What have we learned from 8 years of deep brain stimulation of the anterior thalamic nucleus? Experiences and insights of a single center

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  • 1 Epilepsy Center, Department of Neurology; and Departments of
  • 2 Neurology and
  • 3 Neurosurgery, University Hospital, LMU Munich, Germany
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OBJECTIVE

In the absence of a standard or guideline for the treatment of epilepsy patients with deep brain stimulation (DBS) of the anterior nucleus of the thalamus (ANT), systematic single-center investigations are essential to establish effective approaches. Here, the authors report on the long-term results of one of the largest single-center ANT DBS cohorts.

METHODS

The outcome data of 23 consecutive patients with transventricularly implanted electrodes were retrospectively analyzed with regard to adverse events, lead placement, stimulation-related side effects, and changes in seizure frequency. Depression and quality-of-life scores were collected in a subgroup of 9 patients.

RESULTS

All but 2 patients initially underwent bilateral implantation, and 84.4% of all DBS leads were successfully located within the ANT. The mean follow-up time was 46.57 ± 23.20 months. A seizure reduction > 50% was documented in 73.9% of patients, and 34.6% achieved an Engel class I outcome. In 3 patients, clinical response was achieved by switching the electrode contact or changing from the monopolar to bipolar stimulation mode. Unilateral implantation seemed ineffective, whereas bilateral stimulation with successful ANT implantation only on one side led to a clinical response. Double stimulation with additional vagus nerve stimulation was safe. Changes in cycling mode or stimulation amplitude influenced therapy tolerability and, only to a lesser extent, seizure frequency. Side effects were rare and typically vanished by lowering the stimulation amplitude or changing the active electrode contact. Furthermore, depression and aspects of quality of life significantly improved with ANT DBS treatment.

CONCLUSIONS

The transventricular approach as well as double stimulation proved safe. The anteroventral ANT appeared to be the most efficacious stimulation site. This systematic investigation with reluctant medication changes allowed for the development of a better idea of the association between parameter changes and outcome in ANT DBS patients, but larger samples are still needed to assess the potential of bipolar stimulation and distinct cycling frequencies. Furthermore, more multifaceted and objective assessments of treatment outcome are needed to fully assess the effects of ANT DBS treatment.

ABBREVIATIONS AED = antiepileptic drug; ANT = anterior nucleus of the thalamus; BDI = Beck Depression Inventory; DBS = deep brain stimulation; EEG = electroencephalography; IPG = implantable pulse generator; QOL = quality of life; QOLIE-31 = Quality of Life in Epilepsy 31; SANTE = Stimulation of the Anterior Nucleus of the Thalamus for Epilepsy; VAT = volume of activated tissue; VNS = vagus nerve stimulation.

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Contributor Notes

Correspondence Elisabeth Kaufmann: Epilepsy Center, University Hospital, LMU Munich, Germany. elisabeth.kaufmann@med.uni-muenchen.de.

INCLUDE WHEN CITING Published online October 30, 2020; DOI: 10.3171/2020.6.JNS20695.

J.H.M. and S.N. contributed equally to this work and share senior authorship.

Disclosures All authors are participating in clinical trials collaborated on by Medtronic (Medtronic Registry for Epilepsy [MORE], NCT01521754; Chronic Effects of DBS in Parkinson’s Disease and Dystonia [Activa PC+S], NCT01934296). Dr. Mehrkens: honoraria from Medtronic, Abbott, Boston Scientific, and Brainlab. Drs. Kaufmann and Bötzel: speaker honoraria from Medtronic.

  • 1

    Gooneratne IK, Green AL, Dugan P, Comparing neurostimulation technologies in refractory focal-onset epilepsy. J Neurol Neurosurg Psychiatry. 2016;87(11):11741182.

    • Search Google Scholar
    • Export Citation
  • 2

    Fisher R, Salanova V, Witt T, Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia. 2010;51(5):899908.

    • Search Google Scholar
    • Export Citation
  • 3

    Salanova V, Witt T, Worth R, Long-term efficacy and safety of thalamic stimulation for drug-resistant partial epilepsy. Neurology. 2015;84(10):10171025.

    • Search Google Scholar
    • Export Citation
  • 4

    Hartl E, Feddersen B, Bötzel K, Seizure control and active termination by anterior thalamic deep brain stimulation. Brain Stimul. 2017;10(1):168170.

    • Search Google Scholar
    • Export Citation
  • 5

    Piacentino M, Durisotti C, Garofalo PG, Anterior thalamic nucleus deep brain Stimulation (DBS) for drug-resistant complex partial seizures (CPS) with or without generalization: long-term evaluation and predictive outcome. Acta Neurochir (Wien). 2015;157(9):15251532.

    • Search Google Scholar
    • Export Citation
  • 6

    Tröster AI, Meador KJ, Irwin CP, Fisher RS. Memory and mood outcomes after anterior thalamic stimulation for refractory partial epilepsy. Seizure. 2017;45:133141.

