Impact of Subthalamic Deep Brain Stimulation on Impulse Control Disorders in Parkinson's Disease: A Prospective Study

Marie des Neiges Santin¹, Paul Voulleminot², Agathe Vrillon³, Elodie Hainque^{3

4}, Matthieu Béreau⁵, Ouhaid Lagha-Boukbiza², Thomas Wirth², Solveig Montaut², Eric Bardinet^{5

6}, Maeva Kyheng⁷, Anne-Sophie Rolland⁸, Jimmy Voirin¹, Sophie Drapier⁹, Franck Durif¹⁰, Alexandre Eusebio¹¹, Caroline Giordana¹², Nicolas Auzou¹³, Jean-Luc Houeto¹⁴, Cécile Hubsch¹⁵, Béchir Jarraya¹⁶, Chloé Laurencin¹⁷, David Maltete¹⁸, Mylène Meyer¹⁹, Olivier Rascol²⁰, Tiphaine Rouaud²¹, Mélissa Tir²², Caroline Moreau²³, Jean-Christophe Corvol^{3

4}, François Proust¹, David Grabli³, David Devos^{8

23}, Christine Tranchant², Mathieu Anheim²; Predistim Study Group

Affiliations

¹ Department of Neurosurgery, NS-PARK/F-CRIN, Strasbourg University Hospital, Strasbourg, France.
² Department of Neurology, NS-PARK/F-CRIN, Strasbourg University Hospital, Fédération de Médecine Translationnelle de Médecine de Strasbourg, Strasbourg, France.
³ Department of Neurology, NS-PARK/F-CRIN, Assistance Publique - Hôpitaux de Paris (APHP), Pitié-Salpêtrière Hospital, Paris, France.
⁴ Sorbonne Universités, Assistance Publique - Hôpitaux de Paris (APHP), Inserm, CNRS, Institut du Cerveau et de la Moelle (ICM), Paris, France.
⁵ Department of Neurology, NS-PARK/F-CRIN, University Hospital of Besançon, Besançon, France.
⁶ Centre de Neuroimagerie de Recherche, Institut du Cerveau et de la Moelle (ICM), Paris, France.
⁷ Department of Clinical Research, Lille University Hospital, Lille, France.
⁸ Department of Medical Pharmacology, University Hospital, NS-PARK/F-CRIN, University of Lille, Lille Neuroscience & Cognition, Inserm, UMR-S1172, Lille, France.
⁹ Department of Neurology, NS-PARK/F-CRIN, University Hospital of Rennes, Rennes, France.
¹⁰ Department of Neurology, NS-PARK/F-CRIN, CHU Clermont-Ferrand, Clermont-Ferrand, France.
¹¹ Department of Neurology, NS-PARK/F-CRIN, Assistance Publique - Hôpitaux de Marseille (APHM), Timone University Hospital and Institut de Neurosciences de la Timone, Marseille, France.
¹² Department of Neurology, NS-PARK/F-CRIN, Centre Hospitalier Universitaire de Nice, Nice, France.
¹³ Institute of Neurodegenerative Disorders, NS-PARK/F-CRIN, University Hospital of Bordeaux, Bordeaux, France.
¹⁴ Department of Neurology, NS-PARK/F-CRIN, University Hospital of Poitiers, Poitiers, France.
¹⁵ Department of Neurology, NS-PARK/F-CRIN, Fondation Ophtalmologique Adolphe de Rothschild, Paris, France.
¹⁶ Neuroscience Pole, NS-PARK/F-CRIN, Hôpital Foch, Suresnes, University of Versailles Paris-Saclay, INSERM-CEA NeuroSpin, Saclay, France.
¹⁷ Department of Neurology, NS-PARK/F-CRIN, University Hospital of Lyon, Lyon, France.
¹⁸ Department of Neurology, NS-PARK/F-CRIN, Rouen University Hospital and University of Rouen, France; INSERM U1239, Laboratory of Neuronal and Neuroendocrine Differentiation and Communication, Mont-Saint-Aignan, France.
¹⁹ Department of Neurology, NS-PARK/F-CRIN, University Hospital of Nancy, Nancy, France.
²⁰ Department of Clinical Pharmacology and Neuroscience, NS-Park/F-CRIN, Toulouse University Hospital, Toulouse, France.
²¹ Department of Neurology, NS-PARK/F-CRIN, Nantes University Hospital, Nantes, France.
²² Department of Neurology, NS-PARK/FCRIN, Amiens University Hospital, Amiens, France.
²³ Department of Neurology, University Hospital, NS-PARK/F-CRIN, University of Lille, Lille Neuroscience & Cognition, INSERM, UMR-S1172, Lille, France.

