implantation with a mean PD duration of 11 years. Stimulation significantly improved med-off/stim-on condition up to 9 years, compared to the preoperative off state, and med-on/stim-on condition at 14 years, compared to med-on/stim-off state. Long term improvement specifically involved tremor and rigidity, as well as dopaminergic daily dose. At the same time, STN-DBS had no long-lasting effect on axial symptoms and cognitive functions.
Conclusions
STN-DBS remains an effective therapy for advanced PD, also over the years. Despite the underlying progression of the disease, this treatment extends the period in which the overall quality of life is still acceptable.
Similar content being viewed by others
Availability of data and material
Data and material are available on request.
References
Romito LM, Contarino MF, Vanacore N, Bentivoglio AR, Scerrati M, Albanese A (2009) Replacement of dopaminergic medication with subthalamic nucleus stimulation in Parkinson’s disease: long-term observation. Mov Disord 24:555–561. https://doi.org/10.1002/mds.22390
Witt K, Daniels C, Reiff J, Krack P, Volkmann J, Pinsker MO, Krause M, Tronnier V, Kloss M, Schnitzler A, Wojtecki L, Bötzel K, Danek A, Hilker R, Sturm V, Kupsch A, Karner E, Deuschl G (2008) Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson’s disease: a randomised, multicentre study. Lancet Neurol 7:605–614. https://doi.org/10.1016/S1474-4422(08)70114-5
Miocinovic S, Somayajula S, Chitnis S, Vitek JL (2013) History, applications, and mechanisms of deep brain stimulation. JAMA Neurol 70:163. https://doi.org/10.1001/2013.jamaneurol.45
Castrioto A, Lozano AM, Poon Y-Y, Lang AE, Fallis M, Moro E (2011) Ten-year outcome of subthalamic stimulation in parkinson disease. Arch Neurol 68:1550. https://doi.org/10.1001/archneurol.2011.182
Rizzone MG, Fasano A, Daniele A, Zibetti M, Merola A, Rizzi L, Piano C, Piccininni C, Romito LM, Lopiano L, Albanese A (2014) Long-term outcome of subthalamic nucleus DBS in Parkinson’s disease: From the advanced phase towards the late stage of the disease? Parkinsonism Related Dis 20:376–381. https://doi.org/10.1016/j.parkreldis.2014.01.012
Bang Henriksen M, Johnsen EL, Sunde N, Vase A, Gjelstrup MC, Østergaard K (2016) Surviving 10 years with deep brain stimulation for Parkinson’s disease - a follow-up of 79 patients. Eur J Neurol 23:53–61. https://doi.org/10.1111/ene.12614
Hitti FL, Ramayya AG, McShane BJ, Yang AI, Vaughan KA, Baltuch GH (2019) Long-term outcomes following deep brain stimulation for Parkinson’s disease. J Neurosurg 1:1–6. https://doi.org/10.3171/2018.8.JNS182081
Munhoz RP, Picillo M, Fox SH, Bruno V, Panisset M, Honey CR, Fasano A (2016) Eligibility criteria for deep brain stimulation in parkinson’s disease, tremor, and dystonia. CA J Neurol Sci J Sci Neurol 43:462–471. https://doi.org/10.1017/cjn.2016.35
Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N, Agarwal P, Athar S, Bordelan Y, Bronte-Stewart HM, Camicioli R, Chou K, Cole W, Dalvi A, Delgado H, Diamond A, Dick JP, Duda J, Elble RJ, Evans C, Evidente VG, Fernandez HH, Fox S, Friedman JH, Fross RD, Gallagher D, Goetz CG, Hall D, Hermanowicz N, Hinson V, Horn S, Hurtig H, Kang UJ, Kleiner-Fisman G, Klepitskaya O, Kompoliti K, Lai EC, Leehey ML, Leroi I, Lyons KE, McClain T, Metzer SW, Miyasaki J, Morgan JC, Nance M, Nemeth J, Pahwa R, Parashos SA, Schneider JSJS, Schrag A, Sethi K, Shulman LM, Siderowf A, Silverdale M, Simuni T, Stacy M, Stern MB, Stewart RM, Sullivan K, Swope DM, Wadia PM, Walker RW, Walker R, Weiner WJ, Wiener J, Wilkinson J, Wojcieszek JM, Wolfrath S, Wooten F, Wu A, Zesiewicz TA, Zweig RM (2008) Movement disorder society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170. https://doi.org/10.1002/mds.22340
