Subthalamus stimulation in Parkinson disease: Accounting for the bilaterality of contacts

Background: Deep brain stimulation (DBS) in Parkinson's disease uses bi-hemispheric high-frequency stimulation within the subthalamus, however, the specific impacts of bilaterality of DBS are still not clear. Thus, we aimed to study the individual-level clinical impact of locations of right-left contact pair-up accounting for each subthalamic nucleus (STN) anatomy. Methods: Contact locations and effects at 1 year were studied retrospectively in an unselected series of 53 patients operated between 2004 and 2010. Location of contacts was defined relatively to the main axis of STN used to map longitudinal and transversal positions, and STN membership (out meaning out-of-STN). Contact pairings were described via three methods: (i) Unified contact location (UCL) collapsing DBS into an all-in-one contact; (ii) balance of contact pair-up (BCPU), defined as symmetric or asymmetric regardless of laterality; (iii) hemisphere-wise most frequent contact pair-up (MFCP) regardless of BCPU. Clinical data were: mean levodopa equivalent dose, Unified Parkinson's Disease Rating Scale (UPDRS) motor score III without medication, UPDRS II and III speech sub-scores, UPDRS II freezing sub-score, 1 year versus preoperative values, with and without levodopa. Ad-hoc two-sided tests were used for statistical analysis. Results: Worsening speech, was more frequent for UCL_out patients and when the left MFCP contact was rear and/or superolateral, however, it less frequent for BCPU-asymmetric patients. Worsening freezing was more frequent when the right MFCP contact was rear and superolateral. Conclusions: These results point to strategies for minimizing dysarthria and freezing as adverse effects of DBS.

[1]  P Mertens,et al.  Subthalamic nucleus stimulation in Parkinson's disease , 2002, Journal of Neurology.

[2]  P. Krack,et al.  Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson's disease. , 2001, The New England journal of medicine.

[3]  Antonio Daniele,et al.  Treatment of motor and non-motor features of Parkinson's disease with deep brain stimulation , 2012, The Lancet Neurology.

[4]  C. Clayman,et al.  The Human Central Nervous System: A Synopsis and Atlas , 1979 .

[5]  Y. Agid,et al.  Bilateral subthalamic stimulation for Parkinson's disease by using three-dimensional stereotactic magnetic resonance imaging and electrophysiological guidance. , 2000, Journal of neurosurgery.

[6]  A. Lang,et al.  Ten-year outcome of subthalamic stimulation in Parkinson disease: a blinded evaluation. , 2011, Archives of neurology.

[7]  G. Baltuch,et al.  Bilateral stimulation of the subthalamic nucleus in patients with Parkinson disease: a study of efficacy and safety. , 2002, Journal of neurosurgery.

[8]  J. Molinuevo,et al.  Levodopa withdrawal after bilateral subthalamic nucleus stimulation in advanced Parkinson disease. , 2000, Archives of neurology.

[9]  J. Bloch,et al.  Long-term outcome of 50 consecutive Parkinson's disease patients treated with subthalamic deep brain stimulation. , 2008, Parkinsonism & related disorders.

[10]  W D Heiss,et al.  STN-DBS activates the target area in Parkinson disease , 2008, Neurology.

[11]  J. Obeso,et al.  Effect of deep brain stimulation of the subthalamic nucleus on non-motor fluctuations in Parkinson's disease: two-years' follow-up. , 2013, Parkinsonism & related disorders.

[12]  P. Stanzione,et al.  Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson's disease. , 2007, Brain : a journal of neurology.

[13]  C. Bungener,et al.  Coping and quality of life of patients with Parkinson disease who have undergone deep brain stimulation of the subthalamic nucleus. , 2009, Surgical neurology.

[14]  E. Cuny,et al.  Side‐effects of subthalamic stimulation in Parkinson's disease: clinical evolution and predictive factors , 2006, European journal of neurology.

[15]  J. Péron,et al.  Comparison of weight gain and energy intake after subthalamic versus pallidal stimulation in Parkinson's disease , 2009, Movement disorders : official journal of the Movement Disorder Society.

[16]  Jean Régis,et al.  Effects of chronic subthalamic stimulation on nonmotor fluctuations in Parkinson's disease , 2007, Movement disorders : official journal of the Movement Disorder Society.

[17]  P. Kelly,et al.  Location of the active contact within the subthalamic nucleus (STN) in the treatment of idiopathic Parkinson's disease. , 2004, Surgical neurology.

[18]  P. Patil,et al.  Change in fatigue after bilateral subthalamic nucleus deep brain stimulation for Parkinson's disease. , 2012, Parkinsonism & related disorders.

[19]  E. Moro,et al.  Chronic subthalamic nucleus stimulation reduces medication requirements in Parkinson’s disease , 1999, Neurology.

