Resting-State Functional MRI/PET Profile as a Potential Alternative to Tri-Modality EEG-MR/PET Imaging: An Exploratory Study in Drug-Refractory Epilepsy

Sandhya Mangalore; Sameer Peer; Sunil Kumar Khokhar; Rose Dawn Bharath; Karthik Kulanthaivelu; Jitender Saini; Sanjib Sinha; Vyasaraj Kalya Kishore; Ravindranadh Chowdary Mundlamuri; Ajay Asranna; Vishwanath Lakshminarayanapuram Gopal; Raghavendra Kenchaiah; Arivazhagan Arimappamagan; Nishanth Sadashiva; Malla Bhaskara Rao; Anita Mahadevan; Jamuna Rajeswaran; Keshav Kumar; Kandavel Thennarasu

doi:10.1055/s-0043-1760852

Asian Journal of Neurosurgery, Table of Contents

CC BY-NC-ND 4.0 · Asian J Neurosurg 2023; 18(01): 053-061
DOI: 10.1055/s-0043-1760852

Original Article

Resting-State Functional MRI/PET Profile as a Potential Alternative to Tri-Modality EEG-MR/PET Imaging: An Exploratory Study in Drug-Refractory Epilepsy

Authors

Sandhya Mangalore

¹Department of Neuroimaging and Interventional Radiology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Sameer Peer

¹Department of Neuroimaging and Interventional Radiology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Sunil Kumar Khokhar

¹Department of Neuroimaging and Interventional Radiology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Rose Dawn Bharath

¹Department of Neuroimaging and Interventional Radiology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Karthik Kulanthaivelu

¹Department of Neuroimaging and Interventional Radiology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Jitender Saini

¹Department of Neuroimaging and Interventional Radiology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Sanjib Sinha

²Department of Neurology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Vyasaraj Kalya Kishore

²Department of Neurology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Ravindranadh Chowdary Mundlamuri

²Department of Neurology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Ajay Asranna

²Department of Neurology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Vishwanath Lakshminarayanapuram Gopal

²Department of Neurology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Raghavendra Kenchaiah

²Department of Neurology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Arivazhagan Arimappamagan

³Department of Neurosurgery, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Nishanth Sadashiva

³Department of Neurosurgery, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Malla Bhaskara Rao

³Department of Neurosurgery, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Anita Mahadevan

⁴Department of Neuropathology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Jamuna Rajeswaran

⁵Department of Clinical Psychology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Keshav Kumar

⁵Department of Clinical Psychology, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India
Kandavel Thennarasu

⁶Department of Biostatistics, National Institute of Mental Health and Neurosciences (NIMHANS), Bengaluru, Karnataka, India

Abstract

Objective The study explores whether the epileptic networks associate with predetermined seizure onset zone (SOZ) identified from other modalities such as electroencephalogram/video electroencephalogram/structural MRI (EEG/VEEG/sMRI) and with the degree of resting-state functional MRI/positron emission tomography (RS-fMRI/PET) coupling. Here, we have analyzed the subgroup of patients who reported having a seizure on the day of scan as postictal cases and compared the findings with interictal cases (seizure-free interval).

Methods We performed independent component analysis (ICA) on RS-fMRI and 20 ICA were hand-labeled as large scale, noise, downstream, and epilepsy networks (Epinets) based on their profile in spatial, time series, and power spectrum domains. We had a total of 43 cases, with 4 cases in the postictal group (100%). Of 39 cases, 14 cases did not yield any Epinet and 25 cases (61%) were analyzed for the final study. The analysis was done patient-wise and correlated with predetermined SOZ.

Results The yield of finding Epinets on RS-fMRI is more during the postictal period than in the interictal period, although PET and RS-fMRI spatial, time series, and power spectral patterns were similar in both these subgroups. Overlaps between large-scale and downstream networks were noted, indicating that epilepsy propagation can involve large-scale cognition networks. Lateralization to SOZ was noted as blood oxygen level–dependent activation and correlated with sMRI/PET findings. Postoperative surgical failure cases showed residual Epinet profile.

Conclusion RS-fMRI may be a viable option for trimodality imaging to obtain simultaneous physiological information at the functional network and metabolic level.

