Integrating standard epilepsy protocol, ASL-perfusion, MP2RAGE/EDGE and the MELD-FCD classifier in the detection of subtle epileptogenic lesions: a 3 Tesla MRI pilot study.
ASL
Focal cortical dysplasias
Focal epilepsy
MELD
MOGHE
MP2RAGE
Malformations of cortical development
Polymicrogyria
Journal
Neuroradiology
ISSN: 1432-1920
Titre abrégé: Neuroradiology
Pays: Germany
ID NLM: 1302751
Informations de publication
Date de publication:
23 Oct 2024
23 Oct 2024
Historique:
received:
14
08
2024
accepted:
11
10
2024
medline:
23
10
2024
pubmed:
23
10
2024
entrez:
23
10
2024
Statut:
aheadofprint
Résumé
Malformations of cortical development (MCDs) in children with focal epilepsy pose significant diagnostic challenges, and a precise radiological diagnosis is crucial for surgical planning. New MRI sequences and the use of artificial intelligence (AI) algorithms are considered very promising in this regard, yet studies evaluating the relative contribution of each diagnostic technique are lacking. The study was conducted using a dedicated "EPI-MCD MR protocol" with a 3 Tesla MRI scanner in patients with focal epilepsy and previously negative MRI. MRI sequences evaluated included 3D FLAIR, 3D T1 MPRAGE, T2 Turbo Spin Echo (TSE), 3D T1 MP2RAGE, and Arterial Spin Labelling (ASL). Two paediatric neuroradiologists scored each sequence for localisation and extension of the lesion. The MELD-FCD AI classifier's performance in identifying pathological findings was also assessed. We only included patients where a diagnosis of MCD was subsequently confirmed on histology and/or sEEG. The 3D FLAIR sequence showed the highest yield in detecting epileptogenic lesions, with 3D T1 MPRAGE, T2 TSE, and 3D T1 MP2RAGE sequences showing moderate to low yield. ASL was the least useful. The MELD-FCD classifier achieved a 69.2% true positive rate. In one case, MELD identified a subtle area of cortical dysplasia overlooked by the neuroradiologists, changing the management of the patient. The 3D FLAIR sequence is the most effective in the MRI-based diagnosis of subtle epileptogenic lesions, outperforming other sequences in localisation and extension. This pilot study emphasizes the importance of careful assessment of the value of additional sequences.
Sections du résumé
BACKGROUND
BACKGROUND
Malformations of cortical development (MCDs) in children with focal epilepsy pose significant diagnostic challenges, and a precise radiological diagnosis is crucial for surgical planning. New MRI sequences and the use of artificial intelligence (AI) algorithms are considered very promising in this regard, yet studies evaluating the relative contribution of each diagnostic technique are lacking.
METHODS
METHODS
The study was conducted using a dedicated "EPI-MCD MR protocol" with a 3 Tesla MRI scanner in patients with focal epilepsy and previously negative MRI. MRI sequences evaluated included 3D FLAIR, 3D T1 MPRAGE, T2 Turbo Spin Echo (TSE), 3D T1 MP2RAGE, and Arterial Spin Labelling (ASL). Two paediatric neuroradiologists scored each sequence for localisation and extension of the lesion. The MELD-FCD AI classifier's performance in identifying pathological findings was also assessed. We only included patients where a diagnosis of MCD was subsequently confirmed on histology and/or sEEG.
RESULTS
RESULTS
The 3D FLAIR sequence showed the highest yield in detecting epileptogenic lesions, with 3D T1 MPRAGE, T2 TSE, and 3D T1 MP2RAGE sequences showing moderate to low yield. ASL was the least useful. The MELD-FCD classifier achieved a 69.2% true positive rate. In one case, MELD identified a subtle area of cortical dysplasia overlooked by the neuroradiologists, changing the management of the patient.
CONCLUSIONS
CONCLUSIONS
The 3D FLAIR sequence is the most effective in the MRI-based diagnosis of subtle epileptogenic lesions, outperforming other sequences in localisation and extension. This pilot study emphasizes the importance of careful assessment of the value of additional sequences.
