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Deep brain stimulation of the subthalamic nucleus in severe Parkinson’s disease: relationships between dual-contact topographic setting and 1-year worsening of speech and gait

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Abstract

Background

Subthalamic nucleus (STN) deep brain stimulation (DBS) alleviates severe motor fluctuations and dyskinesia in Parkinson’s disease, but may result in speech and gait disorders. Among the suspected or demonstrated causes of these adverse effects, we focused on the topography of contact balance (CB; individual, right and left relative dual positions), a scantly studied topic, analyzing the relationships between symmetric or non-symmetric settings, and the worsening of these signs.

Method

An observational monocentric study was conducted on a series of 92 patients after ethical approval. CB was specified by longitudinal and transversal positions and relation to the STN (CB sub-aspects) and totalized at the patient level (patient CB). CB was deemed symmetric when the two contacts were at the same locations relative to the STN. CB was deemed asymmetric when at least one sub-aspect differed in the patient CB. Baseline and 1-year characteristics were routinely collected: (i) general, namely, Unified Parkinson’s Disease Rating Scores (UPDRS), II, III motor and IV, daily levodopa equivalent doses, and Parkinson’s Disease Questionnaire of Quality of Life (PDQ39) scores; (ii) specific, namely scores for speech (II-5 and III-18) and axial signs (II-14, III-28, III-29, and III-30). Only significant correlations were considered (p < 0.05).

Results

Baseline characteristics were comparable (symmetric versus asymmetric). CB settings were related to deteriorations of speech and axial signs: communication PDQ39 and UPDRS speech and gait scores worsened exclusively with symmetric settings; the most influential CB sub-aspect was symmetric longitudinal position.

Conclusion

Our findings suggest that avoiding symmetric CB settings, whether by electrode positioning or shaping of electric fields, could reduce worsening of speech and gait.

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Acknowledgements

We thank Dr. Vivien Mendes-Martins (Annecy, France), Dr. François Vassal (Saint-Etienne, France), Dr. François Caire (Limoges, France), Dr. Denys Fontaine (Nice, France), and Dr. Simone Hemm-Ode (Basel, Switzerland), for advice at the start of the study.

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Authors and Affiliations

  1. Université Clermont Auvergne, Clermont Auvergne INP, CHU Clermont-Ferrand, CNRS, Institut Pascal, 63000, Clermont-Ferrand, France

    Youssef El Ouadih, Ana Marques, Maxime Luisoni, Jérôme Coste, Anna Sontheimer, Rémi Chaix, Franck Durif & Jean-Jacques Lemaire

  2. Service de Neurochirurgie, CHU Clermont-Ferrand, 63000, Clermont-Ferrand, France

    Youssef El Ouadih, Jérôme Coste, Anna Sontheimer, Rémi Chaix & Jean-Jacques Lemaire

  3. Service de Neurologie, CHU Clermont-Ferrand, 63000, Clermont-Ferrand, France

    Ana Marques, Bérangère Debilly, Philippe Derost & Franck Durif

  4. Direction de La Recherche Clinique Et de L’Innovation, CHU Clermont-Ferrand, 63000, Clermont-Ferrand, France

    Bruno Pereira & Dominique Morand

  5. Service de Radiologie, Unité de Neuroradiologie, CHU Clermont-Ferrand, 63000, Clermont-Ferrand, France

    Béatrice Claise

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  1. Youssef El Ouadih
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  13. Jean-Jacques Lemaire
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Contributions

Conceptualization, JJL, YEO, AM; methodology, BP, JJL, YEO; validation, YEO, ML, DM, JJL; formal analysis, JJL, YEO, BP; investigation, YEO, AM, ML, BD, PD, DM, FD, JJL; resources, YEO, BC, AS, JC, AM, BD, PD, JJL; data curation, YEO, DM, JC, FD; writing—original draft preparation, JJL, YEO, AM; writing-review and editing, YEO, AM, BP, ML, BC, JC, AS, RC, BD, PD, FD, JJL; visualization, JJL, YEO, BP; supervision, JJL; project administration, BP; All authors have read and agreed to the published version of the manuscript.

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Correspondence to Jean-Jacques Lemaire.

Ethics declarations

Institutional review board statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee: Ethical approval 2020/CE103, South-East VI; agreement approved March 3, 2021.

Informed consent statement

Informed consent was obtained from all the subjects involved in the study, or their representative.

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The authors declare no competing interests.

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Comments

Although deterioration of speech and gait occurring in Parkinson disease (PD) patients over time is a well-known phenomenon; it occurs with or without deep brain stimulation (DBS) surgery and is frequently observed even in patients whose cardinal PD symptoms improve after surgery. Higher incidence of speech and gait worsening after bilateral surgical interventions has been known for decades, but the connection of this phenomenon to specific electrode contact locations, and especially their symmetry, remains unclear. The authors of this large cohort study make a strong argument that symmetricity of contact may be contributing, or directly causing, deterioration of axial issues and speech, but at the same time notice that this may occur with remarkable improvement in other PD symptoms. The question therefore remains if the intentional placement of DBS electrodes in asymmetric locations would eliminate negative effects on speech and gait while maintaining high efficacy for other motor PD manifestations, and whether quality of life in operated PD patients will be higher or lower with alternative electrode setups. It would probably be naïve to expect a panacea-like surgical intervention that would cure a complex neurodegenerative disorder with a simple delivery of electrical impulses, but it is definitely worth trying when it comes to optimization of our surgical approaches and technical nuances. I must admit that I never paid attention to intentional or unintentional symmetry of my implanted DBS electrodes; after reading this study, I would start doing it now.

Konstantin Slavin,

Chicago, USA.

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El Ouadih, Y., Marques, A., Pereira, B. et al. Deep brain stimulation of the subthalamic nucleus in severe Parkinson’s disease: relationships between dual-contact topographic setting and 1-year worsening of speech and gait. Acta Neurochir 165, 3927–3941 (2023). https://doi.org/10.1007/s00701-023-05843-9

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