Neurophysiological investigations of drug resistant epilepsy patients treated with vagus nerve stimulation to differentiate responders from non-responders.


Journal

European journal of neurology
ISSN: 1468-1331
Titre abrégé: Eur J Neurol
Pays: England
ID NLM: 9506311

Informations de publication

Date de publication:
07 2020
Historique:
received: 19 03 2020
accepted: 11 04 2020
pubmed: 21 4 2020
medline: 29 6 2021
entrez: 21 4 2020
Statut: ppublish

Résumé

In patients treated with vagus nerve stimulation (VNS) for drug resistant epilepsy (DRE), up to a third of patients will eventually not respond to the therapy. As VNS therapy requires surgery for device implantation, prediction of response prior to surgery is desirable. It is hypothesized that neurophysiological investigations related to the mechanisms of action of VNS may help to differentiate VNS responders from non-responders prior to the initiation of therapy. In a prospective series of DRE patients, polysomnography, heart rate variability (HRV) and cognitive event related potentials were recorded. Polysomnography and HRV were repeated after 1 year of treatment with VNS. Polysomnography, HRV and cognitive event related potentials were compared between VNS responders (≥50% reduction in seizure frequency) and non-responders. Fifteen out of 30 patients became VNS responders after 1 year of VNS treatment. Prior to treatment with VNS, the amount of deep sleep (NREM 3), the HRV high frequency (HF) power and the P3b amplitude were significantly different in responders compared to non-responders (P = 0.007; P = 0.001; P = 0.03). Three neurophysiological parameters, NREM 3, HRV HF and P3b amplitude, were found to be significantly different in DRE patients who became responders to VNS treatment prior to initiation of their treatment with VNS. These non-invasive recordings may be used as characteristics for response in future studies and help avoid unsuccessful implantations. Mechanistically these findings may be related to changes in brain regions involved in the so-called vagal afferent network.

Sections du résumé

BACKGROUND AND PURPOSE
In patients treated with vagus nerve stimulation (VNS) for drug resistant epilepsy (DRE), up to a third of patients will eventually not respond to the therapy. As VNS therapy requires surgery for device implantation, prediction of response prior to surgery is desirable. It is hypothesized that neurophysiological investigations related to the mechanisms of action of VNS may help to differentiate VNS responders from non-responders prior to the initiation of therapy.
METHODS
In a prospective series of DRE patients, polysomnography, heart rate variability (HRV) and cognitive event related potentials were recorded. Polysomnography and HRV were repeated after 1 year of treatment with VNS. Polysomnography, HRV and cognitive event related potentials were compared between VNS responders (≥50% reduction in seizure frequency) and non-responders.
RESULTS
Fifteen out of 30 patients became VNS responders after 1 year of VNS treatment. Prior to treatment with VNS, the amount of deep sleep (NREM 3), the HRV high frequency (HF) power and the P3b amplitude were significantly different in responders compared to non-responders (P = 0.007; P = 0.001; P = 0.03).
CONCLUSION
Three neurophysiological parameters, NREM 3, HRV HF and P3b amplitude, were found to be significantly different in DRE patients who became responders to VNS treatment prior to initiation of their treatment with VNS. These non-invasive recordings may be used as characteristics for response in future studies and help avoid unsuccessful implantations. Mechanistically these findings may be related to changes in brain regions involved in the so-called vagal afferent network.

Identifiants

pubmed: 32310326
doi: 10.1111/ene.14270
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1178-1189

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2020 European Academy of Neurology.

