Three-dimensional analysis of shear wave propagation observed by in vivo magnetic resonance elastography of the brain☆
Introduction
For centuries, palpation has been used as the primary test for pathological tissue change. The sensitivity of the method is based on the mechanical resistance of soft tissue to compression and shear deformations, which varies in orders of magnitude throughout the human body. However, manual palpation is a subjective method limited to soft tissues in the vicinity of the body surface. Therefore, dynamic magnetic resonance elastography (MRE) was developed as a non-invasive method for quantitatively measuring the viscoelastic properties of human soft tissue in vivo [1], [2], [3], [4], [5], [6], [7], [8], [9], [10]. In contrast to static MRE, where static or quasi-static tissue deformations are applied, dynamic MRE is based on the application of low-frequency acoustic waves penetrating the tissue of interest. Short dynamic excitation pulses are used in transient dynamic MRE, whereas steady-state dynamic MRE – the subject of this study – uses several motion cycles or continuous excitations. The tissue motion is magnetically encoded in the MR phase signal by synchronously oscillating gradients. The wave images display a phase-difference contrast that is sensitive to deflections smaller than 1 μm. In dynamic MRE, if the direction of wave propagation lies in the image plane and boundary effects and viscosity are negligible, the wavelength of the observed wave patterns is related to the elasticity of the tissue.
Comparisons of dynamic MRE with independent shear modulus-determining methods have shown that MRE provides correct quantities in tissue phantoms [1], [11], [12], [13]. Promising studies have recently shown that MRE is able to quantify elastic parameters in well-shielded organs such as the prostate, kidney and liver, where manual palpation is restricted [14], [15], [16], [17].
Dynamic MRE is especially suited for assessing in vivo brain elasticities. In contrast to manual examination, application of static MRE and ultrasound elastography, this technique is capable of producing results despite the mechanical shielding of the skull. The feasibility of using MRE to acquire wave images of the brain has been demonstrated by several studies [18], [19], [20], [21], [22], [23], [24], [25]. For mechanical excitation of the brain, the entire head is vibrated, causing indirectly induced shear waves. Thus, the full three-dimensional (3-D) wave field has to be acquired to correctly measure the resulting convolute wave vector field in the brain. Despite the ability of MRE to detect all components of the full wave field, most brain MRE studies are, in order to save time, based on the acquisition of the wave field in a single image plane followed by a 2-D shear modulus reconstruction. However, a 2-D projection through a 3-D wave field can yield geometrical biases that can result in misinterpretation of the determined planar shear modulus. It has been shown that even for tissue phantoms with simple geometries the wave-propagation process is truly 3-D and the full 3-D wave field has to be considered for an accurate reconstruction of elasticity images [26]. The full 3-D displacement field is particularly important for the brain – with its complex anatomy, shape and mechanisms of indirect wave excitation – in order to deduce correct elastic coefficients.
Thus, in this study, the wave propagation through the brain of a volunteer was analyzed by measuring all wave field components. Assuming isotropy, the final wave field analysis was restricted to the scalar field of the deflection component that has shown the largest penetration depth of the acoustic waves into the brain. The temporal evolution of this component was acquired and these 4-D data were analyzed using a new algorithm that allows the direction of shear wave propagation to be determined. The algorithm is profile-based and assumes that the minimum wavelength indicates the direction of wave propagation from the origin of the ray [27]. The shear modulus of brain tissue determined via this method is compared with the results of a direct inversion of 2-D data and data given in the literature.
The aim of the present study was, therefore, to characterize the regions with the best correlation between wave propagation and images with a transversal, coronal or sagittal orientation. Within these regions, fast in vivo 2-D MRE can then be applied with a minimized error range in order to quantify the shear modulus of brain tissue. This reduction in scan time is a crucial precondition for forthcoming studies of patients suffering from brain diseases.
Section snippets
Materials and methods
The methods of our study can be divided into (i) wave generation, (ii) imaging sequence development, (iii) data acquisition, (iv) data preprocessing and (v) data analysis, which finally results in the determination of wave velocities and directions of wave propagation.
Results
The presentation of the results is divided into (i) evaluation of the proposed algorithm using software phantoms and (ii) analysis of in vivo MRE data of the human brain.
Discussion
Verification of the accuracy of the proposed method was done using software phantoms comparable in size, damping properties, signal-to-noise ratio and spatial resolution to in vivo MRE data of the brain. Variable program parameters were analyzed to optimize the method for application to in vivo MRE data.
Specifically, application of the linear fit procedure yielded clearly better results than calculations based on start and end points of edge segments in spatiotemporal images. This can be
Conclusions
Our results show that quantitative data for in vivo elastic properties of brain tissue can be obtained by combining an EPI–MRE acquisition technique with analysis of the propagating 3-D wave fields. The proposed method uses the effective direction of the shear wave propagation to calculate the shear modulus. A position-dependent overestimation of the shear modulus was demonstrated for inversion techniques on the basis of single-wave images. This was due to a mismatch between the image
Acknowledgement
The project was supported by the Deutsche Forschungsgemeinschaft (Br 2235/2-1, Sa 901/3-1).
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2019, MaterialiaCitation Excerpt :The synthetic materials explored for this study included silicones of different hardness, gelatin with and without a chromium crosslinker, agarose, and two emulsions with varying composition. Brain tissue mechanical properties have been extensively characterized in vitro under the modes of shear [9–13], compression [14–19] and tension [16, 20–24] as well as in situ and in vivo under the modes of magnetic resonance elastography (MRE) [25–30], surface suction [31] and indentation [24,32–35]. The human brain is formed by gray matter that constitutes the brain cortex.
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This work was presented in parts at the First International Conference on Mechanics of Biomaterials & Tissues.