Visual outcomes after anterior temporal lobectomy and transsylvian selective amygdalohippocampectomy: A quantitative comparison of clinical and diffusion data.
ATL
DTI
TLE
optic radiation
tsSAHE
visual field deficit
Journal
Epilepsia
ISSN: 1528-1167
Titre abrégé: Epilepsia
Pays: United States
ID NLM: 2983306R
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
revised:
13
12
2022
received:
26
07
2022
accepted:
13
12
2022
pubmed:
19
12
2022
medline:
15
3
2023
entrez:
18
12
2022
Statut:
ppublish
Résumé
Anterior temporal lobectomy (ATL) and transsylvian selective amygdalohippocampectomy (tsSAHE) are effective treatment strategies for intractable temporal lobe epilepsy but may cause visual field deficits (VFDs) by damaging the optic radiation (OpR). Due to the OpR's considerable variability and because it is indistinguishable from surrounding tissue without further technical guidance, it is highly vulnerable to iatrogenic injury. This imaging study uses a multimodal approach to assess visual outcomes after epilepsy surgery. We studied 62 patients who underwent ATL (n = 32) or tsSAHE (n = 30). Analysis of visual outcomes was conducted in four steps, including the assessment of (1) perimetry outcome (VFD incidence/extent, n = 44/40), (2) volumetric OpR tractography damage (n = 55), and the (3) relation of volumetric OpR tractography damage and perimetry outcome (n = 35). Furthermore, (4) fixel-based analysis (FBA) was performed to assess micro- and macrostructural changes within the OpR following surgery (n = 36). Altogether, 56% of all patients had postoperative VFDs (78.9% after ATL, 36.36% after tsSAHE, p = .011). VFDs and OpR tractography damage tended to be more severe within the ATL group (ATL vs. tsSAHE, integrity of contralateral upper quadrant: 65% vs. 97%, p = .002; OpR tractography damage: 69.2 mm In the context of controversial visual outcomes following epilepsy surgery, this study provides clinical as well as neuroimaging evidence for a higher risk and greater severity of postoperative VFDs after ATL compared to tsSAHE. Volumetric OpR tractography damage is a feasible parameter to reliably predict this morbidity in both treatment groups and may ultimately support personalized planning of surgical candidates. Advanced diffusion analysis tools such as FBA offer a structural explanation of surgically induced visual pathway damage, allowing noninvasive quantification and visualization of micro- and macrostructural tract affection.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
705-717Subventions
Organisme : Medical-Scientific fund of the mayor of the federal capital Vienna
ID : 19012
Informations de copyright
© 2022 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.
Références
Jain P, Tomlinson G, Snead C, Sander B, Widjaja E. Systematic review and network meta-analysis of resective surgery for mesial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry. 2018;89:1138-44.
Dorfer C, Czech T, Rössler K. Chirurgie der Temporallappenepilepsie. Zeitschrift für Epileptologie. 2020;33:37-41.
West S, Nevitt SJ, Cotton J, Gandhi S, Weston J, Sudan A, et al. Surgery for epilepsy. Cochrane Database Syst Rev. 2019;6:CD010541.
Ebeling U, Reulen H-J. Neurosurgical topography of the optic radiation in the temporal lobe. Acta Neurochir. 1988;92:29-36.
Dreessen de Gervai P, Sboto-Frankenstein UN, Bolster RB, Thind S, Gruwel MLH, Smith SD, et al. Tractography of Meyer's loop asymmetries. Epilepsy Res. 2014;108:872-82.
Piper RJ, Yoong MM, Kandasamy J, Chin RF. Application of diffusion tensor imaging and tractography of the optic radiation in anterior temporal lobe resection for epilepsy: a systematic review. Clin Neurol Neurosurg. 2014;124:59-65.
Schmeiser B, Daniel M, Kogias E, Böhringer D, Egger K, Yang S, et al. Visual field defects following different resective procedures for mesiotemporal lobe epilepsy. Epilepsy Behav. 2017;76:39-45.
Pathak-Ray V, Ray A, Walters R, Hatfield R. Detection of visual field defects in patients after anterior temporal lobectomy for mesial temporal sclerosis-establishing eligibility to drive. Eye. 2002;16:744-8.
Beisse F, Lagrèze W, Schmitz J, Schulze-Bonhage A. Visual field defects after epilepsy surgery: implications for driving license tenure. Ophthalmologe. 2014;111:942-7.
