Optimizing Surgical Planning for Epilepsy Patients With Multimodal Neuroimaging and Neurophysiology Integration: A Case Study

Current preoperative evaluation of epilepsy can be challenging because of the lack of a comprehensive view of the network's dysfunctions. To demonstrate the utility of our multimodal neurophysiology and neuroimaging integration approach in the presurgical evaluation, we present a proof-of-conce...

Full description

Saved in:
Bibliographic Details
Published inJournal of clinical neurophysiology Vol. 41; no. 4; p. 317
Main Authors Gong, Ruxue, Bickel, Stephan, Tostaeva, Gelana, Lado, Fred A, Metha, Ashesh D, Kuzniecky, Ruben I, Bonilha, Leonardo F, Gleichgerrcht, Ezequiel L
Format Journal Article
LanguageEnglish
Published United States 01.05.2024
Subjects
Online AccessGet more information

Cover

Loading…
Abstract Current preoperative evaluation of epilepsy can be challenging because of the lack of a comprehensive view of the network's dysfunctions. To demonstrate the utility of our multimodal neurophysiology and neuroimaging integration approach in the presurgical evaluation, we present a proof-of-concept for using this approach in a patient with nonlesional frontal lobe epilepsy who underwent two resective surgeries to achieve seizure control. We conducted a post-hoc investigation using four neuroimaging and neurophysiology modalities: diffusion tensor imaging, resting-state functional MRI, and stereoelectroencephalography at rest and during seizures. We computed region-of-interest-based connectivity for each modality and applied betweenness centrality to identify key network hubs across modalities. Our results revealed that despite seizure semiology and stereoelectroencephalography indicating dysfunction in the right orbitofrontal region, the maximum overlap on the hubs across modalities extended to right temporal areas. Notably, the right middle temporal lobe region served as an overlap hub across diffusion tensor imaging, resting-state functional MRI, and rest stereoelectroencephalography networks and was only included in the resected area in the second surgery, which led to long-term seizure control of this patient. Our findings demonstrated that transmodal hubs could help identify key areas related to epileptogenic network. Therefore, this case presents a promising perspective of using a multimodal approach to improve the presurgical evaluation of patients with epilepsy.
AbstractList Current preoperative evaluation of epilepsy can be challenging because of the lack of a comprehensive view of the network's dysfunctions. To demonstrate the utility of our multimodal neurophysiology and neuroimaging integration approach in the presurgical evaluation, we present a proof-of-concept for using this approach in a patient with nonlesional frontal lobe epilepsy who underwent two resective surgeries to achieve seizure control. We conducted a post-hoc investigation using four neuroimaging and neurophysiology modalities: diffusion tensor imaging, resting-state functional MRI, and stereoelectroencephalography at rest and during seizures. We computed region-of-interest-based connectivity for each modality and applied betweenness centrality to identify key network hubs across modalities. Our results revealed that despite seizure semiology and stereoelectroencephalography indicating dysfunction in the right orbitofrontal region, the maximum overlap on the hubs across modalities extended to right temporal areas. Notably, the right middle temporal lobe region served as an overlap hub across diffusion tensor imaging, resting-state functional MRI, and rest stereoelectroencephalography networks and was only included in the resected area in the second surgery, which led to long-term seizure control of this patient. Our findings demonstrated that transmodal hubs could help identify key areas related to epileptogenic network. Therefore, this case presents a promising perspective of using a multimodal approach to improve the presurgical evaluation of patients with epilepsy.
