Decisions about deep brain stimulation therapy in Parkinson’s disease

Pedro Brandão; Talyta Cortez Grippe; Luiz Cláudio Modesto; André Gustavo Fonseca Ferreira; Flávia Martins da Silva; Flávio Faria Pereira; Marcelo Evangelista Lobo; Nasser Allam; Tiago da Silva Freitas; Renato P. Munhoz

doi:10.1590/0004-282X20180048

Arquivos de Neuro-Psiquiatria, Table of Contents

CC BY-NC-ND 4.0 · Arq Neuropsiquiatr 2018; 76(06): 411-420
DOI: 10.1590/0004-282X20180048

VIEWS AND REVIEWS

Decisions about deep brain stimulation therapy in Parkinson’s disease

Decisões a respeito da terapia com estimulação cerebral profunda na doença de Parkinson

Authors

Pedro Brandão

¹Universidade de Brasília, Laboratório de Neurociência e Comportamento, Brasilia DF, Brasil;

²Câmara dos Deputados, Departamento Médico, Serviço de Neurologia, Brasilia DF, Brasil;
Talyta Cortez Grippe

³Hospital de Base do Distrito Federal, Unidade de Neurologia, Brasilia DF, Brasil;
Luiz Cláudio Modesto

⁴Hospital de Base do Distrito Federal, Unidade de Neurocirurgia, Brasilia DF, Brasil;
André Gustavo Fonseca Ferreira

³Hospital de Base do Distrito Federal, Unidade de Neurologia, Brasilia DF, Brasil;
Flávia Martins da Silva

³Hospital de Base do Distrito Federal, Unidade de Neurologia, Brasilia DF, Brasil;
Flávio Faria Pereira

³Hospital de Base do Distrito Federal, Unidade de Neurologia, Brasilia DF, Brasil;
Marcelo Evangelista Lobo

³Hospital de Base do Distrito Federal, Unidade de Neurologia, Brasilia DF, Brasil;
Nasser Allam

¹Universidade de Brasília, Laboratório de Neurociência e Comportamento, Brasilia DF, Brasil;

³Hospital de Base do Distrito Federal, Unidade de Neurologia, Brasilia DF, Brasil;
Tiago da Silva Freitas

⁴Hospital de Base do Distrito Federal, Unidade de Neurocirurgia, Brasilia DF, Brasil;
Renato P. Munhoz

⁵University of Toronto, Toronto Western Hospital, Movement Disorders Centre, University Health Network, Toronto, Canada.

Abstract

ABSTRACT

Parkinson’s disease can be treated surgically in patients who present with motor complications such as fluctuations and dyskinesias, or medically-refractory disabling tremor. In this review, a group of specialists formulated suggestions for a preoperative evaluation protocol after reviewing the literature published up to October 2017. In this protocol, eligibility and ineligibility criteria for surgical treatment were suggested, as well as procedures that should be carried out before the multidisciplinary therapeutic decisions. The review emphasizes the need to establish “DBS teams”, with professionals dedicated specifically to this area. Finally, surgical target selection (subthalamic nucleus or globus pallidus internus) is discussed briefly, weighing the pros and cons of each target.

RESUMO

A doença de Parkinson pode ser tratada cirurgicamente em pacientes que desenvolveram complicações motoras, como flutuações e discinesias, ou tremores refratários ao uso de medicação. Nesta revisão, um grupo de especialistas formulou sugestões para um protocolo de avaliação pré-operatória, depois de revisar a literatura publicada até outubro de 2017. Neste protocolo, são sugeridos critérios de elegibilidade e inadmissibilidade para tratamento cirúrgico, bem como procedimentos que devem ser realizados antes das decisões terapêuticas multidisciplinares. A revisão enfatiza a necessidade de estabelecer “equipes de DBS”, com profissionais dedicados especialmente a esta área. Ao final, a seleção do alvo cirúrgico (núcleo subtalâmico ou globo pálido interno) é discutida brevemente, ponderando prós e contras de cada escolha.

