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Meta-Analysis
. 2017 Jul 18;7(7):CD008497.
doi: 10.1002/14651858.CD008497.pub3.

Deep brain and cortical stimulation for epilepsy

Mathieu Sprengers  1 , Kristl Vonck, Evelien Carrette, Anthony G Marson, Paul Boon
Affiliations
Meta-Analysis

Deep brain and cortical stimulation for epilepsy

Mathieu Sprengers et al. Cochrane Database Syst Rev. .

Abstract

Background: Despite optimal medical treatment, including epilepsy surgery, many epilepsy patients have uncontrolled seizures. Since the 1970s interest has grown in invasive intracranial neurostimulation as a treatment for these patients. Intracranial stimulation includes both deep brain stimulation (DBS) (stimulation through depth electrodes) and cortical stimulation (subdural electrodes). This is an updated version of a previous Cochrane review published in 2014.

Objectives: To assess the efficacy, safety and tolerability of DBS and cortical stimulation for refractory epilepsy based on randomized controlled trials (RCTs).

Search methods: We searched the Cochrane Epilepsy Group Specialized Register on 29 September 2015, but it was not necessary to update this search, because records in the Specialized Register are included in CENTRAL. We searched the Cochrane Central Register of Controlled Trials (CENTRAL) (the Cochrane Library 2016, Issue 11, 5 November 2016), PubMed (5 November 2016), ClinicalTrials.gov (5 November 2016), the WHO International Clinical Trials Registry Platform ICTRP (5 November 2016) and reference lists of retrieved articles. We also contacted device manufacturers and other researchers in the field. No language restrictions were imposed.

Selection criteria: RCTs comparing deep brain or cortical stimulation versus sham stimulation, resective surgery, further treatment with antiepileptic drugs or other neurostimulation treatments (including vagus nerve stimulation).

Data collection and analysis: Four review authors independently selected trials for inclusion. Two review authors independently extracted the relevant data and assessed trial quality and overall quality of evidence. The outcomes investigated were seizure freedom, responder rate, percentage seizure frequency reduction, adverse events, neuropsychological outcome and quality of life. If additional data were needed, the study investigators were contacted. Results were analysed and reported separately for different intracranial targets for reasons of clinical heterogeneity.

Main results: Twelve RCTs were identified, eleven of these compared one to three months of intracranial neurostimulation with sham stimulation. One trial was on anterior thalamic DBS (n = 109; 109 treatment periods); two trials on centromedian thalamic DBS (n = 20; 40 treatment periods), but only one of the trials (n = 7; 14 treatment periods) reported sufficient information for inclusion in the quantitative meta-analysis; three trials on cerebellar stimulation (n = 22; 39 treatment periods); three trials on hippocampal DBS (n = 15; 21 treatment periods); one trial on nucleus accumbens DBS (n = 4; 8 treatment periods); and one trial on responsive ictal onset zone stimulation (n = 191; 191 treatment periods). In addition, one small RCT (n = 6) compared six months of hippocampal DBS versus sham stimulation. Evidence of selective reporting was present in four trials and the possibility of a carryover effect complicating interpretation of the results could not be excluded in five cross-over trials without any or a sufficient washout period. Moderate-quality evidence could not demonstrate statistically or clinically significant changes in the proportion of patients who were seizure-free or experienced a 50% or greater reduction in seizure frequency (primary outcome measures) after one to three months of anterior thalamic DBS in (multi)focal epilepsy, responsive ictal onset zone stimulation in (multi)focal epilepsy patients and hippocampal DBS in (medial) temporal lobe epilepsy. However, a statistically significant reduction in seizure frequency was found for anterior thalamic DBS (mean difference (MD), -17.4% compared to sham stimulation; 95% confidence interval (CI) -31.2 to -1.0; high-quality evidence), responsive ictal onset zone stimulation (MD -24.9%; 95% CI -40.1 to -6.0; high-quality evidence) and hippocampal DBS (MD -28.1%; 95% CI -34.1 to -22.2; moderate-quality evidence). Both anterior thalamic DBS and responsive ictal onset zone stimulation do not have a clinically meaningful impact on quality life after three months of stimulation (high-quality evidence). Electrode implantation resulted in postoperative asymptomatic intracranial haemorrhage in 1.6% to 3.7% of the patients included in the two largest trials and 2.0% to 4.5% had postoperative soft tissue infections (9.4% to 12.7% after five years); no patient reported permanent symptomatic sequelae. Anterior thalamic DBS was associated with fewer epilepsy-associated injuries (7.4 versus 25.5%; P = 0.01) but higher rates of self-reported depression (14.8 versus 1.8%; P = 0.02) and subjective memory impairment (13.8 versus 1.8%; P = 0.03); there were no significant differences in formal neuropsychological testing results between the groups. Responsive ictal-onset zone stimulation seemed to be well-tolerated with few side effects.The limited number of patients preclude firm statements on safety and tolerability of hippocampal DBS. With regards to centromedian thalamic DBS, nucleus accumbens DBS and cerebellar stimulation, no statistically significant effects could be demonstrated but evidence is of only low to very low quality.

