Prevalence and Significance of the Vessel-Cluster Sign on Susceptibility-Weighted Imaging in Patients With Severe Small Vessel Disease.

CADASIL cavitation cerebrovascular reactivity lacunes small vessel disease susceptibility-weighted imaging venules

Journal

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

Informations de publication

Date de publication:
23 May 2022
Historique:
received: 01 10 2021
accepted: 15 03 2022
entrez: 23 5 2022
pubmed: 24 5 2022
medline: 24 5 2022
Statut: aheadofprint

Résumé

Magnetic resonance susceptibility-weighted imaging (SWI) can identify small brain blood vessels that contain deoxygenated blood due to its induced magnetic field disturbance. We observed focal clusters of possible dilated small vessels on SWI in white matter in severe small vessel disease (SVD). We assessed their prevalence, associations with SVD lesions and vascular reactivity in patients with sporadic SVD and in patients with Cerebral Autosomal Dominant Arteriopathy with Subcortical Infarcts and Leukoencephalopathy (CADASIL). Secondary cross-sectional analysis of a prospective multicentre observational study of patients with either sporadic SVD or CADASIL (INVESTIGATE-SVD) studied with 3 Tesla MRI including blood-oxygen-level-dependent-MRI cerebrovascular reactivity (CVR). Two independent raters evaluated SWI sequences to identify "vessel-clusters" in white matter as focal low-signal dots/lines with small vessel appearance (interrater agreement, kappa statistic= 0.66). We assessed per-patient and per-cluster associations with SVD lesions type and severity on structural MRI sequences. We also assessed CVR within and at 2-voxel concentric intervals around the vessel-clusters using contralateral volumes as reference. Amongst the 77 patients enrolled, 76 had usable SWI sequences, 45 with sporadic SVD [mean age 64 years (SD 11), 26 males (58%)] and 31 with CADASIL [53 years (11), 15 males (48%)]. We identified 94 vessel-clusters in 36/76 patients (15/45 sporadic SVD, 21/31 CADASIL). In covariate-adjusted analysis, patients with vessel-clusters had more lacunes (OR, 95%CI) (1.30, 1.05-1.62), higher white matter hyperintensity (WMH) volume (per-log10 increase, 1.92, 1.04-3.56), lower CVR in normal appearing white matter (per %/mmHg, 0.77 (0.60-0.99), compared with patients without vessel-clusters. Fifty-seven of 94 vessel-clusters (61%) corresponded to non-cavitated or partially-cavitated WMH on Fluid Attenuated Inversion Recovery, and 37/94 (39%) to complete cavities. CVR magnitude was lower than in corresponding contralateral volumes [mean difference (SD), t, p] within vessel-cluster volumes [-0.00046 (0.00088), -3.021, 0.005) and in surrounding volume expansion shells up to 4 voxels [-0.00011 (0.00031), -2.140, 0.039; and -0.00010 (0.00027), -2.295, 0.028] in vessel-clusters with complete cavities, but not in vessel-clusters without complete cavitation. Vessel-clusters might correspond to maximally dilated vessels in white matter that are approaching complete tissue injury and cavitation. The pathophysiological significance of this new feature warrants further longitudinal investigation.

