Direct Current Stimulation of Prefrontal Cortex Is Not Effective in Progressive Supranuclear Palsy: A Randomized Trial.

cognition depression progressive supranuclear palsy stimulation tDCS

Journal

Movement disorders : official journal of the Movement Disorder Society
ISSN: 1531-8257
Titre abrégé: Mov Disord
Pays: United States
ID NLM: 8610688

Informations de publication

Date de publication:
12 Mar 2024
Historique:
revised: 16 02 2024
received: 13 01 2024
accepted: 20 02 2024
medline: 12 3 2024
pubmed: 12 3 2024
entrez: 12 3 2024
Statut: aheadofprint

Résumé

Progressive supranuclear palsy (PSP) is a rare 4R-tauopathy. Transcranial direct current stimulation (tDCS) may improve specific symptoms. This randomized, double-blinded, sham-controlled trial aimed at verifying the short-, mid-, and long-term effect of multiple sessions of anodal tDCS over the left dorsolateral prefrontal cortex (DLPFC) cortex in PSP. Twenty-five patients were randomly assigned to active or sham stimulation (2 mA for 20 minute) for 5 days/week for 2 weeks. Participants underwent assessments at baseline, after the 2-week stimulation protocol, then after 45 days and 3 months from baseline. Primary outcomes were verbal and semantic fluency. The efficacy was verified with analysis of covariance. We failed to detect a significant effect of active stimulation on primary outcomes. Stimulation was associated to worsening of specific behavioral complaints. A 2-week protocol of anodal left DLPFC tDCS is not effective in PSP. Specific challenges in running symptomatic clinical trials with classic design are highlighted. © 2024 International Parkinson and Movement Disorder Society.

Sections du résumé

BACKGROUND BACKGROUND
Progressive supranuclear palsy (PSP) is a rare 4R-tauopathy. Transcranial direct current stimulation (tDCS) may improve specific symptoms.
OBJECTIVES OBJECTIVE
This randomized, double-blinded, sham-controlled trial aimed at verifying the short-, mid-, and long-term effect of multiple sessions of anodal tDCS over the left dorsolateral prefrontal cortex (DLPFC) cortex in PSP.
METHODS METHODS
Twenty-five patients were randomly assigned to active or sham stimulation (2 mA for 20 minute) for 5 days/week for 2 weeks. Participants underwent assessments at baseline, after the 2-week stimulation protocol, then after 45 days and 3 months from baseline. Primary outcomes were verbal and semantic fluency. The efficacy was verified with analysis of covariance.
RESULTS RESULTS
We failed to detect a significant effect of active stimulation on primary outcomes. Stimulation was associated to worsening of specific behavioral complaints.
CONCLUSIONS CONCLUSIONS
A 2-week protocol of anodal left DLPFC tDCS is not effective in PSP. Specific challenges in running symptomatic clinical trials with classic design are highlighted. © 2024 International Parkinson and Movement Disorder Society.

Identifiants

pubmed: 38468604
doi: 10.1002/mds.29774
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024 International Parkinson and Movement Disorder Society.

