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The impact of epilepsy surgery on the structural connectome and its relation to outcome

Peter N. Taylor, Nishant Sinha, Yujiang Wang and 6 more

NeuroImage: Clinical · 2018 · CC BY

doi:10.1016/j.nicl.2018.01.028

Abstract

Background. Temporal lobe surgical resection brings seizure remission in up to 80% of patients, with long-term complete seizure freedom in 41%. However, it is unclear how surgery impacts on the structural white matter network, and how the network changes relate to seizure outcome.

Methods. We used white matter fibre tractography on preoperative diffusion MRI to generate a structural white matter network, and postoperative T1-weighted MRI to retrospectively infer the impact of surgical resection on this network. We then applied graph theory and machine learning to investigate the properties of change between the preoperative and predicted postoperative networks.

Results. Temporal lobe surgery had a modest impact on global network efficiency, despite the disruption caused. This was due to alternative shortest paths in the network leading to widespread increases in betweenness centrality post-surgery. Measurements of network change could retrospectively predict seizure outcomes with 79% accuracy and 65% specificity, which is twice as high as the empirical distribution. Fifteen connections which changed due to surgery were identified as useful for prediction of outcome, eight of which connected to the ipsilateral temporal pole.

Conclusion. Our results suggest that the use of network change metrics may have clinical value for predicting seizure outcome. This approach could be used to prospectively predict outcomes given a suggested resection mask using preoperative data only.

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References 95

  1. 1.
  2. 2.
  3. 3.

    Bennett O., Cardoso J., Duncan J.S., Winston G., Ourselin S. Learning how to See the Invisible - Using Machine Learning to Find Underlying Abnormality Patterns in Reportedly Normal MR Brain Images from Patients with Epilepsy. Proceedings. 2017.

    Not in our library

  4. 4.

    Bernhardt Boris C., Chen Zhang, He Yong, Evans Alan C., Bernasconi Neda. Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. Cereb. Cortex. 2011;21(9):2147-2157.

    Not in our library10.1093/cercor/bhq291

  5. 5.

    Bernhardt Boris C., Hong Seok-Jun, Bernasconi Andrea, Bernasconi Neda. Magnetic resonance imaging pattern learning in temporal lobe epilepsy: classification and prognostics. Ann. Neurol. 2015;77(3):436-446.

    Not in our library10.1002/ana.24341

  6. 6.

    Besson Pierre, Dinkelacker Vera, Valabregue Romain, Thivard Lionel, Leclerc Xavier, Baulac Michel, Sammler Daniela. Structural connectivity differences in left and right temporal lobe epilepsy. NeuroImage. 2014;100:135-144.

    Not in our library10.1016/j.neuroimage.2014.04.071

  7. 7.

    Besson Pierre, Lopes Renaud, Leclerc Xavier, Derambure Philippe, Tyvaert Louise. Intra-subject reliability of the high-resolution whole-brain structural connectome. NeuroImage. 2014;102:283-293.

    Not in our library10.1016/j.neuroimage.2014.07.064

  8. 8.

    Besson Pierre, Kathleen Bandt S., Proix Timothée, Lagarde Stanislas, Jirsa Viktor K., Ranjeva Jean-Philippe, Bartolomei Fabrice, Guye Maxime. Anatomic consistencies across epilepsies: a stereotactic-EEG informed high-resolution structural connectivity study. Brain. 2017;140(10):2639-2652.

    Not in our library10.1093/brain/awx181

  9. 9.
  10. 10.

    Bonilha Leonardo, Nesland Travis, Martz Gabriel U., Joseph Jane E., Spampinato Maria V., Edwards Jonathan C., Tabesh Ali. Medial temporal lobe epilepsy is associated with neuronal fibre loss and paradoxical increase in structural connectivity of limbic structures. J. Neurol. Neurosurg. Psychiatry. 2012;83(9):903-909.

    Not in our library10.1136/jnnp-2012-302476

  11. 11.

