Tensor-valued diffusion MRI of human acute stroke.

Monte Carlo diffusion simulation b-tensor diffusion time neurite beading stroke tensor-valued diffusion encoding

Journal

Magnetic resonance in medicine
ISSN: 1522-2594
Titre abrégé: Magn Reson Med
Pays: United States
ID NLM: 8505245

Informations de publication

Date de publication:
May 2024
Historique:
revised: 18 11 2023
received: 08 08 2023
accepted: 27 11 2023
pubmed: 2 1 2024
medline: 2 1 2024
entrez: 29 12 2023
Statut: ppublish

Résumé

Tensor-valued diffusion encoding can disentangle orientation dispersion and subvoxel anisotropy, potentially offering insight into microstructural changes after cerebral ischemia. The purpose was to evaluate tensor-valued diffusion MRI in human acute ischemic stroke, assess potential confounders from diffusion time dependencies, and compare to Monte Carlo diffusion simulations of axon beading. Linear (LTE) and spherical (STE) b-tensor encoding with inherently different effective diffusion times were acquired in 21 acute ischemic stroke patients between 3 and 57 h post-onset at 3 T in 2.5 min. In an additional 10 patients, STE with 2 LTE yielding different effective diffusion times were acquired for comparison. Diffusional variance decomposition (DIVIDE) was used to estimate microscopic anisotropy (μFA), as well as anisotropic, isotropic, and total diffusional variance (MK MD was ˜40% lower in lesions for all LTE/STE protocols. The DIVIDE parameters varied with effective diffusion time: higher μFA and MK DIVIDE parameters depend on diffusion time in acute stroke but consistently indicate neurite beading and larger intracellular volume fraction.

Identifiants

pubmed: 38156813
doi: 10.1002/mrm.29975
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2126-2141

Subventions

Organisme : Canada Research Chairs program
Organisme : China Scholarship Council
Organisme : Heart and Stroke Foundation of Canada

Informations de copyright

© 2023 The Authors. Magnetic Resonance in Medicine published by Wiley Periodicals LLC on behalf of International Society for Magnetic Resonance in Medicine.

