Journal of Neurology

, Volume 261, Issue 6, pp 1090–1096 | Cite as

Long-term cognitive outcome of bilateral subthalamic deep brain stimulation in Parkinson’s disease

  • Han-Joon Kim
  • Beom S. Jeon
  • Sun Ha Paek
  • Kyoung-Min Lee
  • Ji-Young Kim
  • Jee-Young Lee
  • Hee Jin Kim
  • Ji Young Yun
  • Young Eun Kim
  • Hui-Jun Yang
  • Gwanhee Ehm
Original Communication

Abstract

The effect of subthalamic deep brain stimulation (STN DBS) on cognition in Parkinson’s disease (PD) remains controversial, and it is unclear which factors are related to cognitive decline and dementia after STN DBS, especially over the long term. To this end, we analyzed the cognitive outcome of 103 non-demented patients with PD who were followed-up for at least 12 months after bilateral STN DBS surgery. Preoperatively, the patients were evaluated with the Unified Parkinson's Disease Rating Scale and neuropsychological tests. The rate of global cognitive decline and the incidence of dementia during follow-up for up to 7 years (mean 42.4 ± 24.5 months) were calculated, and preoperative clinical and neuropsychological factors associated with postoperative global cognitive decline or dementia were analyzed. The prevalence of mild cognitive impairment (MCI) and its relation to later cognitive decline or dementia were also evaluated. The annual decline in the mini–mental state examination score was 0.4 ± 1.7 with impaired attention and executive function and a higher levodopa equivalent dose at baseline being the predictors of a faster global cognitive decline after STN DBS. Dementia developed in 13 patients with an incidence rate of 35.7 per 1,000 person-years. Impaired executive function at baseline predicted dementia. At baseline, 63.1 % of the patients had PD-MCI, and these patients were more likely to develop dementia than those without PD-MCI. This study showed that dysfunctions in the frontostriatal circuitry at baseline were associated with a risk of subsequent global cognitive decline and dementia in patients with PD who underwent STN DBS. In addition, preoperative PD-MCI was a risk factor for dementia after STN DBS.

