Distinct patterns of hippocampal subfield volume loss in left and right mesial temporal lobe epilepsy.
Epilepsy
Hippocampus
Magnetic resonance imaging
Temporal lobe
Journal
Neurological sciences : official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology
ISSN: 1590-3478
Titre abrégé: Neurol Sci
Pays: Italy
ID NLM: 100959175
Informations de publication
Date de publication:
Apr 2021
Apr 2021
Historique:
received:
08
04
2020
accepted:
06
08
2020
pubmed:
13
8
2020
medline:
15
5
2021
entrez:
13
8
2020
Statut:
ppublish
Résumé
To investigate the pattern and severity of hippocampal subfield volume loss in patients with left and right mesial temporal lobe epilepsy (mTLE) using quantitative MRI volumetric analysis. A total of 21 left and 14 right mTLE subjects, as well as 15 healthy controls, were enrolled in this cross-sectional study. A publically available magnetic resonance imaging (MRI) brain volumetry system (volBrain) was used for volumetric analysis of hippocampal subfields. The T1-weighted images were processed with a HIPS pipeline. A distinct pattern of hippocampal subfield atrophy was found between left and right mTLE patients when compared with controls. Patients with left mTLE exhibited ipsilateral hippocampal atrophy and segmental volume depletion of the Cornu Ammonis (CA) 2/CA3, CA4/dentate gyrus (DG), and strata radiatum-lacunosum-moleculare (SR-SL-SM). Those with right mTLE exhibited similar ipsilateral hippocampal atrophy but with additional segmental CA1 volume depletion. More extensive bilateral subfield volume loss was apparent with right mTLE patients. We demonstrate that left and right mTLE patients show a dissimilar pattern of hippocampal subfield atrophy, suggesting the pathophysiology of epileptogenesis in left and right mTLE to be different.
Identifiants
pubmed: 32783160
doi: 10.1007/s10072-020-04653-6
pii: 10.1007/s10072-020-04653-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1411-1421Références
Boling WW (2018) Surgical considerations of intractable mesial temporal lobe epilepsy. Brain Sci 8(2):35. https://doi.org/10.3390/brainsci8020035
doi: 10.3390/brainsci8020035
pmcid: 5836054
Thom M (2014) Review: hippocampal sclerosis in epilepsy: a neuropathology review. Neuropathol Appl Neurobiol 40(5):520–543. https://doi.org/10.1111/nan.12150
doi: 10.1111/nan.12150
pubmed: 24762203
pmcid: 4265206
Kemmotsu N, Girard HM, Bernhardt BC, Bonilha L, Lin JJ, Tecoma ES, Iragui VJ, Hagler DJ Jr, Halgren E, McDonald CR (2011) MRI analysis in temporal lobe epilepsy: cortical thinning and white matter disruptions are related to side of seizure onset. Epilepsia 52(12):2257–2266. https://doi.org/10.1111/j.1528-1167.2011.03278.x
doi: 10.1111/j.1528-1167.2011.03278.x
pubmed: 21972957
pmcid: 3230670
Garcia-Finana M, Denby CE, Keller SS, Wieshmann UC, Roberts N (2006) Degree of hippocampal atrophy is related to side of seizure onset in temporal lobe epilepsy. AJNR Am J Neuroradiol 27(5):1046–1052
pubmed: 16687541
Pail M, Brazdil M, Marecek R, Mikl M (2010) An optimized voxel-based morphometric study of gray matter changes in patients with left-sided and right-sided mesial temporal lobe epilepsy and hippocampal sclerosis (MTLE/HS). Epilepsia 51(4):511–518. https://doi.org/10.1111/j.1528-1167.2009.02324.x
doi: 10.1111/j.1528-1167.2009.02324.x
pubmed: 19817822
