Interictal blood-brain barrier dysfunction in piriform cortex of people with epilepsy.
Journal
Annals of clinical and translational neurology
ISSN: 2328-9503
Titre abrégé: Ann Clin Transl Neurol
Pays: United States
ID NLM: 101623278
Informations de publication
Date de publication:
27 Aug 2024
27 Aug 2024
Historique:
revised:
24
07
2024
received:
11
02
2024
accepted:
30
07
2024
medline:
27
8
2024
pubmed:
27
8
2024
entrez:
27
8
2024
Statut:
aheadofprint
Résumé
The piriform cortex is considered to be highly epileptogenic. Its resection during epilepsy surgery is a predictor for postoperative seizure freedom in temporal lobe epilepsy. Epilepsy is associated with a dysfunction of the blood-brain barrier. We investigated blood-brain barrier dysfunction in the piriform cortex of people with temporal lobe epilepsy using quantitative T1-relaxometry. Gadolinium-based contrast agent was administered ictally and interictally in 37 individuals before undergoing quantitative T1-relaxometry. Postictal and interictal images were co-registered, and subtraction maps were created as biomarkers for peri-ictal (∆qT1 In temporal lobe epilepsy (n = 14), ∆qT1 Interictal blood-brain barrier dysfunction occurs in the piriform cortex in temporal lobe epilepsy. This dysfunction is linked to longer disease duration and worse cognitive deficits, emphasizing the central role of the piriform cortex in the epileptogenic network of temporal lobe epilepsy.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : University of Bonn
Informations de copyright
© 2024 The Author(s). Annals of Clinical and Translational Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.
Références
Choi H, Sell RL, Lenert L, et al. Epilepsy surgery for pharmacoresistant temporal lobe epilepsy: a decision analysis. JAMA. 2008;300(21):2497‐2505.
Bar‐Klein G, Lublinsky S, Kamintsky L, et al. Imaging blood‐brain barrier dysfunction as a biomarker for epileptogenesis. Brain J Neurol. 2017;140(6):1692‐1705.
Galovic M, Baudracco I, Wright‐Goff E, et al. Association of Piriform Cortex Resection with surgical outcomes in patients with temporal lobe epilepsy. JAMA Neurol. 2019;76(6):690‐700.
Piredda S, Gale K. A crucial epileptogenic site in the deep prepiriform cortex. Nature. 1985;317(6038):623‐625.
Vaughan DN, Jackson GD. The piriform cortex and human focal epilepsy. Front Neurol. 2014;5:259. doi:10.3389/fneur.2014.00259
Borger V, Schneider M, Taube J, et al. Resection of piriform cortex predicts seizure freedom in temporal lobe epilepsy. Ann Clin Transl Neurol. 2021;8(1):177‐189.
Bar‐Klein G, Cacheaux LP, Kamintsky L, et al. Losartan prevents acquired epilepsy via TGF‐β signaling suppression. Ann Neurol. 2014;75(6):864‐875.
Hanael E, Veksler R, Friedman A, et al. Blood‐brain barrier dysfunction in canine epileptic seizures detected by dynamic contrast‐enhanced magnetic resonance imaging. Epilepsia. 2019;60(5):1005‐1016.
Löscher W, Ebert U. The role of the piriform cortex in kindling. Prog Neurobiol. 1996;50(5–6):427‐481.
Cheng H‐LM, Stikov N, Ghugre NR, Wright GA. Practical medical applications of quantitative MR relaxometry. J Magn Reson Imaging. 2012;36(4):805‐824.
Hattingen E, Jurcoane A, Nelles M, et al. Quantitative MR imaging of brain tissue and brain pathologies. Clin Neuroradiol. 2015;25(2):219‐224.
Friedman A, Kaufer D, Heinemann U. Blood‐brain barrier breakdown‐inducing astrocytic transformation: novel targets for the prevention of epilepsy. Epilepsy Res. 2009;85(2–3):142‐149.
Rüber T, David B, Lüchters G, et al. Evidence for peri‐ictal blood–brain barrier dysfunction in patients with epilepsy. Brain. 2018;141(10):2952‐2965.
Reiter JT, Schulte F, Bauer T, et al. Evidence for interictal blood–brain barrier dysfunction in people with epilepsy. Epilepsia. 2024;65:1462‐1474. doi:10.1111/epi.17929
Helmstaedter C, Pohl C, Hufnagel A, Elger CE. Visual learning deficits in nonresected patients with right temporal lobe epilepsy. Cortex J Devoted Study Nerv Syst Behav. 1991;27(4):547‐555.
Helmstaedter C, Durwen HF. VLMT: Verbaler Lern‐ und Merkfähigkeitstest: Ein praktikables und differenziertes Instrumentarium zur Prüfung der verbalen Gedächtnisleistungen. [VLMT: A useful tool to assess and differentiate verbal memory performance.]. Schweiz Arch Für Neurol Neurochir Psychiatr. 1990;141:21‐30.
