Metabolic connectivity as a predictor of surgical outcome in mesial temporal lobe epilepsy
Language English Country United States Media print-electronic
Document type Journal Article
Grant support
LX22NPO5107
Ministerstvo Školství, Mládeže a Tělovýchovy
00209805
Ministerstvo Zdravotnictví Ceské Republiky
PubMed
37881152
PubMed Central
PMC10839369
DOI
10.1002/epi4.12853
Knihovny.cz E-resources
- Keywords
- mesial temporal lobe epilepsy, metabolic connectivity, positron emission tomography,
- MeSH
- Epilepsy, Temporal Lobe * diagnostic imaging surgery MeSH
- Fluorodeoxyglucose F18 metabolism MeSH
- Hippocampus surgery metabolism MeSH
- Humans MeSH
- Drug Resistant Epilepsy * MeSH
- Temporal Lobe metabolism MeSH
- Treatment Outcome MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Fluorodeoxyglucose F18 MeSH
OBJECTIVE: The study investigated metabolic connectivity (MC) differences between patients with unilateral drug-resistant mesial temporal lobe epilepsy (MTLE) with hippocampal sclerosis (HS) and healthy controls (HCs), based on [18 F]-fluorodeoxyglucose (FDG)-PET data. We focused on the MC changes dependent on the lateralization of the epileptogenic lobe and on correlations with postoperative outcomes. METHODS: FDG-PET scans of 47 patients with unilateral MTLE with histopathologically proven HS and 25 HC were included in the study. All the patients underwent a standard anterior temporal lobectomy and were more than 2 years after the surgery. MC changes were compared between the two HS groups (left HS, right HS) and HC. Differences between the metabolic network of seizure-free and non-seizure-free patients after surgery were depicted afterward. Network changes were correlated with clinical characteristics. RESULTS: The study showed widespread metabolic network changes in the HS patients as compared to HC. The changes were more extensive in the right HS than in the left HS. Unfavorable surgical outcomes were found in patients with decreased MC within the network including both the lesional and contralesional hippocampus, ipsilesional frontal operculum, and contralesional insula. Favorable outcomes correlated with decreased MC within the network involving both orbitofrontal cortices and the ipsilesional temporal lobe. SIGNIFICANCE: There are major differences in the metabolic networks of left and right HS, with more extensive changes in right HS. The changes within the metabolic network could help predict surgical outcomes in patients with HS. MC may identify patients with potentially unfavorable outcomes and direct them to a more detailed presurgical evaluation. PLAIN LANGUAGE SUMMARY: Metabolic connectivity is a promising method for metabolic network mapping. Metabolic networks in mesial temporal lobe epilepsy are dependent on lateralization of the epileptogenic lobe and could predict surgical outcomes.
Central European Institute of Technology Masaryk University Brno Czech Republic
Department of Nuclear Medicine Masaryk Memorial Cancer Institute Brno Czech Republic
See more in PubMed
Kwan P, Brodie MJ. Early identification of refractory epilepsy. The New England Journal of Medicine. 2000;342(5):314–319. PubMed
Malmgren K, Thom M. Hippocampal sclerosis‐origins and imaging: hippocampal sclerosis. Epilepsia. 2012;53:19–33. PubMed
Mathon B, Bielle F, Samson S, Plaisant O, Dupont S, Bertrand A, et al. Predictive factors of long‐term outcomes of surgery for mesial temporal lobe epilepsy associated with hippocampal sclerosis. Epilepsia. 2017;58(8):1473–1485. PubMed
