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Wagstyl K, Whitaker K, Raznahan A, et al. Atlas of lesion locations and postsurgical seizure freedom in focal cortical dysplasia: A MELD study. Epilepsia. 2021;doi: 10.1111/epi.17130.
Wagstyl, K., Whitaker, K., Raznahan, A., Seidlitz, J., Vértes, P. E., Foldes, S., Humphreys, Z., Hu, W., Mo, J., Likeman, M., Davies, S., Lenge, M., Cohen, N. T., Tang, Y., Wang, S., Ripart, M., Chari, A., Tisdall, M., Bargallo, N., Conde-Blanco, E., Pariente, J. C., Pascual-Diaz, S., Delgado-Martínez, I., Pérez-Enríquez, C., Lagorio, I., Abela, E., Mullatti, N., O'Muircheartaigh, J., Vecchiato, K., Liu, Y., Caligiuri, M., Sinclair, B., Vivash, L., Willard, A., Kandasamy, J., McLellan, A., Sokol, D., Semmelroch, M., Kloster, A., Opheim, G., Yasuda, C., Zhang, K., Hamandi, K., Barba, C., Guerrini, R., Gaillard, W. D., You, X., Wang, I., González-Ortiz, S., Severino, M., Striano, P., Tortora, D., Kalviainen, R., Gambardella, A., Labate, A., Desmond, P., Lui, E., O'Brien, T., Shetty, J., Jackson, G., Duncan, J. S., Winston, G. P., Pinborg, L., Cendes, F., Cross, J. H., Baldeweg, T., & Adler, S. (2021). Atlas of lesion locations and postsurgical seizure freedom in focal cortical dysplasia: A MELD study. Epilepsia, . https://doi.org/10.1111/epi.17130
Wagstyl, Konrad, et al. "Atlas of lesion locations and postsurgical seizure freedom in focal cortical dysplasia: A MELD study." Epilepsia vol. (2021). doi: https://doi.org/10.1111/epi.17130
Wagstyl K, Whitaker K, Raznahan A, Seidlitz J, Vértes PE, Foldes S, Humphreys Z, Hu W, Mo J, Likeman M, Davies S, Lenge M, Cohen NT, Tang Y, Wang S, Ripart M, Chari A, Tisdall M, Bargallo N, Conde-Blanco E, Pariente JC, Pascual-Diaz S, Delgado-Martínez I, Pérez-Enríquez C, Lagorio I, Abela E, Mullatti N, O'Muircheartaigh J, Vecchiato K, Liu Y, Caligiuri M, Sinclair B, Vivash L, Willard A, Kandasamy J, McLellan A, Sokol D, Semmelroch M, Kloster A, Opheim G, Yasuda C, Zhang K, Hamandi K, Barba C, Guerrini R, Gaillard WD, You X, Wang I, González-Ortiz S, Severino M, Striano P, Tortora D, Kalviainen R, Gambardella A, Labate A, Desmond P, Lui E, O'Brien T, Shetty J, Jackson G, Duncan JS, Winston GP, Pinborg L, Cendes F, Cross JH, Baldeweg T, Adler S. Atlas of lesion locations and postsurgical seizure freedom in focal cortical dysplasia: A MELD study. Epilepsia. 2021 Nov 29; doi: 10.1111/epi.17130. Epub 2021 Nov 29. PMID: 34845719.
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Epilepsia. 2021 Nov 29; doi: 10.1111/epi.17130. Epub 2021 Nov 29.

Atlas of lesion locations and postsurgical seizure freedom in focal cortical dysplasia: A MELD study.

Epilepsia

Konrad Wagstyl, Kirstie Whitaker, Armin Raznahan, Jakob Seidlitz, Petra E Vértes, Stephen Foldes, Zachary Humphreys, Wenhan Hu, Jiajie Mo, Marcus Likeman, Shirin Davies, Matteo Lenge, Nathan T Cohen, Yingying Tang, Shan Wang, Mathilde Ripart, Aswin Chari, Martin Tisdall, Nuria Bargallo, Estefanía Conde-Blanco, Jose Carlos Pariente, Saül Pascual-Diaz, Ignacio Delgado-Martínez, Carmen Pérez-Enríquez, Ilaria Lagorio, Eugenio Abela, Nandini Mullatti, Jonathan O'Muircheartaigh, Katy Vecchiato, Yawu Liu, Maria Caligiuri, Ben Sinclair, Lucy Vivash, Anna Willard, Jothy Kandasamy, Ailsa McLellan, Drahoslav Sokol, Mira Semmelroch, Ane Kloster, Giske Opheim, Clarissa Yasuda, Kai Zhang, Khalid Hamandi, Carmen Barba, Renzo Guerrini, William Davis Gaillard, Xiaozhen You, Irene Wang, Sofía González-Ortiz, Mariasavina Severino, Pasquale Striano, Domenico Tortora, Reetta Kalviainen, Antonio Gambardella, Angelo Labate, Patricia Desmond, Elaine Lui, Terry O'Brien, Jay Shetty, Graeme Jackson, John S Duncan, Gavin P Winston, Lars Pinborg, Fernando Cendes, Judith Helen Cross, Torsten Baldeweg, Sophie Adler

