Advertisement

Brain Structure and Function

, Volume 223, Issue 7, pp 3063–3072 | Cite as

Anatomical predictors of cognitive decline after subthalamic stimulation in Parkinson’s disease

  • Vincent PlancheEmail author
  • Fanny Munsch
  • Bruno Pereira
  • Emmanuel de Schlichting
  • Tiphaine Vidal
  • Jerome Coste
  • Dominique Morand
  • Ingrid de Chazeron
  • Philippe Derost
  • Bérangère Debilly
  • Pierre-Michel Llorca
  • Jean-Jacques Lemaire
  • Ana Marques
  • Franck Durif
Original Article

Abstract

We investigated whether pre-operative MRI measures of focal brain atrophy could predict cognitive decline occurring after deep brain stimulation (DBS) of the subthalamic nucleus (STN) in patients with Parkinson’s disease (PD). For that purpose, we prospectively collected data of 42 consecutive patients with PD who underwent bilateral STN-DBS. Normalized brain structure volumes and cortical thicknesses were measured on pre-operative T1-weighted MRI. Patients were tested for their cognitive performances before surgery and 1 year after. After controlling for age, gender, pre-operative disease severity, change in dopaminomimetic dose after surgery and contact location, we found correlations: (1) between the variation of the total Mattis dementia rating scale (MDRS) score and left lateral ventricle volume (p = 0.032), (2) between the variation of the initiation/perseveration subscore of the MDRS and the left nucleus accumbens volume (p = 0.042) and the left lateral ventricle volume (p = 0.017) and (3) between the variation of the backward digit-span task and the right and left superior frontal gyrus thickness (p = 0.004 and p = 0.007, respectively). Left nucleus accumbens atrophy was associated with decline in the initiation/perseveration subscore with the largest effect size (d = − 1.64). Pre-operative left nucleus accumbens volume strongly predicted postoperative decline in the initiation/attention subscore (AUC = 0.92, p < 0.001, 96.3% sensitivity, 80.0% specificity, 92.9% PPV and 92.9% NPV). We conclude that the morphometric measures of brain atrophy usually associated with cognitive impairment in PD can also explain or predict a part of cognitive decline after bilateral STN-DBS. In particular, the left accumbens nucleus volume could be considered as a promising marker for guiding surgical decisions.

Keywords

Parkinson’s disease Deep-brain stimulation Subthalamic nucleus Nucleus accumbens MRI Cognition 

Notes

Acknowledgements

The authors want to thank Christine Delaigue, coordinating nurse for the Parkinson’s Disease Center in Clermont-Ferrand University Hospital. They also thank Prof. Thomas Tourdias and Prof. Vincent Dousset from Bordeaux University Hospital for making available their MRI analysis facilities, and Celine Lambert from Clermont-Ferrand University Hospital for her technical assistance.

Author contributions

Conception of the project: VP and FD. Organization: FD. Execution: all authors. Statistical Analysis: VP and BP. Writing of the first draft: VP. Review and Critique: all authors. Study concept and design: VP, BP, JJL and FD.

Funding

Hospital Program for Clinical Research at Clermont-Ferrand University Hospital.

Compliance with ethical standards

Conflict of interest

VP received travel expenses and/or consulting fees from the ARSEP Foundation, Biogen, Teva-Lundbeck and Merk-Serono, unrelated to the submitted work. FD serves on scientific advisory boards and has received honoraria and research support for his institution from Novartis, Teva-Lundbeck, Allergan, Aguettant, Servier and Merz, unrelated to the submitted work. Other authors: no conflict of interests.

