Predictors of short-term anxiety outcome in subthalamic stimulation for Parkinson's disease

Anna Sauerbier^{1

2}, Johanna Herberg³, Vasilija Stopic³, Philipp A Loehrer⁴, Keyoumars Ashkan⁵, Alexandra Rizos⁵, Stefanie T Jost³, Jan Niklas Petry-Schmelzer³, Alexandra Gronostay³, Christian Schneider³, Veerle Visser-Vandewalle⁶, Julian Evans⁷, Christopher Nimsky⁸, Gereon R Fink^{3

9}, Angelo Antonini¹⁰, Pablo Martinez-Martin¹¹, Monty Silverdale⁷, Daniel Weintraub¹², Anette Schrag¹³, K Ray Chaudhuri^{14

5}, Lars Timmermann⁴, Haidar S Dafsari¹⁵; EUROPAR, the German Parkinson Society Non-motor Symptoms Study Group, and the International Parkinson and Movement Disorders Society Non-Motor Parkinson’s Disease Study Group

Collaborators, Affiliations

Collaborators

EUROPAR, the German Parkinson Society Non-motor Symptoms Study Group, and the International Parkinson and Movement Disorders Society Non-Motor Parkinson’s Disease Study Group:
Charles Adler, Roongroj Bhidayasiri, Per Borghammer, Paolo Barone, David J Brooks, Richard Brown, Marc Cantillon, Camille Carroll, Miguel Coelho, Cristian Falup-Pecurariu, Tove Henriksen, Michele Hu, Peter Jenner, Beomseok Jeon, Milica Kramberger, Padma Kumar, Mónica Kurtis, Valentina Leta, Simon Lewis, Irene Litvan, Kelly Lyons, Davide Martino, Mario Masellis, Hideki Mochizuki, James F Morley, Melissa Nirenberg, Per Odin, Javier Pagonabarraga, Jalesh Panicker, Nicola Pavese, Eero Pekkonen, Ron Postuma, Mayela Rodriguez Violante, Raymond Rosales, Anthony Schapira, Tanya Simuni, Fabrizio Stocchi, Alexander Storch, Indu Subramanian, Michele Tagliati, Michele Tinazzi, Jon Toledo, Yoshio Tsuboi, Richard Walker

Affiliations

¹ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Neurology, Cologne, Germany. anna.sauerbier@uk-koeln.de.
² Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK. anna.sauerbier@uk-koeln.de.
³ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Neurology, Cologne, Germany.
⁴ Department of Neurology, University Hospital Giessen and Marburg, Campus Marburg, Marburg, Germany.
⁵ Parkinson Foundation International Centre of Excellence, King's College Hospital, London, UK.
⁶ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Stereotactic and Functional Neurosurgery, Cologne, Germany.
⁷ Department of Neurology and Neurosurgery, Salford Royal NHS Foundation Trust, Manchester Academic Health Science Centre, Greater Manchester, UK.
⁸ Department of Neurosurgery, University Hospital Giessen and Marburg, Campus Marburg, Marburg, Germany.
⁹ Cognitive Neuroscience, Institute of Neuroscience and Medicine (INM-3), Research Centre Jülich, Jülich, Germany.
¹⁰ Parkinson and Movement Disorders Unit, Department of Neurosciences (DNS), University of Padua, Padova, Italy.
¹¹ Center for Networked Biomedical Research in Neurodegenerative Diseases (CIBERNED), Carlos III Institute of Health, Madrid, Spain.
¹² Departments of Psychiatry and Neurology, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-2676, USA.
¹³ Department of Clinical and Movement Neurosciences, UCL Institute of Neurology, University College London, London, UK.
¹⁴ Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹⁵ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Neurology, Cologne, Germany. haidar.dafsari@uk-koeln.de.

PMID: 38851717
PMCID: PMC11162430
DOI: 10.1038/s41531-024-00701-6

Predictors of short-term anxiety outcome in subthalamic stimulation for Parkinson's disease

Anna Sauerbier et al. NPJ Parkinsons Dis. 2024.

. 2024 Jun 8;10(1):114.

doi: 10.1038/s41531-024-00701-6.

Authors

Collaborators

EUROPAR, the German Parkinson Society Non-motor Symptoms Study Group, and the International Parkinson and Movement Disorders Society Non-Motor Parkinson’s Disease Study Group:
Charles Adler, Roongroj Bhidayasiri, Per Borghammer, Paolo Barone, David J Brooks, Richard Brown, Marc Cantillon, Camille Carroll, Miguel Coelho, Cristian Falup-Pecurariu, Tove Henriksen, Michele Hu, Peter Jenner, Beomseok Jeon, Milica Kramberger, Padma Kumar, Mónica Kurtis, Valentina Leta, Simon Lewis, Irene Litvan, Kelly Lyons, Davide Martino, Mario Masellis, Hideki Mochizuki, James F Morley, Melissa Nirenberg, Per Odin, Javier Pagonabarraga, Jalesh Panicker, Nicola Pavese, Eero Pekkonen, Ron Postuma, Mayela Rodriguez Violante, Raymond Rosales, Anthony Schapira, Tanya Simuni, Fabrizio Stocchi, Alexander Storch, Indu Subramanian, Michele Tagliati, Michele Tinazzi, Jon Toledo, Yoshio Tsuboi, Richard Walker

