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      Tensor-valued diffusion encoding for diffusional variance decomposition (DIVIDE): Technical feasibility in clinical MRI systems

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          Abstract

          Microstructure imaging techniques based on tensor-valued diffusion encoding have gained popularity within the MRI research community. Unlike conventional diffusion encoding—applied along a single direction in each shot—tensor-valued encoding employs diffusion encoding along multiple directions within a single preparation of the signal. The benefit is that such encoding may probe tissue features that are not accessible by conventional encoding. For example, diffusional variance decomposition (DIVIDE) takes advantage of tensor-valued encoding to probe microscopic diffusion anisotropy independent of orientation coherence. The drawback is that tensor-valued encoding generally requires gradient waveforms that are more demanding on hardware; it has therefore been used primarily in MRI systems with relatively high performance. The purpose of this work was to explore tensor-valued diffusion encoding on clinical MRI systems with varying performance to test its technical feasibility within the context of DIVIDE. We performed whole-brain imaging with linear and spherical b-tensor encoding at field strengths between 1.5 and 7 T, and at maximal gradient amplitudes between 45 and 80 mT/m. Asymmetric gradient waveforms were optimized numerically to yield b-values up to 2 ms/μm 2. Technical feasibility was assessed in terms of the repeatability, SNR, and quality of DIVIDE parameter maps. Variable system performance resulted in echo times between 83 to 115 ms and total acquisition times of 6 to 9 minutes when using 80 signal samples and resolution 2×2×4 mm 3. As expected, the repeatability, signal-to-noise ratio and parameter map quality depended on hardware performance. We conclude that tensor-valued encoding is feasible for a wide range of MRI systems—even at 1.5 T with maximal gradient waveform amplitudes of 33 mT/m—and baseline experimental design and quality parameters for all included configurations. This demonstrates that tissue features, beyond those accessible by conventional diffusion encoding, can be explored on a wide range of MRI systems.

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          Reliability, repeatability and reproducibility: analysis of measurement errors in continuous variables.

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            Q-space trajectory imaging for multidimensional diffusion MRI of the human brain.

            This work describes a new diffusion MR framework for imaging and modeling of microstructure that we call q-space trajectory imaging (QTI). The QTI framework consists of two parts: encoding and modeling. First we propose q-space trajectory encoding, which uses time-varying gradients to probe a trajectory in q-space, in contrast to traditional pulsed field gradient sequences that attempt to probe a point in q-space. Then we propose a microstructure model, the diffusion tensor distribution (DTD) model, which takes advantage of additional information provided by QTI to estimate a distributional model over diffusion tensors. We show that the QTI framework enables microstructure modeling that is not possible with the traditional pulsed gradient encoding as introduced by Stejskal and Tanner. In our analysis of QTI, we find that the well-known scalar b-value naturally extends to a tensor-valued entity, i.e., a diffusion measurement tensor, which we call the b-tensor. We show that b-tensors of rank 2 or 3 enable estimation of the mean and covariance of the DTD model in terms of a second order tensor (the diffusion tensor) and a fourth order tensor. The QTI framework has been designed to improve discrimination of the sizes, shapes, and orientations of diffusion microenvironments within tissue. We derive rotationally invariant scalar quantities describing intuitive microstructural features including size, shape, and orientation coherence measures. To demonstrate the feasibility of QTI on a clinical scanner, we performed a small pilot study comparing a group of five healthy controls with five patients with schizophrenia. The parameter maps derived from QTI were compared between the groups, and 9 out of the 14 parameters investigated showed differences between groups. The ability to measure and model the distribution of diffusion tensors, rather than a quantity that has already been averaged within a voxel, has the potential to provide a powerful paradigm for the study of complex tissue architecture.
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              Improving diffusion MRI using simultaneous multi-slice echo planar imaging.