Author Bickel, Stephan
Kuzniecky, Ruben I
Tostaeva, Gelana
Lado, Fred A
Metha, Ashesh D
Bonilha, Leonardo F
Gleichgerrcht, Ezequiel L
Gong, Ruxue
Author_xml – sequence: 1
  givenname: Ruxue
  surname: Gong
  fullname: Gong, Ruxue
  organization: Department of Neurology, School of Medicine, Emory University, Atlanta, Georgia, U.S.A
– sequence: 2
  givenname: Stephan
  surname: Bickel
  fullname: Bickel, Stephan
  organization: The Feinstein Institutes for Medical Research, Northwell Health, Manhasset, New York, U.S.A. ; and
– sequence: 3
  givenname: Gelana
  surname: Tostaeva
  fullname: Tostaeva, Gelana
  organization: The Feinstein Institutes for Medical Research, Northwell Health, Manhasset, New York, U.S.A. ; and
– sequence: 4
  givenname: Fred A
  surname: Lado
  fullname: Lado, Fred A
  organization: The Feinstein Institutes for Medical Research, Northwell Health, Manhasset, New York, U.S.A. ; and
– sequence: 5
  givenname: Ashesh D
  surname: Metha
  fullname: Metha, Ashesh D
  organization: The Feinstein Institutes for Medical Research, Northwell Health, Manhasset, New York, U.S.A. ; and
– sequence: 6
  givenname: Ruben I
  surname: Kuzniecky
  fullname: Kuzniecky, Ruben I
  organization: Zucker School of Medicine at Hofstra/Northwell, Hempstead, New York, U.S.A
– sequence: 7
  givenname: Leonardo F
  surname: Bonilha
  fullname: Bonilha, Leonardo F
  organization: School of Medicine Columbia, University of South Carolina, Columbia, South Carolina, U.S.A
– sequence: 8
  givenname: Ezequiel L
  orcidid: 0000-0002-4212-4146
  surname: Gleichgerrcht
  fullname: Gleichgerrcht, Ezequiel L
  organization: Department of Neurology, School of Medicine, Emory University, Atlanta, Georgia, U.S.A
BackLink https://www.ncbi.nlm.nih.gov/pubmed/38376938$$D View this record in MEDLINE/PubMed
BookMark eNpNkF1LwzAUhoMo7kP_gUj-QGfz0WTxboypg7kVNtjliPnoIl1Smvaigv_djil4bg48nOfl5YzAtQ_eAPCA0glKBX_ar_NJ-m9QytEVGKKM8ASxlAzAKMbPnnNC8C0YkCnhTJDpEHxvqsad3JfzBdy2deGULGFeSu_PxIYaLipXmip2MJeNM76JcO-aI3xvy14Muj9fm7YO7iSLsyK9voDq2EUXylB0cOkbU9S9HvwznMG5jAZum1Z3d-DGyjKa-989BruXxW7-lqw2r8v5bJUonLEmyajlWGVminBGsdCKp0oppKVVmNFUU6oY4YJgJjBhlGKrKTfaCpsZLBgeg8dLbNV-nIw-VHXftu4Of2_APxVsYkI
ContentType Journal Article
Copyright Copyright © 2024 by the American Clinical Neurophysiology Society.
Copyright_xml – notice: Copyright © 2024 by the American Clinical Neurophysiology Society.
DBID CGR
CUY
CVF
ECM
EIF
NPM
DOI 10.1097/WNP.0000000000001071
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
DatabaseTitleList MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod no_fulltext_linktorsrc
Discipline Medicine
Anatomy & Physiology
EISSN 1537-1603
ExternalDocumentID 38376938
Genre Journal Article
Case Reports
GrantInformation_xml – fundername: NCATS NIH HHS
  grantid: UL1TR002378
– fundername: NINDS NIH HHS
  grantid: R01 NS110347
– fundername: NCATS NIH HHS
  grantid: KL2 TR002381
– fundername: NINDS NIH HHS
  grantid: R01NS110347
– fundername: NCATS NIH HHS
  grantid: UL1 TR002378
GroupedDBID ---
.-D
.Z2
0R~
5GY
5RE
5VS
AAAAV
AAHPQ
AAIQE
AAQQT
AARTV
AASCR
AAWTL