[20]  G. Cantore,et al.  Stimulation of Subthalamic Nuclei Restores a Near Normal Planning Strategy in Parkinson’s Patients , 2013, PloS one.

[21]  T. Videen,et al.  Mood response to deep brain stimulation of the subthalamic nucleus in Parkinson's disease. , 2012, The Journal of neuropsychiatry and clinical neurosciences.

[22]  Elina Tripoliti,et al.  Effects of contact location and voltage amplitude on speech and movement in bilateral subthalamic nucleus deep brain stimulation , 2008, Movement disorders : official journal of the Movement Disorder Society.

[23]  K. Lyons,et al.  The impact of bilateral subthalamic stimulation on non-motor symptoms of Parkinson's disease. , 2011, Parkinsonism & related disorders.

[24]  C. Moreau,et al.  STN-DBS frequency effects on freezing of gait in advanced Parkinson disease , 2008, Neurology.

[25]  M. Gelabert-González,et al.  [Deep brain stimulation in Parkinson's disease]. , 2013, Revista de neurologia.

[26]  O. Rascol,et al.  Does ageing influence deep brain stimulation outcomes in Parkinson's disease? , 2007, Movement disorders : official journal of the Movement Disorder Society.

[27]  J. Villemure,et al.  Long‐term cognitive profile and incidence of dementia after STN‐DBS in Parkinson's disease , 2007, Movement disorders : official journal of the Movement Disorder Society.

[28]  J. Volkmann,et al.  Deep brain stimulation for gait and postural symptoms in Parkinson's disease , 2013, Movement disorders : official journal of the Movement Disorder Society.

[29]  K J Burchiel,et al.  Comparison of pallidal and subthalamic nucleus deep brain stimulation for advanced Parkinson's disease: results of a randomized, blinded pilot study. , 1999, Neurosurgery.

[30]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[31]  Y Agid,et al.  Subthalamic stimulation in Parkinson disease: a multidisciplinary approach. , 2000, Archives of neurology.

[32]  A. Benabid,et al.  Chronic stimulation of subthalamic nucleus improves levodopa-induced dyskinesias in Parkinson's disease , 1997, The Lancet.

[33]  S. Rehncrona,et al.  Subthalamic deep brain stimulation improves smooth pursuit and saccade performance in patients with Parkinson’s disease , 2013, Journal of NeuroEngineering and Rehabilitation.

[34]  H. Pall,et al.  Deep brain stimulation of the subthalamic nucleus for advanced Parkinson disease using general anesthesia: long-term results. , 2012, Journal of neurosurgery.

[35]  H. Steinbusch,et al.  The functional role of the subthalamic nucleus in cognitive and limbic circuits , 2005, Progress in Neurobiology.

[36]  J. Mink,et al.  Subthalamic nucleus stimulation-induced regional blood flow responses correlate with improvement of motor signs in Parkinson disease. , 2008, Brain : a journal of neurology.

[37]  P. Hogarth,et al.  Pallidal vs subthalamic nucleus deep brain stimulation in Parkinson disease. , 2005, Archives of neurology.

[38]  Yan Xie,et al.  Changes in speech characters of patients with Parkinson's disease after bilateral subthalamic nucleus stimulation. , 2011, Journal of voice : official journal of the Voice Foundation.

[39]  R. Gross Randomized trial of deep brain stimulation for Parkinson disease: Thirty-six-month outcomes , 2012 .

[40]  F. Escamilla-Sevilla,et al.  Cognitive Effects of Subthalamic Nucleus Stimulation in Parkinson’s Disease: A Controlled Study , 2012, European Neurology.

[41]  S. Haber,et al.  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 , 2013, The Journal of Neuroscience.

[42]  Lemlih Ouchchane,et al.  Brain mapping in stereotactic surgery: A brief overview from the probabilistic targeting to the patient-based anatomic mapping , 2007, NeuroImage.

[43]  M I Hariz,et al.  Effects of subthalamic stimulation on speech of consecutive patients with Parkinson disease , 2010, Neurology.

[44]  Laura Mancini,et al.  Functional imaging of subthalamic nucleus deep brain stimulation in Parkinson's disease , 2011, Movement disorders : official journal of the Movement Disorder Society.

[45]  G. Deuschl,et al.  A randomized trial of deep-brain stimulation for Parkinson's disease. , 2006, The New England journal of medicine.

[46]  A. Benabid,et al.  Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. , 1998, The New England journal of medicine.

[47]  D. Wildgruber,et al.  Effects of Subthalamic Nucleus Stimulation on Emotional Prosody Comprehension in Parkinson's Disease , 2011, PloS one.

[48]  K J Rothman,et al.  No Adjustments Are Needed for Multiple Comparisons , 1990, Epidemiology.

[49]  Angelo Antonini,et al.  Clinical and cerebral activity changes induced by subthalamic nucleus stimulation in advanced Parkinson's disease: A prospective case-control study , 2009, Clinical Neurology and Neurosurgery.