Whelan CD, Altmann A, Botía JA, Jahanshad N, Hibar DP, Absil J, Alhusaini S, Alvim MKM, Auvinen P, Bartolini E, Bergo FPG, Bernardes T, Blackmon K, Braga B, Caligiuri ME, Calvo A, Carr SJ, Chen J, Chen S, Cherubini A, David P, Domin M, Foley S, França W, Haaker G, Isaev D, Keller SS, Kotikalapudi R, Kowalczyk MA, Kuzniecky R, Langner S, Lenge M, Leyden KM, Liu M, Loi RQ, Martin P, Mascalchi M, Morita ME, Pariente JC, Rodríguez-Cruces R, Rummel C, Saavalainen T, Semmelroch MK, Severino M, Thomas RH, Tondelli M, Tortora D, Vaudano AE, Vivash L, von Podewils F, Wagner J, Weber B, Yao Y, Yasuda CL, Zhang G, Bargalló N, Bender B, Bernasconi N, Bernasconi A, Bernhardt BC, Blümcke I, Carlson C, Cavalleri GL, Cendes F, Concha L, Delanty N, Depondt C, Devinsky O, Doherty CP, Focke NK, Gambardella A, Guerrini R, Hamandi K, Jackson GD, Kälviäinen R, Kochunov P, Kwan P, Labate A, McDonald CR, Meletti S, O’Brien TJ, Ourselin S, Richardson MP, Striano P, Thesen T, Wiest R, Zhang J, Vezzani A, Ryten M, Thompson PM, Sisodiya SM (2018) Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain 141(2):391–408. https://doi.org/10.1093/brain/awx341
doi: 10.1093/brain/awx341
pubmed: 29365066
pmcid: 5837616
Hunsaker MR, Lee B, Kesner RP (2008) Evaluating the temporal context of episodic memory: the role of CA3 and CA1. Behav Brain Res 188(2):310–315. https://doi.org/10.1016/j.bbr.2007.11.015
doi: 10.1016/j.bbr.2007.11.015
pubmed: 18178264
Yassa MA, Stark CE (2011) Pattern separation in the hippocampus. Trends Neurosci 34(10):515–525. https://doi.org/10.1016/j.tins.2011.06.006
doi: 10.1016/j.tins.2011.06.006
pubmed: 21788086
pmcid: 3183227
Rossler M, Zarski R, Bohl J, Ohm TG (2002) Stage-dependent and sector-specific neuronal loss in hippocampus during Alzheimer’s disease. Acta Neuropathol 103(4):363–369. https://doi.org/10.1007/s00401-001-0475-7
doi: 10.1007/s00401-001-0475-7
pubmed: 11904756
Schonheit B, Zarski R, Ohm TG (2004) Spatial and temporal relationships between plaques and tangles in Alzheimer-pathology. Neurobiol Aging 25(6):697–711. https://doi.org/10.1016/j.neurobiolaging.2003.09.009
doi: 10.1016/j.neurobiolaging.2003.09.009
pubmed: 15165691
Mueller SG, Laxer KD, Scanlon C, Garcia P, McMullen WJ, Loring DW, Meador KJ, Weiner MW (2012) Different structural correlates for verbal memory impairment in temporal lobe epilepsy with and without mesial temporal lobe sclerosis. Hum Brain Mapp 33(2):489–499. https://doi.org/10.1002/hbm.21226
doi: 10.1002/hbm.21226
pubmed: 21438080
Comper SM, Jardim AP, Corso JT, Gaca LB, Noffs MHS, Lancellotti CLP, Cavalheiro EA, Centeno RS, Yacubian EMT (2017) Impact of hippocampal subfield histopathology in episodic memory impairment in mesial temporal lobe epilepsy and hippocampal sclerosis. Epilepsy Behav 75:183–189. https://doi.org/10.1016/j.yebeh.2017.08.013
doi: 10.1016/j.yebeh.2017.08.013
pubmed: 28873362
Winterburn J, Pruessner JC, Sofia C, Schira MM, Lobaugh NJ, Voineskos AN, Chakravarty MM (2015) High-resolution in vivo manual segmentation protocol for human hippocampal subfields using 3T magnetic resonance imaging. J Vis Exp 105:e51861. https://doi.org/10.3791/51861
doi: 10.3791/51861
Kreilkamp BAK, Weber B, Elkommos SB, Richardson MP, Keller SS (2018) Hippocampal subfield segmentation in temporal lobe epilepsy: relation to outcomes. Acta Neurol Scand 137(6):598–608. https://doi.org/10.1111/ane.12926
doi: 10.1111/ane.12926
pubmed: 29572865
pmcid: 5969077
Kim JB, Suh SI, Kim JH (2015) Volumetric and shape analysis of hippocampal subfields in unilateral mesial temporal lobe epilepsy with hippocampal atrophy. Epilepsy Res 117:74–81. https://doi.org/10.1016/j.eplepsyres.2015.09.004
doi: 10.1016/j.eplepsyres.2015.09.004
pubmed: 26425829
Manjon JV, Coupe P (2016) volBrain: an online MRI brain volumetry system. Front Neuroinform 10:30. https://doi.org/10.3389/fninf.2016.00030
doi: 10.3389/fninf.2016.00030
pubmed: 27512372
pmcid: 4961698
Næss-Schmidt E, Tietze A, Blicher JU, Petersen M, Mikkelsen IK, Coupé P, Manjón JV, Eskildsen SF (2016) Automatic thalamus and hippocampus segmentation from MP2RAGE: comparison of publicly available methods and implications for DTI quantification. Int J Comput Assist Radiol Surg 11(11):1979–1991
doi: 10.1007/s11548-016-1433-0