Identifiants
pubmed: 39441414
doi: 10.1007/s00234-024-03488-8
pii: 10.1007/s00234-024-03488-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Rosetrees Trust
ID : A2665
Organisme : Epilepsy Research Institute
ID : P2208
Organisme : UKRI Medical Research Council
ID : MR/W031566/1
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Desikan RS, Barkovich AJ (2016) Malformations of cortical development. Ann Neurol 80:797–810. https://doi.org/10.1002/ana.24793
doi: 10.1002/ana.24793
pubmed: 27862206
pmcid: 5177533
Wang ZI, Alexopoulos AV, Jones SE, Jaisani Z, Najm IM, Prayson RA (2013) The pathology of magnetic-resonance-imaging-negative epilepsy. Mod Pathol 26:1051–1058. https://doi.org/10.1038/modpathol.2013.52
doi: 10.1038/modpathol.2013.52
pubmed: 23558575
So EL, Lee RW (2014) Epilepsy surgery in MRI-negative epilepsies. Curr Opin Neurol 27:206–212. https://doi.org/10.1097/WCO.0000000000000078
doi: 10.1097/WCO.0000000000000078
pubmed: 24553461
Wehner T, Weckesser P, Schulz S, Kowoll A, Fischer S, Bosch J, Weinhold L, Fimmers R, Schmid M, Wellmer J (2021) Factors influencing the detection of treatable epileptogenic lesions on MRI. A randomized prospective study. Neurol Res Pract 3:41. https://doi.org/10.1186/s42466-021-00142-z
doi: 10.1186/s42466-021-00142-z
pubmed: 34365971
pmcid: 8351149
Fauser S, Essang C, Altenmüller D-M, Staack AM, Steinhoff BJ, Strobl K, Bast T, Schubert-Bast S, Stephani U, Wiegand G, Prinz M, Brandt A, Zentner J, Schulze-Bonhage A (2015) Long-term seizure outcome in 211 patients with focal cortical dysplasia. Epilepsia 56:66–76. https://doi.org/10.1111/epi.12876
doi: 10.1111/epi.12876
pubmed: 25495786
Blümcke I, Thom M, Aronica E, Armstrong DD, Vinters HV, Palmini A, Jacques TS, Avanzini G, Barkovich AJ, Battaglia G, Becker A, Cepeda C, Cendes F, Colombo N, Crino P, Cross JH, Delalande O, Dubeau F, Duncan J, Guerrini R, Spreafico R (2011) The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 52:158–174. https://doi.org/10.1111/j.1528-1167.2010.02777.x
doi: 10.1111/j.1528-1167.2010.02777.x
pubmed: 21219302
Lerner JT, Salamon N, Hauptman JS, Velasco TR, Hemb M, Wu JY, Sankar R, Donald Shields W, Engel J, Fried I, Cepeda C, Andre VM, Levine MS, Miyata H, Yong WH, Vinters HV, Mathern GW (2009) Assessment and surgical outcomes for mild type I and severe type II cortical dysplasia: a critical review and the UCLA experience. Epilepsia 50:1310–1335. https://doi.org/10.1111/j.1528-1167.2008.01998.x
doi: 10.1111/j.1528-1167.2008.01998.x
pubmed: 19175385
Urbach H, Kellner E, Kremers N, Blümcke I, Demerath T (2022) MRI of focal cortical dysplasia. Neuroradiology 64:443–452. https://doi.org/10.1007/s00234-021-02865-x
doi: 10.1007/s00234-021-02865-x
pubmed: 34839379
Barkovich AJ (2010) MRI analysis of sulcation morphology in polymicrogyria. Epilepsia 51 Suppl 117–22. https://doi.org/10.1111/j.1528-1167.2009.02436.x
Leventer RJ, Phelan EM, Coleman LT, Kean MJ, Jackson GD, Harvey AS (1999) Clinical and imaging features of cortical malformations in childhood. Neurology 53:715–722. https://doi.org/10.1212/wnl.53.4.715
doi: 10.1212/wnl.53.4.715
pubmed: 10489031