Englot DJ, Raygor KP, Molinaro AM, Garcia PA, Knowlton RC, Auguste KI, et al. Factors associated with failed focal neocortical epilepsy surgery. Neurosurgery. 2014;75(6):648–656. PubMed PMC
Dupont S, Semah F, Clémenceau S, Adam C, Baulac M, Samson Y. Accurate prediction of postoperative outcome in mesial temporal lobe epilepsy: a study using positron emission tomography with 18 Fluorodeoxyglucose. Arch Neurol [Internet]. 2000;57(9):1331–1336. 10.1001/archneur.57.9.1331 PubMed DOI
Choi JY, Kim SJ, Hong SB, Seo DW, Hong SC, Kim BT, et al. Extratemporal hypometabolism on FDG PET in temporal lobe epilepsy as a predictor of seizure outcome after temporal lobectomy. European Journal of Nuclear Medicine and Molecular Imaging. 2003;30(4):581–587. PubMed
Chassoux F, Artiges E, Semah F, Laurent A, Landré E, Turak B, et al. 18F‐FDG‐PET patterns of surgical success and failure in mesial temporal lobe epilepsy. Neurology. 2017;88(11):1045–1053. PubMed
Shim HK, Lee HJ, Kim SE, Lee BI, Park S, Park KM. Alterations in the metabolic networks of temporal lobe epilepsy patients: a graph theoretical analysis using FDG‐PET. NeuroImage Clin. 2020;27:102349. PubMed PMC
Wang KL, Hu W, Liu TH, Zhao XB, Han CL, Xia XT, et al. Metabolic covariance networks combining graph theory measuring aberrant topological patterns in mesial temporal lobe epilepsy. CNS Neuroscience & Therapeutics. 2019;25(3):396–408. PubMed PMC
Haneef Z, Lenartowicz A, Yeh HJ, Levin HS, Engel J, Stern JM. Functional connectivity of hippocampal networks in temporal lobe epilepsy. Epilepsia. 2014;55(1):137–145. PubMed PMC
Strýček O, Lamoš M, Klimeš P, Rektor I. Cognitive task‐related functional connectivity alterations in temporal lobe epilepsy. Epilepsy & Behavior. 2020;112:107409. PubMed
Pail M, Brázdil M, Mareček R, Mikl M. An optimized voxel‐based morphometric study of gray matter changes in patients with left‐sided and right‐sided mesial temporal lobe epilepsy and hippocampal sclerosis (MTLE/HS). Epilepsia. 2010;51(4):511–518. PubMed
Antony AR, Alexopoulos AV, González‐Martínez JA, Mosher JC, Jehi L, Burgess RC, et al. Functional connectivity estimated from intracranial EEG predicts surgical outcome in intractable temporal lobe epilepsy. PLoS ONE. 2013;8(10):e77916. PubMed PMC
Guo D, Feng L, Yang Z, Li R, Xiao B, Wen S, et al. Altered temporal variations of functional connectivity associated with surgical outcomes in drug‐resistant temporal lobe epilepsy. Frontiers in Neuroscience. 2022;16:840481. PubMed PMC
Cho KH, Park KM, Lee H, Cho H, Lee DA, Heo K, et al. Metabolic network is related to surgical outcome in temporal lobe epilepsy with hippocampal sclerosis: a brain FDG‐PET study. Journal of Neuroimaging. 2022;32(2):300–313. PubMed
Arnold S, Schlaug G, Niemann H, Ebner A, Luders H, Witte OW, et al. Topography of interictal glucose hypometabolism in unilateral mesiotemporal epilepsy. Neurology. 1996;46(5):1422–1430. PubMed
Chassoux F, Artiges E, Semah F, Desarnaud S, Laurent A, Landre E, et al. Determinants of brain metabolism changes in mesial temporal lobe epilepsy. Epilepsia. 2016;57(6):907–919. PubMed
Spencer SS. Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia. 2002;43(3):219–227. PubMed
Soma T, Momose T, Takahashi M, Koyama K, Kawai K, Murase K, et al. Usefulness of extent analysis for statistical parametric mapping with asymmetry index using inter‐ictal FGD‐PET in mesial temporal lobe epilepsy. Annals of Nuclear Medicine. 2012;26(4):319–326. PubMed
