EEG Reactivity Predicts Individual Efficacy of Vagal Nerve Stimulation in Intractable Epileptics

. 2019 ; 10 () : 392. [epub] 20190502

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31118916

Background: Chronic vagal nerve stimulation (VNS) is a well-established non-pharmacological treatment option for drug-resistant epilepsy. This study sought to develop a statistical model for prediction of VNS efficacy. We hypothesized that reactivity of the electroencephalogram (EEG) to external stimuli measured during routine preoperative evaluation differs between VNS responders and non-responders. Materials and Methods: Power spectral analyses were computed retrospectively on pre-operative EEG recordings from 60 epileptic patients with VNS. Thirty five responders and 25 non-responders were compared on the relative power values in four standard frequency bands and eight conditions of clinical assessment-eyes opening/closing, photic stimulation, and hyperventilation. Using logistic regression, groups of electrodes within anatomical areas identified as maximally discriminative by n leave-one-out iterations were used to classify patients. The reliability of the predictive model was verified with an independent data-set from 22 additional patients. Results: Power spectral analyses revealed significant differences in EEG reactivity between responders and non-responders; specifically, the dynamics of alpha and gamma activity strongly reflected VNS efficacy. Using individual EEG reactivity to develop and validate a predictive model, we discriminated between responders and non-responders with 86% accuracy, 83% sensitivity, and 90% specificity. Conclusion: We present a new statistical model with which EEG reactivity to external stimuli during routine presurgical evaluation can be seen as a promising avenue for the identification of patients with favorable VNS outcome. This novel method for the prediction of VNS efficacy might represent a breakthrough in the management of drug-resistant epilepsy, with wide-reaching medical and economic implications.

Zobrazit více v PubMed

Englot DJ, Chang EF, Auguste KI. Vagus nerve stimulation for epilepsy: a meta-analysis of efficacy and predictors of response. J Neurosurg. (2011) 115:1248–55. 10.3171/2011.7.JNS11977 PubMed DOI

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) 79:345–53. 10.1227/NEU.0000000000001165 PubMed DOI PMC

Theodore WH, Fisher RS. Brain stimulation for epilepsy. Lancet Neurol. (2004) 3:111–8. 10.1016/S1474-4422(03)00664-1 PubMed DOI

Alexander GM, McNamara JO. Vagus nerve stimulation elevates seizure threshold in the kindling model. Epilepsia. (2012) 53:2043–52. 10.1111/j.1528-1167.2012.03646.x PubMed DOI

Jaseja H. EEG-desynchronization as the major mechanism of anti-epileptic action of vagal nerve stimulation in patients with intractable seizures: clinical neurophysiological evidence. Med Hypotheses. (2010) 74:855–6. 10.1016/j.mehy.2009.11.031 PubMed DOI

Marrosu F, Santoni F, Puligheddu M, Barberini L, Maleci A, Ennas F, et al. Increase in 20-50 Hz (gamma frequencies) power spectrum and synchronization after chronic vagal nerve stimulation. Clin Neurophysiol. (2005) 116:2026–36. 10.1016/j.clinph.2005.06.015 PubMed DOI

Fraschini M, Puligheddu M, Demuru M, Polizzi L, Maleci A, Tamburini G, et al. VNS induced desynchronization in gamma bands correlates with positive clinical outcome in temporal lobe pharmacoresistant epilepsy. Neurosci Lett. (2013) 536:14–8. 10.1016/j.neulet.2012.12.044 PubMed DOI

Bodin C, Aubert S, Daquin G, Carron R, Scavarda D, McGonigal A, et al. Responders to vagus nerve stimulation (VNS) in refractory epilepsy have reduced interictal cortical synchronicity on scalp EEG. Epilepsy Res. (2015) 113:98–103. 10.1016/j.eplepsyres.2015.03.018 PubMed DOI

Landre E. Vagus nerve stimulation and refractory partial epilepsies. Rev Neurol. (2004) 160:S280–7. PubMed

McHugh JC, Singh HW, Phillips J, Murphy K, Doherty CP, Delanty N. Outcome measurement after vagal nerve stimulation therapy: proposal of a new classification. Epilepsia. (2007) 48:375–8. 10.1111/j.1528-1167.2006.00931.x PubMed DOI

Pfurtscheller G, Aranibar A. Event-related cortical desynchronization detected by power measurements of scalp EEG. Electroencephalogr Clin Neurophysiol. (1977) 42:817–26. PubMed

Benjamini Y, Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc B. (1995) 57:289–300.

Liu H, Yang Z, Huang L, Qu W, Hao H, Li L. Heart-rate variability indices as predictors of the response to vagus nerve stimulation in patients with drug-resistant epilepsy. Epilepsia. (2017) 58:1015–22. 10.1111/epi.13738 PubMed DOI

Van der Worp HB, Kraaier V, Wieneke GH, Van Huffelen AC. Quantitative EEG during progressive hypocarbia and hypoxia. Hyperventilation-induced EEG changes reconsidered. Electroencephalogr Clin Neurophysiol. (1991) 79:335–41. PubMed

Wyke BD. Brain function and blood sugar: observations based on a case of islet cell adenoma of the pancreas. Electroencephalogr Clin Neurophysiol. (1952) 4:339–50. PubMed

Neurbauer AC, Sange G, Pfurtscheller G. Psychometric intelligence and event-related desynchronization during performance of a letter matching task. In: Pfurtscheller G, Lopes da Silva FH, editors. Handbook of Electroencephalography nad Clinical Neurophysiology. Amsterdam: Willy; (1999). p. 219–31.

