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Research Papers

Regional Quantification of Brain Tissue Strain Using Displacement-Encoding With Stimulated Echoes Magnetic Resonance Imaging

[+] Author and Article Information
Soroush Heidari Pahlavian

Department of Mechanical Engineering,
Conquer Chiari Research Center,
The University of Akron,
264 Wolf Ledges Parkway 1st floor, RM 211b,
Akron, OH 44325
e-mail: sh113@zips.uakron.edu

John Oshinski

Radiology & Imaging Sciences and Biomedical
Engineering,
Emory University School of Medicine,
1364 Clifton Road NE,
Atlanta, GA 30322
e-mail: jnoshin@emory.edu

Xiaodong Zhong

MR R&D Collaborations,
Siemens Healthcare,
1364 Clifton Road NE,
Atlanta, GA 30322;
Radiology & Imaging Sciences
and Biomedical Engineering,
Emory University School of Medicine,
Atlanta, GA 30322
e-mail: xiaodong.zhong@siemens-healthineers.com

Francis Loth

Department of Mechanical Engineering,
Conquer Chiari Research Center,
The University of Akron,
264 Wolf Ledges Parkway 1st floor, RM 211b,
Akron, OH 44325
e-mail: loth@uakron.edu

Rouzbeh Amini

Department of Biomedical Engineering,
Conquer Chiari Research Center,
The University of Akron,
260 S Forge Street,
Olson Research Center Room 301F,
Akron, OH 44325
e-mail: ramini@uakron.edu

1Corresponding author.

Manuscript received December 1, 2017; final manuscript received May 7, 2018; published online June 15, 2018. Assoc. Editor: Spencer P. Lake.

J Biomech Eng 140(8), 081010 (Jun 15, 2018) (13 pages) Paper No: BIO-17-1563; doi: 10.1115/1.4040227 History: Received December 01, 2017; Revised May 07, 2018

Intrinsic cardiac-induced deformation of brain tissue is thought to be important in the pathophysiology of various neurological disorders. In this study, we evaluated the feasibility of utilizing displacement encoding with stimulated echoes (DENSE) magnetic resonance imaging (MRI) to quantify two-dimensional (2D) neural tissue strain using cardiac-driven brain pulsations. We examined eight adult healthy volunteers with an electrocardiogram-gated spiral DENSE sequence performed at the midsagittal plane on a 3 Tesla MRI scanner. Displacement, pixel-wise trajectories, and principal strains were determined in seven regions of interest (ROI): the brain stem, cerebellum, corpus callosum, and four cerebral lobes. Quantification of small neural tissue motion and strain along with their spatial and temporal variations in different brain regions was found to be feasible using DENSE. The medial and inferior brain structures (brain stem, cerebellum, and corpus callosum) had significantly larger motion and strain compared to structures located more peripherally. The brain stem had the largest peak mean displacement (PMD) (187 ± 50 μm, mean ± SD). The largest mean principal strains in compression and extension were observed in the brain stem (0.38 ± 0.08%) and the corpus callosum (0.37 ± 0.08%), respectively. Measured values in percent strain were altered by as much as 0.1 between repeated scans. This study showed that DENSE can quantify regional variations in brain tissue motion and strain and has the potential to be utilized as a tool to evaluate the changes in brain tissue dynamics resulting from alterations in biomechanical stresses and tissue properties.

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Figures

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Fig. 1

Two-dimensional (2D) tissue displacement quantification from a representative DENSE dataset: (a)–(c) One magnitude and two phase images, with displacement encoding in two orthogonal directions, were loaded into the postprocessing software. (d) and (e) Phase information was converted into the displacement maps in two orthogonal directions and were processed using a 2D low-pass filter. (f) Pixelwise trajectories were calculated using the displacement values throughout the cardiac cycle. Analyses were performed in seven intracranial structures (as shown in 1(a)): 1—brain stem, 2—corpus callosum, 3—cerebellum, 4—frontal lobe, 5—cingulate gyrus, 6—occipital lobe, and 7—parietal lobe. The displacement distributions in this figure were generated at the cardiac time point corresponding to the peak systole.