    • Search Google Scholar
    • Export Citation
  • 7

    Grewal SS, Middlebrooks EH, Kaufmann TJ, Fast gray matter acquisition T1 inversion recovery MRI to delineate the mammillothalamic tract for preoperative direct targeting of the anterior nucleus of the thalamus for deep brain stimulation in epilepsy. Neurosurg Focus. 2018;45(2):E6.

    • Search Google Scholar
    • Export Citation
  • 8

    Jiltsova E, Möttönen T, Fahlström M, Imaging of anterior nucleus of thalamus using 1.5T MRI for deep brain stimulation targeting in refractory epilepsy. Neuromodulation. 2016;19(8):812817.

    • Search Google Scholar
    • Export Citation
  • 9

    Möttönen T, Katisko J, Haapasalo J, The correlation between intraoperative microelectrode recording and 3-tesla MRI in patients undergoing ANT-DBS for refractory epilepsy. Stereotact Funct Neurosurg. 2016;94(2):8692.

    • Search Google Scholar
    • Export Citation
  • 10

    Koeppen JA, Nahravani F, Kramer M, Electrical stimulation of the anterior thalamus for epilepsy: clinical outcome and analysis of efficient target. Neuromodulation. 2019;22(4):465471.

    • Search Google Scholar
    • Export Citation
  • 11

    Lehtimäki K, Coenen VA, Gonçalves Ferreira A, The surgical approach to the anterior nucleus of thalamus in patients with refractory epilepsy: experience from the international multicenter registry (MORE). Neurosurgery. 2019;84(1):141150.

    • Search Google Scholar
    • Export Citation
  • 12

    Lehtimäki K, Möttönen T, Järventausta K, Outcome based definition of the anterior thalamic deep brain stimulation target in refractory epilepsy. Brain Stimul. 2016;9(2):268275.

    • Search Google Scholar
    • Export Citation
  • 13

    Wang YC, Grewal SS, Middlebrooks EH, Targeting analysis of a novel parietal approach for deep brain stimulation of the anterior nucleus of the thalamus for epilepsy. Epilepsy Res. 2019;153:16.

    • Search Google Scholar
    • Export Citation
  • 14

    Rolston JD, Desai SA, Laxpati NG, Gross RE. Electrical stimulation for epilepsy: experimental approaches. Neurosurg Clin N Am. 2011;22(4):425442, v.

    • Search Google Scholar
    • Export Citation
  • 15

    McIntyre CC, Grill WM, Sherman DL, Thakor NV. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J Neurophysiol. 2004;91(4):14571469.

    • Search Google Scholar
    • Export Citation
  • 16

    Laxpati NG, Kasoff WS, Gross RE. Deep brain stimulation for the treatment of epilepsy: circuits, targets, and trials. Neurotherapeutics. 2014;11(3):508526.

    • Search Google Scholar
    • Export Citation
  • 17

    Cheney PD, Griffin DM, Van Acker GM III. Neural hijacking: action of high-frequency electrical stimulation on cortical circuits. Neuroscientist. 2013;19(5):434441.

    • Search Google Scholar
    • Export Citation
  • 18

    Lee KH, Hitti FL, Chang SY, High frequency stimulation abolishes thalamic network oscillations: an electrophysiological and computational analysis. J Neural Eng. 2011;8(4):046001.

    • Search Google Scholar
    • Export Citation
  • 19

    Chkhenkeli SA, Chkhenkeli IS. Effects of therapeutic stimulation of nucleus caudatus on epileptic electrical activity of brain in patients with intractable epilepsy. Stereotact Funct Neurosurg. 1997;69(1-4 Pt 2):221224.

    • Search Google Scholar
    • Export Citation
  • 20

    Dempsey EW, Morison RS. The production of rhythmically recurrent cortical potentials after localized thalamic stimulation. Am J Physiol. 1941;135(2):293300.

    • Search Google Scholar
    • Export Citation
  • 21

    Mirski MA, Rossell LA, Terry JB, Fisher RS. Anticonvulsant effect of anterior thalamic high frequency electrical stimulation in the rat. Epilepsy Res. 1997;28(2):89100.

    • Search Google Scholar
    • Export Citation
  • 22

    Kuncel AM, Grill WM. Selection of stimulus parameters for deep brain stimulation. Clin Neurophysiol. 2004;115(11):24312441.

  • 23

    Upton ARM, Amin I, Garnett S, Evoked metabolic responses in the limbic-striate system produced by stimulation of anterior thalamic nucleus in man. Pacing Clin Electrophysiol. 1987;10(1 Pt 2):217225.

    • Search Google Scholar
    • Export Citation
  • 24

    Lim SN, Lee ST, Tsai YT, Electrical stimulation of the anterior nucleus of the thalamus for intractable epilepsy: a long-term follow-up study. Epilepsia. 2007;48(2):342347.

    • Search Google Scholar
    • Export Citation
  • 25

    Lee KJ, Shon YM, Cho CB. Long-term outcome of anterior thalamic nucleus stimulation for intractable epilepsy. Stereotact Funct Neurosurg. 2012;90(6):379385.