Steriade M, Llinas RR. The functional states of the thalamus and the associated neuronal interplay. Physiol Rev. (1988) 68:649–742. PubMed

Pfurtscheller G, Lopes da Silva FH. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol. (1999) 110:1842–57. PubMed

Venturini R, De Pascalis V, Imperiali MG, Martini PS. EEG alpha reactivity and extraversion-introversion. Pers Indiv Differ. (1981) 2:215–20.

Neubauer A, Freudenthaler HH, Pfurtscheller G. Intelligence and spatiotemporal patterns of event-related desynchronization (ERD). Intelligence. (1995) 20:249–66.

Duffy FH, Albert MS, McAnulty G. Brain electrical activity in patients with presenile and senile dementia of the Alzheimer type. Ann Neurol. (1984) 16:439–48. PubMed

Kononen M, Partanen JV. Blocking of EEG alpha activity during visual performance in healthy adults. A quantitative study. Electroencephalogr Clin Neurophysiol. (1993) 87:164–6. PubMed

Marciani MG, Gotman J. Effect of drug-withdrawal on location of seizure onset. Epilepsia. (1986) 27:423–31. PubMed

Gaal ZA, Boha R, Stam CJ, Molnar M. Age-dependent features of EEG-reactivity–spectral, complexity, and network characteristics. Neurosci Lett. (2010) 479:79–84. 10.1016/j.neulet.2010.05.037 PubMed DOI

Babiloni C, Lizio R, Vecchio F, Frisoni GB, Pievani M, Geroldi C, et al. Reactivity of cortical alpha rhythms to eye opening in mild cognitive impairment and Alzheimer's disease: an EEG study. J Alzheimers Dis. (2010) 22:1047–64. 10.3233/JAD-2010-100798 PubMed DOI

van der Hiele K, Bollen EL, Vein AA, Reijntjes RH, Westendorp RG, van Buchem MA, et al. EEG markers of future cognitive performance in the elderly. J Clin Neurophysiol. (2008) 25:83–9. 10.1097/WNP.0b013e31816a5b25 PubMed DOI

Basar E, Schurmann M, Basar-Eroglu C, Karakas S. Alpha oscillations in brain functioning: an integrative theory. Int J Psychophysiol. (1997) 26:5–29. PubMed

Whithain EM, Pope KJ, Fitzgibbon SP, Lewis T, Clark CR, Loveless S, et al. Scalp electrical recording during paralysis: Quantitative evidence that EEG frequencies above 20 Hz are contaminated by EMG. Clin Neurophysiol. (2007) 118:1877–88. 10.1016/j.clinph.2007.04.027 PubMed DOI

Muthukumaraswamy SD. High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations. Front Hum Neurosci. (2013) 7:138. 10.3389/fnhum.2013.00138 PubMed DOI PMC

Boytsova JA, Danko SG, Medvedev SV. When EMG contamination does not necessarily hide high-frequency EEG: scalp electrical recordings before and after Dysport injections. Exp Brain Res. (2016) 234:3091–106. 10.1007/s00221-016-4708-3 PubMed DOI

Andersen P, Andersson SA, Lomo T. Thalamo-cortical relations during spontaneous barbiturate spindles. Electroencephalogr Clin Neurophysiol. (1968) 24:90. PubMed

Lopes da Silva FH, van Lierop THMT, Schrijer CF, Storm van Leeuwen W. Organization of thalamic and cortical alpha rhythms: Spectra and coherences. Electroencephalogr Clin Neurophysiol. (1973) 35:627–39. PubMed

Timofeev I, Steriade M. Fast (mainly 30-100 Hz) oscillations in the cat cerebellothalamic pathway and their synchronization with cortical potentials. J Physiol. (1997) 504:153–68. PubMed PMC

Bartolomei F, Bonini F, Vidal E, Trebuchon A, Lagarde S, Lambert I, et al. How does vagal nerve stimulation (VNS) change EEG brain functional connectivity? Epilepsy Res. (2016) 126:141–6. 10.1016/j.eplepsyres.2016.06.008 PubMed DOI

Wostyn S, Staljanssens W, De Taeye L, Strobbe G, Gadeyne S, Van Roost D, et al. EEG derived brain activity reflects treatment response from vagus nerve stimulation in patients with epilepsy. Int J Neural Syst. (2017) 27:1650048. 10.1142/S0129065716500489 PubMed DOI

De Herdt V, De Waele J, Raedt R, Wyckhuys T, El Tahry R, Vonck K, et al. Modulation of seizure threshold by vagus nerve stimulation in an animal model for motor seizures. Acta Neurol Scand. (2010) 121:271–6. 10.1111/j.1600-0404.2009.01223.x PubMed DOI

Whittington MA, Traub RD, Kopell N, Ermentrout B, Buhl EH. Inhibition-based rhythms: experimental and mathematical observations on network dynamics. Int J Psychophysiol. (2000) 38:315–36. 10.1016/S0167-8760(00)00173-2 PubMed DOI

Traub RD, Whittington MA, Colling SB, Buzsáki G, Jefferys JG. Analysis of gamma rhythms in the rat hippocampus PubMed PMC

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...