Keywords

epilepsy - epileptic network - resting-state functional MRI - fluorodeoxyglucose - positron emission tomography - temporal lobe epilepsy

Full Text

References

References
1 Zijlmans M, Zweiphenning W, van Klink N. Changing concepts in presurgical assessment for epilepsy surgery. Nat Rev Neurol 2019; 15 (10) 594-606
2 Boerwinkle VL, Mohanty D, Foldes ST. et al. Correlating resting-state functional magnetic resonance imaging connectivity by independent component analysis-based epileptogenic zones with intracranial electroencephalogram localized seizure onset zones and surgical outcomes in prospective pediatric intractable epilepsy study. Brain Connect 2017; 7 (07) 424-442
3 Boerwinkle VL, Cediel EG, Mirea L. et al. Network-targeted approach and postoperative resting-state functional magnetic resonance imaging are associated with seizure outcome. Ann Neurol 2019; 86 (03) 344-356
4 Boerwinkle VL, Foldes ST, Torrisi SJ. et al. Subcentimeter epilepsy surgery targets by resting state functional magnetic resonance imaging can improve outcomes in hypothalamic hamartoma. Epilepsia 2018; 59 (12) 2284-2295
5 Boerwinkle VL, Vedantam A, Lam S, Wilfong AA, Curry DJ. Connectivity changes after laser ablation: resting-state fMRI. Epilepsy Res 2018; 142: 156-160
6 Amboni M, Tessitore A, Esposito F. et al. Resting-state functional connectivity associated with mild cognitive impairment in Parkinson's disease. J Neurol 2015; 262 (02) 425-434
7 Gil F, Padilla N, Soria-Pastor S. et al. Beyond the epileptic focus: functional epileptic networks in focal epilepsy. Cereb Cortex 2020; 30 (04) 2338-2357
8 Hunyadi B, Tousseyn S, Mijović B. et al. ICA extracts epileptic sources from fMRI in EEG-negative patients: a retrospective validation study. PLoS One 2013; 8 (11) e78796
9 Hunyadi B, Tousseyn S, Dupont P, Van Huffel S, De Vos M, Van Paesschen W. A prospective fMRI-based technique for localising the epileptogenic zone in presurgical evaluation of epilepsy. Neuroimage 2015; 113: 329-339
10 Fisher RS, Engel Jr JJ. Definition of the postictal state: when does it start and end?. Epilepsy Behav 2010; 19 (02) 100-104
11 Hu Y, Chen X, Gu H, Yang Y. Resting-state glutamate and GABA concentrations predict task-induced deactivation in the default mode network. J Neurosci 2013; 33 (47) 18566-18573
12 Tatlidil R. Persistent postictal hyperperfusion demonstrated with PET. Epilepsy Res 2000; 42 (2-3): 83-88
13 Storti SF, Del Felice A, Formaggio E. et al. Spatial and temporal EEG-fMRI changes during preictal and postictal phases in a patient with posttraumatic epilepsy. Clin EEG Neurosci 2015; 46 (03) 247-252
14 van Houdt PJ, Ossenblok PPW, Colon AJ. et al. Are epilepsy-related fMRI components dependent on the presence of interictal epileptic discharges in scalp EEG?. Brain Topogr 2015; 28 (04) 606-618
15 Hayes DJ, Huxtable AG. Interpreting deactivations in neuroimaging. Front Psychol 2012; 3: 27
16 Barrington SF, Koutroumanidis M, Agathonikou A. et al. Clinical value of “ictal” FDG-positron emission tomography and the routine use of simultaneous scalp EEG studies in patients with intractable partial epilepsies. Epilepsia 1998; 39 (07) 753-766
17 Chassoux F, Artiges E, Semah F. et al. ¹⁸F-FDG-PET patterns of surgical success and failure in mesial temporal lobe epilepsy. Neurology 2017; 88 (11) 1045-1053
18 Centeno M, Carmichael DW. Network connectivity in epilepsy: resting state fMRI and EEG-fMRI contributions. Front Neurol 2014; 5: 93
19 Gohel SR, Biswal BB. Functional integration between brain regions at rest occurs in multiple-frequency bands. Brain Connect 2015; 5 (01) 23-34
20 Hwang G, Nair VA, Mathis J. et al. Using low-frequency oscillations to detect temporal lobe epilepsy with machine learning. Brain Connect 2019; 9 (02) 184-193
21 Jehi L. The epileptogenic zone: concept and definition. Epilepsy Curr 2018; 18 (01) 12-16
22 Boerwinkle VL, Mirea L, Gaillard WD. et al. Resting-state functional MRI connectivity impact on epilepsy surgery plan and surgical candidacy: prospective clinical work. J Neurosurg Pediatr 2020; 20: 1-8 . Epub ahead of print. PMID: 32197251
23 Shi Y, Zhang X, Yang CL, Ren JC, Li ZM, Wang Q. A review on epileptic foci localization using resting-state functional magnetic resonance imaging. Math Biosci Eng 2020; 17 (03) 2496-2515
24 Nishida M, Juhász C, Sood S, Chugani HT, Asano E. Cortical glucose metabolism positively correlates with gamma-oscillations in nonlesional focal epilepsy. Neuroimage 2008; 42 (04) 1275-1284
25 Smith SM, Fox PT, Miller KL. et al. Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci USA 2009; 106 (31) 13040-13045 . PMID: 19620724; PMCID: PMC2722273

Supplementary Material

Supplementary Material (PDF)