[50]  Marwan Hariz,et al.  Deep brain stimulation: new techniques. , 2014, Parkinsonism & related disorders.

[51]  Ashwini Sharan,et al.  An Evaluation of Neuroplasticity and Behavior After Deep Brain Stimulation of the Nucleus Accumbens in an Animal Model of Depression , 2011, Neurosurgery.

[52]  Niels Sunde,et al.  Effects of bilateral stimulation of the subthalamic nucleus in patients with severe Parkinson's disease and motor fluctuations , 2002, Movement disorders : official journal of the Movement Disorder Society.

[53]  Sébastien Ourselin,et al.  A three-dimensional, histological and deformable atlas of the human basal ganglia. I. Atlas construction based on immunohistochemical and MRI data , 2007, NeuroImage.

[54]  Young Eun Kim,et al.  Initial cognitive dip after subthalamic deep brain stimulation in Parkinson disease , 2013, Journal of Neurology.

[55]  F. Caire,et al.  Contact position analysis of deep brain stimulation electrodes on post-operative CT images , 2009, Acta Neurochirurgica.

[56]  M. Seiwald,et al.  Deep brain stimulation of the subthalamic nucleus for control of extrapyramidal features in advanced idiopathic Parkinson's disease: one year follow-up , 1999, Journal of Neural Transmission.

[57]  G. Cosnard,et al.  Compléments : White matter anatomy of the human deep brain revisited with high resolution DTI fibre tracking , 2011 .

[58]  A. Berardelli,et al.  Effects of subthalamic nucleus deep brain stimulation and l-dopa on blinking in Parkinson's disease , 2012, Experimental Neurology.

[59]  Jens Volkmann,et al.  Bilateral high-frequency stimulation in the subthalamic nucleus for the treatment of Parkinson disease: correlation of therapeutic effect with anatomical electrode position. , 2002, Journal of neurosurgery.

[60]  B Bioulac,et al.  Clinical and economic results of bilateral subthalamic nucleus stimulation in Parkinson’s disease , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[61]  J. Péron,et al.  Subthalamic nucleus stimulation in Parkinson disease induces apathy , 2009, Neurology.

[62]  S L Pullman,et al.  Operative techniques and morbidity with subthalamic nucleus deep brain stimulation in 100 consecutive patients with advanced Parkinson’s disease , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[63]  J. Obeso,et al.  Bilateral deep brain stimulation in Parkinson's disease: a multicentre study with 4 years follow-up. , 2005, Brain : a journal of neurology.

[64]  S. Hemm,et al.  New electrophysiological mapping combined with MRI in parkinsonian’s subthalamic region , 2009, The European journal of neuroscience.

[65]  Y. Agid,et al.  Long‐term results of a multicenter study on subthalamic and pallidal stimulation in Parkinson's disease , 2010, Movement disorders : official journal of the Movement Disorder Society.

[66]  J. Volkmann,et al.  Basic algorithms for the programming of deep brain stimulation in Parkinson's disease , 2006, Movement disorders : official journal of the Movement Disorder Society.

[67]  Clement Hamani,et al.  Unilateral pedunculopontine stimulation improves falls in Parkinson's disease. , 2010, Brain : a journal of neurology.

[68]  M. Rizzone,et al.  Subthalamic nucleus deep brain stimulation outcome in young onset Parkinson's disease: a role for age at disease onset? , 2011, Journal of Neurology, Neurosurgery & Psychiatry.

[69]  A. Lang,et al.  Double-blind evaluation of subthalamic nucleus deep brain stimulation in advanced Parkinson's disease , 1998, Neurology.

[70]  W. J. Elias,et al.  Effective Subthalamic Nucleus Deep Brain Stimulation Sites May Differ for Tremor, Bradykinesia and Gait Disturbances in Parkinson’s Disease , 2011, Stereotactic and Functional Neurosurgery.

[71]  Didier Dormont,et al.  Optimal target localization for subthalamic stimulation in patients with Parkinson disease , 2014, Neurology.

[72]  A. Benabid,et al.  Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. , 2003, The New England journal of medicine.

[73]  K. Lyons,et al.  Bilateral subthalamic stimulation in patients with Parkinson disease: long-term follow up. , 2003, Journal of neurosurgery.

[74]  M. Hariz,et al.  Verbal Fluency in Patients Receiving Bilateral versus Left-Sided Deep Brain Stimulation of the Subthalamic Nucleus for Parkinson's Disease , 2012, Journal of the International Neuropsychological Society.

[75]  Grant D. Huang,et al.  Pallidal versus subthalamic deep-brain stimulation for Parkinson's disease. , 2010, The New England journal of medicine.

[76]  V Sturm,et al.  Safety and efficacy of pallidal or subthalamic nucleus stimulation in advanced PD , 2001, Neurology.