    • Search Google Scholar
    • Export Citation
  • 26

    Oh YS, Kim HJ, Lee KJ, Cognitive improvement after long-term electrical stimulation of bilateral anterior thalamic nucleus in refractory epilepsy patients. Seizure. 2012;21(3):183187.

    • Search Google Scholar
    • Export Citation
  • 27

    Kerrigan JF, Litt B, Fisher RS, Electrical stimulation of the anterior nucleus of the thalamus for the treatment of intractable epilepsy. Epilepsia. 2004;45(4):346354.

    • Search Google Scholar
    • Export Citation
  • 28

    Lim SN, Lee ST, Tsai YT, Long-term anterior thalamus stimulation for intractable epilepsy. Chang Gung Med J. 2008;31(3):287296.

  • 29

    Krishna V, King NKK, Sammartino F, Anterior nucleus deep brain stimulation for refractory epilepsy: insights into patterns of seizure control and efficacious target. Neurosurgery. 2016;78(6):802811.

    • Search Google Scholar
    • Export Citation
  • 30

    Voges BR, Schmitt FC, Hamel W, Deep brain stimulation of anterior nucleus thalami disrupts sleep in epilepsy patients. Epilepsia. 2015;56(8):e99e103.

    • Search Google Scholar
    • Export Citation
  • 31

    Kulju T, Haapasalo J, Lehtimäki K, Similarities between the responses to ANT-DBS and prior VNS in refractory epilepsy. Brain Behav. 2018;8(6):e00983.

    • Search Google Scholar
    • Export Citation
  • 32

    Van Gompel JJ, Klassen BT, Worrell GA, Anterior nuclear deep brain stimulation guided by concordant hippocampal recording. Neurosurg Focus. 2015;38(6):E9.

    • Search Google Scholar
    • Export Citation
  • 33

    Osorio I, Overman J, Giftakis J, Wilkinson SB. High frequency thalamic stimulation for inoperable mesial temporal epilepsy. Epilepsia. 2007;48(8):15611571.

    • Search Google Scholar
    • Export Citation
  • 34

    Hodaie M, Wennberg RA, Dostrovsky JO, Lozano AM. Chronic anterior thalamus stimulation for intractable epilepsy. Epilepsia. 2002;43(6):603608.

    • Search Google Scholar
    • Export Citation
  • 35

    Horn A, Li N, Dembek TA, Lead-DBS v2: towards a comprehensive pipeline for deep brain stimulation imaging. Neuroimage. 2019;184:293316.

    • Search Google Scholar
    • Export Citation
  • 36

    Avants BB, Epstein CL, Grossman M, Gee JC. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal. 2008;12(1):2641.

    • Search Google Scholar
    • Export Citation
  • 37

    Ewert S, Plettig P, Li N, Toward defining deep brain stimulation targets in MNI space: a subcortical atlas based on multimodal MRI, histology and structural connectivity. Neuroimage. 2018;170:271282.

    • Search Google Scholar
    • Export Citation
  • 38

    Hartl E, Bötzel K, Mehrkens J-H, Noachtar S. Seizure reductions outlast DBS explantation. Brain Stimul. 2018;11(3):636638.

  • 39

    Li MCH, Cook MJ. Deep brain stimulation for drug-resistant epilepsy. Epilepsia. 2018;59(2):273290.

  • 40

    Järvenpää S, Rosti-Otajärvi E, Rainesalo S, Executive functions may predict outcome in deep brain stimulation of anterior nucleus of thalamus for treatment of refractory epilepsy. Front Neurol. 2018;9:324.

    • Search Google Scholar
    • Export Citation
  • 41

    Hartikainen KM, Sun L, Polvivaara M, Immediate effects of deep brain stimulation of anterior thalamic nuclei on executive functions and emotion-attention interaction in humans. J Clin Exp Neuropsychol. 2014;36(5):540550.

    • Search Google Scholar
    • Export Citation
  • 42

    Mirski MA, Fisher RS. Electrical stimulation of the mammillary nuclei increases seizure threshold to pentylenetetrazol in rats. Epilepsia. 1994;35(6):13091316.

    • Search Google Scholar
    • Export Citation
  • 43

    Moruzzi G, Magoun HW. Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol. 1949;1(4):455473.

    • Search Google Scholar
    • Export Citation
  • 44

    Hamani C, Ewerton FIS, Bonilha SM, Bilateral anterior thalamic nucleus lesions and high-frequency stimulation are protective against pilocarpine-induced seizures and status epilepticus. Neurosurgery. 2004;54(1):191197.

    • Search Google Scholar
    • Export Citation
  • 45

    Satzer D, Lanctin D, Eberly LE, Abosch A. Variation in deep brain stimulation electrode impedance over years following electrode implantation. Stereotact Funct Neurosurg. 2014;92(2):94102.

    • Search Google Scholar
    • Export Citation

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