Epidemic models characterize seizure propagation and the effects of epilepsy surgery in individualized brain networks based on MEG and invasive EEG recordings.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
08 03 2022
Historique:
received: 12 09 2021
accepted: 24 02 2022
entrez: 9 3 2022
pubmed: 10 3 2022
medline: 21 4 2022
Statut: epublish

Résumé

Epilepsy surgery is the treatment of choice for drug-resistant epilepsy patients. However, seizure-freedom is currently achieved in only 2/3 of the patients after surgery. In this study we have developed an individualized computational model based on MEG brain networks to explore seizure propagation and the efficacy of different virtual resections. Eventually, the goal is to obtain individualized models to optimize resection strategy and outcome. We have modelled seizure propagation as an epidemic process using the susceptible-infected (SI) model on individual brain networks derived from presurgical MEG. We included 10 patients who had received epilepsy surgery and for whom the surgery outcome at least one year after surgery was known. The model parameters were tuned in in order to reproduce the patient-specific seizure propagation patterns as recorded with invasive EEG. We defined a personalized search algorithm that combined structural and dynamical information to find resections that maximally decreased seizure propagation for a given resection size. The optimal resection for each patient was defined as the smallest resection leading to at least a 90% reduction in seizure propagation. The individualized model reproduced the basic aspects of seizure propagation for 9 out of 10 patients when using the resection area as the origin of epidemic spreading, and for 10 out of 10 patients with an alternative definition of the seed region. We found that, for 7 patients, the optimal resection was smaller than the resection area, and for 4 patients we also found that a resection smaller than the resection area could lead to a 100% decrease in propagation. Moreover, for two cases these alternative resections included nodes outside the resection area. Epidemic spreading models fitted with patient specific data can capture the fundamental aspects of clinically observed seizure propagation, and can be used to test virtual resections in silico. Combined with optimization algorithms, smaller or alternative resection strategies, that are individually targeted for each patient, can be determined with the ultimate goal to improve surgery outcome. MEG-based networks can provide a good approximation of structural connectivity for computational models of seizure propagation, and facilitate their clinical use.

Identifiants

pubmed: 35260657
doi: 10.1038/s41598-022-07730-2
pii: 10.1038/s41598-022-07730-2
pmc: PMC8904850
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

4086

Informations de copyright

© 2022. The Author(s).