Références

Moseley ME, Cohen Y, Mintorovitch J, et al. Early detection of regional cerebral ischemia in cats: comparison of diffusion-and T2-weighted MRI and spectroscopy. Magn Reson Med. 1990;14:330-346.
Budde MD, Frank JA. Neurite beading is sufficient to decrease the apparent diffusion coefficient after ischemic stroke. Proc Natl Acad Sci U S A. 2010;107:14472-14477.
Skinner NP, Kurpad SN, Schmit BD, Budde MD. Detection of acute nervous system injury with advanced diffusion-weighted MRI: a simulation and sensitivity analysis. NMR Biomed. 2015;28:1489-1506.
Baron CA, Kate M, Gioia L, et al. Reduction of diffusion-weighted imaging contrast of acute ischemic stroke at short diffusion times. Stroke. 2015;46:2136-2141.
Does MD, Parsons EC, Gore JC. Oscillating gradient measurements of water diffusion in normal and globally ischemic rat brain. Magn Reson Med. 2003;49:206-215.
Wu D, Martin LJ, Northington FJ, Zhang J. Oscillating gradient diffusion MRI reveals unique microstructural information in normal and hypoxia-ischemia injured mouse brains. Magn Reson Med. 2014;72:1366-1374.
Shemesh N, Jespersen SN, Alexander DC, et al. Conventions and nomenclature for double diffusion encoding NMR and MRI. Magn Reson Med. 2016;75:82-87.
Alves R, Henriques RN, Kerkelä L, Chavarrías C, Jespersen SN, Shemesh N. Correlation tensor MRI deciphers underlying kurtosis sources in stroke. Neuroimage. 2022;247:118833.
Shemesh N, Rosenberg JT, Dumez J-N, Muniz JA, Grant SC, Frydman L. Metabolic properties in stroked rats revealed by relaxation-enhanced magnetic resonance spectroscopy at ultrahigh fields. Nat Commun. 2014;5:4958.
Sjölund J, Szczepankiewicz F, Nilsson M, Topgaard D, Westin C-F, Knutsson H. Constrained optimization of gradient waveforms for generalized diffusion encoding. J Magn Reson. 2015;261:157-168.
Szczepankiewicz F, Sjölund J, Ståhlberg F, Lätt J, Nilsson M. Tensor-valued diffusion encoding for diffusional variance decomposition (DIVIDE): technical feasibility in clinical MRI systems. PloS One. 2019;14:e0214238.
Szczepankiewicz F, Westin CF, Nilsson M. Maxwell-compensated design of asymmetric gradient waveforms for tensor-valued diffusion encoding. Magn Reson Med. 2019;82:1424-1437.
Westin C-F, Knutsson H, Pasternak O, et al. Q-space trajectory imaging for multidimensional diffusion MRI of the human brain. Neuroimage. 2016;135:345-362.
Lasič S, Szczepankiewicz F, Eriksson S, Nilsson M, Topgaard D. Microanisotropy imaging: quantification of microscopic diffusion anisotropy and orientational order parameter by diffusion MRI with magic-angle spinning of the q-vector. Frontiers Phys. 2014;2:11.
Szczepankiewicz F, Lasič S, van Westen D, et al. Quantification of microscopic diffusion anisotropy disentangles effects of orientation dispersion from microstructure: applications in healthy volunteers and in brain tumors. Neuroimage. 2015;104:241-252.
Szczepankiewicz F, van Westen D, Englund E, et al. The link between diffusion MRI and tumor heterogeneity: mapping cell eccentricity and density by diffusional variance decomposition (DIVIDE). Neuroimage. 2016;142:522-532.
Nilsson M, Szczepankiewicz F, Brabec J, et al. Tensor-valued diffusion MRI in under 3 minutes: an initial survey of microscopic anisotropy and tissue heterogeneity in intracranial tumors. Magn Reson Med. 2020;83:608-620.
Brabec J, Szczepankiewicz F, Lennartsson F, et al. Histogram analysis of tensor-valued diffusion MRI in meningiomas: relation to consistency, histological grade and type. Neuroimage: Clin. 2022;33:102912.
Li S, Zheng Y, Sun W, et al. Glioma grading, molecular feature classification, and microstructural characterization using MR diffusional variance decomposition (DIVIDE) imaging. Eur Radiol. 2021;31:8197-8207.
Lampinen B, Szczepankiewicz F, Novén M, et al. Searching for the neurite density with diffusion MRI: challenges for biophysical modeling. Hum Brain Mapp. 2019;40:2529-2545.
Lampinen B, Szczepankiewicz F, Mårtensson J, et al. Towards unconstrained compartment modeling in white matter using diffusion-relaxation MRI with tensor-valued diffusion encoding. Magn Reson Med. 2020;84:1605-1623.
Lampinen B, Zampeli A, Björkman-Burtscher IM, et al. Tensor-valued diffusion MRI differentiates cortex and white matter in malformations of cortical development associated with epilepsy. Epilepsia. 2020;61:1701-1713.
Andersen KW, Lasič S, Lundell H, et al. Disentangling white-matter damage from physiological fibre orientation dispersion in multiple sclerosis. Brain Commu. 2020;2:fcaa077.
de Swiet TM, Mitra PP. Possible systematic errors in single-shot measurements of the trace of the diffusion tensor. J Magn Reson B. 1996;111:15-22.
Szczepankiewicz F, Westin C-F, Nilsson M. Gradient waveform design for tensor-valued encoding in diffusion MRI. J Neurosci Methods. 2021;348:109007.
Nilsson M, Szczepankiewicz F, Lampinen B, et al. An open-source framework for analysis of multidimensional diffusion MRI data implemented in MATLAB. In Proceedings of the 26th Annual Meeting of ISMRM; Paris, France. 2018:5355.
Nilsson M, Szczepankiewicz F, van Westen D, Hansson O. Extrapolation-based references improve motion and eddy-current correction of high B-value DWI data: application in Parkinson's disease dementia. PloS One. 2015;10:e0141825.
Klein S, Staring M, Murphy K, Viergever MA, Pluim JP. Elastix: a toolbox for intensity-based medical image registration. IEEE Trans Med Imaging. 2009;29:196-205.
Hall MG, Alexander DC. Convergence and parameter choice for Monte-Carlo simulations of diffusion MRI. IEEE Trans Med Imaging. 2009;28:1354-1364.
Cook PA, Bai Y, Hall MG, Nedjati-Gilani S, Seunarine KK, Alexander DC. Camino: diffusion MRI reconstruction and processing. Proceedings of the 14th Scientific Meeting of ISMRM. Seattle, Washington, USA; 2006:2759.
Lundell H, Nilsson M, Dyrby T, et al. Multidimensional diffusion MRI with spectrally modulated gradients reveals unprecedented microstructural detail. Sci Rep. 2019;9:1-12.
Jespersen SN, Olesen JL, Ianuş A, Shemesh N. Effects of nongaussian diffusion on “isotropic diffusion” measurements: an ex-vivo microimaging and simulation study. J Magn Reson. 2019;300:84-94.
Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med. 2005;53:1432-1440.
Baron CA, Beaulieu C. Oscillating gradient spin-echo (OGSE) diffusion tensor imaging of the human brain. Magn Reson Med. 2014;72:726-736.
Henriques RN, Jespersen SN, Shemesh N. Correlation tensor magnetic resonance imaging. Neuroimage. 2020;211:116605.
Henriques RN, Jespersen SN, Shemesh N. Evidence for microscopic kurtosis in neural tissue revealed by correlation tensor MRI. Magn Reson Med. 2021;86:3111-3130.
Novello L, Henriques RN, Ianuş A, Feiweier T, Shemesh N, Jovicich J. In vivo correlation tensor MRI reveals microscopic kurtosis in the human brain on a clinical 3T scanner. Neuroimage. 2022;254:119137.
Ginsburger K, Matuschke F, Poupon F, Mangin J-F, Axer M, Poupon C. MEDUSA: a GPU-based tool to create realistic phantoms of the brain microstructure using tiny spheres. Neuroimage. 2019;193:10-24.
Lee H-H, Papaioannou A, Kim S-L, Novikov DS, Fieremans E. A time-dependent diffusion MRI signature of axon caliber variations and beading. Commun Biol. 2020;3:354.
Harkins KD, Beaulieu C, Xu J, Gore JC, Does MD. A simple estimate of axon size with diffusion MRI. Neuroimage. 2021;227:117619.