              In diffusion MRI, simultaneous multi-slice single-shot EPI acquisitions have the potential to increase the number of diffusion directions obtained per unit time, allowing more diffusion encoding in high angular resolution diffusion imaging (HARDI) acquisitions. Nonetheless, unaliasing simultaneously acquired, closely spaced slices with parallel imaging methods can be difficult, leading to high g-factor penalties (i.e., lower SNR). The CAIPIRINHA technique was developed to reduce the g-factor in simultaneous multi-slice acquisitions by introducing inter-slice image shifts and thus increase the distance between aliased voxels. Because the CAIPIRINHA technique achieved this by controlling the phase of the RF excitations for each line of k-space, it is not directly applicable to single-shot EPI employed in conventional diffusion imaging. We adopt a recent gradient encoding method, which we termed "blipped-CAIPI", to create the image shifts needed to apply CAIPIRINHA to EPI. Here, we use pseudo-multiple replica SNR and bootstrapping metrics to assess the performance of the blipped-CAIPI method in 3× simultaneous multi-slice diffusion studies. Further, we introduce a novel image reconstruction method to reduce detrimental ghosting artifacts in these acquisitions. We show that data acquisition times for Q-ball and diffusion spectrum imaging (DSI) can be reduced 3-fold with a minor loss in SNR and with similar diffusion results compared to conventional acquisitions. Copyright © 2012 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SoftwareRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                28 March 2019
                2019
                : 14
                : 3
                : e0214238
                Affiliations
                [1 ] Lund University, Department of Clinical Sciences Lund, Medical Radiation Physics, Lund, Sweden
                [2 ] Elekta Instrument AB, Kungstensgatan 18, Stockholm, Sweden
                [3 ] Linköping University, Department of Biomedical Engineering, Linköping, Sweden
                [4 ] Linköping University, Center for Medical Image Science and Visualization (CMIV), Linköping, Sweden
                [5 ] Lund University, Department of Clinical Sciences Lund, Diagnostic Radiology, Lund, Sweden
                [6 ] Skåne University Hospital, Department of Imaging and Function, Lund, Sweden
                [7 ] Lund University, Lund University Bioimaging Center, Lund, Sweden
                McLean Hospital, UNITED STATES
                Author notes

                Competing Interests: MN declares research support from, and ownership interests in, Colloidal Resource and it subsidiary Random Walk Imaging AB. FSz is a former employee of Random Walk Imaging AB. Remaining authors declare no conflict of interest.

                Author information
                http://orcid.org/0000-0002-5251-587X
                http://orcid.org/0000-0002-9099-3522
                Article
                PONE-D-18-30840
                10.1371/journal.pone.0214238
                6438503
                30921381
                37ae5535-d4c4-4054-aeaf-c58ef07111a4
                © 2019 Szczepankiewicz et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 15 November 2018
                : 8 March 2019
                Page count
                Figures: 6, Tables: 2, Pages: 20
                Funding
                This work was supported by: MN: Swedish Research Council. Grant no. 2016-03443, https://www.vr.se/; MN: Swedish Foundation for Strategic Research. Grant no. AM13-0090, https://strategiska.se/en/; and MN: Random Walk Imaging AB. Grant no MN15, www.rwi.se. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                The in vivo data cannot be made publicly available, as this would violate Swedish law. The research was performed under an IRB approval, and required the research subject to sign an informed consent. According to Swedish law applicable to this study, the scope of the consent must be specific (Personal Data Act 1998:204; Swe. “personuppgiftslagen”, http://rkrattsbaser.gov.se/sfst?bet=1998:204). Therefore, we are prohibited from sharing the data publicly for general research that was not described in the consent form. Data are available upon request from researchers who have ethical approval to Prof. Linda Knutsson, head of MRI research (including research data storage), at the Dept. of Medical Radiation Physics, Lund University (Address: Dept. of Medical Radiation Physics, Barngatan 6, Lund 22185, Sweden; Telephone: +4646178547; Email: linda.knutsson@ 123456med.lu.se ).

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