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Imaging multiple sclerosis pathology at 160 μm isotropic resolution by human whole-brain ex vivo magnetic resonance imaging at 3 T.

ABSTRACT: Postmortem magnetic resonance imaging (MRI) of the fixed healthy and diseased human brain facilitates spatial resolutions and image quality that is not achievable with in vivo MRI scans. Though challenging-and almost exclusively performed at 7 T field strength-depicting the tissue architecture of the entire brain in fine detail is invaluable since it enables the study of neuroanatomy and uncovers important pathological features in neurological disorders. The objectives of the present work were (1) to develop a 3D isotropic ultra-high-resolution imaging approach for human whole-brain ex vivo acquisitions working on a standard clinical 3 T MRI system; and (2) to explore the sensitivity and specificity of this concept for specific pathoanatomical features of multiple sclerosis. The reconstructed images demonstrate unprecedented resolution and soft tissue contrast of the diseased human brain at 3 T, thus allowing visualization of sub-millimetric lesions in the different cortical layers and in the cerebellar cortex, as well as unique cortical lesion characteristics such as the presence of incomplete/complete iron rims, and patterns of iron accumulation. Further details such as the subpial molecular layer, the line of Gennari, and some intrathalamic nuclei are also well distinguishable.

SUBMITTER: Weigel M

PROVIDER: S-EPMC8322069 | biostudies-literature | 2021 Jul

REPOSITORIES: biostudies-literature

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Imaging multiple sclerosis pathology at 160 μm isotropic resolution by human whole-brain ex vivo magnetic resonance imaging at 3 T.

Weigel Matthias M Dechent Peter P Galbusera Riccardo R Bahn Erik E Nair Govind G Lu Po-Jui PJ Kappos Ludwig L Brück Wolfgang W Stadelmann Christine C Granziera Cristina C

Scientific reports 20210729 1

Postmortem magnetic resonance imaging (MRI) of the fixed healthy and diseased human brain facilitates spatial resolutions and image quality that is not achievable with in vivo MRI scans. Though challenging-and almost exclusively performed at 7 T field strength-depicting the tissue architecture of the entire brain in fine detail is invaluable since it enables the study of neuroanatomy and uncovers important pathological features in neurological disorders. The objectives of the present work were ( ...[more]

PMID: 34326420

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Project description:In multiple sclerosis (MS), iron accumulates inside activated microglia/macrophages at edges of some chronic demyelinated lesions, forming rims. In susceptibility-based magnetic resonance imaging at 7 T, iron-laden microglia/macrophages induce a rim of decreased signal at lesion edges and have been associated with slowly expanding lesions. We aimed to determine (1) what lesion types and stages are associated with iron accumulation at their edges, (2) what cells at the lesion edges accumulate iron and what is their activation status, (3) how reliably can iron accumulation at the lesion edge be detected by 7 T magnetic resonance imaging (MRI), and (4) if lesions with rims enlarge over time in vivo, when compared to lesions without rims. Double-hemispheric brain sections of 28 MS cases were stained for iron, myelin, and microglia/macrophages. Prior to histology, 4 of these 28 cases were imaged at 7 T using post-mortem susceptibility-weighted imaging. In vivo, seven MS patients underwent annual neurological examinations and 7 T MRI for 3.5 years, using a fluid attenuated inversion recovery/susceptibility-weighted imaging fusion sequence. Pathologically, we found iron rims around slowly expanding and some inactive lesions but hardly around remyelinated shadow plaques. Iron in rims was mainly present in microglia/macrophages with a pro-inflammatory activation status, but only very rarely in astrocytes. Histological validation of post-mortem susceptibility-weighted imaging revealed a quantitative threshold of iron-laden microglia when a rim was visible. Slowly expanding lesions significantly exceeded this threshold, when compared with inactive lesions (p = 0.003). We show for the first time that rim lesions significantly expanded in vivo after 3.5 years, compared to lesions without rims (p = 0.003). Thus, slow expansion of MS lesions with rims, which reflects chronic lesion activity, may, in the future, become an MRI marker for disease activity in MS.

Project description:PurposeTo demonstrate an MRI technique-Submillisecond Periodic Event Encoded Dynamic Imaging (SPEEDI)-for capturing cyclic dynamic events with submillisecond temporal resolution.MethodsThe SPEEDI technique is based on an FID or an echo signal in which each time point in the signal is used to sample a distinct k-space raster, followed by repeated FIDs or echoes to produce the remaining k-space data in each k-space raster. All acquisitions are synchronized with a cyclic event, resulting in a set of time-resolved images of the cyclic event with a temporal resolution determined by the dwell time. In SPEEDI, spatial encoding is accomplished by phase encoding. The SPEEDI technique was demonstrated in two experiments at 3 T to (1) visualize fast-changing electric currents that mimicked the waveform of an action potential, and (2) characterize rapidly decaying eddy currents in an MRI system, with a temporal resolution of 0.2 ms and 0.4 ms, respectively. In both experiments, compressed sensing was incorporated to reduce the scan times. Phase difference maps related to the dynamics of electric currents or eddy currents were then obtained.ResultsIn the first experiment, time-resolved phase maps resulting from the action potential-mimicking current waveform were successfully obtained and agreed well with theoretical calculations (normalized RMS error = 0.07). In the second experiment, spatially resolved eddy current phase maps revealed time constants (27.1 ± 0.2 ms, 41.1 ± 3.5 ms, and 34.8 ± 0.7 ms) that matched well with those obtained from an established method using point sources (26.4 ms, 41.2 ms and 34.8 ms). For both experiments, phase maps from fully sampled and compressed-sensing-accelerated k-space data exhibited a high structural similarity (> 0.8) despite a two-fold to three-fold acceleration.ConclusionsWe have illustrated that SPEEDI can provide submillisecond temporal resolution. This capability will likely lead to future exploration of ultrafast, cyclic biomedical processes using MRI.

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Dataset Information

Imaging multiple sclerosis pathology at 160 μm isotropic resolution by human whole-brain ex vivo magnetic resonance imaging at 3 T.

Publications

Imaging multiple sclerosis pathology at 160 μm isotropic resolution by human whole-brain ex vivo magnetic resonance imaging at 3 T.

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