Neurostimulation in people with drug-resistant epilepsy: Systematic review and meta-analysis from the ILAE Surgical Therapies Commission.

deep brain stimulation drug-resistant epilepsy neurostimulation responsive neurostimulation vagus nerve stimulation

Journal

Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R

Informations de publication

Date de publication:
06 2022
Historique:
revised: 25 03 2022
received: 27 10 2021
accepted: 28 03 2022
pubmed: 31 3 2022
medline: 7 6 2022
entrez: 30 3 2022
Statut: ppublish

Résumé

Summarize the current evidence on efficacy and tolerability of vagus nerve stimulation (VNS), responsive neurostimulation (RNS), and deep brain stimulation (DBS) through a systematic review and meta-analysis. We followed the Preferred Reporting Items of Systematic reviews and Meta-Analyses reporting standards and searched Ovid Medline, Ovid Embase, and the Cochrane Central Register of Controlled Trials. We included published randomized controlled trials (RCTs) and their corresponding open-label extension studies, as well as prospective case series, with ≥20 participants (excluding studies limited to children). Our primary outcome was the mean (or median, when unavailable) percentage decrease in frequency, as compared to baseline, of all epileptic seizures at last follow-up. Secondary outcomes included the proportion of treatment responders and proportion with seizure freedom. We identified 30 eligible studies, six of which were RCTs. At long-term follow-up (mean 1.3 years), five observational studies for VNS reported a pooled mean percentage decrease in seizure frequency of 34.7% (95% confidence interval [CI]: -5.1, 74.5). In the open-label extension studies for RNS, the median seizure reduction was 53%, 66%, and 75% at 2, 5, and 9 years of follow-up, respectively. For DBS, the median reduction was 56%, 65%, and 75% at 2, 5, and 7 years, respectively. The proportion of individuals with seizure freedom at last follow-up increased significantly over time for DBS and RNS, whereas a positive trend was observed for VNS. Quality of life was improved in all modalities. The most common complications included hoarseness, and cough and throat pain for VNS and implant site pain, headache, and dysesthesia for DBS and RNS. Neurostimulation modalities are an effective treatment option for drug-resistant epilepsy, with improving outcomes over time and few major complications. Seizure-reduction rates among the three therapies were similar during the initial blinded phase. Recent long-term follow-up studies are encouraging for RNS and DBS but are lacking for VNS.

Identifiants

pubmed: 35352349
doi: 10.1111/epi.17243
doi:

Types de publication

Journal Article Meta-Analysis Review Systematic Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

1314-1329

Informations de copyright

© 2022 International League Against Epilepsy.