    Bonilha Leonardo, Helpern Joseph A., Sainju Rup, Nesland Travis, Edwards Jonathan C., Glazier Steven S., Tabesh Ali. Presurgical connectome and postsurgical seizure control in temporal lobe epilepsy. Neurology. 2013;81(19):1704-1710.

    Not in our library10.1212/01.wnl.0000435306.95271.5f

  12. 12.

    Bonilha Leonardo, Jensen Jens H., Baker Nathaniel, Breedlove Jesse, Nesland Travis, Lin Jack J., Drane Daniel L., Saindane Amit M., Binder Jeffrey R., Kuzniecky Ruben I. The brain connectome as a personalized biomarker of seizure outcomes after temporal lobectomy. Neurology. 2015;84(18):1846-1853.

    Not in our library10.1212/wnl.0000000000001548

  13. 13.

    Breiman L., Friedman J.H., Alshen R.A., Stone C.J. CART: Classification and Regression Trees. 1984.

    Not in our library

  14. 14.

    Cardoso M. Jorge, Modat Marc, Wolz Robin, Melbourne Andrew, Cash David, Rueckert Daniel, Ourselin Sebastien. Geodesic information flows: spatially-variant graphs and their application to segmentation and fusion. IEEE Trans. Med. Imaging. 2015;34(9):1976-1988.

    Not in our library10.1109/tmi.2015.2418298

  15. 15.
  16. 16.

    Chavez Mario, Valencia Miguel, Navarro Vincent, Latora Vito, Martinerie Jacques. Functional modularity of background activities in normal and epileptic brain networks. Phys. Rev. Lett. 2010;104(11):118701.

    Not in our library10.1103/physrevlett.104.118701

  17. 17.

    Cook Philip A., Symms Mark, Boulby Philip A., Alexander Daniel C. Optimal acquisition orders of diffusion-weighted mri measurements. J. Magn. Reson. Imaging. 2007;25(5):1051-1058.

    Not in our library10.1002/jmri.20905

  18. 18.
  19. 19.

    De Tisi Jane, Bell Gail S., Peacock Janet L., McEvoy Andrew W., Harkness William F.J., Sander Josemir W., Duncan John S. The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study. Lancet. 2011;378(9800):1388-1395.

    Not in our library10.1016/s0140-6736(11)60890-8

  20. 20.

    Desikan Rahul S., Ségonne Florent, Fischl Bruce, Quinn Brian T., Dickerson Bradford C., Blacker Deborah, Buckner Randy L. An automated labeling system for subdividing the human cerebral cortex on Mri scans into gyral based regions of interest. NeuroImage. 2006;31(3):968-980.

    Not in our library10.1016/j.neuroimage.2006.01.021

  21. 21.

    Douw Linda, DeSalvo Matthew N., Tanaka Naoaki, Cole Andrew J., Liu Hesheng, Reinsberger Claus, Stufflebeam Steven M. Dissociated multimodal hubs and seizures in temporal lobe epilepsy. Ann. Clin. Transl. Neurol. 2015;2(4):338-352.

    Not in our library10.1002/acn3.173

  22. 22.

    Duchi John, Shalev-Shwartz Shai, Singer Yoram, Chandra Tushar. Efficient projections onto the L1-ball for learning in high dimensions. Proceedings of the 25th International Conference on Machine Learning. 2008;272-279.

    Not in our library

  23. 23.

    Estrada E., Hatano N. Communicability in complex networks. Phys. Rev. E. 2008;77(3):036111.

    Not in our library10.1103/physreve.77.036111

  24. 24.

    Faber Jennifer, Schoene-Bake Jan-Christoph, Trautner Peter, Lehe Marec, Elger Christian E., Weber Bernd. Progressive fiber tract affections after temporal lobe surgery. Epilepsia. 2013;54(4).

    Not in our library10.1111/epi.12077

  25. 25.

    Feis Delia-Lisa, Schoene-Bake Jan-Christoph, Elger Christian, Wagner Jan, Tittgemeyer Marc, Weber Bernd. Prediction of post-surgical seizure outcome in left mesial temporal lobe epilepsy. Neurol. Clin. 2013;2:903-911.

    Not in our library10.1016/j.nicl.2013.06.010

  26. 26.

