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Metabolic connectivity as a predictor of surgical outcome in mesial temporal lobe epilepsy

. 2024 Feb ; 9 (1) : 187-199. [epub] 20240103

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

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.

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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

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