Références

Kwan P, Brodie MJ. Early identification of refractory epilepsy. N Engl J Med. 2000;3(342):314-9.
Sultana B, Panzini M-A, Veilleux Carpentier A, Comtois J, Rioux B, Gore G, et al. Incidence and prevalence of drug-resistant epilepsy: a systematic review and meta-analysis. Neurology. 2021;27(96):805-17.
Mula M, Cock HR. More than seizures: improving the lives of people with refractory epilepsy. Eur J Neurol. 2015;22:24-30.
Jetté N, Sander JW, Keezer MR. Surgical treatment for epilepsy: the potential gap between evidence and practice. Lancet Neurol. 2016;15:982-94.
Yoo JY, Panov F. Identification and treatment of drug-resistant Epilepsy. Continuum (Minneap Minn). 2019;25:362-80.
Group TVNSS. A randomized controlled trial of chronic vagus nerve stimulation for treatment of medically intractable seizures. Neurology. 1995;45:224-30.
Handforth A, DeGiorgio CM, Schachter SC, Uthman BM, Naritoku DK, Tecoma ES, et al. Vagus nerve stimulation therapy for partial-onset seizures: a randomized active-control trial. Neurology. 1998;51:48-55.
Klinkenberg S, Aalbers MW, Vles JSH, Cornips EMJ, Rijkers K, Leenen L, et al. Vagus nerve stimulation in children with intractable epilepsy: a randomized controlled trial. Dev Med Child Neurol. 2012;54:855-61.
Fisher R, Salanova V, Witt T, Worth R, Henry T, Gross R, et al. Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia. 2010;51:899-908.
Morrell MJ. Responsive cortical stimulation for the treatment of medically intractable partial epilepsy. Neurology. 2011;27(77):1295-304.
Ryvlin P, Rheims S, Hirsch LJ, Sokolov A, Jehi L. Neuromodulation in epilepsy: state-of-the-art approved therapies. Lancet Neurol. 2021;20:1038-47.
Jehi L, Jetté N. Not all that glitters is gold: a guide to surgical trials in epilepsy. Epilepsia Open. 2016;1:22-36.
Gooneratne IK, Green AL, Dugan P, Sen A, Franzini A, Aziz T, et al. Comparing neurostimulation technologies in refractory focal-onset epilepsy. J Neurol Neurosurg Psychiatry. 2016;87:1174-82.
Sprengers M, Vonck K, Carrette E, Marson AG, Boon P. Deep brain and cortical stimulation for epilepsy. Cochrane Database Syst Rev. 2017;(7):CD008497.
Boon P, De Cock E, Mertens A, Trinka E. Neurostimulation for drug-resistant epilepsy: a systematic review of clinical evidence for efficacy, safety, contraindications and predictors for response. Curr Opin Neurol. 2018;31:198-210.
Rolston JD, Englot DJ, Wang DD, Shih T, Chang EF. Comparison of seizure control outcomes and the safety of vagus nerve, thalamic deep brain, and responsive neurostimulation: evidence from randomized controlled trials. Neurosurg Focus. 2012;32:E14.
Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;18(151):264-9, w264.
Bui KT, Abdaem J, Muccilli A, Gore G, Keezer M. Improving the quality of systematic reviews of neurological conditions: an assessment of current practice and the development and validation of six new search strategies. Eur J Neurol. 2018;25:1477-85.
Rothman KJ, Greenland S, Lash TL. Chapter 6: Types of epidemiologic studies. In: Rothman KJ, Greenland S, Lash TL, editors. Modern epidemiology. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins; 1998. p. 87-99.
Reeves BC, Deeks JJ, Higgins JP, Shea B, Tugwell P, Wells GA, et al. Chapter 24: Including non-randomized studies on intervention effects. In: Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA, editors. Cochrane handbook for systematic reviews of interventions version 6.3 (updated February 2022). Cochrane; 2022. www.training.cochrane.org/handbook. Accessed 11 Oct 2021.
Aluko PGE, Craig D, Henderson C, Drummond M, Wilson ECF, Robalino S, et al. Chapter 20: Economic evidence. In: Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA, editors. Cochrane handbook for systematic reviews of interventions version 6.3 (updated February 2022). Cochrane; 2022. www.training.cochrane.org/handbook. Accessed 11 Oct 2021.
Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions. Chichester: John Wiley & Sons; 2008.
Wells GA, Shea B, Higgins JP, Sterne J, Tugwell P, Reeves BC. Checklists of methodological issues for review authors to consider when including non-randomized studies in systematic reviews. Res Synth Methods. 2013;4:63-77.
Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE). Group. JAMA. 2000;19(283):2008-12.
Munn Z, Moola S, Lisy K, Riitano D, Tufanaru C. Methodological guidance for systematic reviews of observational epidemiological studies reporting prevalence and cumulative incidence data. Int J Evid Based Healthc. 2015;13:147-53.
