Repetitive transcranial magnetic stimulation for the treatment of drug-resistant epilepsy: A systematic review and individual participant data meta-analysis of real-world evidence

Yonatan A Cooper, Sean T Pianka, Naif M Alotaibi, Diana Babayan, Bahar Salavati, Alexander G Weil, George M Ibrahim, Anthony C Wang, Aria Fallah, Yonatan A Cooper, Sean T Pianka, Naif M Alotaibi, Diana Babayan, Bahar Salavati, Alexander G Weil, George M Ibrahim, Anthony C Wang, Aria Fallah

Abstract

Objective: To perform a systematic review and meta-analysis of real-world evidence for the use of low-frequency repetitive transcranial magnetic stimulation (rTMS) in the treatment of drug-resistant epilepsy.

Methods: We systematically searched PubMed, Scopus, Medline, and clinicaltrials.gov for all relevant articles. Relevant patient and stimulation predictors as well as seizure outcomes were assessed. For studies with and without individual participant data (IPD), the primary outcomes were the rate of "favorable response" (reduction in seizure frequency ≥50%) and pooled event rate of mean reduction in seizure frequency, respectively. Outcomes were assessed with comparative statistics and random-effects meta-analysis models.

Results: Of 3,477 identified articles, 12 met eligibility and were included in this review. We were able to obtain IPD for 5 articles constituting 34 participants. Univariate analysis on IPD identified greater favorable response event rates between participants with temporal seizure focus versus extratemporal (50% vs. 14%, p = 0.045) and between participants who were stimulated with a figure-8 coil versus other types (47% vs. 0%, p = 0.01). We also performed study-level meta-analysis on the remaining 7 studies without IPD, which included 212 participants. The pooled mean event rate of 50% seizure reduction using low-frequency rTMS was 30% (95% confidence interval [CI] 12-57%). Sensitivity analysis revealed that studies with a mean age ≤21 years and studies using targeted stimulation had the highest seizure reduction rates compared to studies with a mean age >21 years (69% vs. 18%) and not using a targeted stimulation (47% vs. 14-20%). Moreover, we identified high interstudy heterogeneity, moderate study bias, and high publication bias.

Significance: Real-world evidence suggests that low-frequency rTMS using a figure-8 coil may be an effective therapy for the treatment of drug-resistant epilepsy in pediatric patients. This meta-analysis can inform the design and expedite recruitment of a subsequent randomized clinical trial.

Keywords: Epilepsy; Meta‐analysis; Outcome predictors; Repetitive transcranial magnetic stimulation; Treatment.

Figures

Figure 1
Figure 1
Forest plot showing pooled event rates of mean reductions in seizures following rTMS and 95% confidence intervals among all included studies without IPD.