Affiliations

¹ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Neurology, Cologne, Germany. anna.sauerbier@uk-koeln.de.
² Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK. anna.sauerbier@uk-koeln.de.
³ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Neurology, Cologne, Germany.
⁴ Department of Neurology, University Hospital Giessen and Marburg, Campus Marburg, Marburg, Germany.
⁵ Parkinson Foundation International Centre of Excellence, King's College Hospital, London, UK.
⁶ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Stereotactic and Functional Neurosurgery, Cologne, Germany.
⁷ Department of Neurology and Neurosurgery, Salford Royal NHS Foundation Trust, Manchester Academic Health Science Centre, Greater Manchester, UK.
⁸ Department of Neurosurgery, University Hospital Giessen and Marburg, Campus Marburg, Marburg, Germany.
⁹ Cognitive Neuroscience, Institute of Neuroscience and Medicine (INM-3), Research Centre Jülich, Jülich, Germany.
¹⁰ Parkinson and Movement Disorders Unit, Department of Neurosciences (DNS), University of Padua, Padova, Italy.
¹¹ Center for Networked Biomedical Research in Neurodegenerative Diseases (CIBERNED), Carlos III Institute of Health, Madrid, Spain.
¹² Departments of Psychiatry and Neurology, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104-2676, USA.
¹³ Department of Clinical and Movement Neurosciences, UCL Institute of Neurology, University College London, London, UK.
¹⁴ Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
¹⁵ University of Cologne, Faculty of Medicine and University Hospital Cologne, Department of Neurology, Cologne, Germany. haidar.dafsari@uk-koeln.de.

PMID: 38851717
PMCID: PMC11162430
DOI: 10.1038/s41531-024-00701-6

Abstract

The effects of subthalamic nucleus deep brain stimulation (STN-DBS) on anxiety in Parkinson's disease (PD) are understudied. We identified clinical predictors of STN-DBS effects on anxiety in this study. In this prospective, open-label, multicentre study, we assessed patients with anxiety undergoing STN-DBS for PD preoperatively and at 6-month follow-up postoperatively. We assessed the Hospital Anxiety and Depression Scale (HADS-anxiety and depression subscales), Unified PD Rating Scale-motor examination, Scales for Outcomes in PD-motor (SCOPA-M)-activities of daily living (ADL) and -motor complications, Non-Motor Symptom Scale (NMSS), PDQuestionnaire-8 (PDQ-8), and levodopa-equivalent daily dose. We tested changes at follow-up with Wilcoxon signed-rank test and corrected for multiple comparisons (Bonferroni method). We identified patients with a clinically relevant anxiety improvement of anxiety based on a designated threshold of ½ standard deviation of baseline HADS-anxiety. Moreover, we investigated predictors of HADS-anxiety changes with correlations and linear regressions. We included 50 patients with clinically relevant baseline anxiety (i.e., HADS-anxiety ≥ 8) aged 63.1 years ± 8.3 with 10.4 years ± 4.5 PD duration. HADS-anxiety improved significantly at 6-month follow-up as 80% of our cohort experienced clinically relevant anxiety improvement. In predictor analyses, worse baseline SCOPA-ADL and NMSS-urinary domain were associated with greater HADS-anxiety improvements. HADS-anxiety and PDQ-8 changes correlated moderately. Worse preoperative ADL and urinary symptoms predicted favourable postoperative anxiety outcome, which in turn was directly proportionate to greater QoL improvement. This study highlights the importance of detailed anxiety assessments alongside other non-motor and motor symptoms when advising and monitoring patients undergoing STN-DBS for PD.

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Conflict of interest statement