Helmstaedter C, Hansen N, Leelaarporn P, et al. Specific B‐ and T‐cell populations are associated with cognition in patients with epilepsy and antibody positive and negative suspected limbic encephalitis. J Neurol. 2021;268(2):455‐466.
Smith SM, Jenkinson M, Woolrich MW, et al. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage. 2004;23(Suppl 1):S208‐S219.
Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17(2):825‐841.
Lavini C, Verhoeff JJC. Reproducibility of the gadolinium concentration measurements and of the fitting parameters of the vascular input function in the superior sagittal sinus in a patient population. Magn Reson Imaging. 2010;28(10):1420‐1430.
Fischl B. FreeSurfer. NeuroImage. 2012;62(2):774‐781.
Gonçalves Pereira PM, Insausti R, Artacho‐Pérula E, Salmenperä T, et al. MR volumetric analysis of the piriform cortex and cortical amygdala in drug‐refractory temporal lobe epilepsy. AJNR Am J Neuroradiol. 2005;26(2):319‐332.
Leon‐Rojas JE, Iqbal S, Vos SB, Rodionov R, et al. Resection of the piriform cortex for temporal lobe epilepsy: a novel approach on imaging segmentation and surgical application. Br J Neurosurg. 2021;0:1‐6.
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.
Young JC, Vaughan DN, Paolini AG, Jackson GD. Electrical stimulation of the piriform cortex for the treatment of epilepsy: A review of the supporting evidence. Epilepsy Behav. 2018;88:152‐161.
Kim MJ, Hwang BY, Mampre D, et al. Apparent diffusion coefficient of piriform cortex and seizure outcome in mesial temporal lobe epilepsy after MR‐guided laser interstitial thermal therapy: a single‐institution experience. J Neurosurg. 2022;137(6):1601‐1609.
Rigau V, Morin M, Rousset M‐C, et al. Angiogenesis is associated with blood‐brain barrier permeability in temporal lobe epilepsy. Brain J Neurol. 2007;130(Pt 7):1942‐1956.
Marchi N, Angelov L, Masaryk T, et al. Seizure‐promoting effect of blood‐brain barrier disruption. Epilepsia. 2007;48(4):732‐742.
Tomkins O, Shelef I, Kaizerman I, et al. Blood–brain barrier disruption in post‐traumatic epilepsy. J Neurol Neurosurg Psychiatry. 2008;79(7):774‐777.
van Vliet EA, Otte WM, Wadman WJ, et al. Blood‐brain barrier leakage after status epilepticus in rapamycin‐treated rats I: magnetic resonance imaging. Epilepsia. 2016;57(1):59‐69.
Roh H, Kim W, Kim J, Kim JH, Kim JH. Duration‐dependent extensive volume and shape changes of mesolimbic structures in surgically treated unilateral patients with temporal lobe epilepsy. Epilepsy Behav. 2021;114(Pt A):107517.
Sulimai N, Brown J, Lominadze D. Vascular effects on cerebrovascular permeability and neurodegeneration. Biomolecules. 2023;13(4):648.
Wardlaw JM, Makin SJ, Valdés Hernández MC, et al. Blood‐brain barrier failure as a core mechanism in cerebral small vessel disease and dementia: evidence from a cohort study. Alzheimers Dement. 2017;13(6):634‐643.
Sone D, Ahmad M, Thompson PJ, et al. Optimal surgical extent for memory and seizure outcome in temporal lobe epilepsy. Ann Neurol. 2022;91(1):131‐144.
Haberly LB. Recruitment of interictal‐ and ictal‐like discharges in posterior piriform cortex by delta‐rate (1‐4 Hz) focal bursts in anterior piriform cortex in vivo. Epilepsy Res. 2022;187:107032.
Lai N, Cheng H, Li Z, et al. Interictal‐period‐activated neuronal ensemble in piriform cortex retards further seizure development. Cell Rep. 2022;41(11):111798. https://www.cell.com/cell‐reports/abstract/S2211‐1247(22)01686‐2
Steinbart D, Yaakub SN, Steinbrenner M, et al. Automatic and manual segmentation of the piriform cortex: method development and validation in patients with temporal lobe epilepsy and Alzheimer's disease. Hum Brain Mapp. 2023;44(8):3196‐3209.
Reschke CR, Silva LFA, Vangoor VR, et al. Systemic delivery of antagomirs during blood‐brain barrier disruption is disease‐modifying in experimental epilepsy. Mol Ther J Am Soc Gene Ther. 2021;29(6):2041‐2052.
Henshall DC, Hamer HM, Pasterkamp RJ, et al. MicroRNAs in epilepsy: pathophysiology and clinical utility. Lancet Neurol. 2016;15(13):1368‐1376.
Vazana U, Veksler R, Pell GS, et al. Glutamate‐mediated blood‐brain barrier opening: implications for neuroprotection and drug delivery. J Neurosci. 2016;36(29):7727‐7739.