nach oben

Erschienen in:

12.08.2020 | Original Article

Distinct patterns of hippocampal subfield volume loss in left and right mesial temporal lobe epilepsy

verfasst von: Hossein Sanjari Moghaddam, Mohammad Hadi Aarabi, Jafar Mehvari-Habibabadi, Roya Sharifpour, Bahram Mohajer, Neda Mohammadi-Mobarakeh, Seyed Sohrab Hashemi-Fesharaki, Kost Elisevich, Mohammad-Reza Nazem-Zadeh

Erschienen in: Neurological Sciences | Ausgabe 4/2021

Einloggen, um Zugang zu erhalten

Abstract

Objective

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.

Methods

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.

Results

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.

Conclusion

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.

Boling WW (2018) Surgical considerations of intractable mesial temporal lobe epilepsy. Brain Sci 8(2):35. https://doi.org/10.3390/brainsci8020035CrossRefPubMedCentral

Thom M (2014) Review: hippocampal sclerosis in epilepsy: a neuropathology review. Neuropathol Appl Neurobiol 40(5):520–543. https://doi.org/10.1111/nan.12150CrossRefPubMedPubMedCentral

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.xCrossRefPubMedPubMedCentral

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):1046–1052PubMed

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.xCrossRefPubMed

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/awx341CrossRefPubMedPubMedCentral

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.2007.11.015CrossRefPubMed

Yassa MA, Stark CE (2011) Pattern separation in the hippocampus. Trends Neurosci 34(10):515–525. https://doi.org/10.1016/j.tins.2011.06.006CrossRefPubMedPubMedCentral

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/s00401-001-0475-7CrossRefPubMed

10.

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.2003.09.009CrossRefPubMed

11.

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.21226CrossRefPubMed

12.

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.2017.08.013CrossRefPubMed

13.

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/10.3791/51861CrossRef

14.

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.12926CrossRefPubMedPubMedCentral

15.

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.2015.09.004CrossRefPubMed

16.

Manjon JV, Coupe P (2016) volBrain: an online MRI brain volumetry system. Front Neuroinform 10:30. https://doi.org/10.3389/fninf.2016.00030CrossRefPubMedPubMedCentral

17.

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):1979–1991CrossRef

18.

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.xCrossRefPubMed

19.

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):107–118CrossRef

20.

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/10.1118/1.4938411CrossRefPubMedPubMedCentral

21.

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):152–161CrossRef

22.

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 58:1–20CrossRef

23.

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.2010.09.025CrossRefPubMed

24.

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.2010.2046908CrossRefPubMedPubMedCentral

25.

Nyul LG, Udupa JK (1999) On standardizing the MR image intensity scale. Magn Reson Med 42(6):1072–1081CrossRef

26.

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

27.

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

28.

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.2013.02.003CrossRefPubMed

29.

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.2015.01.004CrossRefPubMedPubMedCentral

30.

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.2013.06.030CrossRefPubMed

31.

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.2014.07.003CrossRefPubMed

32.

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

33.

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.0046791CrossRefPubMedPubMedCentral

34.

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

35.

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.0b013e3181b783ddCrossRefPubMed

36.

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.23046CrossRefPubMed

37.

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

38.

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.1110266108CrossRefPubMedPubMedCentral

39.

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

40.

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.0000000000000873CrossRefPubMed

41.

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.0000000000001008CrossRefPubMed

42.

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/10.1177/0284185114531128CrossRef

43.

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):598–622CrossRef

Titel: Distinct patterns of hippocampal subfield volume loss in left and right mesial temporal lobe epilepsy
verfasst von: Hossein Sanjari Moghaddam
Mohammad Hadi Aarabi
Jafar Mehvari-Habibabadi
Roya Sharifpour
Bahram Mohajer
Neda Mohammadi-Mobarakeh
Seyed Sohrab Hashemi-Fesharaki
Kost Elisevich
Mohammad-Reza Nazem-Zadeh
Publikationsdatum: 12.08.2020
Verlag: Springer International Publishing
Erschienen in: Neurological Sciences / Ausgabe 4/2021
Print ISSN: 1590-1874
Elektronische ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-020-04653-6

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

Schützt Olivenöl vor dem Tod durch Demenz?

10.05.2024 Morbus Alzheimer Nachrichten

Konsumieren Menschen täglich 7 Gramm Olivenöl, ist ihr Risiko, an einer Demenz zu sterben, um mehr als ein Vierten reduziert – und dies weitgehend unabhängig von ihrer sonstigen Ernährung. Dafür sprechen Auswertungen zweier großer US-Studien.

Bluttest erkennt Parkinson schon zehn Jahre vor der Diagnose

10.05.2024 Parkinson-Krankheit Nachrichten

Ein Bluttest kann abnorm aggregiertes Alpha-Synuclein bei einigen Menschen schon zehn Jahre vor Beginn der motorischen Parkinsonsymptome nachweisen. Mit einem solchen Test lassen sich möglicherweise Prodromalstadien erfassen und die Betroffenen früher behandeln.

Darf man die Behandlung eines Neonazis ablehnen?

08.05.2024 Gesellschaft Nachrichten

In einer Leseranfrage in der Zeitschrift Journal of the American Academy of Dermatology möchte ein anonymer Dermatologe bzw. eine anonyme Dermatologin wissen, ob er oder sie einen Patienten behandeln muss, der eine rassistische Tätowierung trägt.

Wartezeit nicht kürzer, aber Arbeit flexibler

Psychotherapie Medizin aktuell

Fünf Jahren nach der Neugestaltung der Psychotherapie-Richtlinie wurden jetzt die Effekte der vorgenommenen Änderungen ausgewertet. Das Hauptziel der Novellierung war eine kürzere Wartezeit auf Therapieplätze. Dieses Ziel wurde nicht erreicht, es gab jedoch positive Auswirkungen auf andere Bereiche.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Klimawandel und Gesundheit: Was Sie in der Hausarztpraxis wissen müssen und tun können

Springer Medizin

Abstract

Objective

Methods

Results

Conclusion

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 4/2021

Decreased LF/HF ratio is associated with worse outcomes in patients who received mechanical thrombectomy under general anesthesia for emergent large vessel occlusion: a retrospective study

Perampanel as first add-on choice on the treatment of mesial temporal lobe epilepsy: an observational real-life study

Tetraparesis and sensorimotor axonal polyneuropathy due to co-occurrence of Pompe disease and hereditary ATTR amyloidosis

Scientific productivity in neurology: impact of the socio-economic status

Spontaneous resolution of ruptured dissecting superior cerebellar artery aneurysm