Towards fast and reliable simultaneous EEG-fMRI analysis of epilepsy with automatic spike detection

Journal article

Omidvarnia, Amir, Kowalczyk, Magdalena A., Pedersen, Mangor and Jackson, Graeme D.. (2019). Towards fast and reliable simultaneous EEG-fMRI analysis of epilepsy with automatic spike detection. Clinical Neurophysiology. 130(3), pp. 368-378. https://doi.org/10.1016/j.clinph.2018.11.024
AuthorsOmidvarnia, Amir, Kowalczyk, Magdalena A., Pedersen, Mangor and Jackson, Graeme D.
Abstract

Objective
The process of manually marking up epileptic spikes for simultaneous electroencephalogram (EEG) and resting state functional MRI (rsfMRI) analysis in epilepsy studies is a tedious and subjective task for a human expert. The aim of this study was to evaluate whether automatic EEG spike detection can facilitate EEG-rsfMRI analysis, and to assess its potential as a clinical tool in epilepsy.

Methods
We implemented a fast algorithm for detection of uniform interictal epileptiform discharges (IEDs) in one-hour scalp EEG recordings of 19 refractory focal epilepsy datasets (from 16 patients) who underwent a simultaneous EEG-rsfMRI recording. Our method was based on matched filtering of an IED template (derived from human markup) used to automatically detect other ‘similar’ EEG events. We compared simultaneous EEG-rsfMRI results between automatic IED detection and standard analysis with human EEG markup only.

Results
In contrast to human markup, automatic IED detection takes a much shorter time to detect IEDs and export an output text file containing spike timings. In 13/19 focal epilepsy datasets, statistical EEG-rsfMRI maps based on automatic spike detection method were comparable with human markup, and in 6/19 focal epilepsy cases automatic spike detection revealed additional brain regions not seen with human EEG markup. Additional events detected by our automated method independently revealed similar patterns of activation to a human markup. Overall, automatic IED detection provides greater statistical power in EEG-rsfMRI analysis compared to human markup in a short timeframe.

Conclusions
Automatic spike detection is a simple and fast method that can reproduce comparable and, in some cases, even superior results compared to the common practice of manual EEG markup in EEG-rsfMRI analysis of epilepsy.

Significance
Our study shows that IED detection algorithms can be effectively used in epilepsy clinical settings. This work further helps in translating EEG-rsfMRI research into a fast, reliable and easy-to-use clinical tool for epileptologists.

KeywordsEEG; fMRI; focal epilepsy; spike detection; interictal discharge; matched filtering
Year2019
JournalClinical Neurophysiology
Journal citation130 (3), pp. 368-378
PublisherLippincott Williams & Wilkins
ISSN0736-0258
Digital Object Identifier (DOI)https://doi.org/10.1016/j.clinph.2018.11.024
Scopus EID2-s2.0-85060077845
Research or scholarlyResearch
Page range368-378
FunderNational Health and Medical Research Council (NHMRC)
Publisher's version
License
All rights reserved
File Access Level
Controlled
Output statusPublished
Publication dates
Online17 Dec 2018
Publication process dates
Accepted22 Nov 2018
Deposited12 Jul 2021
Grant IDNHMRC/1091593
NHMRC/1060312
Permalink -

https://acuresearchbank.acu.edu.au/item/8w5qq/towards-fast-and-reliable-simultaneous-eeg-fmri-analysis-of-epilepsy-with-automatic-spike-detection

Log in to edit

Restricted files

Publisher's version

  • 76
    total views
  • 0
    total downloads
  • 0
    views this month
  • 0
    downloads this month
These values are for the period from 19th October 2020, when this repository was created.