Leventer RJ, Jansen A, Pilz DT, Stoodley N, Marini C, Dubeau F, Malone J, Mitchell LA, Mandelstam S, Scheffer IE, Berkovic SF, Andermann F, Andermann E, Guerrini R, Dobyns WB (2010) Clinical and imaging heterogeneity of polymicrogyria: a study of 328 patients. Brain 133:1415–1427. https://doi.org/10.1093/brain/awq078
doi: 10.1093/brain/awq078
pubmed: 20403963
pmcid: 2859156
Koutsouras GW, Hall WA (2023) Surgery for pediatric drug resistant epilepsy: a narrative review of its history, surgical implications, and treatment strategies. Transl Pediatr 12:245–259. https://doi.org/10.21037/tp-22-200
doi: 10.21037/tp-22-200
pubmed: 36891373
pmcid: 9986775
Agarwal A, Bathla G, Soni N, Desai A, Middlebrooks E, Patel V, Gupta V, Vibhute P (2024) Updates from the International League against Epilepsy Classification of Epilepsy (2017) and focal cortical dysplasias (2022): imaging phenotype and genetic characterization. AJNR Am J Neuroradiol. https://doi.org/10.3174/ajnr.A8178
doi: 10.3174/ajnr.A8178
pubmed: 39349309
Schurr J, Coras R, Rössler K, Pieper T, Kudernatsch M, Holthausen H, Winkler P, Woermann F, Bien CG, Polster T, Schulz R, Kalbhenn T, Urbach H, Becker A, Grunwald T, Huppertz H-J, Gil-Nagel A, Toledano R, Feucht M, Mühlebner A, Blümcke I (2017) Mild malformation of Cortical Development with Oligodendroglial Hyperplasia in Frontal Lobe Epilepsy: a New Clinico-Pathological Entity. Brain Pathol 27:26–35. https://doi.org/10.1111/bpa.12347
doi: 10.1111/bpa.12347
pubmed: 26748554
Hartlieb T, Winkler P, Coras R, Pieper T, Holthausen H, Blümcke I, Staudt M, Kudernatsch M (2019) Age-related MR characteristics in mild malformation of cortical development with oligodendroglial hyperplasia and epilepsy (MOGHE). Epilepsy Behav 91:68–74. https://doi.org/10.1016/j.yebeh.2018.07.009
doi: 10.1016/j.yebeh.2018.07.009
pubmed: 30061008
Mata-Mbemba D, Iimura Y, Hazrati LN, Ochi A, Otsubo H, Snead OC, Rutka J, Widjaja E (2018) MRI, Magnetoencephalography, and Surgical Outcome of Oligodendrocytosis versus focal cortical dysplasia type I. AJNR Am J Neuroradiol 39:2371–2377. https://doi.org/10.3174/ajnr.A5877
doi: 10.3174/ajnr.A5877
pubmed: 30442696
pmcid: 7655410
Marques JP, Kober T, van der Krueger G, Gruetter R (2010) MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field. NeuroImage 49:1271–1281. https://doi.org/10.1016/j.neuroimage.2009.10.002
doi: 10.1016/j.neuroimage.2009.10.002
pubmed: 19819338
Middlebrooks EH, Lin C, Westerhold E, Okromelidze L, Vibhute P, Grewal SS, Gupta V (2020) Improved detection of focal cortical dysplasia using a novel 3D imaging sequence: edge-enhancing gradient Echo (3D-EDGE) MRI. Neuroimage Clin 28:102449. https://doi.org/10.1016/j.nicl.2020.102449
doi: 10.1016/j.nicl.2020.102449
pubmed: 33032066
pmcid: 7552096
Lee SM, Kwon S, Lee YJ (2019) Diagnostic usefulness of arterial spin labeling in MR negative children with new onset seizures. Seizure 65:151–158. https://doi.org/10.1016/j.seizure.2019.01.024
doi: 10.1016/j.seizure.2019.01.024
pubmed: 30718217