Références

Höglinger GU, Respondek G, Stamelou M, et al. Clinical diagnosis of progressive supranuclear palsy: the Movement Disorder Society criteria. Mov Disord 2017;32(6):853-886.
Grimm MJ, Respondek G, Stamelou M, et al. How to apply the movement disorder society criteria for diagnosis of progressive supranuclear palsy. Mov Disord 2019;34(8):1228-1232.
Williams DR, Lees AJ. Progressive supranuclear palsy: Clinicopathological concepts and diagnostic challenges. Lancet Neurol 2009;8(3):270-279.
Boxer AL, Yu JT, Golbe LI, Litvan I, Lang AE. Advances in progressive supranuclear palsy: new diagnostic criteria, biomarkers, and therapeutic approaches. Lancet Neurol 2017;16(7):552-563.
Woods AJ, Antal A, Bikson M, et al. A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin Neurophysiol 2016;27(2):1031-1048.
Lefaucheur JP, Antal A, Ayache SS, et al. Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Clin Neurophysiol 2017;128(1):56-92.
Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 2001;57(10):1899-1901.
Elder GJ, Taylor JP. Transcranial magnetic stimulation and transcranial direct current stimulation: treatments for cognitive and neuropsychiatric symptoms in the neurodegenerative dementias? Alzheimers Res Ther 2014;6(9):74.
Benussi A, Dell'Era V, Cosseddu M, et al. Transcranial stimulation in frontotemporal dementia: a randomized, double-blind, sham-controlled trial. Alzheimers Dement (N Y) 2020;6(1):e12033.
Boggio PS, Ferrucci R, Rigonatti SP, et al. Effects of transcranial direct current stimulation on working memory in patients with Parkinson's disease. J Neurol Sci 2006;249(1):31-38.
Pereira JB, Junqué C, Bartrés-Faz D, et al. Modulation of verbal fluency networks by transcranial direct current stimulation (tDCS) in Parkinson's disease. Brain Stimul 2013;6(1):16-24.
Lau CI, Liu MN, Chang KC, et al. Effect of single-session transcranial direct current stimulation on cognition in Parkinson's disease. CNS Neurosci Ther 2019;25(11):1237-1243.
Teichmann M, Lesoil C, Godard J, Vernet M, Bertrand A, Levy R, et al. Direct current stimulation over the anterior temporal areas boosts semantic processing in primary progressive aphasia. Ann Neurol 2016;80(5):693-707.
Paviour DC, Price SL, Jahanshahi M, Lees AJ, Fox NC. Regional brain volumes distinguish PSP, MSA-P, and PD: MRI-based clinico-radiological correlations. Mov Disord 2006;21:989-996.
Cordato NJ, Duggins AJ, Halliday GM, Morris JGL, Pantelis C. Clinical deficits correlate with regional cerebral atrophy in progressive supranuclear palsy. Brain 2005;128:1259-1266.
Valero-Cabré A, Sanches C, Godard J, et al. Language boosting by transcranical stimulation in progressive supranuclear palsy. Neurology 2019;93:1-11.
Wysokiński A, Magierska J, Magierski R. No cognitive effects of computer-assisted cognitive rehabilitation augmented with transcranial direct current stimulation in a patient with progressive Supranuclear palsy. J ECT 2022;38(3):220-221.
Alexoudi A, Patrikelis P, Deftereos S, et al. Effects of anodal transcranial direct current stimulation on cognitive dysfunction in patients with progressive supranuclear palsy. Psychiatriki 2019;30(4):320-328.
Madden DL, Sale MV, O'Sullivan J, Robinson GA. Improved language production with transcranial direct current stimulation in progressive supranuclear palsy. Neuropsychologia 2019;127:148-157.
Roncero C, Friedman M, Whittaker K, Popov A. Administration of 4 mA tDCS to a person with progressive supranuclear palsi leads to improved walking speed. Brain Stimul 2021;14(6):1563-1565.
Avins AL. Can unequal be more fair? Ethics, subject allocation, and randomised clinical trials. J Med Ethics 1998;24(6):401-408.
Golbe LI, Ohman-Strickland PA. A clinical rating scale for progressive supranuclear palsy. Brain 2007;130(6):1552-1565.
Abate F, Russo M, Ricciardi C, et al. Wearable sensors for assessing disease severity and progression in progressive Supranuclear palsy. Parkinsonism Relat Disord 2023;109:105345.
Picillo M, Cuoco S, Tepedino MF, et al. Motor, cognitive and behavioral differences in MDS PSP phenotypes. J Neurol 2019;266(7):1727-1735.
Picillo M, Cuoco S, Amboni M, et al. Validation of the Italian version of the PSP quality of life questionnaire. Neurol Sci 2019;40(12):2587-2594.
Cummings JL, Mega M, Gray K, Rosenberg-Thompson S, Carusi DA, Gornbein J. The neuropsychiatric inventory: comprehensive assessment of psychopathology in dementia. Neurology 1994;44(12):2308-2314.
Schwab RS, England AC. Projection technique for evaluating surgery in Parkinson's disease. In: Gillingham FJ, Donaldson IML, eds. Third Symposium on Parkinson's Disease. Edinburgh: Livingstone; 1969:152-157.
Lawton MP, Brody EM. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist 1969;9(3):179-186.
Zarit SH, Reever KE, Bach-Peterson J. Relatives of the impaired elderly: correlates of feelings of burden. Gerontologist 1980;20(6):649-655.
Busner J, Targum SD. The clinical global impressions scale: applying a research tool in clinical practice. Psychiatry (Edgmont) 2007;4(7):28-37.
Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971;9(1):97-113.
Dagan M, Herman T, Mirelman A, Giladi N, Hausdorff JM. The role of the prefrontal cortex in freezing of gait in Parkinson's disease: insights from a deep repetitive transcranial magnetic stimulation exploratory study. Exp Brain Res 2017;235(8):2463-2472.
Pilotto A, Rizzetti MC, Lombardi A, et al. Cerebellar rTMS in PSP: a double-blind sham-controlled study using Mobile health technology. Cerebellum 2021;20(4):662-666.
Li Y, Izem R. Novel clinical trial design and analytic methods to tackle challenges in therapeutic development in rare diseases. Ann Transl Med 2022;10(18):1034.
Street D, Malpetti M, Rittman T, et al. Clinical progression of progressive supranuclear palsy: impact of trials bias and phenotype variants. Brain Commun 2021;3(3):fcab206.