Auteurs

Mi Zhou (M)

Biomedical Engineering, University of Alberta, Edmonton, Alberta, Canada.

Robert Stobbe (R)

Biomedical Engineering, University of Alberta, Edmonton, Alberta, Canada.
Radiology and Diagnostic Imaging, University of Alberta, Edmonton, Alberta, Canada.

Filip Szczepankiewicz (F)

Clinical Sciences Lund, Lund University, Lund, Scania, Sweden.

Matthew Budde (M)

Neurosurgery, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.

Brian Buck (B)

Neurology, University of Alberta, Edmonton, Alberta, Canada.

Mahesh Kate (M)

Neurology, University of Alberta, Edmonton, Alberta, Canada.

Mar Lloret (M)

Neurology, University of Alberta, Edmonton, Alberta, Canada.

Paige Fairall (P)

Neurology, University of Alberta, Edmonton, Alberta, Canada.

Ken Butcher (K)

School of Clinical Medicine, University of New South Wales, Sydney, New South Wales, Australia.

Ashfaq Shuaib (A)

Neurology, University of Alberta, Edmonton, Alberta, Canada.

Derek Emery (D)

Radiology and Diagnostic Imaging, University of Alberta, Edmonton, Alberta, Canada.

Markus Nilsson (M)

Clinical Sciences Lund, Lund University, Lund, Scania, Sweden.

Carl-Fredrik Westin (CF)

Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.

Christian Beaulieu (C)

Biomedical Engineering, University of Alberta, Edmonton, Alberta, Canada.
Radiology and Diagnostic Imaging, University of Alberta, Edmonton, Alberta, Canada.

Classifications MeSH