Bernasconi A, Cendes F, Theodore WH, Gill RS, Koepp MJ, Hogan RE, Jackson GD, Federico P, Labate A, Vaudano AE, Blümcke I, Ryvlin P, Bernasconi N (2019) Recommendations for the use of structural magnetic resonance imaging in the care of patients with epilepsy: a consensus report from the International League against Epilepsy Neuroimaging Task Force. Epilepsia 60:1054–1068. https://doi.org/10.1111/epi.15612
doi: 10.1111/epi.15612
pubmed: 31135062
Vaudano AE, Ballerini A, Zucchini F, Micalizzi E, Scolastico S, Talami F, Giovannini G, Pugnaghi M, Orlandi N, Biagioli N, Cioclu MC, Vallone S, Genovese M, Todeschini A, Cavalleri F, Malagoli M, Meletti S (2023) Impact of an optimized epilepsy surgery imaging protocol for focal epilepsy: a monocentric prospective study. Epileptic Disord 25:45–56. https://doi.org/10.1002/epd2.20050
doi: 10.1002/epd2.20050
pubmed: 36946331
Kishk NA, Shamloul R, Moawad MK, Hamdi H, Morsy AA, Baghdadi M, Rizkallah M, Nawito A, Mohammad ME, Magdy R, Alsayyad E, Othman AS, Fouad AM, Rizk H (2023) Cost-effectiveness of HARNESS-MRI protocol in focal drug-resistant epilepsy in a limited-resources country: an Egyptian study. Clin Neurol Neurosurg 233:107946. https://doi.org/10.1016/j.clineuro.2023.107946
doi: 10.1016/j.clineuro.2023.107946
pubmed: 37639829
Rubinger L, Chan C, D’Arco F, Moineddin R, Muthaffar O, Rutka JT, Snead OC, Smith ML, Widjaja E (2016) Change in presurgical diagnostic imaging evaluation affects subsequent pediatric epilepsy surgery outcome. Epilepsia 57:32–40. https://doi.org/10.1111/epi.13229
doi: 10.1111/epi.13229
pubmed: 26715387
Spitzer H, Ripart M, Whitaker K, D’Arco F, Mankad K, Chen AA, Napolitano A, De Palma L, De Benedictis A, Foldes S, Humphreys Z, Zhang K, Hu W, Mo J, Likeman M, Davies S, Güttler C, Lenge M, Cohen NT, Tang Y, Wagstyl K (2022) Interpretable surface-based detection of focal cortical dysplasias: a Multi-centre Epilepsy Lesion Detection study. Brain 145:3859–3871. https://doi.org/10.1093/brain/awac224
doi: 10.1093/brain/awac224
pubmed: 35953082
pmcid: 9679165
Gaillard WD, Chiron C, Cross JH, Harvey AS, Kuzniecky R, Hertz-Pannier L, Vezina LG ILAE, Committee for Neuroimaging, Subcommittee for Pediatric (2009) guidelines for imaging infants and children with recent-onset epilepsy. Epilepsia 50:2147–2153. https://doi.org/10.1111/j.1528-1167.2009.02075.x
Fischl B (2012) FreeSurfer Neuroimage 62:774–781. https://doi.org/10.1016/j.neuroimage.2012.01.021
Warren AEL, Dalic LJ, Thevathasan W, Roten A, Bulluss KJ, Archer J (2020) Targeting the centromedian thalamic nucleus for deep brain stimulation. J Neurol Neurosurg Psychiatr 91:339–349. https://doi.org/10.1136/jnnp-2019-322030
doi: 10.1136/jnnp-2019-322030
Kim BS, Lee S-T, Yun TJ, Lee SK, Paeng JC, Jun J, Kang KM, Choi SH, Kim J-H, Sohn C-H (2016) Capability of arterial spin labeling MR imaging in localizing seizure focus in clinical seizure activity. Eur J Radiol 85:1295–1303. https://doi.org/10.1016/j.ejrad.2016.04.015
doi: 10.1016/j.ejrad.2016.04.015
pubmed: 27235877
Von Oertzen J, Urbach H, Jungbluth S, Kurthen M, Reuber M, Fernández G, Elger CE (2002) Standard magnetic resonance imaging is inadequate for patients with refractory focal epilepsy. J Neurol Neurosurg Psychiatr 73:643–647. https://doi.org/10.1136/jnnp.73.6.643
doi: 10.1136/jnnp.73.6.643
