Distinguishing shear and tensile myocardial wall stiffness using ex vivo anisotropic Magnetic Resonance Elastography

ABSTRACT The organized myofiber structure within the myocardium indicates its mechanical anisotropy. By projecting the MR Elastography (MRE) stiffness matrix along either the myocardial fiber or sheet orientations determined by Diffusion Tensor Imaging (DTI), anisotropic MRE (aMRE) maps axial and transverse shear and Young’s moduli into three tensile and six shear deformation modes. Ten healthy ex vivo swine hearts were imaged three times at 3T using MRE and DTI sequences. aMRE results showed a within-subject coefficient of variation at 19% for the fiber model and 28% for the sheet model across specimens and metrics, with coefficients lower than 15% for seven of the ten specimens across models. Repeatability coefficient of ±0.5 kPa for Young’s moduli and ±0.17 kPa for shear’s moduli, demonstrating repeatability within the 95% agreement limit. Isotropic MRE underestimated stiffnesses by 31% compared to aMRE, where anisotropic moduli aligned more closely with prior finite element studies and some mechanical loading tests. The myocardium’s anisotropic elasticity reflects with its helicoidal myofiber microstructure, with mid-wall circumferential fibers requiring twice the force to deform as longitudinal fibers at the epicardium or endocardium. At the mid-wall, fiber model values were μ ax = 1.9 ± 0.1 kPa, μ tra = 1.3 ± 0.1 kPa, E ax = 5.6 ± 0.4 kPa, and E tra = 3.8 ± 0.3 kPa. Identified deformation modes included: (FF), (NN), (FF or SS), (NN or SS), (SN or NS), (FN or FS), (SF or FS), and (SN or NF), where N is normal to both fiber (F) and sheet (S) orientations. By aligning elasticity matrices more accurately with myocardial architecture than isotropic MRE, aMRE was able to reliably measure shear and Young’s moduli in ex vivo swine hearts. These mappings of deformation modes may bring myocardial stiffness assessment closer to clinical application, providing a foundation for a non-invasive methodology capable of true mechanical characterization of the cardiac wall using MR imaging. Statement of Significance The myocardium’s anisotropic elasticity, due to its helicoidal myofiber structure, is revealed through anisotropic MR elastography, using fiber and sheet elastic models. Mid-wall circumferential fibers require twice the force to deform equally compared to epicardial or endocardial fibers. Characterizing shear and Young’s moduli across cardiac modes offers noninvasive measures of ventricular compliance, comparable to pressure-volume relationships. This could enhance early diagnosis of “stiff heart syndrome” and clarify its underlying mechanisms. Additionally, it aids understanding of myocardial pathologies, including amyloidosis, hypertrophic and dilated cardiomyopathies, and ischemic damage. By characterizing tensile and shear interactions, it may inform diagnosis and treatment of conduction issues and arrhythmia, where tissue has lost its normal mechanical behavior, while patient-specific models could optimize surgical and therapeutic outcomes.