Two-trajectory laser amygdalohippocampotomy: Anatomic modeling and initial seizure outcomes.
computer simulation
entorhinal cortex
laser interstitial thermal therapy
medial temporal lobe epilepsy
piriform cortex
Journal
Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
revised:
13
07
2021
received:
08
03
2021
accepted:
14
07
2021
pubmed:
3
8
2021
medline:
19
4
2022
entrez:
2
8
2021
Statut:
ppublish
Résumé
Laser interstitial thermal therapy (LITT) for mesial temporal lobe epilepsy (mTLE) is typically performed with one trajectory to target the medial temporal lobe (MTL). MTL structures such as piriform and entorhinal cortex are epileptogenic, but due to their relative geometry, they are difficult to target with one trajectory while simultaneously maintaining adequate ablation of the amygdala and hippocampus. We hypothesized that a two-trajectory approach could improve ablation of all relevant MTL structures. First, we created large-scale computer simulations to compare idealized one- vs two-trajectory approaches. A two-trajectory approach was then validated in an initial cohort of patients. We used magnetic resonance imaging (MRI) from the Human Connectome Project (HCP) to create subject-specific target structures consisting of hippocampus, amygdala, and piriform/entorhinal/perirhinal cortex. An algorithm searched for safe potential trajectories along the hippocampal axis (catheter one) and along the amygdala-piriform axis (catheter two) and compared this to a single trajectory optimized over all structures. The proportion of each structure ablated at various burn radii was evaluated. A cohort of 11 consecutive patients with mTLE received two-trajectory LITT; demographic, operative, and outcome data were collected. The two-trajectory approach was superior to the one-trajectory approach at nearly all burn radii for all hippocampal subfields and amygdala nuclei (p < .05). Two-laser trajectories achieved full ablation of MTL cortical structures at physiologically realistic burn radii, whereas one-laser trajectories could not. Five patients with at least 1 year of follow-up (mean = 21.8 months) experienced Engel class I outcomes; 6 patients with less than 1 year of follow-up (mean = 6.6 months) are on track for Engel class I outcomes. Our anatomic analyses and initial clinical results suggest that LITT amygdalohippocampotomy performed via two-laser trajectories may promote excellent seizure outcomes. Future studies are required to validate the long-term clinical efficacy and safety of this approach.
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2344-2356Subventions
Organisme : NIH HHS
ID : S10 OD025181
Pays : United States
Organisme : NIMH NIH HHS
ID : T32 MH020068
Pays : United States
Informations de copyright
© 2021 International League Against Epilepsy.
Références
Fisher RS, van Emde BW, Blume W, Elger C, Genton P, Lee P, et al. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia. 2005;46:470-2.
Thurman DJ, Beghi E, Begley CE, Berg AT, Buchhalter JR, Ding D, et al. Standards for epidemiologic studies and surveillance of epilepsy. Epilepsia. 2011;52(Suppl 7):2-26.
Wiebe S, Blume WT, Girvin JP, Eliasziw M. A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med. 2001;345:311-8.
Jermakowicz WJ, Kanner AM, Sur S, Bermudez C, D'Haese PF, Kolcun JPG, et al. Laser thermal ablation for mesiotemporal epilepsy: analysis of ablation volumes and trajectories. Epilepsia. 2017;58:801-10.
Kang JY, Wu C, Tracy J, Lorenzo M, Evans J, Nei M, et al. Laser interstitial thermal therapy for medically intractable mesial temporal lobe epilepsy. Epilepsia. 2016;57:325-34.
Tao JX, Wu S, Lacy M, Rose S, Issa NP, Yang CW, et al. Stereotactic EEG-guided laser interstitial thermal therapy for mesial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry. 2018;89:542-8.
Grewal SS, Zimmerman RS, Worrell G, Brinkmann BH, Tatum WO, Crepeau AZ, et al. Laser ablation for mesial temporal epilepsy: a multi-site, single institutional series. J Neurosurg. 2018;1-8.
Le S, Ho AL, Fisher RS, Miller KJ, Henderson JM, Grant GA, et al. Laser interstitial thermal therapy (LITT): seizure outcomes for refractory mesial temporal lobe epilepsy. Epilepsy Behav. 2018;89:37-41.