Parkinson disease - deep brain stimulation - reference standards - basal ganglia - neurosurgical procedures

doença de Parkinson - estimulação cerebral profunda - padrões de referência - gânglios da base - procedimentos neurocirúrgicos

Full Text

References

References
1 Munhoz RP, Werneck LC, Teive HA. The differential diagnoses of parkinsonism: findings from a cohort of 1528 patients and a 10 years comparison in tertiary movement disorders clinics. Clin Neurol Neurosurg. 2010 Jun;112(5):431-5. https://doi.org/10.1016/j.clineuro.2010.03.003
2 Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W et al. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2015 Oct;30(12):1591-601. https://doi.org/10.1002/mds.26424
3 Pringsheim T, Jette N, Frolkis A, Steeves TD. The prevalence of Parkinson’s disease: a systematic review and meta-analysis. Mov Disord. 2014 Nov;29(13):1583-90. https://doi.org/10.1002/mds.25945
4 Hirsch L, Jette N, Frolkis A, Steeves T, Pringsheim T. The Incidence of Parkinson’s disease: a systematic review and meta-analysis. Neuroepidemiology. 2016;46(4):292-300. https://doi.org/10.1159/000445751
5 Barbosa MT, Caramelli P, Maia DP, Cunningham MC, Guerra HL, Lima-Costa MF et al. Parkinsonism and Parkinson’s disease in the elderly: a community-based survey in Brazil (the Bambuí study). Mov Disord. 2006 Jun;21(6):800-8. https://doi.org/10.1002/mds.20806
6 Connolly BS, Lang AE. Pharmacological treatment of Parkinson disease: a review. JAMA. 2014 Apr;311(16):1670-83. https://doi.org/10.1001/jama.2014.3654
7 Benabid AL, Pollak P, Louveau A, Henry S, Rougemont J. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol. 1987;50(1-6):344-6. https://doi.org/10.1159/000100803
8 Lozano AM, Gross RE. Introduction to deep brain stimulation. Neurosurg Focus. 2017 Apr;42 VideoSuppl2:Intro. https://doi.org/10.3171/2017.2.FocusVid.Intro
9 Souza RM, Moro E, Lang AE, Schapira AH. Timing of deep brain stimulation in Parkinson disease: a need for reappraisal? Ann Neurol. 2013 May;73(5):565-75. https://doi.org/10.1002/ana.23890
10 Okun MS, Fernandez HH, Rodriguez RL, Foote KD. Identifying candidates for deep brain stimulation in Parkinson’s disease: the role of the primary care physician. Geriatrics. 2007 May;62(5):18-24.
11 Fasano A, Lozano AM. Deep brain stimulation for movement disorders: 2015 and beyond. Curr Opin Neurol. 2015 Aug;28(4):423-36. https://doi.org/10.1097/WCO.20180048201800480226
12 Anderson VC, Burchiel KJ, Hogarth P, Favre J, Hammerstad JP. Pallidal vs subthalamic nucleus deep brain stimulation in Parkinson disease. Arch Neurol. 2005 Apr;62(4):554-60. https://doi.org/10.1001/archneur.62.4.554
13 Deuschl G, Schade-Brittinger C, Krack P, Volkmann J, Schäfer H, Bötzel K et al. A randomized trial of deep-brain stimulation for Parkinson’s disease. N Engl J Med. 2006 Aug;355(9):896-908. https://doi.org/10.1056/NEJMoa060281
14 Schüpbach WM, Maltête D, Houeto JL, Montcel ST, Mallet L, Welter ML et al. Neurosurgery at an earlier stage of Parkinson disease: a randomized, controlled trial. Neurology. 2007 Jan;68(4):267-71. https://doi.org/10.1212/01.wnl.0000250253.03919.fb