Affiliations

  1. Wellcome Centre for Human Neuroimaging, London, UK.
  2. Alan Turing Institute, London, UK.
  3. Developmental Neurogenomics, National Institute of Mental Health, Bethesda, Maryland, USA.
  4. Department of Child and Adolescent Psychiatry and Behavioral Science, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.
  5. Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
  6. Department of Psychiatry, Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, UK.
  7. Barrow Neurological Institute at Phoenix Children's Hospital, Phoenix, Arizona, USA.
  8. Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China.
  9. Bristol Royal Hospital for Children, Bristol, UK.
  10. Cardiff University Brain Research Imaging Centre, School of Psychology, Cardiff, UK.
  11. Welsh Epilepsy Unit, Cardiff and Vale University Health Board, University Hospital of Wales, Cardiff, UK.
  12. Neuroscience Department, Meyer Children's Hospital-University of Florence, Florence, Italy.
  13. Center for Neuroscience, Children's National Hospital, Washington, District of Columbia, USA.
  14. Department of Neurology, West China Hospital of Sichuan University, Chengdu, China.
  15. Epilepsy Center, Neurological Institute, Cleveland Clinic, Cleveland, Ohio, USA.
  16. Epilepsy Center, Department of Neurology, Epilepsy Center, Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, China.
  17. University College London Great Ormond Street Institute for Child Health, London, UK.
  18. Great Ormond Street Hospital, National Health Service Foundation Trust, UK.
  19. Hospital Clinic of Barcelona, Barcelona, Spain.
  20. Magnetic Resonance Core Image Facility, August Pi i Sunyer Biomedical Research Institute, Spain.
  21. Hospital of the Sea, Barceloneta Promenade, Barcelona, Spain.
  22. Giannina Gaslini Institute, Scientific Institute for Research and Health Care, Genova, Italy.
  23. Center for Neuropsychiatry and Intellectual Disability, Aargau Psychiatric Services, Windisch, Switzerland.
  24. Institute of Psychiatry, Psychology, and Neuroscience, London, UK.
  25. Department of Neurology, University of Eastern Finland, Kuopio, Finland.
  26. Institute of Neurology, Department of Medical and Surgical Sciences, Magna Graecia University of Catanzaro, Catanzaro, Italy.
  27. Department of Neuroscience, Central Clinical School, Monash University, Melbourne, Victoria, Australia.
  28. Department of Neurology, Alfred Hospital, Melbourne, Victoria, Australia.
  29. Royal Hospital for Children and Young People, Little France Crescent, Edinburgh, UK.
  30. Florey Institute of Neuroscience and Mental Health, Heidelberg, Victoria, Australia.
  31. Neurobiology Research Unit and Epilepsy Clinic, Department of Neurology, Copenhagen University Hospital Rigshopsitalet, Copenhagen, Denmark.
  32. Department of Neurology, University of Campinas, Campinas, Brazil.
  33. Kuopio Epilepsy Center, Neurocenter, Kuopio University Hospital, Kuopio, Finland.
  34. Department of Radiology, Royal Melbourne Hospital, Parkville, Victoria, Australia.
  35. University College London Queen Square Institute of Neurology, London, UK.
  36. Division of Neurology, Department of Medicine, Queen's University, Kingston, Ontario, Canada.

PMID: 34845719 DOI: 10.1111/epi.17130

Abstract

OBJECTIVE: Drug-resistant focal epilepsy is often caused by focal cortical dysplasias (FCDs). The distribution of these lesions across the cerebral cortex and the impact of lesion location on clinical presentation and surgical outcome are largely unknown. We created a neuroimaging cohort of patients with individually mapped FCDs to determine factors associated with lesion location and predictors of postsurgical outcome.

METHODS: The MELD (Multi-centre Epilepsy Lesion Detection) project collated a retrospective cohort of 580 patients with epilepsy attributed to FCD from 20 epilepsy centers worldwide. Magnetic resonance imaging-based maps of individual FCDs with accompanying demographic, clinical, and surgical information were collected. We mapped the distribution of FCDs, examined for associations between clinical factors and lesion location, and developed a predictive model of postsurgical seizure freedom.