Auteurs

Arianna Cappiello (A)

Center for Neurodegenerative diseases (CEMAND), Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana", University of Salerno, Fisciano, Italy.

Filomena Abate (F)

Center for Neurodegenerative diseases (CEMAND), Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana", University of Salerno, Fisciano, Italy.

Sarah Adamo (S)

Department of Electrical Engineering and Information Technology, University of Naples Federico II, Naples, Italy.
Department of Advanced Medical and Surgical Sciences, University of Campania 'Luigi Vanvitelli', Napoli, Italy.

Maria Francesca Tepedino (MF)

Center for Neurodegenerative diseases (CEMAND), Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana", University of Salerno, Fisciano, Italy.

Leandro Donisi (L)

Department of Advanced Medical and Surgical Sciences, University of Campania 'Luigi Vanvitelli', Napoli, Italy.

Carlo Ricciardi (C)

Department of Electrical Engineering and Information Technology, University of Naples Federico II, Naples, Italy.
Department of Advanced Medical and Surgical Sciences, University of Campania 'Luigi Vanvitelli', Napoli, Italy.

Anna Rosa Avallone (AR)

Center for Neurodegenerative diseases (CEMAND), Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana", University of Salerno, Fisciano, Italy.

Miriam Caterino (M)

Center for Neurodegenerative diseases (CEMAND), Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana", University of Salerno, Fisciano, Italy.

Sofia Cuoco (S)

Center for Neurodegenerative diseases (CEMAND), Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana", University of Salerno, Fisciano, Italy.

Maria Teresa Pellecchia (MT)

Center for Neurodegenerative diseases (CEMAND), Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana", University of Salerno, Fisciano, Italy.

Marianna Amboni (M)

Center for Neurodegenerative diseases (CEMAND), Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana", University of Salerno, Fisciano, Italy.
IDC Hermitage-Capodimonte, Naples, Italy.

Paolo Barone (P)

Center for Neurodegenerative diseases (CEMAND), Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana", University of Salerno, Fisciano, Italy.

Roberto Erro (R)

Center for Neurodegenerative diseases (CEMAND), Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana", University of Salerno, Fisciano, Italy.

Marina Picillo (M)

Center for Neurodegenerative diseases (CEMAND), Department of Medicine, Surgery and Dentistry "Scuola Medica Salernitana", University of Salerno, Fisciano, Italy.

Classifications MeSH