Anna Sauerbier is funded by the Gusyk program and the Advanced Cologne Clinician Scientist program of the Medical Faculty of the University of Cologne and has received funding from the Prof. Klaus Thiemann Foundation. Johanna Herberg reports no financial disclosures. Vasilija Stopic is funded as part of the Advanced Cologne Clinician Scientist program. Philipp A. Loehrer was funded by the SUCCESS-Program of the University Hospital Marburg and the Parkinson’s Foundation. He reports travel grants from AbbVie. Keyoumars Ashkan has received honoraria for educational meetings, travel and consultancy from Medtronic, St Jude Medical and Boston Scientific. Alexandra Rizos has received honorarium from UCB and was supported by a grant from Medtronic. Stefanie T. Jost has received funding from the Prof. Klaus Thiemann Foundation. Jan Niklas Petry-Schmelzer has been funded by the Cologne Clinician Scientist Program (CCSP)/ Faculty of Medicine/ University of Cologne. Funded by the German Research Foundation (DFG, FI 773/15-1) and received travel grants from Boston Scientific. Alexandra Gronostay reports no financial disclosures. Veerle Visser-Vandewalle is funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) – Project-ID 431549029 – SFB 1451, is a member of the advisory boards and reports consultancies for Medtronic, Boston Scientific, Abbott, Insightec and LivaNova. Julian Evans reports no financial disclosures. Christopher Nimsky is consultant for Brainlab and received speaker’s honoraria. Gereon R. Fink is funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) – Project-ID 431549029 – SFB 1451. GRF serves as an editorial board member of Cortex, Neurological Research and Practice, NeuroImage: Clinical, Zeitschrift für Neuropsychologie, and DGNeurologie; receives royalties from the publication of the books Funktionelle MRT in Psychiatrie und Neurologie, Neurologische Differentialdiagnose, and SOP Neurologie; receives royalties from the publication of the neuropsychological tests KAS and Köpps; received honoraria for speaking engagements from Bayer, Desitin, DGN, Ergo DKV, Forum für medizinische Fortbildung FomF GmbH, GSK, Medica Academy Messe Düsseldorf, Medicbrain Healthcare, Novartis, Pfizer, and Sportärztebund NRW. Angelo Antonini reports personal consultancy fees from Zambon, AbbVie, Boehringer Ingelheim, GE, Neuroderm, Biogen, Bial, EVER Neuro Pharma, Therevance, Vectura grants from Chiesi Pharmaceuticals, Lundbeck, Horizon 2020 - PD_Pal Grant 825785, Ministry of Education University and Research (MIUR) Grant ARS01_01081, owns Patent WO2015110261-A1, owns shares from PD Neurotechnology Limited. Pablo Martinez-Martin has received honoraria from Editorial Viguera and Movement Disorder Society for lecturing in courses; from AbbVie for speaking in experts’ meetings and from AbbVie and Zambon for participating in the Advisory Board of epidemiological studies. License fee payments for the King’s Parkinson’s Disease Pain Scale, and grants from the International Parkinson and Movement Disorder Society for development and validation of the MDS-Non-Motor Symptoms Scale. Monty Silverdale has received honoraria from Bial, Britannia and Medtronic. Daniel Weintraub reports no financial disclosures. Anette Schrag reports no financial disclosures. K. Ray Chaudhuri has received funding from Parkinson’s UK, NIHR, UCB, and the European Union; he received honoraria from UCB, Abbott, Britannia, US Worldmeds, and Otsuka Pharmaceuticals; and acted as a consultant for AbbVie, UCB, and Britannia. Lars Timmermann reports grants, personal fees and non-financial support from SAPIENS Steering Brain Stimulation, Medtronic, Boston Scientific and St. Jude Medical. Haidar S. Dafsari reports funding of his work by the EU Joint Programme—Neurodegenerative Disease Research (JPND), the Prof. Klaus Thiemann Foundation, the Felgenhauer Foundation, and the Koeln Fortune Program, and honoraria by Boston Scientific, Medtronic, Bial, and Stadapharm.

Figures

**Fig. 1. Flow chart of recruitment and data acquisition.**
DBS Deep Brain Stimulation, MMSE Mini Mental Status Examination, HADS Hospital Anxiety and Depression Scale.

**Fig. 2. Hospital Anxiety and Depression Scale-anxiety subscale outcomes.**
Anxiety significantly improved at 6-month follow-up compared to baseline. The centre line illustrates median, the bounds of box represent the interquartile range (quartile 1 – quartile 3) and the whiskers extend to the furthest data point in each wing that is within 1.5 times the interquartile range. 6 MFU 6-month follow up, HADS-A Hospital Anxiety and Depression Scale-anxiety subscale, pts points.

See this image and copyright information in PMC

References

1. Deuschl G, et al. A randomized trial of deep-brain stimulation for Parkinson’s disease. N. Engl. J. Med. 2006;355:896–908. doi: 10.1056/NEJMoa060281. - DOI - PubMed
1. Dafsari HS, et al. Beneficial effects of bilateral subthalamic stimulation on alexithymia in Parkinson’s disease. Eur. J. Neurol. 2019;26:222–e217. doi: 10.1111/ene.13773. - DOI - PubMed
1. Jost ST, et al. Neurostimulation for Advanced Parkinson Disease and Quality of Life at 5 Years: A Nonrandomized Controlled Trial. JAMA Netw. Open. 2024;7:e2352177. doi: 10.1001/jamanetworkopen.2023.52177. - DOI - PMC - PubMed
1. Barone, P. et al. The PRIAMO study: a multicenter assessment of nonmotor symptoms and their impact on quality of life in Parkinson’s disease. Mov. Disord.24, 10.1002/mds.22643 (2009). - PubMed
1. Upneja A, Paul BS, Jain D, Choudhary R, Paul G. Anxiety in Parkinson’s Disease: Correlation with Depression and Quality of Life. J. Neurosci. Rural Pract. 2021;12:323–328. doi: 10.1055/s-0041-1722840. - DOI - PMC - PubMed

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Predictors of short-term anxiety outcome in subthalamic stimulation for Parkinson's disease

Collaborators

Affiliations

Predictors of short-term anxiety outcome in subthalamic stimulation for Parkinson's disease

Authors

Collaborators

Affiliations

Abstract

Conflict of interest statement

Figures

References

LinkOut - more resources

Full Text Sources