Authors' conclusions: Except for one very small RCT, only short-term RCTs on intracranial neurostimulation for epilepsy are available. Compared to sham stimulation, one to three months of anterior thalamic DBS ((multi)focal epilepsy), responsive ictal onset zone stimulation ((multi)focal epilepsy) and hippocampal DBS (temporal lobe epilepsy) moderately reduce seizure frequency in refractory epilepsy patients. Anterior thalamic DBS is associated with higher rates of self-reported depression and subjective memory impairment. There is insufficient evidence to make firm conclusive statements on the efficacy and safety of hippocampal DBS, centromedian thalamic DBS, nucleus accumbens DBS and cerebellar stimulation. There is a need for more, large and well-designed RCTs to validate and optimize the efficacy and safety of invasive intracranial neurostimulation treatments.

PubMed Disclaimer

Conflict of interest statement

Medtronic Inc has provided support in terms of free devices for a pilot study and an international multicentre randomized trial of hippocampal deep brain stimulation in epilepsy co‐ordinated by Ghent University Hospital.

AGM: A consortium of pharmaceutical companies (GSK, EISAI, UCB Pharma) funded the National Audit of Seizure Management in Hospitals (NASH) through grants paid to the University of Liverpool. Professor Tony Marson is Theme Leader for Managing Complex Needs at NIHR CLAHRC NWC.

Figures

1
1
Study flow diagram.
2
2
'Risk of bias' summary: review authors' judgements about each risk of bias item for each included study.
3
3
Forest plot of comparison: 1 Stimulation versus sham stimulation, outcome: 1.1 Seizure freedom.
4
4
Forest plot of comparison: 1 Stimulation versus sham stimulation, outcome: 1.2 Responder rate.
5
5
Forest plot of comparison: 1 Stimulation versus sham stimulation, outcome: 1.3 Seizure frequency reduction. Note: Fisher 2010 (anterior thalamic nucleus stimulation) and Morrell 2011 (closed‐loop ictal onset zone stimulation) estimated the treatment effect and its standard error on a logarithmic scale, using the generalized estimating equation (GEE) model. As in this figure standard errors could not be inputted on the logarithmic scale, the values for the 95% confidence interval presented here differ slightly from the (more correct) values mentioned in the text. These correct values are ‐17.4% with 95% CI [‐31.2;‐1.0] for Fisher 2010 and ‐24.9% with 95% CI [‐40.1;‐6.0] for Morrell 2011.
6
6
Forest plot of comparison: 1 Stimulation versus sham stimulation, outcome: 1.4 Quality of Life. To measure quality of life, Tellez‐Zenteno 2006 and Morrell 2011 used the QOLIE‐89 questionnaire, Fisher 2010 used the QOLIE‐31 questionnaire (= abbreviated form of the QOLIE‐89 questionnaire) and Kowski 2015 usde the QOLIE‐31‐P questionnaire (slightly modified version of the QOLIE‐31 questionnaire). These questionnaires have the same range and for the QOLIE‐89 and QOLIE‐31 questionnaires very similar means, standard deviations and minimum clinically important change values in the same population have been reported (Cramer 1998; Devinsky 1995; Wiebe 2002). For this reason results from the different trials are presented in one forest plot (see also Methods section). For the QOLIE‐89 and QOLIE‐31 questionnaires, improvements of 5‐11.7 have been defined in literature (Borghs 2012; Cramer 2004; Wiebe 2002) as being clinically meaningful, positive is better.
1.1
1.1. Analysis
Comparison 1 Stimulation versus sham stimulation, Outcome 1 Seizure freedom.
1.2
1.2. Analysis
Comparison 1 Stimulation versus sham stimulation, Outcome 2 Responder rate.
1.3
1.3. Analysis
Comparison 1 Stimulation versus sham stimulation, Outcome 3 Seizure frequency reduction.
1.4
1.4. Analysis
Comparison 1 Stimulation versus sham stimulation, Outcome 4 Quality of Life.
2.1
2.1. Analysis
Comparison 2 Stimulation versus sham stimulation ‐ sensitivity analyses, Outcome 1 Seizure freedom RR.
2.2
2.2. Analysis
Comparison 2 Stimulation versus sham stimulation ‐ sensitivity analyses, Outcome 2 Responder rate RR.
2.3
2.3. Analysis
Comparison 2 Stimulation versus sham stimulation ‐ sensitivity analyses, Outcome 3 Seizure freedom OR 0.25.
2.4
2.4. Analysis
Comparison 2 Stimulation versus sham stimulation ‐ sensitivity analyses, Outcome 4 Responder rate OR 0.25.
2.5
2.5. Analysis
Comparison 2 Stimulation versus sham stimulation ‐ sensitivity analyses, Outcome 5 Seizure freedom RR 0.25.
2.6
2.6. Analysis
Comparison 2 Stimulation versus sham stimulation ‐ sensitivity analyses, Outcome 6 Responder rate RR 0.25.
See this image and copyright information in PMC