Kwan P, Arzimanoglou A, Berg AT, Brodie MJ, Allen Hauser W, Mathern G, Moshe SL, Perucca E, Wiebe S, French J (2010) Definition of drug resistant epilepsy: consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies. Epilepsia 51(6):1069–1077. https://doi.org/10.1111/j.1528-1167.2009.02397.x
doi: 10.1111/j.1528-1167.2009.02397.x
pubmed: 19889013
Nazem-Zadeh M-R, Elisevich KV, Schwalb JM, Bagher-Ebadian H, Mahmoudi F, Soltanian-Zadeh H (2014) Lateralization of temporal lobe epilepsy by multimodal multinomial hippocampal response-driven models. J Neurol Sci 347(1):107–118
doi: 10.1016/j.jns.2014.09.029
Hosseini M-P, Nazem-Zadeh M-R, Pompili D, Jafari-Khouzani K, Elisevich K, Soltanian-Zadeh H (2016) Comparative performance evaluation of automated segmentation methods of hippocampus from magnetic resonance images of temporal lobe epilepsy patients. Med Phys 43(1):538–538. https://doi.org/10.1118/1.4938411
doi: 10.1118/1.4938411
pubmed: 26745947
pmcid: 4706546
Nazem-Zadeh M-R, Schwalb JM, Elisevich KV, Bagher-Ebadian H, Hamidian H, Akhondi-Asl A-R, Jafari-Khouzani K, Soltanian-Zadeh H (2014) Lateralization of temporal lobe epilepsy using a novel uncertainty analysis of MR diffusion in hippocampus, cingulum, and fornix, and hippocampal volume and FLAIR intensity. J Neurol Sci 342(1):152–161
doi: 10.1016/j.jns.2014.05.019
Nazem-Zadeh MR, Chapman CH, Lawrence TS, Tsien CI, Cao Y (2013) Uncertainty in assessment of radiation-induced diffusion index changes in individual patients. Phys Med Biol 58:1–20
doi: 10.1088/0031-9155/58/12/4277
Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2011) A reproducible evaluation of ANTs similarity metric performance in brain image registration. NeuroImage 54(3):2033–2044. https://doi.org/10.1016/j.neuroimage.2010.09.025
doi: 10.1016/j.neuroimage.2010.09.025
pubmed: 20851191
Tustison NJ, Avants BB, Cook PA, Zheng Y, Egan A, Yushkevich PA, Gee JC (2010) N4ITK: improved N3 bias correction. IEEE Trans Med Imaging 29(6):1310–1320. https://doi.org/10.1109/tmi.2010.2046908
doi: 10.1109/tmi.2010.2046908
pubmed: 20378467
pmcid: 3071855
Nyul LG, Udupa JK (1999) On standardizing the MR image intensity scale. Magn Reson Med 42(6):1072–1081
doi: 10.1002/(SICI)1522-2594(199912)42:6<1072::AID-MRM11>3.0.CO;2-M
Romero JE, Coupe P, Manjón JV High resolution hippocampus subfield segmentation using multispectral multiatlas patch-based label fusion. In: Wu G, Coupé P, Zhan Y, Munsell BC, Rueckert D (eds) Patch-based techniques in medical imaging, Cham, 2016// 2016. Springer International Publishing, pp 117–124
Romero JE, Coupé P, Manjón JV (2017) HIPS: a new hippocampus subfield segmentation method. NeuroImage 163:286–295. https://doi.org/10.1016/j.neuroimage.2017.09.049
Winterburn JL, Pruessner JC, Chavez S, Schira MM, Lobaugh NJ, Voineskos AN, Chakravarty MM (2013) A novel in vivo atlas of human hippocampal subfields using high-resolution 3 T magnetic resonance imaging. NeuroImage 74:254–265. https://doi.org/10.1016/j.neuroimage.2013.02.003
doi: 10.1016/j.neuroimage.2013.02.003
pubmed: 23415948
Yushkevich PA, Amaral RS, Augustinack JC, Bender AR, Bernstein JD, Boccardi M, Bocchetta M, Burggren AC, Carr VA, Chakravarty MM, Chetelat G, Daugherty AM, Davachi L, Ding SL, Ekstrom A, Geerlings MI, Hassan A, Huang Y, Iglesias JE, La Joie R, Kerchner GA, LaRocque KF, Libby LA, Malykhin N, Mueller SG, Olsen RK, Palombo DJ, Parekh MB, Pluta JB, Preston AR, Pruessner JC, Ranganath C, Raz N, Schlichting ML, Schoemaker D, Singh S, Stark CE, Suthana N, Tompary A, Turowski MM, Van Leemput K, Wagner AD, Wang L, Winterburn JL, Wisse LE, Yassa MA, Zeineh MM (2015) Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: towards a harmonized segmentation protocol. NeuroImage 111:526–541. https://doi.org/10.1016/j.neuroimage.2015.01.004