Goetz CG, Poewe W, Rascol O, Sampaio C, Stebbins GT, Counsell C, Giladi N, Holloway RG, Moore CG, Wenning GK, Yahr MD, Seidl L, Disease MDSTFoRSfPs (2004) <i>Movement</i> disorder society task force report on the Hoehn and Yahr staging scale: status and recommendations The <i>Movement</i> disorder society task force on rating scales for Parkinson’s disease. Mov Disord 19:1020–1028. https://doi.org/10.1002/mds.20213
Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25(15):2649–2653. https://doi.org/10.1002/mds.23429
Opara JA, Brola W, Leonardi M, Błaszczyk B (2012) Quality of life in Parkinson’s disease. J Med Life 5:375–381
Furukawa TA (2010) Assessment of mood: guides for clinicians. J Psychosom Res 68:581–589. https://doi.org/10.1016/J.JPSYCHORES.2009.05.003
Martinez-Martin P, Jeukens-Visser M, Lyons KE, Rodriguez-Blazquez C, Selai C, Siderowf A, Welsh M, Poewe W, Rascol O, Sampaio C, Stebbins GT, Goetz CG, Schrag A (2011) Health-related quality-of-life scales in Parkinson’s disease: critique and recommendations. Mov Disord 26:2371–2380. https://doi.org/10.1002/mds.23834
Bernard BA, Goldman JG (2010) MMSE - mini-mental state examination. Encycl Move Dis. https://doi.org/10.1016/B978-0-12-374105-9.00186-6
Spinnler H, Tognoni G (1987) Standardizzazione e taratura italiana di test Neuropsicologici. It J Neurol Sci 8(suppl):47–50
Giovagnoli AR, Del Pesce M, Mascheroni S, Simoncelli M, Laiacona M, Capitani E (1996) Trail making test: normative values from 287 normal adult controls. Ital J Neurol Sci 17(4):305–309. https://doi.org/10.1007/bf01997792
Scarpina F, Tagini S (2017) The stroop color and word test. Front Psychol 8:557. https://doi.org/10.3389/fpsyg.2017.00557
Paolo AM, Tröster AI, Blackwell KT, Koller WC, Axelrod BN (1996) Utility of a Wisconsin card sorting test short form in persons with Alzheimer’s and Parkinson’s disease. J Clin Exp Neuropsychol 18:892–897. https://doi.org/10.1080/01688639608408310
Wechsler D (1987) Digit span.
Novelli G, Papagno C, Capitani E, Laiacona M, Cappa SF, Vallar G (1986) Tre test clinici di memoria verbale a lungo termine: taratura su soggetti normali. Arch Psicol Neurol Psic 4:278–296
De Renzi E, Vignolo LA (1962) The Token test: a sensitive test to detect receptive disturbances in aphasics. Brain 85:665–678. https://doi.org/10.1093/brain/85.4.665
Novelli G, Papagno C, Capitani E, Laiacona M, Vallar G, Cappa SF (1986) Tre test clinici di ricerca e produzione lessicale: taratura su soggetti normali. Arch Psicol Neurol Psic 7:477–506
Basso A, Capitani E, Laiacona M (2019) Raven’s coloured progressive matrices: normative values on 305 adult normal controls. Funct Neurol 2:189–194
Limousin P, Foltynie T (2019) Long-term outcomes of deep brain stimulation in Parkinson disease. Nat Rev Neurol 15:234–242. https://doi.org/10.1038/s41582-019-0145-9
Zibetti M, Merola A, Rizzi L, Ricchi V, Angrisano S, Azzaro C, Artusi CA, Arduino N, Marchisio A, Lanotte M, Rizzone M, Lopiano L (2011) Beyond nine years of continuous subthalamic nucleus deep brain stimulation in Parkinson’s disease. Mov Disord 26:2327–2334. https://doi.org/10.1002/mds.23903
Tagliati M, Martin C, Alterman R (2010) Lack of motor symptoms progression in Parkinson’s disease patients with long-term bilateral subthalamic deep brain stimulation. Int J Neurosci 120:717–723. https://doi.org/10.3109/00207454.2010.518777
Wider C, Pollo C, Bloch J, Burkhard PR, Vingerhoets FJG (2008) Long-term outcome of 50 consecutive Parkinson’s disease patients treated with subthalamic deep brain stimulation. Parkinsonism Related Dis 14:114–119. https://doi.org/10.1016/j.parkreldis.2007.06.012
Kishore A, Rao R, Krishnan S, Panikar D, Sarma G, Sivasanakaran MP, Sarma S (2010) Long-term stability of effects of subthalamic stimulation in Parkinson’s disease: Indian experience. Mov Disord 25:2438–2444. https://doi.org/10.1002/mds.23269
George RJ, Nutt JG, Burchiel KJ, Horak FB (2010) A meta-regression of the long-term effects of deep brain stimulation on balance and gait in PD. Neurology 75:1292–1299. https://doi.org/10.1212/WNL.0b013e3181f61329