Références

Morris GL 3rd, Mueller WM. Long-term treatment with vagus nerve stimulation in patients with refractory epilepsy. The Vagus Nerve Stimulation Study Group E01-E05. Neurology 1999; 53: 1731-1735.
Elliott RE, Morsi A, Tanweer O, et al. Efficacy of vagus nerve stimulation over time: review of 65 consecutive patients with treatment-resistant epilepsy treated with VNS > 10 years. Epilepsy Behav 2011; 20: 478-483.
Carrette S, Boon P, Vonck K. A prestimulation evaluation protocol for patients with drug resistant epilepsy. Seizure 2017; 44: 137-142.
Englot DJ, Chang EF, Auguste KI. Vagus nerve stimulation for epilepsy: a meta-analysis of efficacy and predictors of response. J Neurosurg 2011; 115: 1248-1255.
Arya R, Greiner HM, Lewis A, et al. Predictors of response to vagus nerve stimulation in childhood-onset medically refractory epilepsy. J Child Neurol 2014; 29: 1652-1659.
Hachem LD, Wong SM, Ibrahim GM. The vagus afferent network: emerging role in translational connectomics. Neurosurg Focus 2018; 45: E2.
Kristl EJ, Vonck LEL. Vagus nerve stimulation: mechanism of action. Neuromodulation volume 1, 2nd edn. Science Direct, 2018: 221-236.
Benarroch EE. Locus coeruleus. Cell Tissue Res 2018; 373: 221-232.
Carter ME, Yizhar O, Chikahisa S, et al. Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat Neurosci 2010; 13: 1526-1533.
Raedt R, Clinckers R, Mollet L, et al. Increased hippocampal noradrenaline is a biomarker for efficacy of vagus nerve stimulation in a limbic seizure model. J Neurochem 2011; 117: 461-469.
Krahl SE, Clark KB, Smith DC, Browning RA. Locus coeruleus lesions suppress the seizure-attenuating effects of vagus nerve stimulation. Epilepsia 1998; 39: 709-714.
De Taeye L, Vonck K, van Bochove M, et al. The P3 event-related potential is a biomarker for the efficacy of vagus nerve stimulation in patients with epilepsy. Neurotherapeutics 2014; 11: 612-622.
Nieuwenhuis S, Aston-Jones G, Cohen JD. Decision making, the P3, and the locus coeruleus-norepinephrine system. Psychol Bull 2005; 131: 510-532.
Sakaki M, Yoo HJ, Nga L, Lee TH, Thayer JF, Mather M. Heart rate variability is associated with amygdala functional connectivity with MPFC across younger and older adults. NeuroImage 2016; 139: 44-52.
Frysinger RC, Engel J, Harper RM. Interictal heart rate patterns in partial seizure disorders. Neurology 1993; 43: 2136-2139.
Shaffer F, Ginsberg JP. An overview of heart rate variability metrics and norms. Front Public Health 2017; 5: 258.
Saper CB, Scammell TE, Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature 2005; 437: 1257-1263.
Aston-Jones G, Bloom FE. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci 1981; 1: 876-886.
Picchioni D, Pixa ML, Fukunaga M, et al. Decreased connectivity between the thalamus and the neocortex during human nonrapid eye movement sleep. Sleep 2014; 37: 387-397.
Spoormaker VI, Schroter MS, Gleiser PM, et al. Development of a large-scale functional brain network during human non-rapid eye movement sleep. J Neurosci 2010; 30: 11379-11387.
Shaffer F, McCraty R, Zerr CL. A healthy heart is not a metronome: an integrative review of the heart's anatomy and heart rate variability. Front Psychol 2014; 5: 1040.
Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Circulation 1996; 93: 1043-1065.
Addison PS. Wavelet transforms and the ECG: a review. Physiol Meas 2005; 26: R155-R199.
Berry RB, Brooks R, Gamaldo C, et al. Scoring manual updates for 2017 (Version 2.4). J Clin Sleep Med 2017; 13: 665-666.
Knight R. Contribution of human hippocampal region to novelty detection. Nature 1996; 383: 256-259.
Murphy PR, Robertson IH, Balsters JH, O'Connell RG. Pupillometry and P3 index the locus coeruleus-noradrenergic arousal function in humans. Psychophysiology 2011; 48: 1532-1543.
Verleger R, Heide W, Butt C, Kompf D. Reduction of P3b in patients with temporo-parietal lesions. Brain Res Cogn Brain Res 1994; 2: 103-116.
Soltani M, Knight RT. Neural origins of the P300. Crit Rev Neurobiol 2000; 14: 199-224.
Thayer JF, Ahs F, Fredrikson M, Sollers JJ 3rd, Wager TD. A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci Biobehav Rev 2012; 36: 747-756.