Wan X, Wang W, Liu J, Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol. 2014;19(14):135.
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177-88.
Barendregt JJ, Doi SA, Lee YY, Norman RE, Vos T. Meta-analysis of prevalence. J Epidemiol Community Health. 2013;67:974-8.
García-Pallero MA, García-Navarrete E, Torres CV, Pastor J, Navas M, Sola RG. Effectiveness of vagal nerve stimulation in medication-resistant epilepsy. Comparison between Patients with and without Medication. Acta Neurochir (Wien). 2017;159:131-6.
Colicchio G, Montano N, Fuggetta F, Papacci F, Signorelli F, Meglio M. Vagus nerve stimulation in drug-resistant epilepsies. Analysis of potential prognostic factors in a cohort of patients with long-term follow-up. Acta Neurochir (Wien). 2012;154:2237-40.
Ryvlin P, Gilliam FG, Nguyen DK, Colicchio G, Iudice A, Tinuper P, et al. The long-term effect of vagus nerve stimulation on quality of life in patients with pharmacoresistant focal epilepsy: the PuLsE (Open Prospective Randomized Long-term Effectiveness) trial. Epilepsia. 2014;55:893-900.
Heck CN, King-Stephens D, Massey AD, Nair DR, Jobst BC, Barkley GL, et al. Two-year seizure reduction in adults with medically intractable partial onset epilepsy treated with responsive neurostimulation: final results of the rns system pivotal trial. Epilepsia. 2014;55:432-41.
Nair DR, Laxer KD, Weber PB, Murro AM, Park YD, Barkley GL, et al. Nine-year prospective efficacy and safety of brain-responsive neurostimulation for focal epilepsy. Neurology. 2020;1(95):e1244-56.
Bergey GK, Morrell MJ, Mizrahi EM, Goldman A, King-Stephens D, Nair D, et al. Long-term treatment with responsive brain stimulation in adults with refractory partial seizures. Neurology. 2015;24(84):810-7.
Boon P, Vonck K, D'Have M, O'Connor S, Vandekerckhove T, De Reuck J. Cost-benefit of vagus nerve stimulation for refractory epilepsy. Acta Neurol Belg. 1999;99:275-80.
DeGiorgio C, Heck C, Bunch S, Britton J, Green P, Lancman M, et al. Vagus nerve stimulation for epilepsy: randomized comparison of three stimulation paradigms. Neurology. 2005;26(65):317-9.
Hödl S, Carrette S, Meurs A, Carrette E, Mertens A, Gadeyne S, et al. Neurophysiological investigations of drug resistant epilepsy patients treated with vagus nerve stimulation to differentiate responders from non-responders. Eur J Neurol. 2020;27:1178-89.
Pakdaman H, Amini Harandi A, Abbasi M, Karimi M, Arami MA, Mosavi SA, et al. Vagus nerve stimulation in drug-resistant epilepsy: the efficacy and adverse effects in a 5-year follow-up study in Iran. Neurol Sci. 2016;37:1773-8.
Tohanean N, Pinzaru C, Mirea L, Perju-Dumbrava L. Impact of vagal nerve stimulation on quality of life in drug-resistant epilepsy Romanian. J Neurol. 2018;17:144-9.
Tsai JD, Yang RC, Chang MY, Fan HC, Hung KL, Tcns VNS. Vagus nerve stimulation for patients with refractory epilepsy: demographic features and neuropsychological outcomes of the VNS Taiwan Child Neurology Society Database. Epilepsy Behav. 2020;111:107186.
Kawai K, Tanaka T, Baba H, Bunker M, Ikeda A, Inoue Y, et al. Outcome of vagus nerve stimulation for drug-resistant epilepsy: the first three years of a Prospective Japanese Registry. Epileptic Disord. 2017;1(19):327-38.
Klinkenberg S, Majoie HJ, van der Heijden MM, Rijkers K, Leenen L, Aldenkamp AP. Vagus nerve stimulation has a positive effect on mood in patients with refractory epilepsy. Clin Neurol Neurosurg. 2012;114:336-40.
Labar D, Murphy J, Tecoma E. Vagus nerve stimulation for medication-resistant generalized epilepsy. E04 VNS Study Group. Neurology. 1999;22(52):1510-2.
Scherrmann J, Hoppe C, Kral T, Schramm J, Elger CE. Vagus nerve stimulation: clinical experience in a large patient series. J Clin Neurophysiol. 2001;18:408-14.
Chavel SM, Westerveld M, Spencer S. Long-term outcome of vagus nerve stimulation for refractory partial epilepsy. Epilepsy Behav. 2003;4:302-9.
Salanova V, Witt T, Worth R, Henry TR, Gross RE, Nazzaro JM, et al. Long-term efficacy and safety of thalamic stimulation for drug-resistant partial Epilepsy. Neurol. 2015;10(84):1017-25.
Huf RL, Mamelak A, Kneedy-Cayem K. Vagus nerve stimulation therapy: 2-year prospective open-label study of 40 subjects with refractory epilepsy and low IQ who are living in long-term care facilities. Epilepsy Behav. 2005;6:417-23.