RESULTS: FCDs were nonuniformly distributed, concentrating in the superior frontal sulcus, frontal pole, and temporal pole. Epilepsy onset was typically before the age of 10 years. Earlier epilepsy onset was associated with lesions in primary sensory areas, whereas later epilepsy onset was associated with lesions in association cortices. Lesions in temporal and occipital lobes tended to be larger than frontal lobe lesions. Seizure freedom rates varied with FCD location, from around 30% in visual, motor, and premotor areas to 75% in superior temporal and frontal gyri. The predictive model of postsurgical seizure freedom had a positive predictive value of 70% and negative predictive value of 61%.

SIGNIFICANCE: FCD location is an important determinant of its size, the age at epilepsy onset, and the likelihood of seizure freedom postsurgery. Our atlas of lesion locations can be used to guide the radiological search for subtle lesions in individual patients. Our atlas of regional seizure freedom rates and associated predictive model can be used to estimate individual likelihoods of postsurgical seizure freedom. Data-driven atlases and predictive models are essential for evidence-based, precision medicine and risk counseling in epilepsy.

© 2021 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.

Keywords: MRI; drug-resistant epilepsy; focal cortical dysplasia; lesions; neurosurgery

References

  1. US Institute of Medicine Committee on the Public Health Dimensions of the Epilepsies. Epilepsy across the spectrum: promoting health and understanding. England MJ, Liverman CT, Schultz AM, Strawbridge LM, editors. Washington, DC: National Academies Press; 2012. - PubMed
  2. Blümcke I, Thom M, Aronica E, Armstrong DD, Vinters HV, Palmini A, et al. The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia. 2011;52(1):158-74. - PubMed
  3. Blumcke I, Spreafico R, Haaker G, Coras R, Kobow K, Bien CG, et al. Histopathological findings in brain tissue obtained during epilepsy surgery. N Engl J Med. 2017;377(17):1648-56. - PubMed
  4. Lamberink HJ, Otte WM, Blümcke I, Braun KPJ, Aichholzer M, European Epilepsy Brain Bank writing group, study group, et al. Seizure outcome and use of antiepileptic drugs after epilepsy surgery according to histopathological diagnosis: a retrospective multicentre cohort study. Lancet Neurol. 2020;19(9):748-57. - PubMed
  5. Chassoux F, Devaux B, Landré E, Turak B, Nataf F, Varlet P, et al. Stereoelectroencephalography in focal cortical dysplasia: a 3D approach to delineating the dysplastic cortex. Brain. 2000;123(Pt 8):1733-51. - PubMed
  6. Hong S-J, Kim H, Schrader D, Bernasconi N, Bernhardt BC, Bernasconi A. Automated detection of cortical dysplasia type II in MRI-negative epilepsy. Neurology. 2014;83(1):48-55. - PubMed
  7. Adler S, Wagstyl K, Gunny R, Ronan L, Carmichael D, Cross JH, et al. Novel surface features for automated detection of focal cortical dysplasias in paediatric epilepsy. Neuroimage Clin. 2017;14:18-27. - PubMed
  8. Jin B, Krishnan B, Adler S, Wagstyl K, Hu W, Jones S, et al. Automated detection of focal cortical dysplasia type II with surface-based magnetic resonance imaging postprocessing and machine learning. Epilepsia. 2018;59(5):982-92. - PubMed
  9. Whelan CD, Altmann A, Botía JA, Jahanshad N, Hibar DP, Absil J, et al. Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain. 2018;141(2):391-408. - PubMed
  10. Dwivedi R, Ramanujam B, Chandra PS, Sapra S, Gulati S, Kalaivani M, et al. Surgery for drug-resistant epilepsy in children. N Engl J Med. 2017;377(17):1639-47. - PubMed
  11. Krsek P, Maton B, Jayakar P, Dean P, Korman B, Rey G, et al. Incomplete resection of focal cortical dysplasia is the main predictor of poor postsurgical outcome. Neurology. 2009;72(3):217-23. - PubMed
  12. Choi SA, Kim SY, Kim H, Kim WJ, Kim H, Hwang H, et al. Surgical outcome and predictive factors of epilepsy surgery in pediatric isolated focal cortical dysplasia. Epilepsy Res. 2018;139:54-9. - PubMed
  13. Alexandre V Jr, Walz R, Bianchin MM, Velasco TR, Terra-Bustamante VC, Wichert-Ana L, et al. Seizure outcome after surgery for epilepsy due to focal cortical dysplastic lesions. Seizure. 2006;15(6):420-7. - PubMed