Sections du résumé

BACKGROUND BACKGROUND
Magnetic resonance susceptibility-weighted imaging (SWI) can identify small brain blood vessels that contain deoxygenated blood due to its induced magnetic field disturbance. We observed focal clusters of possible dilated small vessels on SWI in white matter in severe small vessel disease (SVD). We assessed their prevalence, associations with SVD lesions and vascular reactivity in patients with sporadic SVD and in patients with Cerebral Autosomal Dominant Arteriopathy with Subcortical Infarcts and Leukoencephalopathy (CADASIL).
METHODS METHODS
Secondary cross-sectional analysis of a prospective multicentre observational study of patients with either sporadic SVD or CADASIL (INVESTIGATE-SVD) studied with 3 Tesla MRI including blood-oxygen-level-dependent-MRI cerebrovascular reactivity (CVR). Two independent raters evaluated SWI sequences to identify "vessel-clusters" in white matter as focal low-signal dots/lines with small vessel appearance (interrater agreement, kappa statistic= 0.66). We assessed per-patient and per-cluster associations with SVD lesions type and severity on structural MRI sequences. We also assessed CVR within and at 2-voxel concentric intervals around the vessel-clusters using contralateral volumes as reference.
RESULTS RESULTS
Amongst the 77 patients enrolled, 76 had usable SWI sequences, 45 with sporadic SVD [mean age 64 years (SD 11), 26 males (58%)] and 31 with CADASIL [53 years (11), 15 males (48%)]. We identified 94 vessel-clusters in 36/76 patients (15/45 sporadic SVD, 21/31 CADASIL). In covariate-adjusted analysis, patients with vessel-clusters had more lacunes (OR, 95%CI) (1.30, 1.05-1.62), higher white matter hyperintensity (WMH) volume (per-log10 increase, 1.92, 1.04-3.56), lower CVR in normal appearing white matter (per %/mmHg, 0.77 (0.60-0.99), compared with patients without vessel-clusters. Fifty-seven of 94 vessel-clusters (61%) corresponded to non-cavitated or partially-cavitated WMH on Fluid Attenuated Inversion Recovery, and 37/94 (39%) to complete cavities. CVR magnitude was lower than in corresponding contralateral volumes [mean difference (SD), t, p] within vessel-cluster volumes [-0.00046 (0.00088), -3.021, 0.005) and in surrounding volume expansion shells up to 4 voxels [-0.00011 (0.00031), -2.140, 0.039; and -0.00010 (0.00027), -2.295, 0.028] in vessel-clusters with complete cavities, but not in vessel-clusters without complete cavitation.
CONCLUSIONS CONCLUSIONS
Vessel-clusters might correspond to maximally dilated vessels in white matter that are approaching complete tissue injury and cavitation. The pathophysiological significance of this new feature warrants further longitudinal investigation.

Identifiants

pubmed: 35606147
pii: WNL.0000000000200614
doi: 10.1212/WNL.0000000000200614
pmc: PMC9421604
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Chief Scientist Office
ID : CZB/4/517
Pays : United Kingdom
Organisme : Chief Scientist Office
ID : ETM/326
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/J006971/1
Pays : United Kingdom

Informations de copyright

Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.

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Auteurs

Salvatore Rudilosso (S)

Comprehensive Stroke Center, Department of Neuroscience, Hospital Clinic, University of Barcelona and August Pi i Sunyer Biomedical Research Institute (IDIBAPS), Villarroel 170, 08036, Barcelona, Spain.

Ernest Chui (E)

Centre for Clinical Brain Sciences, UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK.

Michael S Stringer (MS)

Centre for Clinical Brain Sciences, UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK.

Michael Thrippleton (M)

Centre for Clinical Brain Sciences, UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK.

Francesca Chappell (F)

Centre for Clinical Brain Sciences, UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK.

Gordon Blair (G)

Centre for Clinical Brain Sciences, UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK.

Daniela Jaime GarcÃa (DJ)

Centre for Clinical Brain Sciences, UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK.

Fergus Doubal (F)

Centre for Clinical Brain Sciences, UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK.

Iona Hamilton (I)

Centre for Clinical Brain Sciences, UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK.

Anna Kopczak (A)

Institute for Stroke and Dementia Research, University Hospital, LMU Munich, Munich, Germany.

Michael Ingrish (M)

Department of Radiology, Ludwig-Maximilians-University Hospital Munich, Munich, Germany.

Danielle Kerkhofs (D)

Department of Neurology, CARIM - School for Cardiovascular Diseases Maastricht University Medical Center+, Maastricht, The Netherlands.

Walter H Backes (WH)

Department of Radiology & Nuclear Medicine, School for Mental Health & Neuroscience and School for Cardiovascular Diseases, Maastricht University Medical Centre, Maastricht, Netherlands.

Julie Staals (J)

Department of Neurology, CARIM - School for Cardiovascular Diseases Maastricht University Medical Center+, Maastricht, The Netherlands.

Robert van Oostenbrugge (R)

Department of Neurology, CARIM - School for Cardiovascular Diseases Maastricht University Medical Center+, Maastricht, The Netherlands.

Marco Duering (M)

Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, Munich, Germany.
Medical Image Analysis Center (MIAC AG) and Department of Biomedical Engineering, University of Basel, Basel, Switzerland.

Martin Dichgans (M)

Institute for Stroke and Dementia Research, University Hospital, LMU Munich, Munich, Germany.
Munich Cluster for Systems Neurology (SyNergy), Germany (M.D.).
German Center for Neurodegenerative Diseases (DZNE), Munich, Germany (M.D.).

Joanna M Wardlaw (JM)

Centre for Clinical Brain Sciences, UK Dementia Research Institute, University of Edinburgh, Edinburgh, UK joanna.wardlaw@ed.ac.uk.

Classifications MeSH