15 Weaver FM, Follett K, Stern M, Hur K, Harris C, Marks WJ Jr et al. Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA. 2009 Jan;301(1):63-73. https://doi.org/10.1001/jama.2008.929
16 Williams A, Gill S, Varma T, Jenkinson C, Quinn N, Mitchell R et al. 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. 2010 Jun;9(6):581-91. https://doi.org/10.1016/S1474-4422(10)70093-4
17 Follett KA, Weaver FM, Stern M, Hur K, Harris CL, Luo P et al. Pallidal versus subthalamic deep-brain stimulation for Parkinson’s disease. N Engl J Med. 2010 Jun;362(22):2077-91. https://doi.org/10.1056/NEJMoa0907083
18 Okun MS, Gallo BV, Mandybur G, Jagid J, Foote KD, Revilla FJ et al. Subthalamic deep brain stimulation with a constant-current device in Parkinson’s disease: an open-label randomised controlled trial. Lancet Neurol. 2012 Feb;11(2):140-9. https://doi.org/10.1016/S1474-4422(11)70308-8
19 Schuepbach WM, Rau J, Knudsen K, Volkmann J, Krack P, Timmermann L et al. Neurostimulation for Parkinson’s disease with early motor complications. N Engl J Med. 2013 Feb;368(7):610-22. https://doi.org/10.1056/NEJMoa1205158
20 Kleiner-Fisman G, Herzog J, Fisman DN, Tamma F, Lyons KE, Pahwa R et al. Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov Disord. 2006 Jun;21(S14 Suppl 14):S290-304. https://doi.org/10.1002/mds.20962
21 Andrade P, Carrillo-Ruiz JD, Jiménez F. A systematic review of the efficacy of globus pallidus stimulation in the treatment of Parkinson’s disease. J Clin Neurosci. 2009 Jul;16(7):877-81. https://doi.org/10.1016/j.jocn.2008.11.006
22 Sharma A, Szeto K, Desilets AR. Efficacy and safety of deep brain stimulation as an adjunct to pharmacotherapy for the treatment of Parkinson disease. Ann Pharmacother. 2012 Feb;46(2):248-54. https://doi.org/10.1345/aph.1Q508
23 Volkmann J, Albanese A, Antonini A, Chaudhuri KR, Clarke CE, Bie RM et al. Selecting deep brain stimulation or infusion therapies in advanced Parkinson’s disease: an evidence-based review. J Neurol. 2013 Nov;260(11):2701-14. https://doi.org/10.1007/s00415-012-6798-6
24 Perestelo-Pérez L, Rivero-Santana A, Pérez-Ramos J, Serrano-Pérez P, Panetta J, Hilarion P. Deep brain stimulation in Parkinson’s disease: meta-analysis of randomized controlled trials. J Neurol. 2014 Nov;261(11):2051-60. https://doi.org/10.1007/s00415-014-7254-6
25 Liu Y, Li W, Tan C, Liu X, Wang X, Gui Y et al. Meta-analysis comparing deep brain stimulation of the globus pallidus and subthalamic nucleus to treat advanced Parkinson disease. J Neurosurg. 2014 Sep;121(3):709-18. https://doi.org/10.3171/2014.4.JNS131711
26 Mansouri A, Taslimi S, Badhiwala JH, Witiw CD, Nassiri F, Odekerken VJJ et al. Deep brain stimulation for Parkinson’s disease: meta-analysis of results of randomized trials at varying lengths of follow-up. J Neurosurg. 2018 Apr;128(4):1199-213. https://doi.org/10.3171/2016.11.JNS16715
27 Pahwa R, Factor SA, Lyons KE, Ondo WG, Gronseth G, Bronte-Stewart H et al. Practice Parameter: treatment of Parkinson disease with motor fluctuations and dyskinesia (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology. 2006 Apr;66(7):983-95. https://doi.org/10.1212/01.wnl.0000215250.82576.87
