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High-Definition Transcranial Direct Current Stimulation in Early Onset BRAIN INJURY https://doi.org/10.1080/02699052.2017.1390254 High-Definition transcranial direct current stimulation in early onset epileptic encephalopathy: a case study Oded Meirona, Rena Galeb, Julia Namestnicb, Odeya Bennet-Backc, Jonathan Davida, Nigel Gebodhd, Devin Adaird, Zeinab Esmaeilpourd,e, and Marom Biksond aClinical Research Center for Brain Sciences, Herzog Medical Center, Jerusalem, Israel; bChildren Respiratory Unit, Herzog Medical Center, Jerusalem, Israel; cPediatric Neurology Department, Shaare Zedek Medical Center, Jerusalem, Israel; dDepartment of Biomedical Engineering, The City College of the City University of New York, New York, USA; eBiomedical Engineering Department, Amirkabir University of Technology, Tehran, Iran ABSTRACT ARTICLE HISTORY Primary objective: Early onset epileptic encephalopathy is characterized by high daily seizure-frequency, Received 5 March 2017 multifocal epileptic discharges, severe psychomotor retardation, and death at infancy. Currently, there Revised 3 October 2017 are no effective treatments to alleviate seizure frequency and high-voltage epileptic discharges in these Accepted 5 October 2017 catastrophic epilepsy cases. The current study examined the safety and feasibility of High-Definition KEYWORDS transcranial direct current stimulation (HD-tDCS) in reducing epileptiform activity in a 30-month-old Seizure; video- EEG; child suffering from early onset epileptic encephalopathy. Design and Methods: HD-tDCS was adminis- interictal sharp waves; tered over 10 intervention days spanning two weeks including pre- and post-intervention video-EEG electroclinical syndrome; monitoring. Results: There were no serious adverse events or side effects related to the HD-tDCS hypsarrhythmia intervention. Frequency of clinical seizures was not significantly reduced. However, interictal sharp wave amplitudes were significantly lower during the post-intervention period versus baseline. Vital signs and blood biochemistry remained stable throughout the entire study. Conclusions: These explora- tory findings support the safety and feasibility of 4 ×1 HD-tDCS in early onset epileptic encephalopathy and provide the first evidence of HD-tDCS effects on paroxysmal EEG features in electroclinical cases under the age of 36 months. Extending HD-tDCS treatment may enhance electrographic findings and clinical effects. Introduction subcortical structures (5,6). Based on age-dependent epileptic encephalopathy etiology and prognosis, significantly reducing Epileptic encephalopathy syndromes such as Ohtahara syn- the clinical seizures could have a beneficial impact on the drome (OS), present during infancy (first 3 months), can infant’s survival. It may also significantly alleviate autonomic invoke frequent continuous tonic spasms, focal motor sei- disturbances (such as respiratory distress) and is likely to zures, hemiconvulsions, generalized tonic-clonic seizures, reduce progression of pathology (6,7). focal myoclonus, and suppression-burst pattern (SB), which Suppression of epileptiform discharges and seizure fre- can be detected with electroencephalography (EEG) (1). This quency by application of inhibitory non-invasive neuromodu- “ Downloaded by [95.86.113.107] at 02:25 21 November 2017 severe electroclinical condition is often classified as infantile lation may alter disease progression and improve the clinical spasms with hypsarrhythmia” related to non-metabolic struc- outcome in these “catastrophic epilepsy” conditions (8,9). tural brain abnormalities and hypsarrhythmic EEG features Accordingly, transcranial direct current stimulation (tDCS) consisting of multifocal spikes, sharp wave activity, and high- reduced epileptic discharge frequency in adults, with no ser- voltage slow wave activity (2–5). The prognosis is generally ious adverse events (10). The cathode electrode is typically poor since newborns with Ohtahara syndrome frequently die placed on the scalp over the epileptic focus with the intention during infancy and survivors invariably manifest severe psy- to reduce excitability (11,12). The safety aspects of tDCS are chomotor impairments and remain in a persistent vegetative supported by exhaustive testing across diverse clinical popula- state (6). tions and healthy volunteers (13). Tolerability studies in Only a few clinical case-studies support the use of specific adults have in turn supported judicious clinical trials in chil- antiepileptic drugs to combat the persistent seizures (e.g., dren; there are no reported serious adverse effects over 2,800 tonic spasms) in these severe electroclinical syndromes (1,6). sessions across 500 subjects aged 6 to 18 years old (13). Often Importantly, it has been suggested that clinical seizures might – though not exclusively – children receive moderately lower result from intermittent interference in descending brainstem doses of electrical stimulation than adults (< 2 mA) as com- pathways that control spinal reflex activity; seizure severity is putational models suggest that decreased head size results in correlated with changes in hypsarrhythmic EEG features that comparably smaller brain current density (14). In small clin- may indicate a disconnection between the cortex and ical trials, tDCS reduced epileptic discharge frequency in CONTACT Oded Meiron [email protected] Herzog Medical Center, 96 Givat Shaul Street, Jerusalem 91035. Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/ibij. © 2017 Taylor & Francis Group, LLC 2 O. MEIRON ET AL. children ages 6 to 15 years old (9,15,16). Five consecutive days intervention video-EEG to test for significant changes in of 2 mA of cathodal tDCS reduced seizure frequency in 4- to paroxysmal pathological EEG features (4,24,25) such as inter- 9- year-old patients with LGS. In a case study, epileptic ictal epileptiform discharges (e.g., sharp waves), paroxysmal seizures in an 11-year-old girl were reduced by 50 percent fast-wave activity (20 to 30 Hz), and most importantly, the after 2 mA of tDCS applied 5 times a week for two weeks with frequency of clinical seizures (e.g., tonic spasms, myoclonic the cathodal electrode over the epileptic focus (9) . To our seizures). We preselected hypsarrhythmic sharp waves as an knowledge, tDCS has not previously been assessed in children outcome measure (e.g., peak amplitudes of sharp waves) since under 36 months old, including in any children diagnosed it has been suggested that hypsarrhythmic paroxysmal slow- with neonatal epileptic encephalopathy. wave activity is more closely related to the pathogenetic We hypothesized that tDCS applied with a cathode placed mechanisms than epileptiform discharges in age-dependent over the brain region exhibiting consistent hypsarrhythmic epileptic encephalopathy (5). Additionally, amplitudes of hyp- high-voltage features (e.g., robust excitatory changes in elec- sarrhythmic sharp waves are associated with weaker cortical trical discharges) would attenuate subsequent paroxysmal epi- inhibition over the striatopallidal system. leptiform activity and seizure frequency in children less than Specifically, the baseline-monitoring period consisted of 36 months old. In the current case of a 30-month-old patient, 120 minutes of daily video-EEG recordings (between 14:00 in line with our investigational attempt to significantly reduce to 17:00), where epileptic discharge frequency and foci were seizure-frequency, we suggested applying a cathodal electrode monitored and quantified. Following the baseline period, over areas of paroxysmal ictal-related EEG discharges repeat- verum open-label 4 ×1 HD-tDCS was administered for edly over a period of 10 days. Importantly, in order to 20 minutes each day for 2 weeks (5-days per week), with increase the efficiency and specificity of our intended focal each day having an increased current intensity (0.1–1.0 mA). cathodal (inhibitory) stimulation we employed a 4x1-ring This adaptive stimulation regime was adopted since the over- High-Definition tDCS montage (17), expected to: 1) produce all goal of the study was to attempt to treat seizure-related maximum intensity (18) and neuromodulation (19) at parox- pathological EEG activity. Video-EEG data were acquired ysmal hypsarhythmic target-areas, 2) achieve optimal focality each day concurrently with HD-tDCS administration. On (20), and 3) result in minimum relative intensity outside the intervention days 1, 3, 5, 6, 8 and 10, post HD-tDCS session target area. Recent findings support a HD-tDCS 4x1-Ring (immediately after the stimulation) video-EEG data were configuration as a technique for delivering focal cortical sti- acquired (120 minute sessions, between 14:00 to 17:00). HD- mulation in a predictable and adjustable manner by utilizing tDCS stimulus intensity and locations were chosen based on advanced computational forward models (21). These models baseline EEG monitoring and computational finite element can integrate baseline EEG data (22), individual anatomical model outcomes. Post HD-tDCS treatment effects were data (14,23), and head-size data (as applied in the current assessed by utilizing video-EEG data (120 minutes per day, investigation) in order to predict the optimal parameters for between 14:00 to 17:00) from days, 3, 10, 17, 24, 31, and 41 accurate targeting of most pronounced pathological-hypsar- after the last day (day 10) of intervention (Figure 1). hythmic cortical networks. Specifically, we tested the feasibil- Across the entire study, seizure frequency (number of ity of HD-tDCS
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