Willie JT, Laxpati NG, Drane DL, Gowda A, Appin C, Hao C, et al. Real-time magnetic resonance-guided stereotactic laser amygdalohippocampotomy for mesial temporal lobe epilepsy. Neurosurgery. 2014;74:569-84.
Gross RE, Stern MA, Willie JT, Fasano RE, Saindane AM, Soares BP, et al. Stereotactic laser amygdalohippocampotomy for mesial temporal lobe epilepsy. Ann Neurol. 2018;83:575-87.
Drane DL, Loring DW, Voets NL, Price M, Ojemann JG, Willie JT, et al. Better object recognition and naming outcome with MRI-guided stereotactic laser amygdalohippocampotomy for temporal lobe epilepsy. Epilepsia. 2015;56:101-13.
Donos C, Breier J, Friedman E, Rollo P, Johnson J, Moss L, et al. Laser ablation for mesial temporal lobe epilepsy: surgical and cognitive outcomes with and without mesial temporal sclerosis. Epilepsia. 2018;59:1421-32.
Wu C, Boorman DW, Gorniak RJ, Farrell CJ, Evans JJ, Sharan AD. The effects of anatomic variations on stereotactic laser amygdalohippocampectomy and a proposed protocol for trajectory planning. Neurosurgery. 2015;11(Suppl 2):345-56.
Vaughan DN, Jackson GD. The piriform cortex and human focal epilepsy. Front Neurol. 2014;5:259.
Curia G, Lucchi C, Vinet J, Gualtieri F, Marinelli C, Torsello A, et al. Pathophysiogenesis of mesial temporal lobe epilepsy: is prevention of damage antiepileptogenic? Curr Med Chem. 2014;21:663-88.
Galovic M, Baudracco I, Wright-Goff E, Pillajo G, Nachev P, Wandschneider B, et al. Association of piriform cortex resection with surgical outcomes in patients with temporal lobe epilepsy. JAMA Neurol. 2019;76:690-700.
Van Essen DC, Smith SM, Barch DM, Behrens TE, Yacoub E, Ugurbil K, et al. The WU-Minn human connectome project: an overview. NeuroImage. 2013;80:62-79.
Marcus DS, Harwell J, Olsen T, Hodge M, Glasser MF, Prior F, et al. Informatics and data mining tools and strategies for the human connectome project. Front Neuroinform. 2011;5:4.
Fischl B. FreeSurfer. Neuroimage. 2012;62:774-81.
Iglesias JE, Augustinack JC, Nguyen K, Player CM, Player A, Wright M, et al. A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: application to adaptive segmentation of in vivo MRI. NeuroImage. 2015;115:117-37.
Glasser MF, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, et al. A multi-modal parcellation of human cerebral cortex. Nature. 2016;536:171-8.
Argall BD, Saad ZS, Beauchamp MS. Simplified intersubject averaging on the cortical surface using SUMA. Hum Brain Mapp. 2006;27:14-27.
Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res. 1996;29:162-73.
Saad ZS, Reynolds RC. SUMA. Neuroimage. 2012;62:768-73.
Kikinis R, Pieper SD, Vosburgh KG. 3D slicer: A platform for subject-specific image analysis, visualization, and clinical support. In: Jolesz FA, editor. Intraoperative Imaging and Image-Guided Therapy. New York, NY: Springer; 2014. p. 277-89.
Fonov VS, Evans AC, McKinstry RC, Almli CR, Collins DL. Unbiased nonlinear average age-appropriate brain templates from birth to adulthood. NeuroImage. 2009;47:S102.
Fasano A, Hömberg D, Naumov D. On a mathematical model for laser-induced thermotherapy. Appl Math Model. 2010;34:3831-40.
Vakharia VN, Sparks R, Li K, O'Keeffe AG, Miserocchi A, McEvoy AW, et al. Automated trajectory planning for laser interstitial thermal therapy in mesial temporal lobe epilepsy. Epilepsia. 2018;59:814-24.
Wu C, Jermakowicz WJ, Chakravorti S, Cajigas I, Sharan AD, Jagid JR, et al. Effects of surgical targeting in laser interstitial thermal therapy for mesial temporal lobe epilepsy: a multicenter study of 234 patients. Epilepsia. 2019;60:1171-83.
Satzer D, Tao JX, Warnke PC. Extent of parahippocampal ablation is associated with seizure freedom after laser amygdalohippocampotomy. J Neurosurg. 2021;aop:1-10.
