Visualization and quantification of whole rat heart laminar structure using high-spatial resolution contrast-enhanced MRI

Abstract

. Visualization and quantification of whole rat heart laminar structure using highspatial resolution contrast-enhanced MRI. Am J Physiol Heart Circ Physiol 302: H287-H298, 2012. First published October 21, 2011; doi:10.1152/ajpheart.00824.2011.-It has been shown by histology that cardiac myocytes are organized into laminae and this structure is important in function, both influencing the spread of electrical activation and enabling myocardial thickening in systole by laminar sliding. We have carried out high-spatial resolution three-dimensional MRI of the ventricular myolaminae of the entire volume of the isolated rat heart after contrast perfusion [dimeglumine gadopentate (Gd-DTPA)]. Four ex vivo rat hearts were perfused with Gd-DTPA and fixative and high-spatial resolution MRI was performed on a 9.4T MRI system. After MRI, cryosectioning followed by histology was performed. Images from MRI and histology were aligned, described, and quantitatively compared. In the three-dimensional MR images we directly show the presence of laminae and demonstrate that these are highly branching and are absent from much of the subepicardium. We visualized these MRI volumes to demonstrate laminar architecture and quantitatively demonstrated that the structural features observed are similar to those imaged in histology. We showed qualitatively and quantitatively that laminar architecture is similar in the four hearts. MRI can be used to image the laminar architecture of ex vivo hearts in three dimensions, and the images produced are qualitatively and quantitatively comparable with histology. We have demonstrated in the rat that: 1) laminar architecture is consistent between hearts; 2) myolaminae are absent from much of the subepicardium; and 3) although localized orthotropy is present throughout the myocardium, tracked myolaminae are branching structures and do not have a discrete identity. myocardium; magnetic resonance imaging; ventricles; small animal imaging MYOCARDIAL STRUCTURE IS CENTRALLY important to cardiac mechanical function in health and disease (6), and myolaminar sliding is thought to be the principle mechanism of myocardial thickening in systole (10). Myolaminar structure has recently been shown to substantially influence the spread of activation in the myocardium (8,20).The myocardium is structured as stacked laminae of myocytes 4 -6 cells thick (ϳ80 -120 m), also known as myolaminae or sheets (24). These laminae are organized together in a complex fashion in which there are some regions of abrupt transmural change in laminar organization. The long axes of the myocytes, which make up the laminae, have a regular helical organization: the orientation of their long axes (with respect to the cardiac short axis) varies through ϳ120°trans-murally from endocardium to epicardium (33). The average orientation of the long axes of neighboring myocytes is known as the fiber-orientation (16). The myocardium therefore has regular lower order fiber architecture, with a more irregular and locally distinct higher order laminar arc...

Three-Dimensional Impulse Propagation in Myocardium

“…These layers form a branching network, and they have been referred to as sheets, 45 myolaminae, 10 and, more recently, sheetlets. 6 The laminar architecture described here has been confirmed with contrast-enhanced high-resolution magnetic resonance imaging 6 and diffusion tensor magnetic resonance imaging. 5 Therefore, ventricular tissue is not uniformly connected transverse to the myofiber direction.…”

“…At the whole-organ level, the geometry of the heart and the muscular architecture of atria and ventricles can be reconstructed in 3D at tissue-scale resolution using various imaging modalities. [5][6][7] However, it is not possible to measure 3D electric activity in the heart wall with equivalent precision.…”

“…6,10 Distinct layers or bundles of myocytes are evident in atria, 11 ventricles, 6 and the cardiac conduction system 12 at dimensions ranging from ≈100 µm to several millimeters. Furthermore, the fibrosis that accompanies aging, heart disease, and heart failure (HF) increases the extent and heterogeneity of structural discontinuity.…”

Antenatal architecture and activity of the human heart

“…This method is similar to that previously described [16]. Cardiac geometry, anisotropy and orthotropy were imaged in Fomblin with DT-MRI to acquire a resolution of 100-170 mm, a matrix size of 128 Â 128 Â 128, TE ¼ 15 ms, TR ¼ 500 ms and a b value of 1000 s mm 22 .…”

Generalized Minimal Principle for Rotor Filaments

“…From histological [32] and high-resolution MRI studies [33], however, the cardiac myofibers in the midwall region were found to be organized in sheets, separated by cleavage planes that reduce mechanical shear stresses during contraction [19,20]. We shall here model the layered architecture of myocardial tissue by reducing diffusivity along the sheet normal direction in the central part of the myocardial wall in the direction normal to the cleavage plane orientation.…”