Références

F1000Prime Rep. 2013;5:6
pubmed: 23513178
Phys Rev E Stat Nonlin Soft Matter Phys. 2013 Jan;87(1):012811
pubmed: 23410392
J Neurosci. 2020 Jul 15;40(29):5572-5588
pubmed: 32513827
Epileptic Disord. 2006 Aug;8 Suppl 2:S1-9
pubmed: 17012067
Science. 2013 Dec 13;342(6164):1337-42
pubmed: 24337289
Neuroimage Clin. 2015 May 22;8:536-42
pubmed: 26110111
Brain. 2011 Oct;134(Pt 10):2912-28
pubmed: 21975588
Curr Biol. 2021 Oct 25;31(20):4436-4448.e5
pubmed: 34437842
Clin Neurophysiol. 2020 Jan;131(1):225-234
pubmed: 31812920
Neuroimage. 2012 Feb 15;59(4):3909-21
pubmed: 22122866
PLoS Comput Biol. 2015 Dec 10;11(12):e1004642
pubmed: 26657566
Neurosurgery. 2017 Sep 1;81(3):N25-N26
pubmed: 28859458
Hum Brain Mapp. 2009 May;30(5):1524-34
pubmed: 18661502
Phys Med Biol. 2006 Apr 7;51(7):1759-68
pubmed: 16552102
Sci Rep. 2021 Jan 26;11(1):2213
pubmed: 33500494
Cereb Cortex. 2011 Sep;21(9):2147-57
pubmed: 21330467
IEEE Trans Biomed Eng. 2004 Oct;51(10):1726-34
pubmed: 15490820
Int J Psychophysiol. 2016 May;103:149-60
pubmed: 25678023
Front Neurol. 2018 Aug 07;9:647
pubmed: 30131762
J Neurosci Methods. 2009 Sep 30;183(1):42-8
pubmed: 19481573
Sci Rep. 2016 Jul 07;6:29215
pubmed: 27384316
Front Comput Neurosci. 2010 Sep 24;4:
pubmed: 20953245
Oper Neurosurg (Hagerstown). 2020 May 1;18(5):531-541
pubmed: 31342073
Science. 1983 May 13;220(4598):671-80
pubmed: 17813860
Epilepsia. 2012 Jun;53(6):1013-23
pubmed: 22578020
Epilepsy Res. 2009 Jul;85(1):31-45
pubmed: 19369037
Brain. 2010 Aug;133(Pt 8):2348-64
pubmed: 20826432
Clin Neurophysiol. 2013 Jan;124(1):107-13
pubmed: 22832101
BMC Neurosci. 2010 Aug 23;11:103
pubmed: 20731854
J Neurosci Methods. 2016 Feb 15;260:233-51
pubmed: 25843066
Sci Rep. 2018 Jul 2;8(1):9910
pubmed: 29967410
Lancet Neurol. 2005 Jan;4(1):42-53
pubmed: 15620856
Epilepsia. 2013 May;54(5):772-82
pubmed: 23586531
Neurobiol Dis. 2019 Oct;130:104485
pubmed: 31150792
Cereb Cortex. 2021 Nov 23;32(1):15-28
pubmed: 34274966
Proc Natl Acad Sci U S A. 2008 Apr 22;105(16):6179-84
pubmed: 18375756
Nat Rev Neurosci. 2009 Sep;10(9):647-58
pubmed: 19693029
Brain. 2016 Feb;139(Pt 2):415-30
pubmed: 26754787
Neuroimage. 2011 Jun 1;56(3):1082-104
pubmed: 21352925
Clin Neurophysiol. 2004 May;115(5):1001-9
pubmed: 15066523
Neuroimage. 2002 Jul;16(3 Pt 1):638-50
pubmed: 12169249
Sci Rep. 2021 Sep 24;11(1):19025
pubmed: 34561483
Nat Commun. 2022 Jan 25;13(1):499
pubmed: 35078990
Nature. 2005 Nov 17;438(7066):355-9
pubmed: 16292310
Epilepsia. 2015 May;56(5):772-9
pubmed: 25809843
Front Neurol. 2019 Oct 01;10:1045
pubmed: 31632339
Epilepsia. 2015 Jun;56(6):949-58
pubmed: 25921215
PLoS Comput Biol. 2019 Feb 25;15(2):e1006805
pubmed: 30802239
Clin Neurophysiol. 2011 Jun;122(6):1106-16
pubmed: 21185775
Hum Brain Mapp. 2009 May;30(5):1580-91
pubmed: 18661506
JAMA. 2015 Jan 20;313(3):285-93
pubmed: 25602999
Front Neurol. 2018 Mar 14;9:143
pubmed: 29593641
PLoS One. 2013 Jul 04;8(7):e68910
pubmed: 23861951
Phys Rev E Stat Nonlin Soft Matter Phys. 2002 May;65(5 Pt 2):055103
pubmed: 12059627
Neuron. 2013 Oct 2;80(1):184-97
pubmed: 24094111
Nat Commun. 2018 Jun 8;9(1):2236
pubmed: 29884799
Proc Natl Acad Sci U S A. 2016 Apr 5;113(14):3867-72
pubmed: 27001844
Phys Rev Lett. 2012 Aug 10;109(6):068702
pubmed: 23006310
Brain. 2014 May;137(Pt 5):1439-53
pubmed: 24691395
Neuroimage. 2017 Jan 15;145(Pt B):377-388
pubmed: 27477535
Epilepsia. 2017 Oct;58(10):e147-e151
pubmed: 28744852
Hum Brain Mapp. 2017 May;38(5):2509-2531
pubmed: 28205340
Brain. 2017 Feb;140(2):319-332