Export as

Related outputs

Do mindfulness-based interventions change brain function in people with substance dependence? A systematic review of the fMRI evidence
Lorenzetti, Valentina, Gaillard, Alexandra, Beyer, Emillie, Kowalczyk, Magdalena, Kamboj, Sunjeev K., Manning, Victoria and Gleeson, John Francis Martin. (2023). Do mindfulness-based interventions change brain function in people with substance dependence? A systematic review of the fMRI evidence. BMC Psychiatry. 23(1), p. Article 407. https://doi.org/10.1186/s12888-023-04789-7
Structural network alterations in focal and generalized epilepsy assessed in a worldwide ENIGMA study follow axes of epilepsy risk gene expression
Larivière, Sara, Royer, Jessica, Rodríguez-Cruces, Raúl, Paquola, Casey, Caligiuri, Maria Eugenia, Gambardella, Antonio, Concha, Luis, Keller, Simon S., Cendes, Fernando, Yasuda, Clarissa L., Bonilha, Leonardo, Gleichgerrcht, Ezequiel, Focke, Niels K., Domin, Martin, von Podewills, Felix, Langner, Soenke, Rummel, Christian, Wiest, Roland, Martin, Pascal, ... Bernhardt, Boris C.. (2022). Structural network alterations in focal and generalized epilepsy assessed in a worldwide ENIGMA study follow axes of epilepsy risk gene expression. Nature Communications. 13(1), p. Article 4320. https://doi.org/10.1038/s41467-022-31730-5
Topographic divergence of atypical cortical asymmetry and atrophy patterns in temporal lobe epilepsy
Park, Bo-yong, Larivière, Sara, Rodríguez-Cruces, Raul, Royer, Jessica, Tavakol, Shahin, Wang, Yezhou, Caciagli, Lorenzo, Caligiuri, Maria Eugenia, Gambardella, Antonio, Concha, Luis, Keller, Simon S, Cendes, Fernando, Alvim, Marina K M, Yasuda, Clarissa, Bonilha, Leonardo, Gleichgerrcht, Ezequiel, Focke, Niels K, Kreilkamp, Barbara A K, Domin, Martin, ... Bernhardt, Boris C. (2022). Topographic divergence of atypical cortical asymmetry and atrophy patterns in temporal lobe epilepsy. Brain. 145(4), pp. 1285-1298. https://doi.org/10.1093/brain/awab417
Brain anatomical alterations in young cannabis users : Is it all hype? A meta-analysis of structural neuroimaging studies
Lorenzetti, Valentina, Kowalczyk, Magdalena, Duehlmeyer, Leonie, Greenwood, Lisa-Marie, Chye, Yann, Yücel, Murat, Whittle, Sarah and Roberts, Carl A.. (2022). Brain anatomical alterations in young cannabis users : Is it all hype? A meta-analysis of structural neuroimaging studies. Cannabis and Cannabinoid Research. 8(1), pp. 184-196. https://doi.org/10.1089/can.2021.0099
A systems-level analysis highlights microglial activation as a modifying factor in common epilepsies
Altmann, Andre, Ryten, Mina, Di Nunzio, Martina, Ravizza, Teresa, Tolomeo, Daniele, Reynolds, Regina H., Somani, Alyma, Bacigaluppi, Marco, Iori, Valentina, Micotti, Edoardo, Di Sapia, Rossella, Cerovic, Milica, Palma, Eleonora, Ruffolo, Gabriele, Botía, Juan A., Absil, Julie, Alhusaini, Saud, Alvim, Marina K. M., Auvinen, Pia, ... Sisodiya, Sanjay M.. (2022). A systems-level analysis highlights microglial activation as a modifying factor in common epilepsies. Neuropathology and Applied Neurobiology. 48(1), p. Article e12758. https://doi.org/10.1111/nan.12758
Patterns of brain function associated with cannabis cue-reactivity in regular cannabis users : A systematic review of fMRI studies
Sehl, Hannah, Terrett, Gill, Greenwood, Lisa-Marie, Kowalczyk, Magdalena, Thomson, Hannah, Poudel, Govinda, Manning, Victoria and Lorenzetti, Valentina. (2021). Patterns of brain function associated with cannabis cue-reactivity in regular cannabis users : A systematic review of fMRI studies. Psychopharmacology. 238(10), pp. 2709-2728. https://doi.org/10.1007/s00213-021-05973-x
Do comorbid personality disorders in cocaine dependence exacerbate neuroanatomical alterations? A structural neuroimaging study
Roberts, Carl A., Lorenzetti, Valentina, Albein-Urios, Natalia, Kowalczyk, Magdalena A., Martinez-Gonzalez, Jose M. and Verdejo-Garcia, Antonio. (2021). Do comorbid personality disorders in cocaine dependence exacerbate neuroanatomical alterations? A structural neuroimaging study. Progress in Neuropsychopharmacology and Biological Psychiatry. 110, p. 110298. https://doi.org/10.1016/j.pnpbp.2021.110298