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Fig. 2

Principal strain quantification from a representative DENSE dataset: (a) and (b) Principal compression and extension strain magnitudes were calculated based on the reconstructed displacement maps (Figs. 1(d) and 1(e)). (c) Distribution of principal strain modes. (d) Cerebellum principal strain histograms showing the distribution of compression and extension principal strains over the tissue pixels outlined by the ROI (structure #3 in Fig. 1(a)). Strain distributions in this figure were generated at the cardiac time point corresponding to the peak systole.

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Fig. 3

Regional differences in PMD, MCS, and MES, and estimated mean through-plane strain quantified using DENSE in eight healthy volunteers. Bar plots and error bars depict the mean and standard deviation for each parameter, respectively. The significance of the observed differences between each of the two structures is presented in the p-value chart at the bottom. The locations of each brain structure are shown in Fig. 1(a). *Note that mean through-plane strain values were estimated using the deformation gradients measured in two in-plane directions, assuming tissue incompressibility and zero out-of-plane shear strain.

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Fig. 4

Averaged normalized principal strain histograms calculated by aggregating the pixelwise principal strain values of each brain region from all eight subjects. Contribution of each subject to the average distribution was normalized by the ROI size (pixel count) corresponding to that subject. An example of a principal strain histogram for a representative subject and a representative brain structure (cerebellum) is shown in Fig. 2(d).

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Fig. 5

The averaged normalized polar histograms of principal compression and extension orientations. A histogram for each brain region was generated by aggregating the pixelwise principal direction vectors from all eight subjects. The contribution of each subject to the average distribution was normalized by the ROI size (pixel count) corresponding to that subject. The average orientations of 0 deg and 90 deg denote the dominance of the strain along the anteroposterior direction and the craniocaudal direction, respectively. The uniformity of the distribution for each histogram is quantified by the UI, as defined in Eq. (5). Smaller UIs denote more dominant principal orientations.

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Fig. 6

The distribution of neural tissue motion and strain in a healthy volunteer: (a) and (b) brain stem, (c) and (d) cerebellum, and (e) and (f) parietal lobe. For each structure, the left and right frames show the pixelwise trajectories and principal compression strain maps, respectively. The insets in the strain maps for the brain stem and cerebellum depict the principal strain orientations for the highlighted regions. White arrows point to the regions in which the localized increase of the strain could be caused by ROI selection errors and/or partial volume averaging artifacts, and the numbers in brackets indicate the range of the principal compression strains for each distribution map. Note that all three structures are plotted on the same spatial scale.

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Fig. 7

Evaluating the impact of displacement noise on strain calculations using a synthetic displacement field and a representative in vivo cerebellum measurement: (a) Noise-free synthetic displacement field as reference. (b) Synthetic displacement with added noise from DENSE stationary phantom measurement. (c) Noise-filtered synthetic displacement field. (d) In Vivo anteroposterior displacement field on the cerebellum for a representative subject measured using DENSE. (e) Noise-filtered in vivo displacement field. (f) Strain map calculated from the noise-free synthetic displacement as reference. (g) Strain map calculated from the noise-contaminated synthetic displacement field. (h) Strain map calculated from the noise-filtered synthetic displacement field. (i) Strain map calculated from the in vivo measured displacement without noise filtering. (j) Strain map calculated from the noise-filtered in vivo displacement field. The numbers in brackets in Figs. 7(g) and 7(i) indicate the variable range for noise-contaminated strain maps.

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Fig. 8

Bland–Altman plots showing the correlation and the confidence intervals for two subsequent measurements of PMD, MCS, and MES over seven brain regions in three subjects

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Fig. 9

Mediolateral tissue displacement on various coronal planes measured on one healthy volunteer. The numbers in brackets for each plane denote the maximum right-to-left (negative) and maximum left-to-right (positive) displacements (in microns). The displacement distributions in this figure were generated at the cardiac time point corresponding to the peak systole.

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