Vakharia VN, Sparks RE, Li K, O'Keeffe AG, Pérez-García F, França LGS, et al. Multicenter validation of automated trajectories for selective laser amygdalohippocampectomy. Epilepsia. 2019;60:1949-59.
Li K, Vakharia VN, Sparks R, França LGS, Granados A, McEvoy AW, et al. Optimizing trajectories for cranial laser interstitial thermal therapy using computer-assisted planning: a machine learning approach. Neurotherapeutics. 2019;16:182-91.
O'Connor KP, Palejwala AH, Milton CK, Lu VM, Glenn CA, Sughrue ME, et al. Laser interstitial thermal therapy case series: choosing the correct number of fibers depending on lesion size. Oper Neurosurg. 2020;20:18-23.
Lauro PM, Lee S, Ahn M, Barborica A, Asaad WF. DBStar: an open-source tool kit for imaging analysis with patient-customized deep brain stimulation platforms. Stereotact Funct Neurosurg. 2018;96:13-21.
Wicks RT, Jermakowicz WJ, Jagid JR, Couture DE, Willie JT, Laxton AW, et al. Laser interstitial thermal therapy for mesial temporal lobe epilepsy. Neurosurgery. 2016;79:S83-91.
Cajigas I, Kanner AM, Ribot R, Casabella AM, Mahavadi A, Jermakowicz W, et al. Magnetic resonance-guided laser interstitial thermal therapy for mesial temporal epilepsy: a case series analysis of outcomes and complications at 2-year follow-up. World Neurosurg. 2019;126:e1121-9.
Vismer MS, Forcelli PA, Skopin MD, Gale K, Koubeissi MZ. The piriform, perirhinal, and entorhinal cortex in seizure generation. Front Neural Circuits. 2015;9:27.
Piredda S, Gale K. A crucial epileptogenic site in the deep prepiriform cortex. Nature. 1985;317:623-5.
Li D, Luo D, Wang J, Wang W, Yuan Z, Xing Y, et al. Electrical stimulation of the endopiriform nucleus attenuates epilepsy in rats by network modulation. Ann Clin Transl Neurol. 2020;7:2356-69.
Janz P, Savanthrapadian S, Häussler U, Kilias A, Nestel S, Kretz O, et al. Synaptic remodeling of entorhinal input contributes to an aberrant hippocampal network in temporal lobe epilepsy. Cereb Cortex. 2016;27:2348-64.
Lu Y, Zhong C, Wang L, Wei P, He W, Huang K, et al. Optogenetic dissection of ictal propagation in the hippocampal-entorhinal cortex structures. Nat Commun. 2016;7:e10962.
Kelly ME, McIntyre DC. Perirhinal cortex involvement in limbic kindled seizures. Epilepsy Res. 1996;26:233-43.
Bernasconi N, Bernasconi A, Caramanos Z, Antel SB, Andermann F, Arnold DL. Mesial temporal damage in temporal lobe epilepsy: a volumetric MRI study of the hippocampus, amygdala and parahippocampal region. Brain. 2003;126:462-9.
Bernasconi N, Bernasconi A, Andermann F, Dubeau F, Feindel W, Reutens DC. Entorhinal cortex in temporal lobe epilepsy: a quantitative MRI study. Neurology. 1999;52:1870.
Malikova H, Liscak R, Vojtech Z, Prochazka T, Vymazal J, Vladyka V, et al. Stereotactic radiofrequency amygdalohippocampectomy: does reduction of entorhinal and perirhinal cortices influence good clinical seizure outcome? Epilepsia. 2011;52:932-40.
Jooma R, Yeh HS, Privitera MD, Rigrish D, Gartner M. Seizure control and extent of mesial temporal resection. Acta Neurochir. 1995;133:44-9.
Chan S, Erickson JK, Yoon SS. Limbic system abnormalities associated with mesial temporal sclerosis: a model of chronic cerebral changes due to seizures. Radiographics. 1997;17:1095-110.
Coan AC, Kubota B, Bergo FPG, Campos BM, Cendes F. 3T MRI quantification of hippocampal volume and signal in mesial temporal lobe epilepsy improves detection of hippocampal sclerosis. Am J Neuroradiol. 2014;35:77-83.