doi: 10.1016/j.neuroimage.2015.01.004
pubmed: 25596463
pmcid: 4387011
Coupe P, Manjon JV, Chamberland M, Descoteaux M, Hiba B (2013) Collaborative patch-based superresolution for diffusion-weighted images. NeuroImage 83:245–261. https://doi.org/10.1016/j.neuroimage.2013.06.030
doi: 10.1016/j.neuroimage.2013.06.030
pubmed: 23791914
Steve TA, Jirsch JD, Gross DW (2014) Quantification of subfield pathology in hippocampal sclerosis: a systematic review and meta-analysis. Epilepsy Res 108(8):1279–1285. https://doi.org/10.1016/j.eplepsyres.2014.07.003
doi: 10.1016/j.eplepsyres.2014.07.003
pubmed: 25107686
Ahmadi ME, Hagler DJ Jr, McDonald CR, Tecoma ES, Iragui VJ, Dale AM, Halgren E (2009) Side matters: diffusion tensor imaging tractography in left and right temporal lobe epilepsy. AJNR Am J Neuroradiol 30(9):1740–1747. https://doi.org/10.3174/ajnr.A1650
Keller SS, Schoene-Bake JC, Gerdes JS, Weber B, Deppe M (2012) Concomitant fractional anisotropy and volumetric abnormalities in temporal lobe epilepsy: cross-sectional evidence for progressive neurologic injury. PLoS One 7(10):e46791. https://doi.org/10.1371/journal.pone.0046791
doi: 10.1371/journal.pone.0046791
pubmed: 23071638
pmcid: 3469561
Sanjari Moghaddam H, Rahmani F, Aarabi MH, Nazem-Zadeh MR, Davoodi-Bojd E, Soltanian-Zadeh H (2019) White matter microstructural differences between right and left mesial temporal lobe epilepsy. Acta Neurol Belg. https://doi.org/10.1007/s13760-019-01074-x
Coan AC, Appenzeller S, Bonilha L, Li LM, Cendes F (2009) Seizure frequency and lateralization affect progression of atrophy in temporal lobe epilepsy. Neurology 73(11):834–842. https://doi.org/10.1212/WNL.0b013e3181b783dd
doi: 10.1212/WNL.0b013e3181b783dd
pubmed: 19752449
Liu M, Bernhardt BC, Bernasconi A, Bernasconi N (2016) Gray matter structural compromise is equally distributed in left and right temporal lobe epilepsy. Hum Brain Mapp 37(2):515–524. https://doi.org/10.1002/hbm.23046
doi: 10.1002/hbm.23046
pubmed: 26526187
Ji J, Maren S Differential roles for hippocampal areas CA1 and CA3 in the contextual encoding and retrieval of extinguished fear. Learn Mem 15(4):244–251. https://doi.org/10.1101/lm.794808
Bartsch T, Döhring J, Rohr A, Jansen O, Deuschl G (2011) CA1 neurons in the human hippocampus are critical for autobiographical memory, mental time travel, and autonoetic consciousness. Proc Natl Acad Sci U S A 108(42):17562–17567. https://doi.org/10.1073/pnas.1110266108
doi: 10.1073/pnas.1110266108
pubmed: 21987814
pmcid: 3198338
Barrientos SA, Tiznado V (2016) Hippocampal CA1 subregion as a context decoder. 36 (25):6602-6604. https://doi.org/10.1523/JNEUROSCI.1107-16.2016 The Journal of Neuroscience
Abdel Razek AAK, Talaat M, El-Serougy L, Gaballa G, Abdelsalam M (2019) Clinical applications of arterial spin labeling in brain tumors. J Comput Assist Tomogr 43(4):525–532. https://doi.org/10.1097/rct.0000000000000873
doi: 10.1097/rct.0000000000000873
pubmed: 31162240
Razek A, Taman SE, El Regal ME, Megahed A, Elzeny S, El Tantawi N (2020) Diffusion tensor imaging of microstructural changes in the gray and white matter in patients with Crigler-Najjar syndrome type I. J Comput Assist Tomogr 44(3):393–398. https://doi.org/10.1097/rct.0000000000001008
doi: 10.1097/rct.0000000000001008
pubmed: 32217895
Oner AY, Eryurt B, Ucar M, Capraz I, Kurt G, Bilir E, Tali T (2015) pASL versus DSC perfusion MRI in lateralizing temporal lobe epilepsy. Acta Radiologica (Stockholm, Sweden : 1987) 56(4):477–481. https://doi.org/10.1177/0284185114531128
doi: 10.1177/0284185114531128
Nazem-Zadeh MR, Bowyer SM, Moran JE, Davoodi-Bojd E, Zillgitt A, Weiland BJ, Bagher-Ebadian H, Mahmoudi F, Elisevich KV, Soltanian-Zadeh H (2016) MEG coherence and DTI connectivity in mTLE. Brain Topogr 29(4):598–622
doi: 10.1007/s10548-016-0488-0