Yogarajah M, Focke NK, Bonelli S, Cercignani M, Acheson J, Parker GJM, et al. Defining Meyer's loop-temporal lobe resections, visual field deficits and diffusion tensor tractography. Brain. 2009;132:1656-68.
Vakharia VN, Vos SB, Winston GP, Gutman MJ, Wykes V, McEvoy AW, et al. Intraoperative overlay of optic radiation tractography during anteromesial temporal resection: a prospective validation study. J Neurosurg. 2022;136:543-52.
Thudium MO, Campos AR, Urbach H, Clusmann H. The basal temporal approach for mesial temporal surgery: sparing the Meyer loop with navigated diffusion tensor tractography. Oper Neurosurg. 2010;67:ons385-90.
Winston GP, Daga P, White MJ, Micallef C, Miserocchi A, Mancini L, et al. Preventing visual field deficits from neurosurgery. Neurology. 2014;83:604-11.
Xu K, Wang X, Guan Y, Zhao M, Zhou J, Zhai F, et al. Comparisons of the seizure-free outcome and visual field deficits between anterior temporal lobectomy and selective amygdalohippocampectomy: a systematic review and meta-analysis. Seizure. 2020;81:228-35.
Tournier JD, Smith R, Raffelt D, Tabbara R, Dhollander T, Pietsch M, et al. MRtrix3: a fast, flexible and open software framework for medical image processing and visualisation. Neuroimage. 2019;202:116137.
Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC. A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage. 2011;54:2033-44.
Zentner J. Anterior temporal lobectomy (ATL). In: Surgical treatment of epilepsies. Cham: Springer; 2020;87-128.
Dorfer C, Czech T, Aull-Watschinger S, Baumgartner C, Jung R, Kasprian G, et al. Mesial temporal lobe epilepsy: long-term seizure outcome of patients primarily treated with transsylvian selective amygdalohippocampectomy. J Neurosurg. 2018;129:174-81.
Yasargil MG, Türe U, Yasargil DC. Impact of temporal lobe surgery. J Neurosurg. 2004;101:725-38.
Yaşargil MG, Teddy PJ, Roth P. Selective amygdalo-hippocampectomy. Operative anatomy and surgical technique. Adv Tech Stand Neurosurg. 1985;12:93-123.
Winston GP, Daga P, Stretton J, Modat M, Symms MR, McEvoy AW, et al. Optic radiation tractography and vision in anterior temporal lobe resection. Ann Neurol. 2012;71:334-41.
Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004;23(Suppl 1):S208-19.
Andersson JLR, Sotiropoulos SN. An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage. 2016;125:1063-78.
Dhollander T, Mito R, Raffelt D, Connelly A. Improved white matter response function estimation for 3-tissue constrained spherical deconvolution. Proc Intl Soc Mag Reson Med. 2019;555.
Jeurissen B, Tournier JD, Dhollander T, Connelly A, Sijbers J. Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data. Neuroimage. 2014;103:411-26.
Smith RE, Tournier JD, Calamante F, Connelly A. Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage. 2012;62:1924-38.
Tournier J-D, Calamante F, Connelly A. Improved probabilistic streamlines tractography by 2 nd order integration over fibre orientation distributions. In Proceedings of the International Society for Magnetic Resonance in Medicine. Hoboken, NJ: John Wiley & Sons, Inc; 2010. p. 1670.
Fischl B. FreeSurfer. Neuroimage. 2012;62:774-81.
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.
Babb TL, Wilson CL, Crandall PH. Asymmetry and ventral course of the human geniculostriate pathway as determined by hippocampal visual evoked potentials and subsequent visual field defects after temporal lobectomy. Exp Brain Res. 1982;47:317-28.
Dhollander T, Clemente A, Singh M, Boonstra F, Civier O, Duque JD, et al. Fixel-based analysis of diffusion MRI: methods, applications, challenges and opportunities. Neuroimage. 2021;241:118417.
Veraart J, Fieremans E, Novikov DS. Diffusion MRI noise mapping using random matrix theory. Magn Reson Med. 2016;76:1582-93.
Tustison NJ, Avants BB, Cook PA, Zheng Y, Egan A, Yushkevich PA, et al. N4ITK: improved N3 bias correction. IEEE Trans Med Imaging. 2010;29:1310-20.
Tournier JD, Calamante F, Connelly A. Determination of the appropriate b value and number of gradient directions for high-angular-resolution diffusion-weighted imaging. NMR Biomed. 2013;26:1775-86.