Network-based atrophy modeling in the common epilepsies: A worldwide ENIGMA study
Larivière, Sara, Rodríguez-Cruces, Raúl, Royer, Jessica, Caligiuri, Maria Eugenia, Gambardella, Antonio, Concha, Luis, Keller, Simon S., Cendes, Fernando, Yasuda, Clarissa, Bonilha, Leonardo, Gleichgerrcht, Ezequiel, Focke, Niels K., Domin, Martin, von Podewills, Felix, Langner, Soenke, Rummel, Christian, Wiest, Roland, Martin, Pascal, Kotikalapudi, Raviteja, ... Bernhardt, Boris C.. (2020). Network-based atrophy modeling in the common epilepsies: A worldwide ENIGMA study. Science Advances. 6(47), p. eabc6457. https://doi.org/10.1126/sciadv.abc6457
Dynamic analysis of fMRI activation during epileptic spikes can help identify the seizure origin
Kowalczyk, Magdalena A., Omidvarnia, Amir, Dhollander, Thijs and Jackson, Graeme D.. (2020). Dynamic analysis of fMRI activation during epileptic spikes can help identify the seizure origin. Epilepsia. 61(11), pp. 2558-2571. https://doi.org/10.1111/epi.16695
Normal cerebral cortical thickness in first-degree relatives of temporal lobe epilepsy patients
Alhusaini, Saud, Kowalczyk, Magdalena A., Yasuda, Clarissa L., Semmelroch, Mira K., Katsurayama, Marilise, Zabin, Matheus, Zanão, Tamires, Nogueira, Mateus H., Alvim, Marina K. M., Ferraz, Victória R., Tsai, Meng-Han, Fitzsimons, Mary, Lopes-Cendes, Iscia, Doherty, Colin P., Cavalleri, Gianpiero L., Cendes, Fernando, Jackson, Graeme D. and Delanty, Norman. (2019). Normal cerebral cortical thickness in first-degree relatives of temporal lobe epilepsy patients. Neurology. 92(4), pp. e351-e358. https://doi.org/10.1212/WNL.0000000000006834
Human GABRG2 generalized epilepsy : Increased somatosensory and striato-thalamic connectivity
Pedersen, Mangor, Kowalczyk, Magdalena, Omidvarnia, Amir, Perucca, Piero, Gooley, Samuel, Petrou, Steven, Scheffer, Ingrid E., Berkovic, Samuel F. and Jackson, Graeme D.. (2019). Human GABRG2 generalized epilepsy : Increased somatosensory and striato-thalamic connectivity. Neurology Genetics. 5(4), p. e340. https://doi.org/10.1212/NXG.0000000000000340
Clinical benefit of presurgical EEG-fMRI in difficult-to-localize focal epilepsy : A single-institution retrospective review.
Kowalczyk, Magdalena A., Omidvarnia, Amir, Abbott, David F., Tailby, Chris, Vaughan, David N. and Jackson, Graeme D.. (2019). Clinical benefit of presurgical EEG-fMRI in difficult-to-localize focal epilepsy : A single-institution retrospective review. Epilepsia. 61(1), pp. 49-60. https://doi.org/10.1111/epi.16399
Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study
Whelan, Christopher D., Altmann, Andre, Botía, Juan A., Jahanshad, Neda, Hibar, Derrek P., Absil, Julie, Alhusaini, Saud, Alvim, Marina K. M., Auvinen, Pia, Bartolini, Emanuele, Bergo, Felipe P. G., Bernardes, Tauana, Blackmon, Karen, Braga, Barbara, Caligiuri, Maria Eugenia, Calvo, Anna, Carr, Sarah J., Chen, Jian, Chen, Shuai, ... Sisodiya, Sanjay M.. (2018). Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain: a journal of neurology. 141(2), pp. 391-408. https://doi.org/10.1093/brain/awx341
Cognitive impairment in epilepsy : The role of reduced network flexibility
Tailby, Chris, Kowalczyk, Magdalena A. and Jackson, Graeme D.. (2018). Cognitive impairment in epilepsy : The role of reduced network flexibility. Annals of Clinical and Translational Neurology. 5(1), pp. 29-40. https://doi.org/10.1002/acn3.503
Mapping the verbal semantic memory network before anterior temporal lobectomy using a combination of rTMS and fMRI
Sethi, M., Carney, P., Kowalczyk, M., Pedersen, M., Tailby, C. and Jackosn, G.. (2001). Mapping the verbal semantic memory network before anterior temporal lobectomy using a combination of rTMS and fMRI. Epilepsia. 58(Suppl. 5), p. S182. https://doi.org/10.1111/epi.13944