PMID: 33022101
DOI: 10.1002/mds.28320

Impact of Subthalamic Deep Brain Stimulation on Impulse Control Disorders in Parkinson's Disease: A Prospective Study

Marie des Neiges Santin et al. Mov Disord. 2021 Mar.

. 2021 Mar;36(3):750-757.

doi: 10.1002/mds.28320. Epub 2020 Oct 6.

Authors

Affiliations

¹ Department of Neurosurgery, NS-PARK/F-CRIN, Strasbourg University Hospital, Strasbourg, France.
² Department of Neurology, NS-PARK/F-CRIN, Strasbourg University Hospital, Fédération de Médecine Translationnelle de Médecine de Strasbourg, Strasbourg, France.
³ Department of Neurology, NS-PARK/F-CRIN, Assistance Publique - Hôpitaux de Paris (APHP), Pitié-Salpêtrière Hospital, Paris, France.
⁴ Sorbonne Universités, Assistance Publique - Hôpitaux de Paris (APHP), Inserm, CNRS, Institut du Cerveau et de la Moelle (ICM), Paris, France.
⁵ Department of Neurology, NS-PARK/F-CRIN, University Hospital of Besançon, Besançon, France.
⁶ Centre de Neuroimagerie de Recherche, Institut du Cerveau et de la Moelle (ICM), Paris, France.
⁷ Department of Clinical Research, Lille University Hospital, Lille, France.
⁸ Department of Medical Pharmacology, University Hospital, NS-PARK/F-CRIN, University of Lille, Lille Neuroscience & Cognition, Inserm, UMR-S1172, Lille, France.
⁹ Department of Neurology, NS-PARK/F-CRIN, University Hospital of Rennes, Rennes, France.
¹⁰ Department of Neurology, NS-PARK/F-CRIN, CHU Clermont-Ferrand, Clermont-Ferrand, France.
¹¹ Department of Neurology, NS-PARK/F-CRIN, Assistance Publique - Hôpitaux de Marseille (APHM), Timone University Hospital and Institut de Neurosciences de la Timone, Marseille, France.
¹² Department of Neurology, NS-PARK/F-CRIN, Centre Hospitalier Universitaire de Nice, Nice, France.
¹³ Institute of Neurodegenerative Disorders, NS-PARK/F-CRIN, University Hospital of Bordeaux, Bordeaux, France.
¹⁴ Department of Neurology, NS-PARK/F-CRIN, University Hospital of Poitiers, Poitiers, France.
¹⁵ Department of Neurology, NS-PARK/F-CRIN, Fondation Ophtalmologique Adolphe de Rothschild, Paris, France.
¹⁶ Neuroscience Pole, NS-PARK/F-CRIN, Hôpital Foch, Suresnes, University of Versailles Paris-Saclay, INSERM-CEA NeuroSpin, Saclay, France.
¹⁷ Department of Neurology, NS-PARK/F-CRIN, University Hospital of Lyon, Lyon, France.
¹⁸ Department of Neurology, NS-PARK/F-CRIN, Rouen University Hospital and University of Rouen, France; INSERM U1239, Laboratory of Neuronal and Neuroendocrine Differentiation and Communication, Mont-Saint-Aignan, France.
¹⁹ Department of Neurology, NS-PARK/F-CRIN, University Hospital of Nancy, Nancy, France.
²⁰ Department of Clinical Pharmacology and Neuroscience, NS-Park/F-CRIN, Toulouse University Hospital, Toulouse, France.
²¹ Department of Neurology, NS-PARK/F-CRIN, Nantes University Hospital, Nantes, France.
²² Department of Neurology, NS-PARK/FCRIN, Amiens University Hospital, Amiens, France.
²³ Department of Neurology, University Hospital, NS-PARK/F-CRIN, University of Lille, Lille Neuroscience & Cognition, INSERM, UMR-S1172, Lille, France.