Kojan M, Doležalová I, Koriťáková E, Mareček R, Řehák Z, Hermanová M, et al. Predictive value of preoperative statistical parametric mapping of regional glucose metabolism in mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsy & Behavior. 2018;79:46–52. PubMed
Hsiao IT, Huang CC, Hsieh CJ, Wey SP, Kung MP, Yen TC, et al. Perfusion‐like template and standardized normalization‐based brain image analysis using 18F‐florbetapir (AV‐45/Amyvid) PET. European Journal of Nuclear Medicine and Molecular Imaging. 2013;40(6):908–920. PubMed
Tzourio‐Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical Parcellation of the MNI MRI single‐subject brain. NeuroImage. 2002;15(1):273–289. PubMed
Huang SY, Hsu JL, Lin KJ, Hsiao IT. A novel individual metabolic brain network for 18F‐FDG PET imaging. Frontiers in Neuroscience. 2020;14:344. PubMed PMC
Chassoux F. Metabolic changes and electro‐clinical patterns in mesio‐temporal lobe epilepsy: a correlative study. Brain. 2004;127(1):164–174. PubMed
Vielhaber S, Niessen HG, Debska‐Vielhaber G, Kudin AP, Wellmer J, Kaufmann J, et al. Subfield‐specific loss of hippocampal N‐acetyl aspartate in temporal lobe epilepsy. Epilepsia. 2008;49(1):40–50. PubMed
Leiva‐Salinas C, Quigg M, Elias WJ, Patrie JT, Flors L, Fountain NB, et al. Earlier seizure onset and longer epilepsy duration correlate with the degree of temporal hypometabolism in patients with mesial temporal lobe sclerosis. Epilepsy Research. 2017;138:105–109. PubMed
Koutroumanidis M, Hennessy MJ, Seed PT, Elwes RDC, Jarosz J, Morris RG, et al. Significance of interictal bilateral temporal hypometabolism in temporal lobe epilepsy. Neurology. 2000;54(9):1811–1821. PubMed
Wieser HG. Epilepsy surgery: past, present and future. Seizure. 1998;7(3):173–184. PubMed
Aparicio J, Carreño M, Bargalló N, Setoain X, Rubí S, Rumià J, et al. Combined 18F‐FDG‐PET and diffusion tensor imaging in mesial temporal lobe epilepsy with hippocampal sclerosis. NeuroImage Clin. 2016;12:976–989. PubMed PMC
Blauwblomme T, David O, Minotti L, Job AS, Chassagnon S, Hoffman D, et al. Prognostic value of insular lobe involvement in temporal lobe epilepsy: a stereoelectroencephalographic study. Epilepsia. 2013;54(9):1658–1667. PubMed
Barba C, Barbati G, Minotti L, Hoffmann D, Kahane P. Ictal clinical and scalp‐EEG findings differentiating temporal lobe epilepsies from temporal ‘plus’ epilepsies. Brain. 2007;130(7):1957–1967. PubMed
Bansal L, Miller I, Hyslop A, Bhatia S, Duchowny M, Jayakar P. PET hypermetabolism in medically resistant childhood epilepsy: incidence, associations, and surgical outcome. Epilepsia. 2016;57(3):436–444. PubMed
Tang Y, Liao G, Li J, Long T, Li Y, Feng L, et al. FDG‐PET profiles of Extratemporal metabolism as a predictor of surgical failure in temporal lobe epilepsy. Frontiers in Medicine. 2020;7:605002. PubMed PMC
Laufs H, Rodionov R, Thornton R, Duncan JS, Lemieux L, Tagliazucchi E. Altered fMRI connectivity dynamics in temporal lobe epilepsy might explain seizure semiology. Front Neurol. 2014;5:175. 10.3389/fneur.2014.00175 PubMed DOI PMC
Bettus G, Bartolomei F, Confort‐Gouny S, Guedj E, Chauvel P, Cozzone PJ, et al. Role of resting state functional connectivity MRI in presurgical investigation of mesial temporal lobe epilepsy. Journal of Neurology, Neurosurgery, and Psychiatry. 2010;81(10):1147–1154. PubMed
Bartolomei F, Chauvel P, Wendling F. Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain. 2008;131(7):1818–1830. PubMed
Xia M, Wang J, He Y. BrainNet viewer: a network visualization tool for human brain Connectomics. PLoS ONE. 2013;8(7):e68910. PubMed PMC