Associations of Cerebral Blood Flow Patterns With Gray and White Matter Structure in Patients With Temporal Lobe Epilepsy.


Journal

Neurology
ISSN: 1526-632X
Titre abrégé: Neurology
Pays: United States
ID NLM: 0401060

Informations de publication

Date de publication:
13 Aug 2024
Historique:
medline: 15 7 2024
pubmed: 15 7 2024
entrez: 15 7 2024
Statut: ppublish

Résumé

Neuroimaging studies in patients with temporal lobe epilepsy (TLE) show widespread brain network alterations beyond the mesiotemporal lobe. Despite the critical role of the cerebrovascular system in maintaining whole-brain structure and function, changes in cerebral blood flow (CBF) remain incompletely understood in the disease. Here, we studied whole-brain perfusion and vascular network alterations in TLE and assessed its associations with gray and white matter compromises and various clinical variables. We included individuals with and without pharmaco-resistant TLE who underwent multimodal 3T MRI, including arterial spin labelling, structural, and diffusion-weighted imaging. Using surface-based MRI mapping, we generated individualized cortico-subcortical profiles of perfusion, morphology, and microstructure. Linear models compared regional CBF in patients with controls and related alterations to morphological and microstructural metrics. We further probed interregional vascular networks in TLE, using graph theoretical CBF covariance analysis. The effects of disease duration were explored to better understand the progressive changes in perfusion. We assessed the utility of perfusion in separating patients with TLE from controls using supervised machine learning. Compared with control participants (n = 38; mean ± SD age 34.8 ± 9.3 years; 20 females), patients with TLE (n = 24; mean ± SD age 35.8 ± 10.6 years; 12 females) showed widespread CBF reductions predominantly in fronto-temporal regions (Cohen Our multimodal findings provide insights into vascular contributions to TLE pathophysiology affecting and extending beyond mesiotemporal structures and highlight their clinical potential in epilepsy diagnosis. As our work was cross-sectional and based on a single site, it motivates future longitudinal studies to confirm progressive effects, ideally in a multicentric setting.

Sections du résumé

BACKGROUND AND OBJECTIVES OBJECTIVE
Neuroimaging studies in patients with temporal lobe epilepsy (TLE) show widespread brain network alterations beyond the mesiotemporal lobe. Despite the critical role of the cerebrovascular system in maintaining whole-brain structure and function, changes in cerebral blood flow (CBF) remain incompletely understood in the disease. Here, we studied whole-brain perfusion and vascular network alterations in TLE and assessed its associations with gray and white matter compromises and various clinical variables.
METHODS METHODS
We included individuals with and without pharmaco-resistant TLE who underwent multimodal 3T MRI, including arterial spin labelling, structural, and diffusion-weighted imaging. Using surface-based MRI mapping, we generated individualized cortico-subcortical profiles of perfusion, morphology, and microstructure. Linear models compared regional CBF in patients with controls and related alterations to morphological and microstructural metrics. We further probed interregional vascular networks in TLE, using graph theoretical CBF covariance analysis. The effects of disease duration were explored to better understand the progressive changes in perfusion. We assessed the utility of perfusion in separating patients with TLE from controls using supervised machine learning.
RESULTS RESULTS
Compared with control participants (n = 38; mean ± SD age 34.8 ± 9.3 years; 20 females), patients with TLE (n = 24; mean ± SD age 35.8 ± 10.6 years; 12 females) showed widespread CBF reductions predominantly in fronto-temporal regions (Cohen
DISCUSSION CONCLUSIONS
Our multimodal findings provide insights into vascular contributions to TLE pathophysiology affecting and extending beyond mesiotemporal structures and highlight their clinical potential in epilepsy diagnosis. As our work was cross-sectional and based on a single site, it motivates future longitudinal studies to confirm progressive effects, ideally in a multicentric setting.

Identifiants

pubmed: 39008785
doi: 10.1212/WNL.0000000000209528
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e209528

Auteurs

Alexander Ngo (A)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Jessica Royer (J)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Raul Rodriguez-Cruces (R)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Ke Xie (K)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Jordan DeKraker (J)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Hans Auer (H)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Shahin Tavakol (S)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Jack Lam (J)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Dewi V Schrader (DV)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Roy W R Dudley (RWR)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Andrea Bernasconi (A)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Neda Bernasconi (N)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Birgit Frauscher (B)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Sara Lariviere (S)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

Boris C Bernhardt (BC)

From the Department of Neurology and Neurosurgery (A.N., J.R., R.R.-C., K.X., J.D., H.A., S.T., J.L., A.B., N.B., B.F., B.C.B.), Montreal Neurological Institute and Hospital, McGill University, Montreal, Québec; Department of Pediatrics (D.V.S.), University of British Columbia, Vancouver; Department of Pediatric Surgery (R.W.R.D.), Montreal Children's Hospital, McGill University, Montreal, Québec, Canada; and Center for Brain Circuit Therapeutics (S.L.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA.

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