Mather M, Joo Yoo H, Clewett DV, et al. Higher locus coeruleus MRI contrast is associated with lower parasympathetic influence over heart rate variability. NeuroImage 2017; 150: 329-335.
Lu J, Greco MA, Shiromani P, Saper CB. Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J Neurosci 2000; 20: 3830-3842.
Chou TC, Bjorkum AA, Gaus SE, Lu J, Scammell TE, Saper CB. Afferents to the ventrolateral preoptic nucleus. J Neurosci 2002; 22: 977-990.
Hale JR, White TP, Mayhew SD, et al. Altered thalamocortical and intra-thalamic functional connectivity during light sleep compared with wake. NeuroImage 2016; 125: 657-667.
Aghakhani Y, Kobayashi E, Bagshaw AP, et al. Cortical and thalamic fMRI responses in partial epilepsy with focal and bilateral synchronous spikes. Clin Neurophysiol 2006; 117: 177-191.
Vonck K, De Herdt V, Bosman T, Dedeurwaerdere S, Van Laere K, Boon P. Thalamic and limbic involvement in the mechanism of action of vagus nerve stimulation, a SPECT study. Seizure 2008; 17: 699-706.
Henry TR, Engel J Jr, Mazziotta JC. Clinical evaluation of interictal fluorine-18-fluorodeoxyglucose PET in partial epilepsy. J Nucl Med 1993; 34: 1892-1898.
Ibrahim GM, Sharma P, Hyslop A, et al. Presurgical thalamocortical connectivity is associated with response to vagus nerve stimulation in children with intractable epilepsy. Neuroimage Clin 2017; 16: 634-642.
Bartolomei F, Lagarde S, Wendling F, et al. Defining epileptogenic networks: contribution of SEEG and signal analysis. Epilepsia 2017; 58: 1131-1147.
Coito A, Plomp G, Genetti M, et al. Dynamic directed interictal connectivity in left and right temporal lobe epilepsy. Epilepsia 2015; 56: 207-217.
Rush AJ, George MS, Sackeim HA, et al. Vagus nerve stimulation (VNS) for treatment-resistant depressions: a multicenter study. Biol Psychiat 2000; 47: 276-286.
Licht CM, de Geus EJ, Zitman FG, Hoogendijk WJ, van Dyck R, Penninx BW. Association between major depressive disorder and heart rate variability in the Netherlands Study of Depression and Anxiety (NESDA). Arch Gen Psychiatry 2008; 65: 1358-1367.
Kemp AH, Quintana DS, Gray MA, Felmingham KL, Brown K, Gatt JM. Impact of depression and antidepressant treatment on heart rate variability: a review and meta-analysis. Biol Psychiat 2010; 67: 1067-1074.
Iseger TA, van Bueren NER, Kenemans JL, Gevirtz R, Arns M. A frontal-vagal network theory for major depressive disorder: implications for optimizing neuromodulation techniques. Brain Stimul 2020; 13: 1-9.
Marshe VS, Maciukiewicz M, Rej S, et al. Norepinephrine transporter gene variants and remission from depression with venlafaxine treatment in older adults. Am J Psychiatry 2017; 174: 468-475.
Marzec M, Edwards J, Sagher O, Fromes G, Malow BA. Effects of vagus nerve stimulation on sleep-related breathing in epilepsy patients. Epilepsia 2003; 44: 930-935.
Parhizgar F, Nugent K, Raj R. Obstructive sleep apnea and respiratory complications associated with vagus nerve stimulators. J Clin Sleep Med 2011; 7: 401-417.
Englot DJ, Rolston JD, Wright CW, Hassnain KH, Chang EF. Rates and predictors of seizure freedom with vagus nerve stimulation for intractable epilepsy. Neurosurgery 2016; 79: 345-353.

Auteurs

S Hödl (S)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

S Carrette (S)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

A Meurs (A)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

E Carrette (E)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

A Mertens (A)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

S Gadeyne (S)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

L Goossens (L)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

F Dewaele (F)

Department of Neurosurgery, Ghent University Hospital, Ghent, Belgium.

C Bouckaert (C)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

I Dauwe (I)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

S Proesmans (S)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

R Raedt (R)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

P Boon (P)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

K Vonck (K)

Department of Neurology, 4Brain, Institute for Neuroscience, Reference Center for Refractory Epilepsy, Ghent University Hospital, Ghent, Belgium.

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