Keywords

Parkinson’s disease DBS Dementia Mild cognitive impairment 

References

  1. 1.
    Castrioto A, Lhommée E, Moro E, Krack P (2014) Mood and behavioural effects of subthalamic stimulation in Parkinson’s disease. Lancet Neurol 13:287–305CrossRefPubMedGoogle Scholar
  2. 2.
    Massano J, Garrett C (2012) Deep brain stimulation and cognitive decline in Parkinson’s disease: a clinical review. Front Neurol 3:66. doi:10.3389/fneur.2012.00066 PubMedCentralPubMedGoogle Scholar
  3. 3.
    Fasano A, Romito LM, Daniele A, Piano C, Zinno M, Bentivoglio AR, Albanese A (2010) Motor and cognitive outcome in patients with Parkinson’s disease 8 years after subthalamic implants. Brain 133:2664–2676CrossRefPubMedGoogle Scholar
  4. 4.
    Merola A, Zibetti M, Angrisano S, Rizzi L, Ricchi V, Artusi CA, Lanotte M, Rizzone MG, Lopiano L (2011) Parkinson’s disease progression at 30 years: a study of subthalamic deep brain-stimulated patients. Brain 134:2074–2084CrossRefPubMedGoogle Scholar
  5. 5.
    Witt K, Daniels C, Reiff J, Krack P, Volkmann J, Pinsker MO, Krause M, Tronnier V, Kloss M, Schnitzler A (2008) Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson’s disease: a randomised, multicentre study. Lancet Neurol 7:605–614CrossRefPubMedGoogle Scholar
  6. 6.
    Zangaglia R, Pasotti C, Mancini F, Servello D, Sinforiani E, Pacchetti C (2012) Deep brain stimulation and cognition in Parkinson’s disease: an eight-year follow-up study. Mov Disord 27:1192–1194CrossRefPubMedGoogle Scholar
  7. 7.
    Castrioto A, Lozano AM, Poon Y-Y, Lang AE, Fallis M, Moro E (2011) Ten-year outcome of subthalamic stimulation in Parkinson disease: a blinded evaluation. Arch Neurol 68:1550–1556CrossRefPubMedGoogle Scholar
  8. 8.
    Zibetti M, Merola A, Rizzi L, Ricchi V, Angrisano S, Azzaro C, Artusi CA, Arduino N, Marchisio A, Lanotte M (2011) Beyond nine years of continuous subthalamic nucleus deep brain stimulation in Parkinson’s disease. Mov Disord 26:2327–2334CrossRefPubMedGoogle Scholar
  9. 9.
    Hoops S, Nazem S, Siderowf A, Duda J, Xie S, Stern M, Weintraub D (2009) Validity of the MoCA and MMSE in the detection of MCI and dementia in Parkinson disease. Neurology 73:1738–1745PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    Muslimović D, Post B, Speelman JD, Schmand B (2005) Cognitive profile of patients with newly diagnosed Parkinson disease. Neurology 65:1239–1245CrossRefPubMedGoogle Scholar
  11. 11.
    Pai MC, Chan SH (2001) Education and cognitive decline in Parkinson’s disease: a study of 102 patients. Acta Neurol Scand 103:243–247CrossRefPubMedGoogle Scholar
  12. 12.
    Siderowf A, Xie S, Hurtig H, Weintraub D, Duda J, Chen-Plotkin A, Shaw L, Van Deerlin V, Trojanowski J, Clark C (2010) CSF amyloid β 1-42 predicts cognitive decline in Parkinson disease. Neurology 75:1055–1061PubMedCentralCrossRefPubMedGoogle Scholar
  13. 13.
    Williams-Gray C, Foltynie T, Brayne C, Robbins T, Barker R (2007) Evolution of cognitive dysfunction in an incident Parkinson’s disease cohort. Brain 130:1787–1798CrossRefPubMedGoogle Scholar
  14. 14.
    Kim HJ, Jeon BS, Paek SH, Lee JY, Kim HJ, Kim CK, Kim DG (2010) Bilateral subthalamic deep brain stimulation in Parkinson disease patients with severe tremor. Neurosurgery 67:626–632CrossRefPubMedGoogle Scholar
  15. 15.
    Kim HJ, Paek SH, Kim JY, Lee JY, Lim YH, Kim DG, Jeon BS (2009) Two-year follow-up on the effect of unilateral subthalamic deep brain stimulation in highly asymmetric Parkinson’s disease. Mov Disord 24:329–335. doi:10.1002/mds.22211 CrossRefPubMedGoogle Scholar
  16. 16.
    Lee JY, Han JH, Kim HJ, Jeon BS, Kim DG, Paek SH (2008) STN DBS of advanced Parkinson’s disease experienced in a specialized monitoring unit with a prospective protocol. J Korean Neurosurg Soc 44:26–35. doi:10.3340/jkns.2008.44.1.26 PubMedCentralCrossRefPubMedGoogle Scholar
  17. 17.
    Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198CrossRefPubMedGoogle Scholar
  18. 18.
    Heo JH, Lee KM, Paek SH, Kim MJ, Lee JY, Kim JY, Cho SY, Lim YH, Kim MR, Jeong SY (2008) The effects of bilateral subthalamic nucleus deep brain stimulation (STN DBS) on cognition in Parkinson disease. J Neurol Sci 273:19–24CrossRefPubMedGoogle Scholar
  19. 19.
    Litvan I, Goldman JG, Tröster AI, Schmand BA, Weintraub D, Petersen RC, Mollenhauer B, Adler CH, Marder K, Williams-Gray CH (2012) Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: Movement Disorder Society Task Force guidelines. Mov Disord 27:349–356PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Emre M, Aarsland D, Brown R, Burn DJ, Duyckaerts C, Mizuno Y, Broe GA, Cummings J, Dickson DW, Gauthier S (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22:1689–1707CrossRefPubMedGoogle Scholar
  21. 21.
    Aybek S, Gronchi-Perrin A, Berney A, Chiuvé SC, Villemure JG, Burkhard PR, Vingerhoets FJG (2007) Long-term cognitive profile and incidence of dementia after STN-DBS in Parkinson’s disease. Mov Disord 22:974–981CrossRefPubMedGoogle Scholar
  22. 22.
    Smeding HMM, Speelman JD, Huizenga HM, Schuurman PR, Schmand B (2011) Predictors of cognitive and psychosocial outcome after STN DBS in Parkinson’s disease. J Neurol Neurosurg Psychiatry 82:754–760CrossRefPubMedGoogle Scholar
  23. 23.
    Cools R, Stefanova E, Barker RA, Robbins TW, Owen AM (2002) Dopaminergic modulation of high-level cognition in Parkinson’s disease: the role of the prefrontal cortex revealed by PET. Brain 125:584–594CrossRefPubMedGoogle Scholar
  24. 24.
    Williams-Gray CH, Evans JR, Goris A, Foltynie T, Ban M, Robbins TW, Brayne C, Kolachana BS, Weinberger DR, Sawcer SJ (2009) The distinct cognitive syndromes of Parkinson’s disease: 5-year follow-up of the CamPaIGN cohort. Brain 132:2958–2969CrossRefPubMedGoogle Scholar
  25. 25.
    Castelli L, Rizzi L, Zibetti M, Angrisano S, Lanotte M, Lopiano L (2010) Neuropsychological changes 1 year after subthalamic DBS in PD patients: a prospective controlled study. Parkinsonism Relat Disord 16:115–118CrossRefPubMedGoogle Scholar
  26. 26.
    Daniels C, Krack P, Volkmann J, Pinsker MO, Krause M, Tronnier V, Kloss M, Schnitzler A, Wojtecki L, Bötzel K (2010) Risk factors for executive dysfunction after subthalamic nucleus stimulation in Parkinson’s disease. Mov Disord 25:1583–1589CrossRefPubMedGoogle Scholar
  27. 27.
    Williams AE, Arzola GM, Strutt AM, Simpson R, Jankovic J, York MK (2011) Cognitive outcome and reliable change indices two years following bilateral subthalamic nucleus deep brain stimulation. Parkinsonism Relat Disord 17:321–327PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    de Lau LM, Schipper CMA, Hofman A, Koudstaal PJ, Breteler M (2005) Prognosis of Parkinson disease: risk of dementia and mortality: the Rotterdam Study. Arch Neurol 62:1265–1269CrossRefPubMedGoogle Scholar
  29. 29.
    Goetz CG, Emre M, Dubois B (2008) Parkinson’s disease dementia: definitions, guidelines, and research perspectives in diagnosis. Ann Neurol 64:S81–S92CrossRefPubMedGoogle Scholar
  30. 30.
    Aarsland D, Bronnick K, Williams-Gray C, Weintraub D, Marder K, Kulisevsky J, Burn D, Barone P, Pagonabarraga J, Allcock L (2010) Mild cognitive impairment in Parkinson disease: a multicenter pooled analysis. Neurology 75:1062–1069PubMedCentralCrossRefPubMedGoogle Scholar
  31. 31.
    Litvan I, Aarsland D, Adler CH, Goldman JG, Kulisevsky J, Mollenhauer B, Rodriguez-Oroz MC, Tröster AI, Weintraub D (2011) MDS task force on mild cognitive impairment in Parkinson’s disease: critical review of PD-MCI. Mov Disord 26:1814–1824PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Janvin C, Larsen J, Aarsland D, Hugdahl K (2006) Subtypes of mild cognitive impairment in Parkinson’s disease: progression to dementia. Mov Disord 21:1343–1349CrossRefPubMedGoogle Scholar
  33. 33.
    Pedersen KF, Larsen JP, Tysnes O-B, Alves G (2013) Prognosis of mild cognitive impairment in early Parkinson disease: the Norwegian Park West Study. JAMA Neurol 70:580–586CrossRefPubMedGoogle Scholar
  34. 34.
    Lessig S, Nie D, Xu R, Corey-Bloom J (2012) Changes on brief cognitive instruments over time in Parkinson’s disease. Mov Disord 27:1125–1128CrossRefPubMedGoogle Scholar
  35. 35.
    Aarsland D, Muniz G, Matthews F (2011) Nonlinear decline of mini-mental state examination in Parkinson’s disease. Mov Disord 26:334–337CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Han-Joon Kim
    • 1
  • Beom S. Jeon
    • 1
  • Sun Ha Paek
    • 2
  • Kyoung-Min Lee
    • 1
  • Ji-Young Kim
    • 3
  • Jee-Young Lee
    • 4
  • Hee Jin Kim
    • 5
  • Ji Young Yun
    • 6
  • Young Eun Kim
    • 7
  • Hui-Jun Yang
    • 8
  • Gwanhee Ehm
    • 1
  1. 1.Department of Neurology and Movement Disorder Center, Parkinson Study Group, and Neuroscience Research Institute, College of MedicineSeoul National UniversitySeoulKorea
  2. 2.Department of Neurosurgery, Movement Disorder Center, and Neuroscience Research Institute, College of MedicineSeoul National University HospitalSeoulKorea
  3. 3.Department of NeurologyInje University Seoul Paik HospitalSeoulKorea
  4. 4.Department of Neurology, College of MedicineSeoul National University, Metropolitan Boramae HospitalSeoulKorea
  5. 5.Department of NeurologyKonkuk University Medical CenterSeoulKorea
  6. 6.Department of NeurologyEwha Womans University Mokdong HospitalSeoulKorea
  7. 7.Department of NeurologySeoul National University Bundang HospitalSongnamKorea
  8. 8.Department of NeurologyUlsan University HospitalUlsanKorea

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