van Lanen RHGJ, Colon AJ, Wiggins CJ, Hoeberigs MC, Hoogland G, Roebroeck A, Ivanov D, Poser BA, Rouhl RPW, Hofman PAM, Jansen JFA, Backes W, Rijkers K, Schijns OEMG (2021) Ultra-high field magnetic resonance imaging in human epilepsy: a systematic review. Neuroimage Clin 30:102602. https://doi.org/10.1016/j.nicl.2021.102602
doi: 10.1016/j.nicl.2021.102602
pubmed: 33652376
pmcid: 7921009
Wellmer J, Quesada CM, Rothe L, Elger CE, Bien CG, Urbach H (2013) Proposal for a magnetic resonance imaging protocol for the detection of epileptogenic lesions at early outpatient stages. Epilepsia 54:1977–1987. https://doi.org/10.1111/epi.12375
doi: 10.1111/epi.12375
pubmed: 24117218
Chen X, Qian T, Kober T, Zhang G, Ren Z, Yu T, Piao Y, Chen N, Li K (2018) Gray-Matter-specific MR imaging improves the detection of epileptogenic zones in focal cortical dysplasia: a new sequence called fluid and white matter suppression (FLAWS). Neuroimage Clin 20:388–397. https://doi.org/10.1016/j.nicl.2018.08.010
doi: 10.1016/j.nicl.2018.08.010
pubmed: 30128277
pmcid: 6095948
Ganji Z, Hakak MA, Zamanpour SA, Zare H (2021) Automatic detection of focal cortical dysplasia type II in MRI: is the application of surface-based Morphometry and Machine Learning Promising? Front Hum Neurosci 15:608285. https://doi.org/10.3389/fnhum.2021.608285
doi: 10.3389/fnhum.2021.608285
pubmed: 33679343
pmcid: 7933541
Jiménez-Murillo D, Castro-Ospina AE, Duque-Muñoz L, Martínez-Vargas JD, Suárez-Revelo JX, Vélez-Arango JM, de la Iglesia-Vayá M (2023) Automatic detection of focal cortical dysplasia using MRI: a systematic review. Sensors 23. https://doi.org/10.3390/s23167072
Hinde S, Soares M, Burch J, Marson A, Woolacott N, Palmer S (2014) The added clinical and economic value of diagnostic testing for epilepsy surgery. Epilepsy Res 108:775–781. https://doi.org/10.1016/j.eplepsyres.2014.02.002
doi: 10.1016/j.eplepsyres.2014.02.002
pubmed: 24630045
pmcid: 4000270
Kwon C-S, Chang EF, Jetté N (2020) Cost-effectiveness of Advanced Imaging Technologies in the Presurgical Workup of Epilepsy. Epilepsy Curr 20:7–11. https://doi.org/10.1177/1535759719894307
doi: 10.1177/1535759719894307
pubmed: 31910665
pmcid: 7020533
Whiting P, Gupta R, Burch J, Mota REM, Wright K, Marson A, Weishmann U, Haycox A, Kleijnen J, Forbes C (2006) A systematic review of the effectiveness and cost-effectiveness of neuroimaging assessments used to visualise the seizure focus in people with refractory epilepsy being considered for surgery. Health Technol Assess 10:1–250, iii. https://doi.org/10.3310/hta10040
Widjaja E, Li B, Schinkel CD, Puchalski Ritchie L, Weaver J, Snead OC, Rutka JT, Coyte PC (2011) Cost-effectiveness of pediatric epilepsy surgery compared to medical treatment in children with intractable epilepsy. Epilepsy Res 94:61–68. https://doi.org/10.1016/j.eplepsyres.2011.01.005
doi: 10.1016/j.eplepsyres.2011.01.005
pubmed: 21306874
Lorio S, Adler S, Gunny R, D’Arco F, Kaden E, Wagstyl K, Jacques TS, Clark CA, Cross JH, Baldeweg T, Carmichael DW (2020) MRI profiling of focal cortical dysplasia using multi-compartment diffusion models. Epilepsia 61:433–444. https://doi.org/10.1111/epi.16451
doi: 10.1111/epi.16451
pubmed: 32065673
pmcid: 7154549