References

  1. Alegret M, Junqué C, Valldeoriola F et al (2001) Effects of bilateral subthalamic stimulation on cognitive function in Parkinson disease. Arch Neurol 58:1223–1227CrossRefGoogle Scholar
  2. Altman DG (1990) Practical statistics for medical research. CRC Press, Boca RatonGoogle Scholar
  3. Aybek S, Lazeyras F, Gronchi-Perrin A et al (2009) Hippocampal atrophy predicts conversion to dementia after STN-DBS in Parkinson’s disease. Parkinsonism Relat Disord 15:521–524CrossRefGoogle Scholar
  4. Bonneville F, Welter ML, Elie C et al (2005) Parkinson disease, brain volumes, and subthalamic nucleus stimulation. Neurology 64:1598–1604CrossRefGoogle Scholar
  5. Camicioli R, Sabino J, Gee M et al (2011) Ventricular dilatation and brain atrophy in patients with Parkinson’s disease with incipient dementia. Mov Disord 26:1443–1450CrossRefGoogle Scholar
  6. Carriere N, Besson P, Dujardin K et al (2014) Apathy in Parkinson’s disease is associated with nucleus accumbens atrophy: a magnetic resonance imaging shape analysis. Mov Disord 29:897–903CrossRefGoogle Scholar
  7. Charles PD, Van Blercom N, Krack P et al (2002) Predictors of effective bilateral subthalamic nucleus stimulation for PD. Neurology 59:932–934CrossRefGoogle Scholar
  8. Contarino MF, Daniele A, Sibilia AH et al (2007) Cognitive outcome 5 years after bilateral chronic stimulation of subthalamic nucleus in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 78:248–252CrossRefGoogle Scholar
  9. Daniels C, Krack P, Volkmann J et al (2010) Risk factors for executive dysfunction after subthalamic nucleus stimulation in Parkinson’s disease. Mov Disord 25:1583–1589CrossRefGoogle Scholar
  10. de Chazeron I, Pereira B, Chereau-Boudet I et al (2016) Impact of localisation of deep brain stimulation electrodes on motor and neurobehavioural outcomes in Parkinson’s disease. J Neurol Neurosurg Psychiatry 87:758–766CrossRefGoogle Scholar
  11. Desikan RS, Ségonne F, Fischl B et al (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31:968–980CrossRefGoogle Scholar
  12. Dujardin K, Devos D, Duhem S et al (2006) Utility of the Mattis dementia rating scale to assess the efficacy of rivastigmine in dementia associated with Parkinson’s disease. J Neurol 253:1154–1159CrossRefGoogle Scholar
  13. Emre M (2004) Dementia in Parkinson’s disease: cause and treatment. Curr Opin Neurol 17:399–404CrossRefGoogle Scholar
  14. Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055CrossRefGoogle Scholar
  15. Funkiewiez A, Ardouin C, Caputo E et al (2004) Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease. J Neurol Neurosurg Psychiatry 75:834–839CrossRefGoogle Scholar
  16. Hanganu A, Bedetti C, Degroot C et al (2014) Mild cognitive impairment is linked with faster rate of cortical thinning in patients with Parkinson’s disease longitudinally. Brain 137:1120–1129CrossRefGoogle Scholar
  17. Houvenaghel J-F, Le Jeune F, Dondaine T et al (2015) Reduced verbal fluency following subthalamic deep brain stimulation: a frontal-related cognitive deficit? PloS One 10:e0140083CrossRefGoogle Scholar
  18. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184CrossRefGoogle Scholar
  19. Ibarretxe-Bilbao N, Junque C, Segura B et al (2012) Progression of cortical thinning in early Parkinson’s disease. Mov Disord 27:1746–1753CrossRefGoogle Scholar
  20. Kim H-J, Jeon BS, Paek SH et al (2014) Long-term cognitive outcome of bilateral subthalamic deep brain stimulation in Parkinson’s disease. J Neurol 261:1090–1096CrossRefGoogle Scholar
  21. 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 349:1925–1934CrossRefGoogle Scholar
  22. Lang AE, Houeto J-L, Krack P et al (2006) Deep brain stimulation: preoperative issues. Mov Disord 21(Suppl 14):S171–S196CrossRefGoogle Scholar
  23. Le Goff F, Derrey S, Lefaucheur R et al (2015) Decline in verbal fluency after subthalamic nucleus deep brain stimulation in Parkinson’s disease: a microlesion effect of the electrode trajectory? J Park Dis 5:95–104Google Scholar
  24. 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):S109-115Google Scholar
  25. 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:S837–S847CrossRefGoogle Scholar
  26. Mak E, Su L, Williams GB et al (2015) Baseline and longitudinal grey matter changes in newly diagnosed Parkinson’s disease: ICICLE-PD study. Brain 138:2974–2986CrossRefGoogle Scholar