Update of

References

References to studies included in this review

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Lim 2007 {published data only}
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Marras 2011 {published data only}
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Tanriverdi 2009 {published data only}
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Velasco 2009 {published data only}
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Vonck 2013 {published data only}
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Wakerley 2011 {published data only}
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Wei 2016 {published data only}
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Wille 2011 {published data only}
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Yamamoto 2006 {published data only}
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References to studies awaiting assessment

Chabardes 2005 {published data only (unpublished sought but not used)}
    1. Chabardes S. Assessment of subthalamic nucleus stimulation in drug resistant epilepsy associated with dopaminergic metabolism deficit. a randomized, double blind, controlled trial. www.clinicaltrials.gov/ct/show/NCT00228371. September 2005, last update May 2015. [CENTRAL: CN‐00643474; CTG: NCT00228371]
van Rijckevorsel 2004 {published data only (unpublished sought but not used)}
    1. Raftopoulos C, Rijckevorsel K, Abu Serieh B, Tourtchaninoff M, Ivanoiu A, Mary G, et al. Epileptic discharges in a mammillary body of a patient with refractory epilepsy. Neuromodulation 2005;8(4):236‐40. - PubMed
    1. Raftopoulos C, Rijckevorsel K, Abu Serieh B, Tourtchaninoff M, Ivanoiu A, Mary G, et l. Chronic electrical stimulation of the mammillary bodies and the mammillothalamic tracts in chronic refractory epilepsy. Neuromodulation 2004;7(2):148.
    1. Rijckevorsel K, Abu Serieh B, Tourtchaninoff M, Ivanoiu A, Mary G, Gradin C, et al. Safety and tolerability of deep brain stimulation of mammillary bodies and mammillothalamic area in patients with chronic refractory epilepsy. Epilepsia 2004;45 Suppl 7:164.
    1. Rijckevorsel K, Abu Serieh B, Tourtchaninoff M, Raftopoulos C. Deep EEG recordings of the mammillary body in epilepsy patients. Epilepsia 2005;46(5):781‐5. - PubMed

References to ongoing studies

Boon 2007b {published data only}
    1. Boon P. Prospective randomized controlled study of neurostimulation in the medial temporal lobe for patients with medically refractory medial temporal lobe epilepsy; Controlled Randomized Stimulation Versus Resection (CoRaStiR). http://www.clinicaltrials.gov/ct2/show/NCT00431457 February 2007, last update: December 2014. [CTG: NCT00431457]
    1. Schulze‐Bonhage A. Hippocampus stimulation instead of amygdalohippocampectomy. Prospective, randomized study for treatment of mesiotemporal epilepsy [Hippocampusstimulation statt Amygdalohippokampektomie. Prospektive, randomisierte Behandlungsstudie bei mesiotemporaler Epilepsie]. Zeitschrift fur Epileptologie 2009;22(2):89‐92. [CENTRAL: CN‐00754119; EMBASE: EMBASE 2009227430]
Chabardes 2014 {published data only}
    1. Chabardes S. Deep brain stimulation of the anterior nucleus of the thalamus in epilepsy (FRANCE). https://www.clinicaltrials.gov/ct2/show/NCT02076698 February 2014, last update December 2015. [CTG: NCT02076698]
Koubeissi 2015 {published data only}
    1. Koubeissi MZ. Low frequency electrical stimulation of the fornix in intractable Mesial Temporal Lobe Epilepsy (MTLE) (MTLE‐DBS). https://www.clinicaltrials.gov/ct2/show/NCT02383407 February 2015, last update March 2015. [CTG: NCT02383407]
Zhang 2015 {published data only}
    1. Zhang K, Zhang C. Prospective randomized trial comparing vagus nerve stimulation and deep brain stimulation of the anterior nucleus of the thalamus in patient with pharmacoresistant epilepsy. http://www.chictr.org.cn/showproj.aspx?proj=10139 December 2014, last update May 2015. [ChiCTR: IPR‐14005721]

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Publication types