  14. Mühlebner A, Gröppel G, Dressler A, Reiter-Fink E, Kasprian G, Prayer D, et al. Epilepsy surgery in children and adolescents with malformations of cortical development-outcome and impact of the new ILAE classification on focal cortical dysplasia. Epilepsy Res. 2014;108(9):1652-61. - PubMed
  15. Téllez-Zenteno JF, Ronquillo LH, Moien-Afshari F, Wiebe S. Surgical outcomes in lesional and non-lesional epilepsy: a systematic review and meta-analysis. Epilepsy Res. 2010;89(2):310-8. - PubMed
  16. Fischl B. FreeSurfer. NeuroImage. 2012;62(2):774-81. - PubMed
  17. MELD Project MELD project’s protocols. 1st January 2019. https://doi.org/10.17504/protocols.io.n3ddgi6 - PubMed
  18. Figueroa RL, Zeng-Treitler Q, Kandula S, Ngo LH. Predicting sample size required for classification performance. BMC Med Inform Decis Mak. 2012;12:8. - PubMed
  19. Sydnor VJ, Larsen B, Bassett DS, Alexander-Bloch A, Fair DA, Liston C, et al. Neurodevelopment of the association cortices: patterns, mechanisms, and implications for psychopathology. Neuron. 2021;109(18):2820-46. - PubMed
  20. Alexander-Bloch AF, Shou H, Liu S, Satterthwaite TD, Glahn DC, Shinohara RT, et al. On testing for spatial correspondence between maps of human brain structure and function. NeuroImage. 2018;178:540-51. - PubMed
  21. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol. 1995;57(1):289-300. - PubMed
  22. Rodin RE, Dou Y, Kwon M, Sherman MA, D’Gama AM, Doan RN, et al. The landscape of somatic mutation in cerebral cortex of autistic and neurotypical individuals revealed by ultra-deep whole-genome sequencing. Nat Neurosci. 2021;24(2):176-85. - PubMed
  23. Hawrylycz M, Miller JA, Menon V, Feng D, Dolbeare T, Guillozet-Bongaarts AL, et al. Canonical genetic signatures of the adult human brain. Nat Neurosci. 2015;18(12):1832-44. - PubMed
  24. Frauscher B, von Ellenrieder N, Zelmann R, Doležalová I, Minotti L, Olivier A, et al. Atlas of the normal intracranial electroencephalogram: neurophysiological awake activity in different cortical areas. Brain. 2018;141(4):1130-44. - PubMed
  25. Wagstyl K, Larocque S, Cucurull G, Lepage C, Cohen JP, Bludau S, et al. BigBrain 3D atlas of cortical layers: cortical and laminar thickness gradients diverge in sensory and motor cortices. PLoS Biol. 2020;18(4):e3000678. - PubMed
  26. Yeo BTT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106(3):1125-65. - PubMed
  27. Raznahan A, Shaw P, Lalonde F, Stockman M, Wallace GL, Greenstein D, et al. How does your cortex grow? J Neurosci. 2011;31(19):7174-7. - PubMed
  28. Whitaker KJ, Vértes PE, Romero-Garcia R, Váša F, Moutoussis M, Prabhu G, et al. Adolescence is associated with genomically patterned consolidation of the hubs of the human brain connectome. Proc Natl Acad Sci U S A. 2016;113(32):9105-10. - PubMed
  29. Fauser S, Bast T, Altenmüller D-M, Schulte-Mönting J, Strobl K, Steinhoff BJ, et al. Factors influencing surgical outcome in patients with focal cortical dysplasia. J Neurol Neurosurg Psychiatry. 2008;79(1):103-5. - PubMed
  30. Vakharia VN, Duncan JS, Witt J-A, Elger CE, Staba R, Engel J Jr. Getting the best outcomes from epilepsy surgery. Ann Neurol. 2018;83(4):676-90. - PubMed
  31. Ramantani G, Kadish NE, Mayer H, Anastasopoulos C, Wagner K, Reuner G, et al. Frontal lobe epilepsy surgery in childhood and adolescence: predictors of long-term seizure freedom, overall cognitive and adaptive functioning. Neurosurgery. 2018;83(1):93-103. - PubMed
  32. Rowland NC, Englot DJ, Cage TA, Sughrue ME, Barbaro NM, Chang EF. A meta-analysis of predictors of seizure freedom in the surgical management of focal cortical dysplasia. J Neurosurg. 2012;116(5):1035-41. - PubMed
  33. Garcia Gracia C, Yardi R, Kattan MW, Nair D, Gupta A, Najm I, et al. Seizure freedom score: a new simple method to predict success of epilepsy surgery. Epilepsia. 2015;56(3):359-65. - PubMed
  34. Jack CR Jr, Bernstein MA, Fox NC, Thompson P, Alexander G, Harvey D, et al. The Alzheimer’s disease neuroimaging initiative (ADNI): MRI methods. J Magn Reson Imaging. 2008;27(4):685-91. - PubMed
  35. Di Martino A, Yan C-G, Li Q, Denio E, Castellanos FX, Alaerts K The autism brain imaging data exchange: towards a large-scale evaluation of the intrinsic brain architecture in autism. Mol. Psychiatry. 2013;19(6):659-667. - PubMed

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