Marras CE, Chiesa V, De Benedictis A, Franzini A, Rizzi M, Villani F, et al. Vagus nerve stimulation in refractory epilepsy: new indications and outcome assessment. Epilepsy Behav. 2013;28:374-8.
Amar AP, DeGiorgio CM, Tarver WB, Apuzzo ML. Long-term multicenter experience with vagus nerve stimulation for intractable partial seizures: results of the XE5 trial. Stereotact Funct Neurosurg. 1999;73:104-8.
Salinsky MC, Uthman BM, Ristanovic RK, Wernicke JF, Tarver WB. Vagus nerve stimulation for the treatment of medically intractable seizures. Results of a 1-year open-extension trial. Vagus Nerve Stimulation Study Group. Arch Neurol. 1996;53:1176-80.
Salanova V, Sperling MR, Gross RE, Irwin CP, Vollhaber JA, Giftakis JE, et al. The SANTE study at 10 years of follow-up: effectiveness, safety, and sudden unexpected death in epilepsy. Epilepsia. 2021;62:1306-17.
Spencer D. Responsive neurostimulation and cognition. Epilepsy Curr. 2016;16:98-100.
Loring DW, Kapur R, Meador KJ, Morrell MJ. Differential neuropsychological outcomes following targeted responsive neurostimulation for partial-onset epilepsy. Epilepsia. 2015;56:1836-44.
Sarkis RA, McGinnis S, Rushia SN, Park S, Ansari EE, Willment KC. Growing older with drug-resistant epilepsy: cognitive and psychosocial outcomes. J Neurol. 2018;265:1059-64.
Gavrilovic A, Toncev G, Boskovic Matic T, Vesic K, Ilic Zivojinovic J, Gavrilovic J. Impact of epilepsy duration, seizure control and EEG abnormalities on cognitive impairment in drug-resistant epilepsy patients. Acta Neurol Belg. 2019;119:403-10.
Wiebe S, Matijevic S, Eliasziw M, Derry PA. Clinically important change in quality of life in epilepsy. J Neurol Neurosurg Psychiatry. 2002;73:116-20.
Granbichler CA, Nashef L, Selway R, Polkey CE. Mortality and SUDEP in epilepsy patients treated with vagus nerve stimulation. Epilepsia. 2015;56:291-6.
Ryvlin P, So EL, Gordon CM, Hesdorffer DC, Sperling MR, Devinsky O, et al. Long-term surveillance of SUDEP in drug-resistant epilepsy patients treated with VNS therapy. Epilepsia. 2018;59:562-72.
Devinsky O, Friedman D, Duckrow RB, Fountain NB, Gwinn RP, Leiphart JW, et al. Sudden unexpected death in epilepsy in patients treated with brain-responsive neurostimulation. Epilepsia. 2018;59:555-61.
Ryvlin P, Cucherat M, Rheims S. Risk of sudden unexpected death in epilepsy in patients given adjunctive antiepileptic treatment for refractory seizures: a meta-analysis of placebo-controlled randomised trials. Lancet Neurol. 2011;10:961-8.
Nilsson L, Ahlbom A, Farahmand BY, Tomson T. Mortality in a population-based Cohort of Epilepsy Surgery Patients. Epilepsia. 2003;44:575-81.
Sperling MR, Harris A, Nei M, Liporace JD, O'Connor MJ. Mortality after epilepsy surgery. Epilepsia. 2005;46(Suppl 11):49-53.
Panebianco M, Rigby A, Weston J, Marson AG. Vagus nerve stimulation for partial seizures. Cochrane Database Syst Rev. 2015;(4):CD002896.
Youngerman BE, Mahajan UV, Dyster TG, Srinivasan S, Halpern CH, McKhann GM, et al. Cost-effectiveness analysis of responsive neurostimulation for drug-resistant focal onset epilepsy. Epilepsia. 2021;62:2804-13.
Wiebe S, Wahby S, Lawal OA, Sajobi TT, Keezer MR, Nguyen DK, et al. Development and validation of the Epilepsy Surgery Satisfaction Questionnaire (ESSQ-19). Epilepsia. 2020;61:2729-38.
The Vagus Nerve Stimulation Study Group. A randomized controlled trial of chronic vagus nerve stimulation for treatment of medically intractable seizures. Neurology. 1995;45:224-30.
Ben-Menachem E, Hellström K, Waldton C, Augustinsson LE. Evaluation of refractory epilepsy treated with vagus nerve stimulation for up to 5 years. Neurology. 1999;12(52):1265-7.
Fisher RS, Afra P, Macken M, Minecan DN, Bagić A, Benbadis SR, et al. Automatic Vagus Nerve Stimulation Triggered by Ictal Tachycardia: clinical outcomes and device performance-The U.S. E-37 Trial. Neuromodulation. 2016;19:188-95.
Tanganelli P, Ferrero S, Colotto P, Regesta G. Vagus nerve stimulation for treatment of medically intractable seizures. Evaluation of long-term Outcome. Clin Neurol Neurosurg. 2002;105:9-13.
Morrell MJ. Responsive cortical stimulation for the treatment of medically intractable partial epilepsy. Neurology. 2011;77:1295-304.
Salanova V, Witt T, Worth R, Henry TR, Gross RE, Nazzaro JM, et al. Long-term efficacy and safety of thalamic stimulation for drug-resistant partial epilepsy. Neurology. 2015;84:1017-25.