28 Lang AE, Houeto JL, Krack P, Kubu C, Lyons KE, Moro E et al. Deep brain stimulation: preoperative issues. Mov Disord. 2006 Jun;21(S14 Suppl 14):S171-96. https://doi.org/10.1002/mds.20955
29 Bronstein JM, Tagliati M, Alterman RL, Lozano AM, Volkmann J, Stefani A et al. Deep brain stimulation for Parkinson disease: an expert consensus and review of key issues. Arch Neurol. 2011 Feb;68(2):165. https://doi.org/10.1001/archneurol.2010.260
30 Fox SH, Katzenschlager R, Lim SY, Ravina B, Seppi K, Coelho M et al. The movement disorder society evidence-based medicine review update: treatments for the motor symptoms of Parkinson’s disease. Mov Disord. 2011 Oct;26(S3 Suppl 3):S2-41. https://doi.org/10.1002/mds.23829
31 Rieder CR, Silva DJ. Indicações de tratamento cirúrgico na doença de Parkinson. In: Dias-Tosta E, Rieder CRM, Borges V, Correa-Neto Y. Doença de Parkinson: recomendações. São Paulo: Omnifarma, 2010. p. 129-39.
32 Ferreira JJ, Katzenschlager R, Bloem BR, Bonuccelli U, Burn D, Deuschl G et al. Summary of the recommendations of the EFNS/MDS-ES review on therapeutic management of Parkinson’s disease. Eur J Neurol. 2013 Jan;20(1):5-15. https://doi.org/10.1111/j.1468-1331.2012.03866.x
33 Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry. 1992 Mar;55(3):181-4. https://doi.org/10.1136/jnnp.55.3.181
34 Fahn S, Elton RL. Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Goldstein M, Calne DB, ditors. Recent developments in Parkinson’s disease. Florham Park: Macmillan Healthcare Information; 1987. Vol. 2.
35 Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P et al. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord. 2008 Nov;23(15):2129-70. https://doi.org/10.1002/mds.22340
36 Katayama Y, Kasai M, Oshima H, Fukaya C, Yamamoto T, Ogawa K et al. Subthalamic nucleus stimulation for Parkinson disease: benefits observed in levodopa-intolerant patients. J Neurosurg. 2001 Aug;95(2):213-21. https://doi.org/10.3171/jns.2001.95.2.0213
37 Okun MS, Foote KD. Parkinson’s disease DBS: what, when, who and why? The time has come to tailor DBS targets. Expert Rev Neurother. 2010 Dec;10(12):1847-57. https://doi.org/10.1586/ern.10.156
38 England AC Jr, Schwab RS. Postoperative medical evaluation of 26 selected patients with Parkinson’s disease. J Am Geriatr Soc. 1956 Dec;4(12):1219-32. https://doi.org/10.1111/j.1532-5415.1956.tb01156.x
39 Peto V, Jenkinson C, Fitzpatrick R, Greenhall R. The development and validation of a short measure of functioning and well being for individuals with Parkinson’s disease. Qual Life Res. 1995 Jun;4(3):241-8. https://doi.org/10.1007/BF02260863
40 Fasano A, Aquino CC, Krauss JK, Honey CR, Bloem BR. Axial disability and deep brain stimulation in patients with Parkinson disease. Nat Rev Neurol. 2015 Feb;11(2):98-110. https://doi.org/10.1038/nrneurol.2014.252
41 Moum SJ, Price CC, Limotai N, Oyama G, Ward H, Jacobson C et al. Effects of STN and GPi deep brain stimulation on impulse control disorders and dopamine dysregulation syndrome. PLoS One. 2012;7(1):e29768. https://doi.org/10.1371/journal.pone.0029768
42 Broen M, Duits A, Visser-Vandewalle V, Temel Y, Winogrodzka A. Impulse control and related disorders in Parkinson’s disease patients treated with bilateral subthalamic nucleus stimulation: a review. Parkinsonism Relat Disord. 2011 Jul;17(6):413-7. https://doi.org/10.1016/j.parkreldis.2011.02.013
43 Lim SY, O’Sullivan SS, Kotschet K, Gallagher DA, Lacey C, Lawrence AD et al. Dopamine dysregulation syndrome, impulse control disorders and punding after deep brain stimulation surgery for Parkinson’s disease. J Clin Neurosci. 2009 Sep;16(9):1148-52. https://doi.org/10.1016/j.jocn.2008.12.010
44 Knobel D, Aybek S, Pollo C, Vingerhoets FJ, Berney A. Rapid resolution of dopamine dysregulation syndrome (DDS) after subthalamic DBS for Parkinson disease (PD): a case report. Cogn Behav Neurol. 2008 Sep;21(3):187-9. https://doi.org/10.1097/WNN.0b013e318185e6e2
45 Eusebio A, Witjas T, Cohen J, Fluchère F, Jouve E, Régis J et al. Subthalamic nucleus stimulation and compulsive use of dopaminergic medication in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2013 Aug;84(8):868-74. https://doi.org/10.1136/jnnp-2012-302387
46 Defer GL, Widner H, Marié RM, Rémy P, Levivier M. Core assessment program for surgical interventional therapies in Parkinson’s disease (CAPSIT-PD). Mov Disord. 1999 Jul;14(4):572-84. https://doi.org/10.1002/1531-8257(199907)14:4<572::AID-MDS1005>3.0.CO;2-C
47 Sudhyadhom A, Haq IU, Foote KD, Okun MS, Bova FJ. A high resolution and high contrast MRI for differentiation of subcortical structures for DBS targeting: the Fast Gray Matter Acquisition T1 Inversion Recovery (FGATIR). Neuroimage. 2009 Aug;47 Suppl 2:T44-52. https://doi.org/10.1016/j.neuroimage.2009.04.018
48 Emre M, Aarsland D, Brown R, Burn DJ, Duyckaerts C, Mizuno Y. Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord. 2007 Sep;22(12):1689-707. https://doi.org/10.1002/mds.21507
49 Litvan I, Goldman JG, Tröster AI, Schmand BA, Weintraub D, Petersen RC et al. Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: Movement Disorder Society Task Force guidelines. Mov Disord. 2012 Mar;27(3):349-56. https://doi.org/10.1002/mds.24893
50 Williams-Gray CH, Mason SL, Evans JR, Foltynie T, Brayne C, Robbins TW et al. The CamPaIGN study of Parkinson’s disease: 10-year outlook in an incident population-based cohort. J Neurol Neurosurg Psychiatry. 2013 Nov;84(11):1258-64. https://doi.org/10.1136/jnnp-2013-305277
51 Hu MT, Szewczyk-Królikowski K, Tomlinson P, Nithi K, Rolinski M, Murray C et al. Predictors of cognitive impairment in an early stage Parkinson’s disease cohort. Mov Disord. 2014 Mar;29(3):351-9. https://doi.org/10.1002/mds.25748
52 Fereshtehnejad SM, Romenets SR, Anang JB, Latreille V, Gagnon JF, Postuma RB. New clinical subtypes of Parkinson disease and their longitudinal progression: a prospective cohort comparison with other phenotypes. JAMA Neurol. 2015 Aug;72(8):863-73. https://doi.org/10.1001/jamaneurol.2015.0703
53 Fasano A, Appel-Cresswell S, Jog M, Zurowkski M, Duff-Canning S, Cohn M et al. Medical management of Parkinson’s Disease after initiation of deep brain stimulation. Can J Neurol Sci. 2016 Sep;43(5):626-34. https://doi.org/10.1017/cjn.2016.274
54 Panisset M, Picillo M, Jodoin N, Poon YY, Valencia-Mizrachi A, Fasano A et al. Establishing a standard of care for deep brain stimulation centers in Canada. Can J Neurol Sci. 2017 Mar;44(2):132-8. https://doi.org/10.1017/cjn.2016.409