PMID: 33022101
DOI: 10.1002/mds.28320

Abstract

Background: Impact of subthalamic deep brain stimulation (DBS) on impulse control disorders (ICD) in Parkinson's disease (PD) remains controversial.

Objectives: The objectives of this study were to analyze the natural history of ICD between baseline and 1 year after subthalamic DBS in patients with PD and to identify predictive factors, taking into account the positions of the active contact and stimulation parameters.

Methods: We analyzed postoperative modifications of ICD based on the multicentric, prospective Predictive Factors and Subthalamic Stimulation in Parkinson's Disease cohort. ICD status and Ardouin Scale of Behaviour in PD were assessed at baseline and 1 year following subthalamic DBS. Location of active contacts within the 3 subthalamic nucleus functional territories was investigated.

Results: A total of 217 were patients included. Of the patients, 10.6% had ICD at baseline of which 95.6% improved at 1 year following subthalamic DBS; 3.6% of the patients experienced de novo ICD at 1 year following subthalamic DBS. Dopamine agonist dose reduction (from 309.8 to 109.3 mg) was the main driver of ICD regression (P = 0.05). Higher preoperative dyskinesias were associated with poorer ICD evolution (P = 0.04). Whereas baseline apathy was a risk factor of de novo ICD (P = 0.02), ICD improvement correlated with postoperative apathy (P = 0.004). Stimulation power and position of active contacts-mainly located within the sensorimotor part of the subthalamic nucleus-did not influence ICD.

Conclusions: This 1-year, postoperative follow-up study showed ICD regression and dopaminergic drug reduction with optimal position of the active contacts within the subthalamic nucleus. Whereas patients with PD with preoperative ICD were prone to postoperative apathy, we also showed that those with preoperative apathy had a higher risk to experience postoperative de novo ICD, further highlighting the meaningful influence of postoperative management of dopaminergic medication on outcome and the continuum between apathy and ICD. © 2020 International Parkinson and Movement Disorder Society.

Trial registration: ClinicalTrials.gov NCT02360683.

Keywords: impulse control disorder; deep brain stimulation; STN functional territories; Parkinson's disease; prognosis.

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References

1. Vilas D, Pont-Sunyer C, Tolosa E. Impulse control disorders in Parkinson's disease. Parkinsonism Relat Disord 2012;18:S80-S84.
1. Lhommée E, Klinger H, Thobois S, et al. Subthalamic stimulation in Parkinson's disease: restoring the balance of motivated behaviours. Brain 2012;135(5):1463-1477.
1. Lhommée E, Wojtecki L, Czernecki V, et al. Behavioural outcomes of subthalamic stimulation and medical therapy versus medical therapy alone for Parkinson's disease with early motor complications (EARLYSTIM trial): secondary analysis of an open-label randomised trial. Lancet Neurol 2018;17(3):223-231.
1. Amami P, Dekker I, Piacentini S, 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 Psychiat 2015;86(5):562-564.
1. Kasemsuk C, Oyama G, Hattori N. Management of impulse control disorders with deep brain stimulation: a double-edged sword. J Neurol Sci 2017;374:63-68.

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Impact of Subthalamic Deep Brain Stimulation on Impulse Control Disorders in Parkinson's Disease: A Prospective Study

Affiliations

Impact of Subthalamic Deep Brain Stimulation on Impulse Control Disorders in Parkinson's Disease: A Prospective Study

Authors

Affiliations

Abstract

References

Publication types

MeSH terms

Associated data

LinkOut - more resources

Full Text Sources

Medical