Combining Multimodal Biomarkers to Guide Deep Brain Stimulation Programming in Parkinson Disease

Ashesh Shah; Thuy-Anh Khoa Nguyen; Katrin Peterman; Saed Khawaldeh; Ines Debove; Syed Ahmar Shah; Flavie Torrecillos; Huiling Tan; Alek Pogosyan; Martin Lenard Lachenmayer; Joan Michelis; Peter Brown; Claudio Pollo; Paul Krack; Andreas Nowacki; Gerd Tinkhauser

doi:10.1016/j.neurom.2022.01.017

Combining Multimodal Biomarkers to Guide Deep Brain Stimulation Programming in Parkinson Disease

Neuromodulation. 2023 Feb;26(2):320-332. doi: 10.1016/j.neurom.2022.01.017. Epub 2022 Feb 24.

Authors

Ashesh Shah¹, Thuy-Anh Khoa Nguyen², Katrin Peterman¹, Saed Khawaldeh³, Ines Debove¹, Syed Ahmar Shah⁴, Flavie Torrecillos⁵, Huiling Tan⁵, Alek Pogosyan⁵, Martin Lenard Lachenmayer¹, Joan Michelis¹, Peter Brown⁵, Claudio Pollo⁶, Paul Krack¹, Andreas Nowacki⁶, Gerd Tinkhauser⁷

Affiliations

¹ Department of Neurology, Bern University Hospital, University of Bern, Bern, Switzerland.
² Department of Neurosurgery, Bern University Hospital, University of Bern, Bern, Switzerland; ARTORG Center for Biomedical Engineering Research, University of Bern, Bern, Switzerland.
³ MRC Brain Network Dynamics Unit, University of Oxford, Oxford, UK; Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK; Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, Oxford, UK.
⁴ Usher Institute, Edinburgh Medical School, The University of Edinburgh, Edinburgh, UK.
⁵ MRC Brain Network Dynamics Unit, University of Oxford, Oxford, UK; Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK.
⁶ Department of Neurosurgery, Bern University Hospital, University of Bern, Bern, Switzerland.
⁷ Department of Neurology, Bern University Hospital, University of Bern, Bern, Switzerland. Electronic address: gerd.tinkhauser@insel.ch.

Abstract

Background: Deep brain stimulation (DBS) programming of multicontact DBS leads relies on a very time-consuming manual screening procedure, and strategies to speed up this process are needed. Beta activity in subthalamic nucleus (STN) local field potentials (LFP) has been suggested as a promising marker to index optimal stimulation contacts in patients with Parkinson disease.

Objective: In this study, we investigate the advantage of algorithmic selection and combination of multiple resting and movement state features from STN LFPs and imaging markers to predict three relevant clinical DBS parameters (clinical efficacy, therapeutic window, side-effect threshold).

Materials and methods: STN LFPs were recorded at rest and during voluntary movements from multicontact DBS leads in 27 hemispheres. Resting- and movement-state features from multiple frequency bands (alpha, low beta, high beta, gamma, fast gamma, high frequency oscillations [HFO]) were used to predict the clinical outcome parameters. Subanalyses included an anatomical stimulation sweet spot as an additional feature.

Results: Both resting- and movement-state features contributed to the prediction, with resting (fast) gamma activity, resting/movement-modulated beta activity, and movement-modulated HFO being most predictive. With the proposed algorithm, the best stimulation contact for the three clinical outcome parameters can be identified with a probability of almost 90% after considering half of the DBS lead contacts, and it outperforms the use of beta activity as single marker. The combination of electrophysiological and imaging markers can further improve the prediction.

Conclusion: LFP-guided DBS programming based on algorithmic selection and combination of multiple electrophysiological and imaging markers can be an efficient approach to improve the clinical routine and outcome of DBS patients.

Keywords: DBS programming; Parkinson disease; deep brain stimulation; local field potentials; subthalamic nucleus.

MeSH terms

Biomarkers
Deep Brain Stimulation* / methods
Humans
Movement / physiology
Parkinson Disease* / diagnostic imaging
Parkinson Disease* / therapy
Subthalamic Nucleus* / diagnostic imaging
Subthalamic Nucleus* / physiology
Treatment Outcome

Substances

Biomarkers

Abstract

MeSH terms

Substances

Grants and funding