Lopiano L, Rizzone M, Bergamasco B, Tavella A, Torre E, Perozzo P, Valentini MC, Lanotte M (2001) Deep brain stimulation of the subthalamic nucleus: clinical effectiveness and safety. Neurology 56:552–554. https://doi.org/10.1212/wnl.56.4.552
Foubert-Samier A, Maurice S, Hivert S, Guelh D, Rigalleau V, Burbaud P, Cuny E, Meissner W, Tison F (2012) A long-term follow-up of weight changes in subthalamic nucleus stimulated Parkinson’s disease patients. Revue Neurologique 168:173–176. https://doi.org/10.1016/j.neurol.2011.04.006
Lezcano E, Gómez-Esteban JC, Tijero B, Bilbao G, Lambarri I, Rodriguez O, Villoria R, Dolado A, Berganzo K, Molano A, de Gopegui ER, Pomposo I, Gabilondo I, Zarranz JJ (2016) Long-term impact on quality of life of subthalamic nucleus stimulation in Parkinson’s disease. J Neurol 263:895–905. https://doi.org/10.1007/s00415-016-8077-4
Aviles-Olmos I, Kefalopoulou Z, Tripoliti E, Candelario J, Akram H, Martinez-Torres I, Jahanshahi M, Foltynie T, Hariz M, Zrinzo L, Limousin P (2014) Long-term outcome of subthalamic nucleus deep brain stimulation for Parkinson’s disease using an MRI-guided and MRI-verified approach. J Neurol Neurosurg Psychiatry 85:1419–1425. https://doi.org/10.1136/jnnp-2013-306907
Parsons TD, Rogers SA, Braaten AJ, Woods SP, Tröster AI (2006) Cognitive sequelae of subthalamic nucleus deep brain stimulation in Parkinson’s disease: a meta-analysis. Lancet Neurol 5:578–588. https://doi.org/10.1016/S1474-4422(06)70475-6
Contarino MF, Daniele A, Sibilia AH, Romito LMA, Bentivoglio AR, Gainotti G, Albanese A (2007) Cognitive outcome 5 years after bilateral chronic stimulation of subthalamic nucleus in patients with Parkinson’s disease. J Neurol Neurosurg Psyc 78:248–252. https://doi.org/10.1136/jnnp.2005.086660
Caffarra P, Vezzadini G, Dieci F, Zonato F, Venneri A (2004) Modified card sorting test: normative data. J Clin Exp Neuropsychol 26:246–250
Caffarra P, Vezzadini G, Dieci F, Zonato F, Venneri A (2002) Una versione abbreviata del test di Stroop: dati normativi nella popolazione Italiana. Nuova Rivista Neurol 12:111–115
Wu B, Han L, Sun B-M, Hu X-W, Wang X-P (2014) Influence of deep brain stimulation of the subthalamic nucleus on cognitive function in patients with Parkinson’s disease. Neurosci Bull 30:153–161. https://doi.org/10.1007/s12264-013-1389-9
Kaiser I, Kryspin-Exner I, Brücke T, Volc D, Alesch F (2008) Long-term effects of STN DBS on mood: psychosocial profiles remain stable in a 3-year follow-up. BMC Neurol 8:43. https://doi.org/10.1186/1471-2377-8-43
Acknowledgements
We thank F. Spagnolo, D. Ceppi, S. Lalli, M. Fichera, R. Balestrino, E. Bonavertura, M. Impellizzeri, P. Picozzi, A. Franzin; and patients, caregivers and volunteers for their participation in our research.
Funding
No funding.
Author information
Authors and Affiliations
Contributions
Authors whose names appear on the submission. MAV, GC, SG, PGS, RC, LRB, MF, PM: made substantial contributions to the conception or design of the work; or the acquisition, analysis, or interpretation of data; or the creation of new software used in the work; MF,PGS, SG, MAV: drafted the work or revised it critically for important intellectual content; MAV, GC, PGS, SG: approved the version to be published; MAV, PGS, SG, GC: agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Corresponding author
Ethics declarations
Conflicts of interest
Nothing to report.
Ethical Standards
The Study was approved by the Ethics Committe of IRCCS San Raffaele Scientific Institute, Milan, Italy. All Participants provided informed consent.
Rights and permissions
About this article
Cite this article
Volonté, M.A., Clarizio, G., Galantucci, S. et al. Long term follow-up in advanced Parkinson’s disease treated with DBS of the subthalamic nucleus. J Neurol 268, 2821–2830 (2021). https://doi.org/10.1007/s00415-021-10430-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00415-021-10430-y