Smith RE, Tournier JD, Calamante F, Connelly A. SIFT: Spherical-deconvolution informed filtering of tractograms. Neuroimage. 2013;67:298-312.
Raffelt D, Tournier JD, Rose S, Ridgway GR, Henderson R, Crozier S, et al. Apparent fibre density: a novel measure for the analysis of diffusion-weighted magnetic resonance images. Neuroimage. 2012;59:3976-94.
Raffelt DA, Smith RE, Ridgway GR, Tournier JD, Vaughan DN, Rose S, et al. Connectivity-based fixel enhancement: whole-brain statistical analysis of diffusion MRI measures in the presence of crossing fibres. Neuroimage. 2015;117:40-55.
Smith RD, Vaughan D, Parker D, Dhollander T, Jackson G, Connelly A. Intrinsic non-stationarity correction for fixel-based analysis. In Proc OHBM 2019 M7892019.
Winston GP. Epilepsy surgery, vision, and driving: what has surgery taught us and could modern imaging reduce the risk of visual deficits? Epilepsia. 2013;54:1877-88.
Jeelani NU, Jindahra P, Tamber MS, Poon TL, Kabasele P, James-Galton M, et al. 'Hemispherical asymmetry in the Meyer's Loop': a prospective study of visual-field deficits in 105 cases undergoing anterior temporal lobe resection for epilepsy. J Neurol Neurosurg Psychiatry. 2010;81:985-91.
Springer JA, Binder JR, Hammeke TA, Swanson SJ, Frost JA, Bellgowan PSF, et al. Language dominance in neurologically normal and epilepsy subjects: a functional MRI study. Brain. 1999;122(Pt 11):2033-46.
Vakharia VN, Diehl B, Tisdall M. Visual field defects in temporal lobe epilepsy surgery. Curr Opin Neurol. 2021;34:188-96.
Choi C, Rubino PA, Fernandez-Miranda JC, Abe H, Rhoton AL Jr. Meyer's loop and the optic radiations in the transsylvian approach to the mediobasal temporal lobe. Neurosurgery. 2006;59:ONS228-35. discussion ONS235-226.
de Souza J, Pimentel-Silva LR, Ayub G, Nogueira MH, Zanao T, Yasuda CL, et al. Transsylvian amygdalohippocampectomy for mesial temporal lobe epilepsy: comparison of three different approaches. Epilepsia. 2021;62:439-49.
Manji H, Plant GT. Epilepsy surgery, visual fields, and driving: a study of the visual field criteria for driving in patients after temporal lobe epilepsy surgery with a comparison of Goldmann and Esterman perimetry. J Neurol Neurosurg Psychiatry. 2000;68:80-2.
Yeni SN, Tanriover N, Uyanik O, Ulu MO, Özkara Ç, Karaağaç N, et al. Visual field defects in selective amygdalohippocampectomy for hippocampal sclerosis: the fate of Meyer's loop during the transsylvian approach to the temporal horn. Neurosurgery. 2008;63:507-13. discussion 513-5.
de Souza JPSAS, Ayub G, Nogueira M, Zanao T, Lopes TM, Pimentel-Silva LR, et al. Temporopolar amygdalohippocampectomy: seizure control and postoperative outcomes. J Neurosurg. 2021;134:1044-53.
Delev D, Wabbels B, Schramm J, Nelles M, Elger CE, von Lehe M, et al. Vision after trans-sylvian or temporobasal selective amygdalohippocampectomy: a prospective randomised trial. Acta Neurochir. 2016;158:1757-65.
Chamberland M, Tax CMW, Jones DK. Meyer's loop tractography for image-guided surgery depends on imaging protocol and hardware. Neuroimage Clin. 2018;20:458-65.
Wilkins B, Lee N, Gajawelli N, Law M, Leporé N. Fiber estimation and tractography in diffusion MRI: development of simulated brain images and comparison of multi-fiber analysis methods at clinical b-values. Neuroimage. 2015;109:341-56.
James JS, Radhakrishnan A, Thomas B, Madhusoodanan M, Kesavadas C, Abraham M, et al. Diffusion tensor imaging tractography of Meyer's loop in planning resective surgery for drug-resistant temporal lobe epilepsy. Epilepsy Res. 2015;110:95-104.
Chen X, Weigel D, Ganslandt O, Buchfelder M, Nimsky C. Prediction of visual field deficits by diffusion tensor imaging in temporal lobe epilepsy surgery. Neuroimage. 2009;45:286-97.