pubmed: 28011454
Phys Rev E Stat Nonlin Soft Matter Phys. 2008 Apr;77(4 Pt 2):046117
pubmed: 18517700
J Math Biol. 2020 Dec;81(6-7):1299-1355
pubmed: 32959068
Front Neurol. 2018 Mar 01;9:98
pubmed: 29545769
Brain. 2017 Mar 1;140(3):641-654
pubmed: 28364550
Sci Rep. 2016 Jul 11;6:29640
pubmed: 27404281
Front Neurol. 2014 Jul 04;5:93
pubmed: 25071695
Neuroreport. 2000 May 15;11(7):1509-14
pubmed: 10841367
Front Hum Neurosci. 2021 Feb 25;15:646268
pubmed: 33716700
Brain. 2019 Dec 1;142(12):3892-3905
pubmed: 31599323
J Clin Neurophysiol. 2010 Dec;27(6):360-71
pubmed: 21076318
Neuron. 2018 Feb 7;97(3):698-715.e10
pubmed: 29420935
Alzheimers Dement (Amst). 2019 Jan 18;11:98-107
pubmed: 30723773
PLoS Comput Biol. 2019 Jun 26;15(6):e1007051
pubmed: 31242177
J Neurosci Methods. 2014 Oct 30;236:51-7
pubmed: 25149109
Neuroimage. 2020 Aug 15;217:116839
pubmed: 32387625
PLoS Comput Biol. 2021 Feb 17;17(2):e1008689
pubmed: 33596194
Sci Rep. 2019 May 14;9(1):7351
pubmed: 31089190
Hum Brain Mapp. 2009 Apr;30(4):1077-86
pubmed: 18465745
Epilepsia. 2010 Apr;51(4):676-85
pubmed: 20196795
Epilepsia. 2003;44 Suppl 12:72-83
pubmed: 14641563
Nat Neurosci. 2012 Jun;15(6):884-90
pubmed: 22561454
Neuroimage. 2016 Sep;138:284-293
pubmed: 27262239
PLoS One. 2010 Jan 08;5(1):e8525
pubmed: 20072616
Epilepsia. 2010 Jun;51(6):1069-77
pubmed: 19889013
Clin Neurophysiol. 2007 Aug;118(8):1691-704
pubmed: 17587643
Curr Neurol Neurosci Rep. 2016 Nov;16(11):97
pubmed: 27662895
Neuroscientist. 2012 Aug;18(4):360-72
pubmed: 22235060
Nat Rev Neurosci. 2014 Oct;15(10):683-95
pubmed: 25186238
Epilepsia. 2017 Jan;58(1):137-148
pubmed: 27888520
Neuroimage. 2017 Jan 15;145(Pt A):118-129
pubmed: 27666386
Trends Cogn Sci. 2013 Dec;17(12):683-96
pubmed: 24231140
Epilepsia. 2019 Apr;60(4):593-604
pubmed: 30889276
PLoS Comput Biol. 2017 Aug 17;13(8):e1005637
pubmed: 28817568
Brain. 2014 Aug;137(Pt 8):2382-95
pubmed: 25057133
J Neural Eng. 2020 Nov 11;17(6):
pubmed: 33086212
Phys Rev E Stat Nonlin Soft Matter Phys. 2002 Mar;65(3 Pt 2A):036104
pubmed: 11909162
Nat Neurosci. 2017 Feb 23;20(3):327-339
pubmed: 28230841
Cell Rep. 2020 Dec 8;33(10):108471
pubmed: 33296654
Cereb Cortex. 2016 Aug;26(8):3508-26
pubmed: 27230218
Clin Neurophysiol. 2020 Jan;131(1):88-95
pubmed: 31759193
PLoS One. 2011;6(5):e20071
pubmed: 21625517

Auteurs

Ana P Millán (AP)

Department of Clinical Neurophysiology and MEG Center, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands. a.p.millanvidal@amsterdamumc.nl.

Elisabeth C W van Straaten (ECW)

Department of Clinical Neurophysiology and MEG Center, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands.

Cornelis J Stam (CJ)

Department of Clinical Neurophysiology and MEG Center, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands.

Ida A Nissen (IA)

Department of Clinical Neurophysiology and MEG Center, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands.

Sander Idema (S)

Department of Neurosurgery, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands.

Johannes C Baayen (JC)

Department of Neurosurgery, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands.

Piet Van Mieghem (P)

Faculty of Electrical Engineering, Mathematics and Computer Science, Delft University of Technology, Delft, The Netherlands.

Arjan Hillebrand (A)

Department of Clinical Neurophysiology and MEG Center, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, Amsterdam, The Netherlands.

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