Impact of axisymmetric deformation on MR elastography of a nonlinear tissue-mimicking material and implications in peri-tumour stiffness quantification.

Marco Fiorito,Myrianthi Hadjicharalambous,Ralph Sinkus,Daniel Fovargue,David Nordsletten,Jack Lee,Adela Capilnasiu

doi:10.1371/journal.pone.0253804

Marco Fiorito, Myrianthi Hadjicharalambous + Show 5 more

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https://doi.org/10.1371/journal.pone.0253804

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Abstract

Solid tumour growth is often associated with the accumulation of mechanical stresses acting on the surrounding host tissue. Due to tissue nonlinearity, the shear modulus of the peri-tumoural region inherits a signature from the tumour expansion which depends on multiple factors, including the soft tissue constitutive behaviour and its stress/strain state. Shear waves used in MR-elastography (MRE) sense the apparent change in shear modulus along their propagation direction, thereby probing the anisotropic stiffness field around the tumour. We developed an analytical framework for a heterogeneous shear modulus distribution using a thick-shelled sphere approximation of the tumour and soft tissue ensemble. A hyperelastic material (plastisol) was identified to validate the proposed theory in a phantom setting. A balloon-catheter connected to a pressure sensor was used to replicate the stress generated from tumour pressure and growth while MRE data were acquired. The shear modulus anisotropy retrieved from the reconstructed elastography data confirmed the analytically predicted patterns at various levels of inflation. An alternative measure, combining the generated deformation and the local wave direction and independent of the reconstruction strategy, was also proposed to correlate the analytical findings with the stretch probed by the waves. Overall, this work demonstrates that MRE in combination with non-linear mechanics, is able to identify the apparent shear modulus variation arising from the strain generated by a growth within tissue, such as an idealised model of tumour. Investigation in real tissue represents the next step to further investigate the implications of endogenous forces in tissue characterisation through MRE.

Highlights

Solid tumour growth is often associated with an increase of mechanical stresses acting on the surrounding host tissue
Solid: cancer cell proliferation associated to tumour progression [2], electrostatic repulsive forces generated among closely spaced hyaluronan chains [3] and the resistance of the host tissue to the deformation generated by the growing tumour mass [4] define the solid-phase component of the total stress;
In this article we have developed an analytical framework to describe the apparent variation in shear modulus generated by an axisymmetric deformation of a Impact of axisymmetric deformation on MR elastography and implications in peri-tumour stiffness quantification nonlinear viscoelastic material, as probed by shear waves

Summary

Introduction

Solid tumour growth is often associated with an increase of mechanical stresses acting on the surrounding host tissue. Solid stress presents two directionality-dependent components: a radial and a circumferential component While the former acts compressively and gradually decreases when moving away from the tumour rim, the latter turns from compressive to tensile at the soft tissue interface with the tumour [6]. Mathematical models and experimental data have instead shown that IFP is responsible for compressive stress and uniformly distributed throughout the tumour core. These two components add up to define a total stress, which simultaneously compresses the tumour core and pushes against the host tissue. The amplitude and distribution of the generated variation in elastic properties will depends on the tumour shape, the magnitude and direction of the generated deformation field, as well as on the underlying nonlinearity of the tissue

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