    Fischl Bruce. FreeSurfer. NeuroImage. 2012;62(2):774-781.

    Not in our library10.1016/j.neuroimage.2012.01.021

  27. 27.

    Fischl Bruce, Salat David H., Busa Evelina, Albert Marilyn, Dieterich Megan, Haselgrove Christian, van der Kouwe Andre. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33(3):341-355.

    Not in our library10.1016/s0896-6273(02)00569-x

  28. 28.

    Fischl Bruce, van der Kouwe André, Destrieux Christophe, Halgren Eric, Ségonne Florent, Salat David H., Busa Evelina. Automatically parcellating the human cerebral cortex. Cereb. Cortex. 2004;14(1):11-22.

    Not in our library10.1093/cercor/bhg087

  29. 29.

    Focke Niels K., Yogarajah Mahinda, Symms Mark R., Gruber Oliver, Paulus Walter, Duncan John S. Automated Mr image classification in temporal lobe epilepsy. NeuroImage. 2012;59(1):356-362.

    Not in our library10.1016/j.neuroimage.2011.07.068

  30. 30.

    Goñi J., van den Heuvel M.P., Avena-Koenigsberger A., Velez de Mendizabal N., Betzel R.F., Griffa A., Sporns O. Resting-brain functional connectivity predicted by analytic measures of network communication. Proc. Natl. Acad. Sci. U. S. A. 2014;111(2):833-838.

    Not in our library10.1073/pnas.1315529111

  31. 31.
  32. 32.

    Gooneratne I.K., Mannan S., de Tisi J., Gonzalez J.C., McEvoy A.W., Miserocchi A., Diehl B., Wehner T., Bell G.S., Sander J.W., Duncan J.S. Somatic complications of epilepsy surgery over 25 years at a single center. Epilepsy Res. 2017;132:70-77.

    Not in our library10.1016/j.eplepsyres.2017.02.016

  33. 33.

    Hardy Steven G., Miller John W., Holmes Mark D., Born Donald E., Ojemann George A., Dodrill Carl B., Hallam Danial K. Factors predicting outcome of surgery for intractable epilepsy with pathologically verified mesial temporal sclerosis. Epilepsia. 2003;44(4):565-568.

    Not in our library10.1046/j.1528-1157.2003.39202.x

  34. 34.

    He X., Doucet G.E., Pustina D., Sperling M.R., Sharan A.D., Tracy J.I. Presurgical thalamic “hubness” predicts surgical outcome in temporal lobe epilepsy. Neurology. 2017;10-1212.

    Not in our library10.1212/wnl.0000000000004035

  35. 35.

    van den Heuvel M.P., Stam C.J., Kahn R.S., Pol H.E.H. Efficiency of functional brain networks and intellectual performance. J. Neurosci. 2009;29(23):7619-7624.

    Not in our library10.1523/jneurosci.1443-09.2009

  36. 36.

    Hoerl A.E., Kennard R.W. Ridge Regression. 2004;9780471667193.

    Not in our library

  37. 37.

    Irimia Andrei, Van Horn John Darrell. Scale-dependent variability and quantitative regimes in graph-theoretic representations of human cortical networks. Brain Connect. 2016;6(2):152-163.

    Not in our library10.1089/brain.2015.0360

  38. 38.

    Jehi L., Yardi R., Chagin K., Tassi L., Russo G.L., Worrell G., Chauvel P. Development and validation of nomograms to provide individualised predictions of seizure outcomes after epilepsy surgery: a retrospective analysis. Lancet Neurol. 2015;14(3):283-290.

    Not in our library10.1016/s1474-4422(14)70325-4

  39. 39.

    Jenkinson Mark, Smith Stephen. A global optimisation method for robust affine registration of brain images. Med. Image Anal. 2001;5(2):143-156.

    Not in our library10.1016/s1361-8415(01)00036-6

  40. 40.

    Jenkinson Mark, Bannister Peter, Brady Michael, Smith Stephen. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17(2):825-841.

    Not in our library10.1016/s1053-8119(02)91132-8

All 95 references

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