AAYEP
ABASU
ABBUW
ABDIG
ABJNI
ABVCZ
ABXVJ
ACDDN
ACEWG
ACGFO
ACGFS
ACILI
ACWDW
ACWRI
ACXJB
ACXNZ
ADGGA
ADHPY
AE6
AENEX
AFDTB
AGINI
AHQNM
AHVBC
AINUH
AJIOK
AJNWD
AJZMW
ALMA_UNASSIGNED_HOLDINGS
ALMTX
AMJPA
AMKUR
AMNEI
AOHHW
BQLVK
C45
CGR
CS3
CUY
CVF
DIWNM
DU5
E.X
EBS
ECM
EEVPB
EIF
EJD
EX3
F2K
F2L
F5P
FCALG
FL-
GNXGY
GQDEL
H0~
HLJTE
HZ~
IKREB
IN~
IPNFZ
JK8
K8S
KD2
KMI
L-C
N9A
NPM
O9-
ODA
OL1
OLG
OLV
OLW
OLZ
OPUJH
OVD
OVDNE
OWW
OXXIT
P2P
RIG
RLZ
S4S
TEORI
TSPGW
V2I
VVN
W3M
WOQ
WOW
YFH
YOC
ZFV
ID FETCH-LOGICAL-c256t-54f72c5e8125429dc70ccc1dafc2640d44c63793269236442fd47edf9f5e2962
IngestDate Wed Oct 23 09:57:59 EDT 2024
IsPeerReviewed true
IsScholarly true
Issue 4
Language English
License Copyright © 2024 by the American Clinical Neurophysiology Society.
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c256t-54f72c5e8125429dc70ccc1dafc2640d44c63793269236442fd47edf9f5e2962
ORCID 0000-0002-4212-4146
PMID 38376938
ParticipantIDs pubmed_primary_38376938
PublicationCentury 2000
PublicationDate 2024-May-01
PublicationDateYYYYMMDD 2024-05-01
PublicationDate_xml – month: 05
  year: 2024
  text: 2024-May-01
  day: 01
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Journal of clinical neurophysiology
PublicationTitleAlternate J Clin Neurophysiol
PublicationYear 2024
SSID ssj0017332
Score 2.4598987
Snippet Current preoperative evaluation of epilepsy can be challenging because of the lack of a comprehensive view of the network's dysfunctions. To demonstrate the...
SourceID pubmed
SourceType Index Database
StartPage 317
SubjectTerms Adult
Brain - diagnostic imaging
Brain - physiopathology
Brain - surgery
Diffusion Tensor Imaging
Electroencephalography - methods
Epilepsy - diagnostic imaging
Epilepsy - physiopathology
Epilepsy - surgery
Epilepsy, Frontal Lobe - diagnostic imaging
Epilepsy, Frontal Lobe - physiopathology
Epilepsy, Frontal Lobe - surgery
Female
Humans
Magnetic Resonance Imaging - methods
Male
Multimodal Imaging
Neuroimaging - methods
Title Optimizing Surgical Planning for Epilepsy Patients With Multimodal Neuroimaging and Neurophysiology Integration: A Case Study
URI https://www.ncbi.nlm.nih.gov/pubmed/38376938
Volume 41
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9NAEF6lIFW9oNLyLKA5IC7IJVmvvTE3qypqURsqFNTeKnsfUiRsR5CgtlJ_FP-Q2ZfthhYBOVjRrrNydj7Pzs7OfEPIa1wiJC9pGcUsxQ3KuNTRWPIkUopmTGlDDmmjfCfpwRf28Sw5Gwx-9qKWlotyV1zdmlfyP1LFNpSryZL9B8m2g2IDfkf54hUljNe_kvEnfN-r2ZUl1V5-czosVCGy8YP7c3zp598vDRP_zOaynRq_q826rRqJt1tyjlnlahUZJ7ptsP4Ox8506PkkfAxI_nYP1z0bfnjjQLhn2LbJlvXNodpQHx8F_Hl5sezO9GeoTr62cWcdZqcN2q_qR-Ec-Pjn2nXkqJCNs73RaM777gvKumDBXRVULo9Mseu-TnZkWB57rKdgY5fp-Zvid4TCp5MTR0jpP7i3HfVvx3maVxYMZmOeZo5Y5s-9K3TcoWuNrPGxUakT4x7yx1Y8jmnIz8z4u9seZ4OshyFWdjLWoplukgdeYpA7XD0kA1Vvke28LhZNdQlv4KSV3BZZP_YxGNvkukMdBNRBQB0g6iCgDgLqwKAOOtRBH3WAqIMV1EEPde8hB4M5sJh7RKYf9qd7B5Ev4hEJtKYXUcI0pyJRaEia0mhS8KEQYiQLLdAWH0rGRBpzs4vITC0DRrVkXEmd6QTVRUofk3t1U6unBOIRLVlZavwh3jKmuEwPiyKlTGBPJvkz8sRN5_ncEbWch4l-fmfPDtnoQPmC3NeoGdRLNDMX5Ssr2l-0Hn_q
link.rule.ids 786
linkProvider National Library of Medicine
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Optimizing+Surgical+Planning+for+Epilepsy+Patients+With+Multimodal+Neuroimaging+and+Neurophysiology+Integration%3A+A+Case+Study&rft.jtitle=Journal+of+clinical+neurophysiology&rft.au=Gong%2C+Ruxue&rft.au=Bickel%2C+Stephan&rft.au=Tostaeva%2C+Gelana&rft.au=Lado%2C+Fred+A&rft.date=2024-05-01&rft.eissn=1537-1603&rft.volume=41&rft.issue=4&rft.spage=317&rft_id=info:doi/10.1097%2FWNP.0000000000001071&rft_id=info%3Apmid%2F38376938&rft_id=info%3Apmid%2F38376938&rft.externalDocID=38376938