[77]  Keith Wheatley,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 , 2010, The Lancet Neurology.

[78]  G. Deuschl,et al.  Neurostimulation for Parkinson's disease with early motor complications. , 2013, The New England journal of medicine.

[79]  P. Jannin,et al.  Anatomo-clinical atlases correlate clinical data and electrode contact coordinates: Application to subthalamic deep brain stimulation , 2013, Journal of Neuroscience Methods.

[80]  J. Obeso,et al.  Functional organization of the basal ganglia: Therapeutic implications for Parkinson's disease , 2008, Movement disorders : official journal of the Movement Disorder Society.

[81]  Y. Ben-Shlomo,et al.  Stimulation of the caudal zona incerta is superior to stimulation of the subthalamic nucleus in improving contralateral parkinsonism. , 2006, Brain : a journal of neurology.

[82]  André Parent,et al.  Chemical anatomy of primate basal ganglia , 1995, Progress in Neurobiology.

[83]  Ron Alterman,et al.  Subthalamic deep brain stimulation with a constant-current device in Parkinson's disease: an open-label randomised controlled trial , 2012, The Lancet Neurology.

[84]  Y. Agid,et al.  Long‐term effects of pallidal or subthalamic deep brain stimulation on quality of life in Parkinson's disease , 2009, Movement disorders : official journal of the Movement Disorder Society.

[85]  M. Lanotte,et al.  Comparison of subthalamic nucleus deep brain stimulation and Duodopa in the treatment of advanced Parkinson's disease , 2011, Movement disorders : official journal of the Movement Disorder Society.

[86]  A. Bentivoglio,et al.  Long-term follow up of subthalamic nucleus stimulation in Parkinson's disease. , 2002, Neurology.

[87]  Adrian Danek,et al.  Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson's disease: a randomised, multicentre study , 2008, The Lancet Neurology.

[88]  L. Defebvre,et al.  Exhaustive, one-year follow-up of subthalamic nucleus deep brain stimulation in a large, single-center cohort of parkinsonian patients. , 2007, Neurosurgery.

[89]  G. Gao,et al.  Long-term effects of bilateral deep brain stimulation of the subthalamic nucleus on depression in patients with Parkinson's disease. , 2009, Parkinsonism & related disorders.

[90]  M. Merello,et al.  Deep Brain Stimulation of the Subthalamic Nucleus for the Treatment of Parkinson's Disease , 2008 .

[91]  Young Eun Kim,et al.  Impulse control and related behaviors after bilateral subthalamic stimulation in patients with Parkinson’s disease , 2013, Journal of Clinical Neuroscience.

[92]  S. Rehncrona,et al.  Multicenter study on deep brain stimulation in Parkinson's disease: An independent assessment of reported adverse events at 4 years , 2008, Movement disorders : official journal of the Movement Disorder Society.

[93]  B Bioulac,et al.  POSTMORTEM PROOF OF EFFECTIVENESS OF ZONA INCERTA STIMULATION IN PARKINSON DISEASE , 2008, Neurology.

[94]  P. Derost,et al.  Mechanisms of body weight gain in patients with Parkinson's disease after subthalamic stimulation. , 2007, Brain : a journal of neurology.

[95]  P. Perozzo,et al.  Deep brain stimulation of the subthalamic nucleus: Clinical effectiveness and safety , 2001, Neurology.

[96]  E. Scarnati,et al.  Effects of unilateral pedunculopontine stimulation on electromyographic activation patterns during gait in individual patients with Parkinson’s disease , 2011, Journal of Neural Transmission.

[97]  S. Chabardès,et al.  Deep Brain Stimulation: Are Astrocytes a Key Driver Behind the Scene? , 2014, CNS neuroscience & therapeutics.

[98]  L. Bour,et al.  Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson's disease (NSTAPS study): a randomised controlled trial , 2013, The Lancet Neurology.

[99]  T. Videen,et al.  Cerebral blood flow responses to dorsal and ventral STN DBS correlate with gait and balance responses in Parkinson's disease , 2013, Experimental Neurology.

[100]  P. Llorca,et al.  Is DBS-STN appropriate to treat severe Parkinson disease in an elderly population? , 2007, Neurology.

[101]  J. van Doorn,et al.  Pitch variability in patients with Parkinson's disease: effects of deep brain stimulation of caudal zona incerta and subthalamic nucleus. , 2013, Journal of speech, language, and hearing research : JSLHR.

[102]  [Subthalamic deep brain stimulation for severe idiopathic Parkinson's disease. Location study of the effective contacts]. , 2006, Neuro-Chirurgie.

[103]  Marco Sassi,et al.  Deep brain stimulation and cognitive functions in Parkinson's disease: A three‐year controlled study , 2009, Movement disorders : official journal of the Movement Disorder Society.