Auteurs

Lahoud Touma (L)

Research Centre of the Centre Hospitalier de l'Université de Montréal (CRCHUM), Montréal, Quebec, Canada.
Department of Neurosciences, Université de Montréal, Montréal, Quebec, Canada.

Bénédicte Dansereau (B)

Research Centre of the Centre Hospitalier de l'Université de Montréal (CRCHUM), Montréal, Quebec, Canada.
Department of Neurosciences, Université de Montréal, Montréal, Quebec, Canada.

Alvin Y Chan (AY)

Department of Neurological Surgery, School of Medicine, University of California, Irvine, Orange, California, USA.

Nathalie Jetté (N)

Department of Neurosurgery and Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York, USA.

Churl-Su Kwon (CS)

Department of Neurosurgery and Neurology, Icahn School of Medicine at Mount Sinai, New York City, New York, USA.

Kees P J Braun (KPJ)

Department of Child Neurology, University Medical Center Utrecht, Utrecht, The Netherlands.

Daniel Friedman (D)

Department of Neurology, New York University Langone Health, New York City, New York, USA.

Lara Jehi (L)

Department of Neurology, Neurological Institute, Cleveland Clinic, Cleveland, Ohio, USA.

John D Rolston (JD)

Department of Neurosurgery, University of Utah, Salt Lake City, Utah, USA.

Sumeet Vadera (S)

Department of Neurological Surgery, School of Medicine, University of California, Irvine, Orange, California, USA.

Lily C Wong-Kisiel (LC)

Department of Neurology, Mayo Clinic, Rochester, Minnesota, USA.

Dario J Englot (DJ)

Departments of Neurological Surgery, Neurology, Radiological, Electrical Engineering, and Biomedical Engineering, Vanderbilt University Medical Center, Nashville, TN, USA.

Mark R Keezer (MR)

Research Centre of the Centre Hospitalier de l'Université de Montréal (CRCHUM), Montréal, Quebec, Canada.
Department of Neurosciences, Université de Montréal, Montréal, Quebec, Canada.
Honorary Researcher, Stichting Epilepsie Instellingen Nederland (SEIN), Heemstede, The Netherlands.
School of Public Health, Université de Montréal, Montréal, Quebec, Canada.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH