The aim of the present study was to describe the fibre architecture of the fetal heart at mid gestation, and to clarify some persistent controversies concerning the architecture of the myofibres in the right ventricular wall and the muscular ventricular septum. We used quantitative polarized light microscopy to obtain information about the orientation of myocardial cells in the ventricular mass. These cells, joined into a network by anastomoses, have at any point in the ventricular mass a principal direction--the fibre direction. We have quantitated this information in the form of maps of the azimuth and elevation angles, in 18 midgestation fetal hearts. Our findings show that the fibre architecture of the heart can be conceptualised as myocardial fibres running like geodesics on a nested set of warped "pretzels". This model is an extension to the whole ventricular mass of Krehl's Triebwerk, and Streeter's model which was restricted to the left ventricle. A "pretzel" itself can be considered as two doughnuts joined side-by-side, with the tunnel at the center of each doughnut corresponding to the ventricular cavity. Over and above the excellence of the fit between the data and the geodesic representation, three strong arguments support this model. First, it is the only existing model that explains the observed rolling over of fibres around the atrioventricular valvar orifices. Second, it explains the trajectory of the fibres from the epicardium to the endocardium at the basal parts of both ventricles and at the apical part of the left ventricle. Third, the predicted topological singularities of the model are systematically observed in each of the 18 hearts studied.
Present limitations of quantitative polarized light analysis can neither confirm nor discard the existing models of fiber orientation in the whole ventricular mass after the neonatal period. However, the problems of mathematical and experimental validation of these two models have been posed in a rigorous manner. Non-ambiguous fiber tracking and demonstration of these models will require significant improvement of the definition range of the elevation angle that should be extended to 180 degrees .
Summary
A series of three‐dimensional image analysis tools are used to measure the three‐dimensional orientation of nuclei of myocardial cells. Confocal scanning laser microscopy makes it possible to acquire series of sections up to 100 μm inside thick tissue sections. A mean orientation vector of unit length is calculated for each segmented nucleus. The global orientation statistics are obtained by calculating the vectorial sum of the nuclear unit vectors. The final orientation is expressed by a mean azimuth angle, an elevation angle and a measure of the angular homogeneity. The method is illustrated for two different regions of the myocardium (interventricular septum and papillary muscle) of a normal human fetal heart. This quantitative method will be used to assess and calibrate the information provided by polarized light microscopy.
The study of the topological organisation of myocardial cells is a basic requirement for the understanding of the mechanical design of the normal and pathological heart. We developed a technique based on multiparametric image analysis of transmitted polarized light to generate maps of the azimuth and the elevation angles of the myocardial cells. The properties of birefringence of the myocardium embedded in methylmetacrylate were measured in papillary muscles with monitored 3D orientation. This birefringence is positive uniaxial with a 0 degree extinction angle when the axis of the fiber is parallel to the axis of the polarizer or the analyzer. Thick sections were studied between crossed polars, and four images of each section were digitized for an angle of the polarizer with the section varying from 0-67.5 degrees in steps of 22.5 degrees. The amounts of transmitted light for each setup of the polarizer were combined in order to extract the values of the azimuth angle (modulo 90 degrees) and the elevation angle of the myocardial cells, according to the Johannsen equation. The respective maps of these angles were calculated and then assessed with confocal scanning laser microscopy. This method provides an efficient and accurate tool for the study of the histological architecture of the fetal and neonatal heart.
International audienceThis paper investigates the 3D microscopic structure of ex-vivo human cardiac muscle. Usual 3D imaging techniques such as DMRI or CT do not achieve the required resolution to visualise cardio-myocytes, therefore we employ X-ray phase contrast micro-CT, developed at the European Synchrotron Radiation Facility (ESRF). Nine tissue samples from the left ventricle and septum were prepared and imaged at an isotropic resolution of 3.5 μm, which is sufficient to visualise cardio-myocytes. The obtained volumes are compared with 2D histological examinations, which serve as a basis for interpreting the 3D X-ray phase-contrast results. Our experiments show that 3D X-ray phase-contrast micro-CT is a viable technique for investigating the 3D arrangement of myocytes ex-vivo at a microscopic level, allowing a better understanding of the 3D cardiac tissue architecture
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