55 Picillo M, Lozano AM, Kou N, Puppi Munhoz R, Fasano A. Programming deep brain stimulation for Parkinson’s disease: the Toronto Western Hospital Algorithms. Brain Stimul. 2016 May-Jun;9(3):425-37. https://doi.org/10.1016/j.brs.2016.02.004
56 Saint-Cyr JA, Trépanier LL, Kumar R, Lozano AM, Lang AE. Neuropsychological consequences of chronic bilateral stimulation of the subthalamic nucleus in Parkinson’s disease. Brain. 2000 Oct;123(Pt 10):2091-108. https://doi.org/10.1093/brain/123.10.2091
57 Odekerken VJ, Boel JA, Schmand BA, Haan RJ, Figee M, Munckhof P et al. GPi vs STN deep brain stimulation for Parkinson disease: three-year follow-up. Neurology. 2016 Feb;86(8):755-61. https://doi.org/10.1212/WNL.20180048201800482401
58 Okun MS, Fernandez HH, Wu SS, Kirsch-Darrow L, Bowers D, Bova F et al. Cognition and mood in Parkinson’s disease in subthalamic nucleus versus globus pallidus interna deep brain stimulation: the COMPARE trial. Ann Neurol. 2009 May;65(5):586-95. https://doi.org/10.1002/ana.21596
59 Rothlind JC, Cockshott RW, Starr PA, Marks WJ Jr. Neuropsychological performance following staged bilateral pallidal or subthalamic nucleus deep brain stimulation for Parkinson’s disease. J Int Neuropsychol Soc. 2007 Jan;13(1):68-79. https://doi.org/10.1017/S1355617707070105
60 Witt K, Granert O, Daniels C, Volkmann J, Falk D, Eimeren T et al. Relation of lead trajectory and electrode position to neuropsychological outcomes of subthalamic neurostimulation in Parkinson’s disease: results from a randomized trial. Brain. 2013 Jul;136(Pt 7):2109-19. https://doi.org/10.1093/brain/awt151
61 Mirza S, Yazdani U, Dewey Iii R, Patel N, Dewey RB Jr, Miocinovic S et al. Comparison of globus pallidus interna and subthalamic nucleus in deep brain stimulation for Parkinson disease: an institutional experience and review. Parkinsons Dis. 2017;2017:3410820. https://doi.org/10.1155/2017/3410820
62 Amami P, Dekker I, Piacentini S, Ferré F, Romito LM, Franzini A et al. Impulse control behaviours in patients with Parkinson’s disease after subthalamic deep brain stimulation: de novo cases and 3-year follow-up. J Neurol Neurosurg Psychiatry. 2015 May;86(5):562-4. https://doi.org/10.1136/jnnp-2013-307214
63 Troche MS, Brandimore AE, Foote KD, Okun MS. Swallowing and deep brain stimulation in Parkinson’s disease: a systematic review. Parkinsonism Relat Disord. 2013 Sep;19(9):783-8. https://doi.org/10.1016/j.parkreldis.2013.05.001
64 Sako W, Miyazaki Y, Izumi Y, Kaji R. Which target is best for patients with Parkinson’s disease? A meta-analysis of pallidal and subthalamic stimulation. J Neurol Neurosurg Psychiatry. 2014 Sep;85(9):982-6. https://doi.org/10.1136/jnnp-2013-306090
65 Toft M, Dietrichs E. Medication costs following subthalamic nucleus deep brain stimulation for Parkinson’s disease. Mov Disord. 2014 Feb;29(2):275-6. https://doi.org/10.1002/mds.25504
66 Wang JW, Zhang YQ, Zhang XH, Wang YP, Li JP, Li YJ. Cognitive and psychiatric effects of STN versus GPi deep brain stimulation in Parkinson’s disease: a meta-analysis of randomized controlled trials. PLoS One. 2016 Jun;11(6):e0156721. https://doi.org/10.1371/journal.pone.0156721