References

    1. Rossini PM, Rossi S. Transcranial magnetic stimulation: diagnostic, therapeutic, and research potential. Neurology 2007;68:484–488.
    1. Auriat AM, Neva JL, Peters S, et al. A review of transcranial magnetic stimulation and multimodal neuroimaging to characterize post‐stroke neuroplasticity. Front Neurol 2015;6:226.
    1. Hallett M. Transcranial magnetic stimulation and the human brain. Nature 2000;406:147–150.
    1. Santiago‐Rodriguez E, Cardenas‐Morales L, Harmony T, et al. Repetitive transcranial magnetic stimulation decreases the number of seizures in patients with focal neocortical epilepsy. Seizure 2008;17:677–683.
    1. Chervyakov AV, Chernyavsky AY, Sinitsyn DO, et al. Possible mechanisms underlying the therapeutic effects of transcranial magnetic stimulation. Front Hum Neurosci 2015;9:303.
    1. Bae EH, Schrader LM, Machii K, et al. Safety and tolerability of repetitive transcranial magnetic stimulation in patients with epilepsy: a review of the literature. Epilepsy Behav 2007;10:521–528.
    1. Fregni F, Pascual‐Leone A. Technology insight: noninvasive brain stimulation in neurology‐perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol 2007;3:383–393.
    1. Freitas C, Fregni F, Pascual‐Leone A. Meta‐analysis of the effects of repetitive transcranial magnetic stimulation (rTMS) on negative and positive symptoms in schizophrenia. Schizophr Res 2009;108:11–24.
    1. Hesdorffer DC, Logroscino G, Benn EK, et al. Estimating risk for developing epilepsy: a population‐based study in Rochester, Minnesota. Neurology 2011;76:23–27.
    1. Goldenberg MM. Overview of drugs used for epilepsy and seizures: etiology, diagnosis, and treatment. P & T 2010;35:392–415.
    1. Spencer S, Huh L. Outcomes of epilepsy surgery in adults and children. Lancet Neurol 2008;7:525–537.
    1. Sun W, Fu W, Mao W, et al. Low‐frequency repetitive transcranial magnetic stimulation for the treatment of refractory partial epilepsy. Clin EEG Neurosci 2011;42:40–44.
    1. Fregni F, Otachi PTM, Do Valle A, et al. A randomized clinical trial of repetitive transcranial magnetic stimulation in patients with refractory epilepsy. Ann Neurol 2006;60:447–455.
    1. Hsu WY, Cheng CH, Lin MW, et al. Antiepileptic effects of low frequency repetitive transcranial magnetic stimulation: a meta‐analysis. Epilepsy Res 2011;96:231–240.
    1. Kinoshita M, Ikeda A, Begum T, et al. Low‐frequency repetitive transcranial magnetic stimulation for seizure suppression in patients with extratemporal lobe epilepsy—a pilot study. Seizure 2005;14:387–392.
    1. Sun W, Mao W, Meng X, et al. Low‐frequency repetitive transcranial magnetic stimulation for the treatment of refractory partial epilepsy: a controlled clinical study. Epilepsia 2012;53:1782–1789.
    1. Cantello R, Rossi S, Varrasi C, et al. Slow repetitive TMS for drug‐resistant epilepsy: clinical and EEG findings of a placebo‐controlled trial. Epilepsia 2007;48:366–374.
    1. Seynaeve L, Devroye A, Dupont P, et al. Randomized crossover sham‐controlled clinical trial of targeted low‐frequency transcranial magnetic stimulation comparing a figure‐8 and a round coil to treat refractory neocortical epilepsy. Epilepsia 2016;57:141–150.
    1. Theodore WH, Hunter K, Chen R, et al. Transcranial magnetic stimulation for the treatment of seizures: a controlled study. Neurology 2002;59:560–562.
    1. Tergau F, Neumann D, Rosenow F, et al. Can epilepsies be improved by repetitive transcranial magnetic stimulation? Interim analysis of a controlled study. Suppl Clin Neurophysiol 2003;56:400–405.
    1. Brasil‐Neto JP, Araújo DPD, Teixeira WA, et al. Experimental therapy of epilepsy with transcranial magnetic stimulation: lack of additional benefit with prolonged treatment. Arq Neuropsiquiatr 2004;62:21–25.
    1. Daniele O, Brighina F, Piazza A, et al. Low‐frequency transcranial magnetic stimulation in patients with cortical dysplasia—a preliminary study. J Neurol 2003;250:761–762.
    1. Hubbard TE, Paradis R. Real world evidence: a new era for health care innovation. Available at: . Accessed June 2, 2017.
    1. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta‐analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 2009;339:b2700.
    1. Stroup DF, Berlin JA, Morton SC, et al. Meta‐analysis of observational studies in epidemiology: a proposal for reporting. Meta‐analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000;283:2008–2012.
    1. Cyr L, Francis K. Measures of clinical agreement for nominal and categorical data: the kappa coefficient. Comput Biol Med 1992;22:239–246.
    1. Fallah A, Guyatt GH, Snead OC 3rd, et al. Predictors of seizure outcomes in children with tuberous sclerosis complex and intractable epilepsy undergoing resective epilepsy surgery: an individual participant data meta‐analysis. PLoS ONE 2013;8:e53565.
    1. DerSimonian R, Laird N. Meta‐analysis in clinical trials. Control Clin Trials 1986;7:177–188.
    1. Fregni F, Thome‐Souza S, Bermpohl F, et al. Antiepileptic effects of repetitive transcranial magnetic stimulation in patients with cortical malformations: an EEG and clinical study. Stereotact Funct Neurosurg 2005;83:57–62.
    1. Joo EY, Han SJ, Chung S‐H, et al. Antiepileptic effects of low‐frequency repetitive transcranial magnetic stimulation by different stimulation durations and locations. Clin Neurophysiol 2007;118:702–708.
    1. Feifel D, Pappas K. Treating clinical depression with repetitive deep transcranial magnetic stimulation using the Brainsway H1‐coil. J Vis Exp 2016; (116):53858.
    1. Deng Z‐D, Lisanby SH, Peterchev AV. Coil design considerations for deep transcranial magnetic stimulation. Clin Neurophysiol 2014;125:1202–1212.
    1. Donaldson AE, Gordon MS, Melvin GA, et al. Addressing the needs of adolescents with treatment resistant depressive disorders: a systematic review of rTMS. Brain Stimul 2014;7:7–12.
    1. Figiel GS, Epstein C, McDonald WM, et al. The use of rapid‐rate transcranial magnetic stimulation (rTMS) in refractory depressed patients. J Neuropsychiatry Clin Neurosci 1998;10:20–25.
    1. Johnson SB, Blum RW, Giedd JN. Adolescent maturity and the brain: the promise and pitfalls of neuroscience research in adolescent health policy. J Adolesc Health 2009;45:216–221.
    1. Téllez‐Zenteno JF, Dhar R, Wiebe S. Long‐term seizure outcomes following epilepsy surgery: a systematic review and meta‐analysis. Brain 2005;128:1188–1198.
    1. Chen H, Modur PN, Barot N, et al. Predictors of postoperative seizure recurrence: a longitudinal study of temporal and extratemporal resections. Epilepsy Res Treat 2016;2016:1–7.
    1. Gersner R, Oberman L, Sanchez MJ, et al. H‐coil repetitive transcranial magnetic stimulation for treatment of temporal lobe epilepsy: a case report. Epilepsy Behav Case Rep 2016;5:52–56.
    1. Pereira LS, Muller VT, da Mota Gomes M, et al. Safety of repetitive transcranial magnetic stimulation in patients with epilepsy: a systematic review. Epilepsy Behav 2016;57:167–176.

Source: PubMed

3
Abonnieren