  27. Manjón JV, Coupé P (2016) volBrain: an online MRI brain volumetry system. Front Neuroinform 10:30CrossRefGoogle Scholar
  28. Markser A, Maier F, Lewis CJ et al (2015) Deep brain stimulation and cognitive decline in Parkinson’s disease: the predictive value of electroencephalography. J Neurol 262:2275–2284. dCrossRefGoogle Scholar
  29. Marson DC, Dymek MP, Duke LW, Harrell LE (1997) Subscale validity of the Mattis dementia rating scale. Arch Clin Neuropsychol 12:269–275CrossRefGoogle Scholar
  30. Næss-Schmidt E, Tietze A, Blicher JU et al (2016) Automatic thalamus and hippocampus segmentation from MP2RAGE: comparison of publicly available methods and implications for DTI quantification. Int J Comput Assist Radiol Surg 11:1979–1991CrossRefGoogle Scholar
  31. Parsons TD, Rogers SA, Braaten AJ et al (2006) Cognitive sequelae of subthalamic nucleus deep brain stimulation in Parkinson’s disease: a meta-analysis. Lancet Neurol 5:578–588CrossRefGoogle Scholar
  32. Pessoa L (2009) How do emotion and motivation direct executive control? Trends Cognit Sci 13:160–166CrossRefGoogle Scholar
  33. Pigott K, Rick J, Xie SX et al (2015) Longitudinal study of normal cognition in Parkinson disease. Neurology 85:1276–1282CrossRefGoogle Scholar
  34. Saint-Cyr JA, Trépanier LL, Kumar R et al (2000) Neuropsychological consequences of chronic bilateral stimulation of the subthalamic nucleus in Parkinson’s disease. Brain 123(Pt 10):2091–2108CrossRefGoogle Scholar
  35. Schuepbach WMM, Rau J, Knudsen K et al (2013) Neurostimulation for Parkinson’s disease with early motor complications. N Engl J Med 368:610–622CrossRefGoogle Scholar
  36. Segura B, Baggio HC, Marti MJ et al (2014) Cortical thinning associated with mild cognitive impairment in Parkinson’s disease. Mov Disord 29:1495–1503CrossRefGoogle Scholar
  37. Smeding HMM, Speelman JD, Huizenga HM et al (2011) Predictors of cognitive and psychosocial outcome after STN DBS in Parkinson’s Disease. J Neurol Neurosurg Psychiatry 82:754–760CrossRefGoogle Scholar
  38. Thobois S (2006) Proposed dose equivalence for rapid switch between dopamine receptor agonists in Parkinson’s disease: a review of the literature. Clin Ther 28:1–12CrossRefGoogle Scholar
  39. Tsai S-T, Lin S-H, Lin S-Z et al (2007) Neuropsychological effects after chronic subthalamic stimulation and the topography of the nucleus in Parkinson’s disease. Neurosurgery 61:E1024–E1029 (discussion E1029–E1030).CrossRefGoogle Scholar
  40. Welter ML, Houeto JL, Tezenas du Montcel S et al (2002) Clinical predictive factors of subthalamic stimulation in Parkinson’s disease. Brain 125:575–583CrossRefGoogle Scholar
  41. Welter M-L, Schüpbach M, Czernecki V et al (2014) Optimal target localization for subthalamic stimulation in patients with Parkinson disease. Neurology 82:1352–1361CrossRefGoogle Scholar
  42. Witt K, Daniels C, Reiff J et al (2008) Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson’s disease: a randomised, multicentre study. Lancet Neurol 7:605–614CrossRefGoogle Scholar
  43. Witt K, Granert O, Daniels C et al (2013) Relation of lead trajectory and electrode position to neuropsychological outcomes of subthalamic neurostimulation in Parkinson’s disease: results from a randomized trial. Brain 136:2109–2119CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Vincent Planche
    • 1
    Email author
  • Fanny Munsch
    • 2
  • Bruno Pereira
    • 3
  • Emmanuel de Schlichting
    • 4
  • Tiphaine Vidal
    • 5
  • Jerome Coste
    • 4
  • Dominique Morand
    • 3
  • Ingrid de Chazeron
    • 6
  • Philippe Derost
    • 1
  • Bérangère Debilly
    • 1
  • Pierre-Michel Llorca
    • 6
  • Jean-Jacques Lemaire
    • 4
  • Ana Marques
    • 1
  • Franck Durif
    • 1
  1. 1.Service de Neurologie, CHU Clermont-FerrandUniversité Clermont AuvergneClermont-FerrandFrance
  2. 2.Service de Neuroradiologie diagnostique et thérapeutique, CHU BordeauxUniversité BordeauxBordeauxFrance
  3. 3.Unité de Biostatistiques, Direction à la Recherche Clinique et à l’Innovation (DRCI)CHU Clermont-FerrandClermont-FerrandFrance
  4. 4.Service de Neurochirurgie, CHU Clermont-Ferrand, Centre National de la Recherche Scientifique (CNRS)Université Clermont AuvergneClermont-FerrandFrance
  5. 5.Centre Mémoire de Ressources et de Recherche (CMRR)CHU Clermont-FerrandClermont-FerrandFrance
  6. 6.Centre Médico-Psychologique B (CMP-B), CHU Clermont-FerrandUniversité Clermont AuvergneClermont-FerrandFrance

Personalised recommendations