Microstructural deformation observed by Mueller polarimetry during traction assay on myocardium samples

Nicole Tueni,Jérémy Vizet,Martin Genet,Angelo Pierangelo,Jean-Marc Allain

doi:10.1038/s41598-020-76820-w

Abstract

Despite recent advances, the myocardial microstructure remains imperfectly understood. In particular, bundles of cardiomyocytes have been observed but their three-dimensional organisation remains debated and the associated mechanical consequences unknown. One of the major challenges remains to perform multiscale observations of the mechanical response of the heart wall. For this purpose, in this study, a full-field Mueller polarimetric imager (MPI) was combined, for the first time, with an in-situ traction device. The full-field MPI enables to obtain a macroscopic image of the explored tissue, while providing detailed information about its structure on a microscopic scale. Specifically it exploits the polarization of the light to determine various biophysical quantities related to the tissue scattering or anisotropy properties. Combined with a mechanical traction device, the full-field MPI allows to measure the evolution of such biophysical quantities during tissue stretch. We observe separation lines on the tissue, which are associated with a fast variation of the fiber orientation, and have the size of cardiomyocyte bundles. Thus, we hypothesize that these lines are the perimysium, the collagen layer surrounding these bundles. During the mechanical traction, we observe two mechanisms simultaneously. On one hand, the azimuth shows an affine behavior, meaning the orientation changes according to the tissue deformation, and showing coherence in the tissue. On the other hand, the separation lines appear to be resistant in shear and compression but weak against traction, with a forming of gaps in the tissue.

Highlights

Despite recent advances, the myocardial microstructure remains imperfectly understood
We investigated the role of the myocardium mesoscale organization in its mechanical response, with a particular interest in the response of the perimysium—the collagen layer which surrounds cardiomyocyte bundles—as the role of this structure remains unclear
The samples were fixed at both extremities of a custom-made traction device[36] and were kept immersed in a physiological buffered saline solution (PBS) to prevent any drying of the tissue during measurements

Summary

Introduction

Millimeter-long lateral surfaces of rectangular pieces of the heart wall have been observed with this approach It provides specificity, high resolution and a large field of view, but requires very long scanning times, making it incompatible with mechanical assays. Sparse layers will tend to behave like lines of weakness, strong in compression but weak under traction, whilst denser layers will behave like stiff sheets These contrasts raise questions about the mechanical properties of the collagen walls. To our best knowledge, no experiment has probed the mechanical response at the scale of the cardiomyocyte bundle ( this has been done on skeletal muscle[29]) These questions require new experimental approaches, that allow to obtain mesostructural information for a large field of view and at a rate comparable to that of the mechanical loading

Methods

Results

Conclusion